Roles of MADS-box transcription factors in plant responses to abiotic and biotic stresses.

Roles of MADS-box transcription factors in plant responses to abiotic and biotic stresses - PMC Skip to main content An official website of the United States government Here's how you know Here's how you know Official websites use .gov A .gov website belongs to an official government organization in the United States. Secure .gov websites use HTTPS A lock ( Lock Locked padlock icon ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites. Search Log in Dashboard Publications Account settings Log out Search… Search NCBI Primary site navigation Search Logged in as: Dashboard Publications Account settings Log in Search PMC Full-Text Archive Search in PMC Journal List User Guide PERMALINK Copy As a library, NLM provides access to scientific literature. Inclusion in an NLM database does not imply endorsement of, or agreement with, the contents by NLM or the National Institutes of Health. Learn more: PMC Disclaimer | PMC Copyright Notice Plant Commun . 2026 Feb 16;7(4):101778. doi: 10.1016/j.xplc.2026.101778 Search in PMC Search in PubMed View in NLM Catalog Add to search Roles of MADS-box transcription factors in plant responses to abiotic and biotic stresses Na Liu Na Liu 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Na Liu 1, ∗ , Zihao Liu Zihao Liu 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Zihao Liu 1 , Guangxiang Tian Guangxiang Tian 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Guangxiang Tian 1 , Shijia Zhao Shijia Zhao 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Shijia Zhao 1 , Hao Chu Hao Chu 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Hao Chu 1 , Yiheng Hu Yiheng Hu 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Yiheng Hu 1 , Yingfan Zhao Yingfan Zhao 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Yingfan Zhao 1 , Yanyan Zhang Yanyan Zhang 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Yanyan Zhang 1 , Kun Cheng Kun Cheng 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Kun Cheng 1 , Daowen Wang Daowen Wang 2 State Key Laboratory of Wheat and Maize Crop Science, College of Agronomy and Center for Crop Genome Engineering, Henan Agricultural University, Longzi Lake Campus, Zhengzhou 450046, China Find articles by Daowen Wang 2 , Wenming Zheng Wenming Zheng 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Wenming Zheng 1, ∗∗ , Zheng Qing Fu Zheng Qing Fu 3 Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA Find articles by Zheng Qing Fu 3, ∗∗∗ , Xu Wang Xu Wang 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China Find articles by Xu Wang 1, ∗∗∗∗ Author information Article notes Copyright and License information 1 College of Life Sciences, Henan Agricultural University, Zhengzhou 450046, China 2 State Key Laboratory of Wheat and Maize Crop Science, College of Agronomy and Center for Crop Genome Engineering, Henan Agricultural University, Longzi Lake Campus, Zhengzhou 450046, China 3 Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA ∗ Corresponding author [email protected] ∗∗ Corresponding author [email protected] ∗∗∗ Corresponding author [email protected] ∗∗∗∗ Corresponding author [email protected] Received 2025 Aug 15; Revised 2025 Oct 16; Accepted 2026 Feb 12; Collection date 2026 Apr 13. © 2026 The Author(s) This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). PMC Copyright notice PMCID: PMC13084090  PMID: 41703934 Abstract Plants deploy sophisticated adaptive mechanisms to mitigate the detrimental effects of abiotic stresses (drought, salinity, temperature extremes, and heavy metals) and biotic stresses (pathogens and senescence) on growth and productivity. Central to these responses are transcription factors (TFs) that orchestrate stress-responsive gene networks. Among TF families, MADS-box proteins, characterized by their evolutionarily conserved DNA-binding domain, function as pivotal regulators of developmental plasticity and stress adaptation. While recent advances have clarified their roles in abiotic stress tolerance, a systematic integration of their functions in biotic stress responses has yet to be achieved. This review synthesizes current knowledge on how MADS-box TFs mediate plant adaptation to both abiotic and biotic stresses through the regulation of intricate transcriptional networks. By integrating these multifaceted insights, we advance toward a unified understanding of the molecular mechanisms by which MADS-box TFs coordinate plant responses to dual environmental challenges. Our analysis provides mechanistic insights into enhancing plant resilience through the targeted modulation of MADS-box genes and their regulatory networks. We further propose translational strategies for crop improvement, focusing on molecular breeding approaches to engineer stress-tolerant varieties that balance stress adaptation with developmental processes. This comprehensive assessment establishes MADS-box TFs as master regulators at the stress–development interface and proposes novel biotechnological avenues for sustainable agriculture. Key words: abiotic stresses, biotic stresses, MADS-box, transcription factors, crop improvement, stress signaling Positioning MADS-box proteins as pivotal regulators, this review synthesizes their roles in coordinating plant adaptation to diverse abiotic and biotic stresses. It highlights mechanistic insights relevant to crop improvement, particularly pathways that may enable the decoupling of stress tolerance from growth penalties to support sustainable agricultural solutions. Introduction Terrestrial plants, owing to their immobile nature, are continually exposed to diverse abiotic and biotic stresses, including drought, salinity, extreme temperatures, and pathogen infection, that constrain growth and reduce agricultural productivity. To mitigate these challenges, plants deploy integrated developmental, physiological, and molecular adaptations ( Kumari et al., 2019 ; Du et al., 2024 ). Central to this adaptive capacity is transcriptional reprogramming, orchestrated by transcription factors (TFs) that fine-tune gene expression networks in response to stress ( Bhoite et al., 2025 ). MADS-box TFs, distinguished by their evolutionarily conserved DNA-binding domain ( Shore and Sharrocks, 1995 ), are broadly classified into two major types ( Gramzow and Theißen, 2013 ). Type I proteins generally contain only the MADS (M) domain and exhibit a relatively simple overall architecture; they are further subdivided into the Mα, Mβ, and Mγ lineages based on sequence characteristics ( Parenicová et al., 2003 ). In angiosperms, type I genes are frequently associated with reproductive processes, particularly gametophyte, endosperm, embryo, and seed development, although their functional characterization remains comparatively limited relative to type II factors ( Qiu and Köhler, 2022 ). In contrast, type II (MIKC-type) MADS-box proteins possess a characteristic four-domain architecture (M–I–K–C). The M domain mediates DNA binding, the intervening (I) domain facilitates dimerization, the keratin-like (K) domain contributes to protein–protein interactions, and the C-terminal (C) domain modulates transcriptional activation and partner specificity ( Theissen et al., 1996 ; Henschel et al., 2002 ; de Folter et al., 2005 ; Kaufmann et al., 2005 ; Lai et al., 2021 ). This complex domain organization underpins the predominant role of MIKC-type MADS-box TFs in regulating intricate developmental programs, particularly those controlling organ identity and floral development ( Kaufmann et al., 2005 ). Recent phylogenomic analyses have redefined MIKC∗-type TFs as the closest relatives of ancestral M-type factors, challenging earlier assumptions of a close evolutionary relationship between MIKC∗ and MIKC C proteins ( Qiu et al., 2023 ; 2024 ). In parallel, Han et al. (2025) proposed a polyphyletic origin for plant type I genes and suggested that the two subfamilies of plant type II genes (MIKC C and MIKC∗) arose from an ancient gene duplication event in the stem group of streptophytes, rather than in land plants. MIKC C -type MADS-box genes are further classified into numerous highly conserved subfamilies, including AG, DEF (AP3), GLO (PI), SEP, SOC1 (TM3), FLC, SHORT VEGETATIVE PHASE (SVP), AGL6, AGL15, and AGL17 ( Martinez-Castilla and Alvarez-Buylla, 2003 ; Nam et al., 2003 ; Gramzow and Theißen, 2013 ). Importantly, our analysis reveals that MADS-box genes implicated in both biotic and abiotic stress responses are distributed across 12 distinct MIKC C -type subfamilies ( Supplemental Table 1 ). This broad phylogenetic distribution underscores the pivotal role of the MADS regulatory network in integrating developmental programs with environmental signaling. At the molecular level, the MADS domain recognizes CArG-box motifs in the promoters of target genes, while the K and C domains facilitate protein complex formation and transcriptional activation, respectively ( Egea-Cortines et al., 1999 ; de Folter and Angenent, 2006 ). As one of the largest plant TF families in plants, MADS-box proteins regulate pivotal developmental processes ranging from floral organogenesis to fruit maturation through homo- and heteromeric complex formation ( Egea-Cortines et al., 1999 ; Theissen et al., 2000 ; Zhang et al., 2024 ). Importantly, they also function as master regulators of stress adaptation. Castelán-Muñoz et al. (2019) proposed that MADS-box TFs function as evolutionary hubs, integrating abiotic stress signals—including drought, salinity, temperature, and oxidative stress—to direct developmental plasticity and survival responses. Consistent with this view, ancestral MADS-box proteins are thought to have primarily functioned in stress perception ( Qiu et al., 2023 ), with their contemporary roles expanding to encompass both abiotic stress resilience ( Tapia-López et al., 2008 ; Wang and Cheng, 2017 ; Chen et al., 2018a ; Jiang et al., 2025 ; Zhang et al., 2025 ) and biotic defense ( Arne et al., 2014 ). Genomic and transcriptomic studies in Arabidopsis thaliana , rice, and wheat further confirm the broad conservation of MADS-box genes and their frequent stress-inducible expression patterns ( Parenicová et al., 2003 ; Arora et al., 2007 ; Schilling et al., 2020 ). This review synthesizes key advances in our understanding of MADS-box-mediated stress regulatory networks, highlighting their mechanistic importance in translating environmental cues into adaptive phenotypes. By integrating both shared and species-specific mechanisms identified across model plants and crops, we provide a comprehensive framework to support evidence-based strategies for future gene editing and plant resilience research. MADS-box TFs in abiotic stress Plants exist in a world fraught with environmental adversity, where survival hinges on their ability to sense, respond to, and adapt to a diverse array of abiotic stresses. Among the key molecular architects guiding this adaptive process are MADS-box TFs, dynamic regulators renowned for their multifaceted roles in plant growth, development, and environmental resilience. From drought and high temperatures to heavy metal toxicity, chilling, nutrient deficiencies, and salinity stress, plants often encounter multiple challenges simultaneously, demanding finely tuned and integrated response systems. MADS-box TFs emerge as chief mediators in this battle, orchestrating hormone signaling pathways, modulating metabolic networks, and driving stress-mitigation strategies to bolster survival. Their ability to coordinate responses across overlapping stresses reflects a remarkable versatility that not only equips plants to endure hostile environments but also positions these TFs as indispensable players in abiotic stress biology ( Supplemental Table 1 ). Understanding the breadth and precision of MADS-box TF function offers exciting opportunities to unlock their potential for advancing agricultural sustainability in an era of global climate challenges. Harnessing drought stress Drought has a profound impact on global food security by reducing transpiration and crop yields, thereby forcing plants to rely on molecular defense systems activated through complex signaling networks ( Figure 1 ) ( Ahluwalia et al., 2021 ). MADS-box TFs, long recognized for their roles in plant development and flowering, have emerged as key regulators of drought adaptation, primarily through modulation of stomatal behavior and hormonal signaling ( Zhang et al., 2006 ; Awad et al., 2019 ). In Arabidopsis , the AGL17-like clade member AGL16 acts as a negative regulator of drought tolerance by coordinately controlling stomatal development and ABA homeostasis. AGL16 represses the expression of STOMATAL DENSITY AND DISTRIBUTION 1 ( SDD1 ) and ABSCISIC ALDEHYDE OXIDASE 3 ( AAO3 ), thereby constraining stomatal developmental programs and ABA biosynthesis. In parallel, AGL6 promotes ABA catabolism through upregulation of CYP707A3 . Under drought conditions, AGL16 is transcriptionally downregulated, which relieves repression of SDD1 and AAO3 and attenuates CYP707A3 -mediated ABA degradation. This regulatory shift results in elevated ABA accumulation, enhanced stomatal closure, and improved relative water content (RWC) ( Zhao et al., 2020 ). Similarly, SVP promotes ABA accumulation by suppressing the ABA catabolic genes CYP707A1 and CYP707A3 while upregulating AtBG1 , which encodes a β-glucosidase that contributes to ABA accumulation. Consistently, svp mutants display wider stomatal apertures and increased water loss, underscoring the critical role of SVP in drought adaptation ( Wang et al., 2018 ; Allen et al., 2019 ). Figure 1. Open in a new tab Regulatory circuits mediated by MADS-box genes in response to drought stress. In Arabidopsis , AGL16 acts as a direct regulator of CYP707A , promoting ABA catabolism while simultaneously suppressing the expression of SDD1 , which influences stomatal development, and AAO3 , a key gene in ABA biosynthesis. Through these combined activities, AGL16 modulates ABA accumulation and affects stomatal density and movement, thereby functioning as a negative regulator of drought resistance. SVP/AGL22 binds to and upregulates AtBG1 , facilitating the hydrolysis of ABA glucosyl esters (ABA-GEs). In rice, hydrolysis of ABA-GEs releases active ABA, thereby activates SAPK9, which then phosphorylates OsMADS23, a process essential for drought tolerance. Knockout mutants of OsMADS23 exhibit reduced drought resistance. OsMADS23 promotes the expression of ABA biosynthesis genes OsNCED2 , OsNCED3 , and OsNCED4 , thereby increasing endogenous ABA levels and proline accumulation. In addition, OsMADS26 functions as an upstream negative regulator of the drought-responsive gene RAB21 , while SlMBP8 negatively regulates drought resistance in tomato by modulating the proline biosynthesis gene P5CS1 . Under drought conditions, altered expression of OsMADS26 and S l MBP8 affects physiological parameters associated with drought tolerance, including relative water content (RWC), relative water loss, malondialdehyde (MDA) levels, and chlorophyll content. In rice ( Oryza sativa ), a globally important food crop, distinct MADS-box TFs govern drought responses. OsMADS23 acts as a positive regulator: its overexpression enhances drought tolerance, partly by synergistically activating ABA biosynthesis genes ( NCEDs ), thereby elevating ABA levels. Moreover, phosphorylation of OsMADS23 by the SnRK2 protein kinase SAPK9 enhances its activity, further promoting ABA accumulation and proline synthesis—both of which are essential for osmotic adjustment under water deficit ( Li et al., 2021b ). In contrast, OsMADS26 functions as a negative regulator of stress responses. Its overexpression leads to severe stress sensitivity, including growth retardation, sterility, root curling, chlorosis, and high mortality, highlighting its critical role in restraining stress-responsive pathways ( Khong et al., 2015 ). Together, the opposing roles of OsMADS23 and OsMADS26 illustrate how different paralogs within a single species can be deployed in distinct regulatory contexts—potentially across developmental stages—to fine-tune drought responses. In tomato ( Solanum lycopersicum ), the MADS-box TF SlMBP8 also negatively regulates drought resistance. SlMBP8 suppresses the expression of stress-responsive genes, including P5CS1 , which is involved in proline biosynthesis. Transgenic plants with reduced SlMBP8 expression display improved RWC, higher chlorophyll contents, reduced oxidative damage (as indicated by lower malondialdehyde [MDA] content), and consequently enhanced water retention and stress resilience ( Yin et al., 2017a ). Collectively, by modulating core processes such as stomatal dynamics, osmotic adjustment, and oxidative homeostasis, MADS-box TFs constitute an integral yet highly context-dependent regulatory layer within plant drought-response networks. Enduring salt stress Coastal wetlands and agricultural systems are increasingly affected by salinity arisingfrom seawater intrusion, which imposes osmotic stress and ionic imbalance that desiccate plant tissues. Under these saline conditions, MADS-box TFs function as molecular sentinels, activating conserved survival programs to mitigate salt toxicity ( Castelán-Muñoz et al., 2019 ). A major challenge during salinity stress is maintaining K + /Na + homeostasis and minimizing Na + cytotoxicity, which disrupts membrane potential and nutrient uptake ( Wang et al., 2013 ; Hussain et al., 2021 ). Plants rapidly elevate ABA levels to suppress growth under stress ( Alfatih et al., 2023 ). In Arabidopsis , AGL16 functions as a negative regulator of salt tolerance, with its expression modulated by both salt stress and ABA. The agl16 mutant exhibits elevated expression of ABA biosynthesis genes ABA2 , NCED3 , and AAO3 , resulting in increased ABA accumulation. Additionally, AGL16 represses stress-responsive genes such as HKT1;1 , HsfA6a , and MYB102 , thereby disrupting ion homeostasis ( Zhao et al., 2021 ). The function of AGL16 is likely spatially specific. Its repression of the root-specific ion transporter gene HKT1;1 suggests a primary role in regulating root ion uptake, which may differ from its functions in shoot tissues. In contrast, AGL21 promotes salt sensitivity during germination by enhancing ABA signaling through transcriptional activation of ABI5 , a key TF whose stability is controlled by ABA-mediated degradation of its E3 ligase, KEEP ON GOING (KEG) ( Stone et al., 2006 ). The rice orthologs OsMADS25 and OsMADS27, both members of the AGL17-like clade, contribute to salt tolerance through distinct mechanisms. OsMADS25 enhances salt tolerance by upregulating genes involved in reactive oxygen species (ROS) detoxification (such as OsGST4 ) and proline biosynthesis (such as OsP5CR ), thereby alleviating oxidative damage ( Xu et al., 2018 ). In contrast, OsMADS27 promotes Na + exclusion via OsHKT1;1 and helps maintain ROS homeostasis, in part through its interaction with OsABI5 ( Alfatih et al., 2023 ). In addition, SAPK9-mediated phosphorylation activates OsMADS23 to enhance ABA and proline biosynthesis under salt stress ( Li et al., 2021b ), revealing a conserved adaptive module shared between salt and drought responses. In tomato, SlMBP11 enhances salt tolerance by reducing electrolyte leakage and MDA content while increasing water retention and chlorophyll levels through activation of osmolyte biosynthesis genes ( Guo et al., 2016 ). Conversely, suppression of SlMBP8 activates stress-response cascades, conferring dual drought and salinity tolerance ( Yin et al., 2017b ). In pepper, silencing of CaMADS compromises seed germination, root elongation, and oxidative stress tolerance ( Chen et al., 2019 ). Notably, even in gymnosperms, overexpression of GbMADS9 in ginkgo increases chlorophyll and proline accumulation while reducing MDA levels, thereby enhancing osmotic stress tolerance ( Yang et al., 2016 ). Together, the conservation of core functions across diverse plant species—including regulation of ion homeostasis, ABA signaling, and ROS scavenging—highlights the fundamental role of MADS-box TFs in salt adaptation ( Figure 2 ). Figure 2. Open in a new tab Regulatory functions of various MADS-box TFs in enhancing salinity tolerance across different plant species. In Arabidopsis , AGL16 regulates ABA biosynthesis, enhancing the activation of stress-responsive genes while suppressing a range of abiotic stress-responsive genes to maintain ion homeostasis and cope effectively with salinity stress. AGL21 functions as a negative modulator of seed germination and post-germination growth by influencing ABI5 expression. AGL21 -overexpression ( AGL21 -OE) plants exhibit heightened sensitivity to ABA and salt stress. In rice, overexpression of OsMADS27 significantly improves salinity tolerance by regulating ion homeostasis, reactive oxygen species (ROS) balance, and nitrate accumulation. OsSLR1 interacts with OsABI5 and OsMADS27, leading to elevated endogenous ABA levels and enhanced sensitivity to exogenous ABA. OsMADS25 boosts salinity tolerance primarily through an ABA-mediated pathway by increasing ROS-scavenging capacity and proline accumulation. OsMADS25 regulates key salt stress-responsive genes, including OsABI5 , OsNAC6 , and OsDREB2A , and activates auxin signaling via OsYUC4 . In tomato, elevated expression of SlMBP11 improves salt stress tolerance, as evidenced by reduced electrolyte leakage and MDA content, together with enhanced water retention and chlorophyll levels. In contrast, SlMBP8 functions as a negative regulator in high-salinity signaling pathways. In pepper, CaMADS overexpression results in improved germination rates, increased green cotyledon percentages, higher fresh weight, and longer root lengths. Conversely, CaMADS -silenced plants exhibit increased electrolyte leakage, reduced chlorophyll content, and elevated MDA levels. Finally, in ginkgo, overexpression of GbMADS9 enhances the activities of antioxidant enzymes (SOD, APX, and CAT) under osmotic stress, conferring increased osmotic tolerance. Adaptation to rising temperatures Rising global temperatures pose a severe threat to plant productivity by impairing leaf function, disrupting photosynthesis, and compromising protein stability, particularly in heat-sensitive crops ( Teixeira et al., 2013 ). Rice exemplifies this vulnerability: each 1 °C increase during critical growth phases can reduce yields by approximately 10%, with early seed-development stages being especially susceptible due to disrupted physiological processes and gene regulation ( Peng et al., 2004 ; Mthiyane et al., 2024 ). In this context, the MADS-box TF family has emerged as a key mediator of thermotolerance ( Supplemental Figure 1 ). Reproductive development in rice is particularly sensitive to high temperatures, especially during early seed formation, which coincides with endosperm cellularization ( Begcy et al., 2018 ). Elucidating the molecular mechanisms governing this transition is therefore essential for identifying targets to improve heat resilience. Transcriptomic profiling has shown that intense heat stress induces a coordinated reduction in the expression of genes involved in major developmental pathways, potentially underlying the observed physiological impairments ( Wang et al., 2025 ). Moreover, type I MADS-box genes expressed during the syncytial endosperm stage display differential sensitivity to heat stress. Among these, OsMADS87 plays a pivotal role in regulating seed size and the timing of endosperm cellularization. Loss of OsMADS87 function accelerates cellularization, reduces seed size, and decreases sensitivity to moderate heat stress, highlighting its potential as a target for enhancing reproductive heat tolerance ( Chen et al., 2016 ; Kambale et al., 2021 ). Beyond reproductive development, heat stress profoundly affects seed germination in Arabidopsis through thermoinhibition, a process that suppresses germination by activating ABA biosynthesis and inhibiting gibberellic acid (GA) pathways. The MADS-box TF AGAMOUS-LIKE67 (AGL67) plays a pivotal role in this response by interacting indirectly with SOMNUS (SOM), a zinc-finger protein that modulates GA and ABA metabolism ( Li et al., 2020 ). AGL67 recruits the histone mark reader EARLY BOLTING IN SHORT DAY (EBS), which recognizes H3K4me3 at the SOM locus. Under high-temperature conditions, enrichment of AGL67 and EBS at the SOM promoter facilitates histone H4K5 acetylation, activating SOM expression and ultimately inhibiting seed germination ( Li et al., 2020 ). Heat stress also severely compromises chloroplast function, thereby impairing photosynthesis and chloroplast biogenesis ( Zahra et al., 2023 ). The MADS-box TF SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1/AGL20), best known as a floral integrator in Arabidopsis , also functions as a transcriptional regulator of heat responses. Overexpression of SOC1/AGL20 , as well as its functional homologs from Petunia ( FBP21 and FBP22 ), enhances the expression of chlorophyll biosynthesis genes, improves chloroplast protein import and processing, and mitigates the detrimental effects of heat stress ( Wang et al., 2019 ). These findings suggest that SOC1’s protective role is likely tissue- or cell-type specific, particularly in photosynthetic tissues where maintaining chloroplast integrity is essential. Furthermore, floral development is highly sensitive to elevated temperatures. In tomato, continuous mild heat stress increases the frequency of stamen abnormalities, including reduced pollen viability and anther deformation. Heat stress disrupts tomato stamen development through the coordinated suppression of key MADS-box genes. Under elevated temperatures, downregulation of TM6 , TAP3 , and LePI in anthers compromises stamen identity, leading to homeotic transformations and reduced pollen viability ( Müller et al., 2016 ). Among these factors, TAP3 plays a particularly critical role, as its suppression alone is sufficient to trigger anther-to-pistil conversions. Concurrent downregulation of TM6 and LePI further exacerbates these developmental defects, demonstrating that this specific suite of MADS-box genes constitutes a thermally vulnerable regulatory module essential for maintaining reproductive organ identity under heat stress ( Müller et al., 2016 ). Together, these findings highlight the multifaceted roles of MADS-box TFs in coordinating plant responses to heat stress across key developmental stages, including seed germination and reproductive development. Dealing with cold stress Cold stress poses a significant threat to crop productivity and agricultural sustainability. To mitigate this challenge, plants employ genetically encoded regulatory networks in which MADS-box TFs function as molecular thermometers that are rapidly activated upon temperature decline ( Figure 3 ). These TFs integrate cold signaling across plant species by modulating diverse adaptive responses, including flowering transitions, ROS homeostasis, osmotic balance, and stress-responsive gene expression. Figure 3. Open in a new tab Regulatory networks associated with MADS-box genes in response to cold stress. In rice, OsMADS25 acts as a positive regulator of chilling tolerance by upregulating the expression of ROS scavenging-related genes, including LTG1 , OsDREB6 , and OsTPP1 . OsMADS57 activates OsWRKY94 transcription in response to cold stress. In addition, OsMADS57 can directly promote D14 transcription, thereby inhibiting tillering under low-temperature conditions, activating cold-responsive genes (e.g., OsWRKY94 ), and restricting organ formation. In Arabidopsis , the flowering-time gene SOC1 / AGL20 serves as a negative regulator of cold-response pathways. It directly represses CBF genes, delays flowering by increasing FLC expression during transient cold periods in autumn or early spring, and suppresses cold responses during floral induction through SOC1/AGL20-mediated repression of cold-inducible genes. In tomato, the MADS-box genes TM4 , TM5 , TM6 , and TAG1 are strongly upregulated under low-temperature conditions and may be linked to flower abnormalities. In ginkgo, GbMADS9 positively regulates cold tolerance through mechanisms similar to those involved in osmotic stress regulation. In pepper, CaMADS mitigates cold-induced oxidative stress, resulting in reduced oxidative damage in CaMADS -overexpressing plants. At the molecular level, OsMADS25 exemplifies how MADS-box TFs mediate cold tolerance in rice. OsMADS25 enhances cold tolerance by upregulating ROS-scavenging genes such as LTG1 (involved in auxin signaling), OsDREB6 (involved in osmotic regulation), and OsTPP1 (which promotes trehalose accumulation), thereby reducing oxidative damage and improving osmotic adjustment under cold stress ( Yan et al., 2021 ). Notably, OsMADS25 also contributes to salt tolerance, underscoring the capacity of MADS-box TFs to function across multiple abiotic stress pathways. In addition to transcriptional regulation, developmental plasticity further underpins cold adaptation. In rice, cold stress triggers a regulatory mechanism in which OsTB1 inhibits OsMADS57-mediated activation of D14 . This interaction enhances tiller formation, activates cold-responsive genes such as OsWRKY94 , and alleviates developmental constraints imposed by low temperatures ( Minakuchi et al., 2010 ; Guo et al., 2013 ; Chen et al., 2018b ). In Arabidopsis , cold-induced activation of C-REPEAT BINDING FACTORs (CBFs) elevates FLOWERING LOCUS C ( FLC ) expression, which in turn represses the floral integrators FLOWERING LOCUS T ( FT ) and SOC1/AGL20 , thereby delaying flowering and enhancing freezing tolerance. Conversely, SOC1/AGL20 suppresses CBF expression, increasing cold susceptibility during vegetative growth ( Michaels and Amasino, 1999 ; Lee et al., 2000 ; Seo et al., 2009 ). This flowering-time decision is coordinated by the repressive FLC–SVP complex ( Lee et al., 2005 ). Together, these findings exemplify time-specific functional roles of MADS-box TFs, such as FLC and SOC1, which dynamically balance developmental timing and stress responses according to growth stage and external conditions. Similarly, cold-inducible expression of MADS-box genes—including TOMATO MADS-BOX GENE 4 ( TM4 ), TM5 , TM6 , and TOMATO AGAMOUS1 ( TAG1 )—in tomato is associated with floral abnormalities and altered organ maturation ( Lozano et al., 1998 ; Postma et al., 2014 ). Enhanced cold tolerance through physiological adjustments and activation of antioxidant systems is also mediated by MADS-box factors such as CaMADS in pepper ( Capsicum annuum ) and GbMADS9 in ginkgo ( Ginkgo biloba ) ( Yang et al., 2016 ; Chen et al., 2019 ). Collectively, MADS-box TFs function as critical, evolutionarily conserved regulators of cold-stress responses throughout plant development. By coordinating key physiological and developmental processes—including flowering-time control, reinforcement of antioxidant defenses, maintenance of osmotic homeostasis, and modulation of stress-responsive signaling pathways—these TFs form an integrated regulatory hub that underpins resilience to low temperatures and facilitates plant survival and adaptation under cold stress. Fighting nutrient stresses Nutrient deficiencies—particularly nitrogen (N), phosphorus (P), and sulfur (S)—severely constrain plant development and agricultural productivity by disrupting essential metabolic processes and signaling pathways ( Chiou and Lin, 2011 ; de Bang et al., 2021 ; Narayan et al., 2023 ). MADS-box TFs function as central sensors and regulators within nutrient-responsive networks ( Figure 4 ).In Arabidopsis , ARABIDOPSIS NITRATE REGULATED 1/AtAGL44 (ANR1) governs lateral root development in direct response to external nitrate (NO₃ − ) availability and is rapidly transcriptionally repressed upon NO₃ − resupply through a feedback mechanism ( Gan et al., 2005 , 2012 ). This nitrate-specific regulation by ANR1 contrasts with the broader stress-integrative role of SOC1/AGL20. SOC1 is upregulated not only under N deficiency but also during P and S deprivation, positioning it as a central coordinator of growth responses across multiple nutrient stresses ( Gan et al., 2005 ). In addition, several MADS-box genes—including AGL8 , AGL28 , AGL104 , AGL67 , and MAF3 —exhibit distinct expression patterns under N starvation and resupply, enabling fine-tuned adaptive responses ( Gan et al., 2005 ). Figure 4. Open in a new tab Regulatory dynamics involving MADS-box genes during plant responses to nutrient deficiency. In the NO 3 − signaling pathway, AGL8 , AGL28 , and AGL104 are significantly downregulated under nitrogen (N) starvation and induced by short-term NO₃ − resupply, whereas AGL67 and MAF3 are strongly upregulated during N starvation and suppressed upon NO₃ − resupply. ANR1/AtAGL44 is specifically regulated by N availability and controls lateral root growth in response to changes in external NO₃ − supply. In rice, miR444 targets four ANR1-like homologs— OsMADS23 , OsMADS27a , OsMADS27b , and OsMADS57 —to modulate root development under nitrate signaling. AGL21 expression is markedly induced by nitrate deficiency during seed germination and may function as a regulator of nutrient stress responses. Under phosphate deprivation, TaMADS51 , TaMADS4 , TaMADS5 , TaMADS6 , and TaMADS18 are upregulated, whereas TaMADAGL2 , TaMADWM31C , TaMADAGL17 , and TaMADS14 are downregulated. TaMADS51 regulates phosphorus acquisition by modulating root system architecture. Collectively, TaMADS-box genes participate in phosphate-starvation responses (PSRs) by regulating ROS homeostasis, root development, PSR gene expression, and Pi uptake. −N, N starvation; ++N, N resupply. In rice, the orthologs OsMADS25, OsMADS27, OsMADS57, OsMADS61, and OsMADS23 mediate NO 3 − signaling and influence root system architecture. OsMADS25 specifically promotes lateral and primary root growth in a NO₃ − -dependent manner, whereas OsMADS57 expression increases upon NO₃ − replenishment following starvation ( Yu et al., 2014a ). The microRNA miR444 targets several MADS-box genes (incuding OsMADS23 , OsMADS27a , OsMADS27b , and OsMADS57 ) to optimize root architecture under nitrate signaling ( Sunkar et al., 2005 ; Lu et al., 2008 ; Wu et al., 2009 ; Li et al., 2010 ; Pachamuthu et al., 2022 ). Similarly, AGAMOUS-LIKE21 (AGL21) promotes lateral root initiation and elongation across different N regimes by stimulating cell division in root primordia ( Yu et al., 2014b ). Under P limitation, plants activate phosphate starvation responses (PSRs) to maintain nutrient homeostasis. MADS-box TFs coordinate these adaptations by triggering changes in root architecture ( Han et al., 2022 ). In wheat ( Triticum aestivum ), several MADS-box genes have been implicated in the regulation of P-limitation responses ( Han et al., 2022 ). Notably, overexpression of TaMADS51 enhances P acquisition, promotes plant growth, and improves photosynthetic performance under P-deficient conditions ( Shi et al., 2016 ). Transcriptomic analyses further revealed that multiple MADS-box genes in wheat are differentially expressed under P stress, including upregulation of TaMADS4 , TaMADS5 , TaMADS6 , and TaMADS18 , and downregulation of TaMADAGL2 , TaMADAGL17 , TaMADWM31C , and TaMADS14 ( Shi et al., 2016 ). Beyond P-specific responses, several MADS-box genes participate in crosstalk among P, N, and S signaling pathways ( Supplemental Figure 2 ). In rice, for example, ANR1-like genes such as OsMADS23 , OsMADS25 , and OsMADS27 are suppressed under P stress, whereas all five members of this subfamily ( OsMADS23 , OsMADS25 , OsMADS27 , OsMADS57 , and OsMADS61 ) are induced by S starvation ( Yu et al., 2014a ). Most of these genes also respond to fluctuations in N availability, supporting their broader role in integrated nutrient signaling ( Yu et al., 2014a ). This regulatory network extends to nutrient transport systems. In rice, expression of OsNRT2.1 and OsNAR2.1 is influenced by both P and S availability; the phosphate transporter OsIPS1 responds to N and S status; and the sulfate transporter OsSULTR1;1 is repressed upon P resupply ( Yu et al., 2014a ). Together, these findings highlight a coordinated nutrient signaling network in which MADS-box TFs may help integrate P, N, and S responses. Navigating heavy-metal stresses Industrial pollution introduces persistent toxic metals such as cadmium (Cd), nickel (Ni), and aluminum (Al) into soils, posing serious threats to plant growth and ecosystem integrity. To counteract metal toxicity, plants deploy molecular defense mechanisms in which MADS-box TFs act as key orchestrators of adaptive responses ( Figure 5 ). Figure 5. Open in a new tab Regulatory network of MADS-box genes in response to heavy metal stress. Overexpression of GsMAS1 confers Al 3+ tolerance in Arabidopsis , enhancing root growth and proline accumulation. This tolerance is mediated by phosphorylated STOP1, which upregulates Al-chelating transporters AtMATE (citrate efflux) and AtALMT1 (malate efflux), while evading ubiquitin-mediated degradation through inhibition of AtRAE1 binding. In GsMAS1 -overexpressing lines, Al 3+ stress also activates PGIP1 and PGIP2 , a process mediated by the TF STOP2 that is critical for cell-wall stabilization under low-pH conditions. In addition, AGL62 is specifically induced in Al 3+ -resistant flax genotypes. Under cadmium stress, the MADS-box gene EcAGL from Erigeron canadensis is strongly induced. When heterologously expressed in Arabidopsis , EcAGL significantly restricts cadmium translocation to aerial tissues without affecting root accumulation, indicating a role in metal partitioning that enhances tolerance ( Zuo et al., 2023 ). Similarly, nickel exposure upregulates a set of MADS-box genes ( HuMADS-1/22/35/42 ) in pitaya ( Selenicereus undatus L.), implicating these TFs in nickel stress adaptation ( Hui et al., 2024 ). In acidic soils, aluminum toxicity inhibits root growth and nutrient uptake ( Shetty et al., 2021 ; Ryan and Yang, 2024 ). The MADS-box factor GsMAS1 from Glycine soja enhances aluminum resistance by activating ALMT1 , STOP1 , MATE , and STOP2 , while also contributing to cell wall integrity ( Kobayashi et al., 2014 ; Zhang et al., 2020 ). This regulatory network is further fine-tuned by calcium-dependent protein kinases CPK21 and CPK23, which stabilize STOP1 by preventing its interaction with the E3 ubiquitin ligase RAE1, thereby reinforcing aluminum resistance ( Zhang et al., 2019 ; Cao et al., 2025 ). In flax, elevated expression of AGL62 is specifically associated with aluminum-tolerant genotypes, suggesting a role in natural variation in aluminum tolerance ( Krasnov et al., 2019 ). Together, these findings establish MADS-box TFs as integral components of plant metal detoxification systems, modulating metal transport, stress signaling, and structural adaptation across diverse plant species in response to toxic metal exposure. Orchestrating waterlogging responses Although research on MADS-box TFs in hypoxia responses remains less extensive than that on other abiotic stresses, emerging evidence positions them as key regulators of flooding adaptation across diverse plant species. These TFs exhibit temporally coordinated expression patterns that enable staged and dynamic responses to oxygen deprivation. In Rhododendron hainanense , multiple MADS-box genes display precisely timed induction under submergence ( Supplemental Table 1 ). RhMADS24 , RhMADS25 , and RhMADS44 show distinct expression peaks at 3, 12, and 24 h, respectively, indicating specialized functions at different phases of hypoxic stress. Meanwhile, RhMADS22 , RhMADS27 , and RhMADS29 form a co-regulated module with synchronized upregulation at 3 h, suggesting synergistic roles in early waterlogging signaling ( Huo et al., 2021 ). This temporal specialization is conserved in barley, where HvMADS13 , HvMADS35 , and HvMADS70 constitute a core hypoxia-responsive circuit with complementary expression dynamics. HvMADS13 responds to both waterlogging and salt stress, indicating pleiotropic functions in abiotic stress adaptation. HvMADS35 exhibits root-specific induction and is predicted to interact with expansins EXPA2 and EXPA7, potentially facilitating cell-wall remodeling during prolonged hypoxia. In contrast, HvMADS70 shows transient early induction followed by suppression after 10 days, reflecting a specialized role in initial stress perception ( Wang et al., 2023 ). Together, these findings establish MADS-box TFs as temporally programmed regulators that orchestrate waterlogging resilience through stage-specific functions. Their coordinated expression patterns provide a molecular framework for understanding how plants adapt to fluctuating oxygen environments and offer potential targets for improving crop tolerance to waterlogging stress through temporal modulation of hypoxia responses. MADS-box TFs in biotic stress Global agricultural productivity is severely constrained by biotic stressors, including fungal, bacterial, and viral pathogens, as well as insect infestations. Collectively, these agents cause widespread plant diseases, leading to annual crop yield losses of up to 40% and imposing a substantial economic burden estimated at approximately $220 billion ( FAO, 2019 ). To combat these multifaceted threats, plants deploy a combination of passive physical and chemical barriers and active recognition systems that trigger dynamic immune responses ( Zavaliev and Dong, 2024 ). Notably, the MADS-box TF family—long recognized for its central roles in developmental programming and adaptation to abiotic stress—has emerged as a central coordinator of biotic stress resilience. Accumulating evidence indicates that MADS-box TFs orchestrate transcriptional reprogramming essential for resistance to viruses, bacteria, and fungi, while also regulating biotic stress-induced senescence ( Zhang et al., 2024 ). This dual regulatory capacity highlights the intricate molecular strategies by which plants integrate defense signaling with physiological and developmental processes, thereby enhancing survival under sustained pathogen pressure. Taking on challenges from plant pathogens Plant pathogenic viruses, bacteria, fungi, and oomycetes pose serious threats to global ecosystems and agricultural production, endangering both biodiversity and food security ( Savary et al., 2019 ; Wu et al., 2024 ). To establish infection, these pathogens deploy effector proteins that manipulate host cellular processes. In response, plants activate a two-layered immune system: recognition of pathogen-associated molecular patterns (PAMPs) by cell-surface receptors initiates PAMP triggered immunity (PTI) ( Jones et al., 2024 ), whereas recognition of specific effectors by intracellular resistance proteins induces a potent effector-triggered immunity (ETI) response ( Ngou et al., 2021 ; Yuan et al., 2021 ; Islam et al., 2024 ). Both PTI and ETI are essential for mounting rapid and robust defenses that restrict pathogen proliferation ( Yuan et al., 2021 ; Chang et al., 2022 ). These immune responses are governed by intricate and interconnected signaling pathways ( Overmyer et al., 2018 ; Ding et al., 2022 ), with TFs serving as pivotal regulators that transmit immune signals, control defense gene expression, and coordinate crosstalk between pathways ( Amorim et al., 2017 ; Meraj et al., 2020 ). A comprehensive understanding of this complex regulatory network is therefore critical for developing durable disease-resistance strategies. In this context, the MADS-box TF family emerges as a central coordinator of transcriptional reprogramming in response to diverse pathogens, as discussed in the following sections focusing on viral, bacterial, and fungal infections ( Figure 6 ). Figure 6. Open in a new tab Regulatory responses mediated by MADS-box genes in plant defense against biotic stressors. (1) Bacteria. In plants, SOC1/AGL20 negatively influences age-related resistance (ARR) by inhibiting ICS1 expression and salicylic acid (SA) accumulation. SVP is essential for ARR, as it counteracts the detrimental effects of SOC1/AGL20 on SA levels. Elevated SA reduces the growth and biofilm formation of P. syringae pv. tomato in a dose-dependent manner. In Nicotiana benthamiana, silencing of NbMADS1 suppresses harpin Xoo -triggered hypersensitive response (HR); the NbMADS1–H 2 O 2 –NO pathway mediates multiple defense responses to harpin Xoo , including stomatal closure, cell death, and defense-related gene expression. In rice, downregulation of OsMADS26 enhances resistance and reduces susceptibility to the major pathogens, Magnaporthe oryzae ( M. oryzae) and Xanthomonas oryzae . (2) Fungi. PpMADS2 interacts with NPR1, forming a transcriptional complex that activates SA-dependent pathogenesis-related genes ( PR1 , PR2 , and PR5 ) as well as ABA-inducible genes ( ABI1 , RAB18 , and PpCalS) , thereby promoting callose accumulation. This regulatory module underlies β-aminobutyric acid (BABA)-induced resistance in harvested peach fruit. The MADS-box gene AY332478 is induced following M. oryzae inoculation and is associated with plant defense signaling during incompatible host–pathogen interactions. (3) Viruses. OsMADS23, OsMADS27a, and OsMADS57 form homo- and heterodimers that repress OsRDR1 expression, while simultaneously activating the OsRDR1-dependent antiviral RNA-silencing pathway. In tomato, S l MBP8 expression is strongly influenced by 1-aminocyclopropane-1-carboxylic acid and methyl jasmonate, indicating its potential involvement in plant adaptation to abiotic stress. Bacteria The control of bacterial diseases in plants remains a major challenge, largely due to the persistent lack of effective management strategies. Addressing this issue requires in-depth investigation of bacterial pathogenicity mechanisms and host defense regulation. MADS-box TFs have emerged as important regulators of plant resistance, coordinating multiple defense pathways ( Figure 6 ). In Arabidopsis , the MADS-domain TF SVP regulates age-related resistance, a defense mechanism activated during late vegetative and reproductive stages ( Kus et al., 2002 ; Whalen, 2005 ; Wilson et al., 2017 ). SVP functions by repressing SOC1 / AGL20 , which in turn suppresses the expression of ISOCHORISMATE SYNTHASE 1 ( ICS1 ), a key enzyme in salicylic acid (SA) biosynthesis ( Wildermuth et al., 2001 ; Li et al., 2008 ). Through this regulatory cascade, SVP promotes SA accumulation within plant cells, directly inhibiting the growth and biofilm formation of Pseudomonas syringae pv. tomato and limiting bacterial proliferation ( Wilson et al., 2017 ). Similarly, the MADS-box gene AGL8 is downregulated in pine following colonization by the endosymbiotic bacterium Methylorubrum extorquens ( Koskimäki et al., 2022 ), suggesting that modulation of specific MADS-box genes may represent a common strategy in diverse plant–microbe interactions. Beyond SA-mediated defenses, MADS-box TFs also participate in elicitor-triggered immunity. For example, the MIKC-type gene NbMADS1 plays a critical role in defense signaling activated by the bacterial elicitor harpin Xoo ( Xanthomonas oryzae pv. oryzae) in Nicotiana benthamiana ( Zou et al., 2006 ; Zhang et al., 2016 ; Ke et al., 2017 ). Silencing of NbMADS1 significantly impairs the hypersensitive response (HR) and reduces ROS accumulation by downregulating ROS-producing genes ( NbrbohA and NbrbohB ). In addition, NbMADS1 affects nitric oxide (NO) production by repressing the transcription of NbNOA1 and NbNR2 , leading to impaired downstream defense responses, including stomatal closure, HR-associated cell death, and the expression of defense-related genes ( Zhang et al., 2016 ). In rice, OsMADS26 is involved in modulating pathogen-resistance pathways ( Khong et al., 2015 ). Downregulation of OsMADS26 enhances tolerance to water deficit but renders plants more susceptible to pathogens such as Magnaporthe oryzae and X. oryzae . In contrast, overexpression of OsMADS26 suppresses the expression of key defense-related genes ( POX223 , CHI7 , PR5 , NH1/OsNPR1 , FLS2 , and WRKY28 ) both constitutively and after infection. Moreover, OsMADS26 overexpression upregulates RH1 , a negative regulator that suppresses NH1 / OsNPR1 , a central activator of defense gene expression and systemic acquired resistance, while concurrently downregulating WAK25 , a positive regulator of resistance to Xanthomonas ( Seo et al., 2011 ; Chern et al., 2012 ). This coordinated dysregulation of defense activators and repressors contributes to the increased pathogen susceptibility observed in OsMADS26 -overexpressing plants. Supporting their roles in defense complexes, CaAGL8 interacts with CaSWC4 in pepper, a positive regulator of defense against Ralstonia solanacearum . This complex is essential for HR cell death and the upregulation of defense-related genes. Reciprocal gene-silencing experiments show that loss of either partner abolishes these immune responses, highlighting their functional interdependence ( Zhang et al., 2023 ). Extending this pattern, infection by Paulownia witches’ broom phytoplasma induces the expression of PfMADS54 and PfMADS3 , suggesting that the upregulation of specific MADS-box genes may represent a conserved host response to bacterial invasion ( Fan et al., 2024 ). Despite the plant’s active defense strategies, bacterial pathogens can actively subvert this intricate defense network by targeting and destabilizing MADS-box TFs, thereby suppressing host immunity and promoting disease. Phytoplasmas, for example, secrete effector proteins such as SAP54, which hijack critical MADS-domain TFs to facilitate infection. SAP54 directly interacts with and mediates the degradation of key floral MADS-box proteins, including SEPALLATA3 and APETALA1, via the host RAD23 shuttle proteins and the proteasome system ( MacLean et al., 2014 ). This degradation leads to the conversion of flowers into leaf-like structures (phyllody), increasing the plant’s attractiveness to phytoplasma-transmitting leafhopper vectors and thereby enhancing pathogen spread ( MacLean et al., 2014 ). Similarly, SAP54 employs a ubiquitin-independent mechanism by bridging MADS-box TFs to RAD23 and directing them to the proteasome for degradation ( Kitazawa et al., 2022 ). The elimination of floral identity factors not only disrupts reproductive development but may also compromise defense-associated regulatory networks, ultimately facilitating pathogen transmission. Together, these findings illustrate the dual role of MADS-box proteins in plant–bacterial interactions, functioning as critical components of plant immunity while simultaneously representing vulnerable targets for microbial manipulation. Fungi MADS-box TFs integrate plant developmental programs with defense signaling against diverse fungal pathogens ( Figure 6 ). In peach, these TFs participate in resistance mechanisms against Rhizopus stolonifer , the causative agent of Rhizopus rot, a significant threat to global fruit production ( Fan and Tian, 2000 ). Pretreatment of peach fruits with β-aminobutyric acid (BABA) primes defense responses, characterized by hydrogen peroxide bursts, abscisic acid accumulation, and enhanced callose deposition. Callose acts as a physical barrier to pathogen penetration, and BABA-induced resistance is closely associated with the formation of callose-rich papillae beneath infection sites. This induced resistance depends on SA signaling, which is essential for defense against biotrophic pathogens ( Wang et al., 2021 ). Mechanistically, BABA-induced H 2 O 2 activates PpMAPK1, which phosphorylates the nuclear TF PpMADS2. Phosphorylated PpMADS2 interacts with the co-regulator PpNPR1, enhancing its DNA-binding activity and promoting transcription of SA-responsive pathogenesis-related genes ( PpPR1 , PpPR2 , and PpPR5 ), as well as the ABA-inducible callose synthase gene PpCalS . Functional analyses confirm PpMADS2 as a positive regulator of fungal resistance: its overexpression enhances PR expression and fungal resistance in Arabidopsis , whereas loss of function increases susceptibility. Together, these findings demonstrate that PpMADS2 orchestrates BABA-induced resistance through coordinated SA–NPR1 signaling and ABA-mediated callose deposition ( Li et al., 2022 ). Consistent with this regulatory role, MADS-box genes also contribute to immunity in other species. In tomato, the MADS-box TF RIN enhances ripening-associated resistance to the necrotrophic fungus Botrytis cinerea by upregulating pathogen-resistance genes (e.g., PR1a and PR-STH2 ), defense-related TFs (AP2/ERF family), and genes encoding defense enzymes such as phenylalanine ammonia-lyase and chitinase. Concurrently, RIN represses the expression of cell-wall-modifying enzyme genes, including XTH5 , XTH8 , and MAN4a , thereby reinforcing the cell wall and limiting fungal degradation and invasion ( Zheng et al., 2021 ). In sugarcane, infection by the smut fungus Sporisorium scitamineum alters floral development and is accompanied by changes in MADS-box gene expression, suggesting that these TFs participate in pathogen-induced morphological remodeling ( Shuai et al., 2023 ). In wheat, expression profiling analyses reveal that subsets of MADS-box genes are dynamically regulated in response to multiple fungal pathogens, including Fusarium graminearum , Zymoseptoria tritici , stripe rust, and powdery mildew. This coordinated yet differential regulation suggests that these genes participate in a shared defense-related regulatory network. Several responsive genes—such as TaMADS1 , TaMADS41 , TaMADS120 , and TaMADS135 , as well as TaMADS16 , TaMADS27 , TaMADS33 , TaMADS49 , TaMADS52 , TaMADS55 , TaMADS56 , TaMADS58 , TaMADS59 , and TaMADS72 —exhibit pathogen-specific expression patterns. For example, TaMADS19 is upregulated following Z. tritici infection, whereas TaMADS117 is downregulated in response to powdery mildew ( Ma et al., 2017 ). Highlighting their functional relevance in immunity, the wheat MADS-box protein TaMADS2 physically interacts with TaTBL21 to form a complex that transcriptionally activates TaGKL . This regulatory cascade promotes the accumulation of defense-related metabolites, including SA and glycerol-3-phosphate (G3P), thereby enhancing wheat resistance to stripe rust ( Zhao et al., 2025 ). MADS-box TFs also contribute to resistance against M. oryzae , the causal agent of rice blast disease. Transcriptomic analyses of Pi54 -mediated incompatible interactions reveal coordinated upregulation of defense-related genes, including those involved in callose biosynthesis and peroxidase activity, which are potentially regulated by MADS-box, bZIP, and WRKY TFs. Specific MADS-box genes, such as AY332478 , display differential expression upon M. oryzae inoculation, suggesting their active participation in modulating signaling pathways critical for blast resistance ( Gupta et al., 2012 ; Xiao et al., 2020 ). Collectively, these findings demonstrate the critical contribution of MADS-box TFs to plant immunity against fungal pathogens, underscoring their importance in coordinating defense-related signaling networks and physiological responses. Viruses As major pathogens, plant viruses account for nearly half of all plant disease-related issues, posing substantial threats to global food security and economic stability ( Nicaise, 2014 ; He and Creasey Krainer, 2020 ). Plant antiviral defenses predominantly rely on the RNA-silencing pathway, in which three ANR1-like genes have been shown to critically enhance rice resistance. MicroRNAs (miRNAs) are well-established regulators of plant immunity against diverse pathogens, including viruses, bacteria, and fungi ( Ruiz-Ferrer and Voinnet, 2009 ; Katiyar-Agarwal and Jin, 2010 ; Arne et al., 2014 ). Among these, rice miR444 has been implicated in responses to both bacterial and fungal infections ( Li et al., 2014 ). RNA silencing, mediated by core components such as RNA-Dependent RNA Polymerase 1 (RDR1), is essential for host defense against viral pathogens ( Ding and Voinnet, 2007 ; Pumplin and Voinnet, 2013 ; Li et al., 2021a ). Upon infection with rice stripe virus, the expression of miR444 increases, leading to enhanced antiviral resistance through the upregulation of the key silencing factor OsRDR1 ( Wang et al., 2016 ). Additionally, miR444 regulates the expression of several resistance ( R ) genes in rice by targeting MADS-box TFs such as OsMADS23, OsMADS27a, and OsMADS57. These TFs, which are capable of forming homo- and heterodimers, directly repress OsRDR1 expression by binding to CArG motifs in its promoter ( Aerts et al., 2018 ). Elevated miR444 levels counteract this inhibition, thereby activating the OsRDR1-dependent antiviral RNA-silencing pathway ( Wang et al., 2016 ; Aerts et al., 2018 ). Beyond this indirect regulatory role mediated by miRNAs, MADS-box TFs can also function as direct positive regulators of antiviral immunity. This is exemplified in soybean, where the MADS-box gene GmCAL acts as a positive regulator conferring broad-spectrum resistance to multiple strains of soybean mosaic virus, with its overexpression significantly reducing viral accumulation ( Ren et al., 2022 ). Although some MADS-box genes have been characterized for their roles in pathogen defense ( Figure 6 ), many others remain unexplored in this context. Notably, SlMBP8, previously shown to respond to abiotic stresses such as salinity and drought, positively regulates the pathogenesis-related genes PR1 and PR5 . Its transcription is influenced by key biotic stress-associated signaling molecules, including 1-aminocyclopropane-1-carboxylic acid and methyl jasmonate, suggesting that SlMBP8 integrates signals from both abiotic and biotic stresses and may therefore represent a promising candidate for pathogen defense ( Yin et al., 2017b ). Embracing senescence Senescence, the programmed terminal phase of development associated with aging, is an active and highly regulated process rather than a passive decline. In plants, this fundamental transition—spanning stages from leaf maturation to fruit abscission—is governed by complex hormonal networks. Among these, ethylene functions as a central promoter of plant senescence ( Khan et al., 2014 ). Overexpression of the MADS-box TF SlFYFL has been shown to delay senescence in both fruit sepals and whole plants by suppressing ethylene biosynthesis ( Xie et al., 2014 ) ( Supplemental Figure 3 ). Transgenic lines overexpressing SlFYFL maintain higher chlorophyll levels than wild-type plants, which exhibit early sepal yellowing and accelerated chlorophyll loss. This delayed senescence phenotype is associated with the downregulation of key ethylene biosynthesis genes ( ACS1A , ACS2 , ACS6 , and ACO1 ) as well as ripening-associated regulatory factors, including RIN , JOINTLESS ( JL ), and MADS-MC ( Tan et al., 1997 ; Xie et al., 2014 ). SlFYFL likely modulates ethylene production and ripening gene expression through interactions with factors such as the ethylene biosynthesis inhibitor SlMADS1 and the ripening promoter RIN. In addition, SlFYFL regulates abscission zone formation, potentially via known abscission regulators JL and MC ( Xie et al., 2014 ). The involvement of other MADS-box TFs, such as SlMBP8 , which is upregulated in senescent leaves ( Yin et al., 2017a ), further underscores the broader role of this TF family in senescence regulation. Collectively, SlFYFL functions as a central regulator within a complex network that coordinates tomato senescence and ripening, primarily by fine-tuning ethylene signaling. More broadly, MADS-box TFs coordinate stress adaptation through interconnected hormonal and transcriptional networks, enabling balanced and context-dependent responses to environmental challenges. These regulators fine-tune defense priorities by mediating strategic interactions among major hormone pathways while establishing cooperative relationships with diverse TF families. Under abiotic stress conditions, specific MADS factors exhibit remarkable regulatory versatility. For instance, OsMADS23 enhances osmotic adjustment through coordinated activation of ABA biosynthesis and proline accumulation pathways ( Li et al., 2021b ). In parallel, SVP contributes to water conservation by modulating key enzymes in ABA metabolism ( Wang et al., 2018 ; Allen et al., 2019 ), whereas AGL16 fine-tunes ionic balance through selective repression of stress-responsive transporters and TFs ( Zhao et al., 2021 ). During pathogen challenge, MADS proteins implement integrated defense strategies through hormone signaling coordination. Notably, PpMADS2 simultaneously activates SA-dependent defense genes and ABA-mediated structural barriers, thereby establishing a multilayered protection system ( Li et al., 2022 ). Similarly, SlMBP8 integrates ethylene and jasmonate signaling to optimize defense gene expression, illustrating the capacity of MADS-box TFs to process multiple biotic stress signals ( Yin et al., 2017b ). The regulatory capacity of MADS-box factors extends through both physical and functional interactions with other TF families. Evidence indicates that AGL16 coordinates drought responses through direct repression of heat shock and MYB TFs ( Zhao et al., 2020 ). Meanwhile, SOC1/AGL20 interacts with cold-responsive CBF regulators to modulate freezing tolerance ( Michaels and Amasino, 1999 ; Lee et al., 2000 ; Seo et al., 2009 ), and specific MADS-box variants form functional complexes with WRKY proteins to amplify immune signaling ( Gupta et al., 2012 ; Xiao et al., 2020 ). Concluding remarks and perspectives Plants are continuously exposed to diverse and often concurrent abiotic and biotic stresses, necessitating regulatory systems capable of integrating environmental cues with intrinsic developmental programs ( Figure 7 ). MADS-box TFs have emerged as pivotal components of such systems, operating at the interface between stress signaling and developmental regulation. Through gene duplication followed by subfunctionalization and neofunctionalization, distinct MADS-box subfamilies—most notably the AGL17 -like clade and the SVP clade—have partitioned ancestral developmental functions from newly acquired stress-responsive roles. This evolutionary diversification has generated subfamily-specific regulatory architectures that preserve conserved developmental cores while differentially elaborating stress-related functions ( Parenicová et al., 2003 ; Panchy et al., 2016 ). Figure 7. Open in a new tab Overview of MADS-box genes across various stress conditions. MADS-box family genes play important roles in multiple stress conditions, including heat stress, cold stress, nutrient stress, salt stress, and disease resistance. Crosstalk among these stress responses highlights the significant contributions of MADS-box genes to plant stress resistance. Consistent with this regulatory architecture, evidence synthesized at the subfamily level indicates that MADS-box TFs function predominantly as integrative hubs rather than as strictly stress-specific regulators, providing a mechanistic basis for the extensive crosstalk observed among multiple stress responses ( Supplemental Figure 4 ). Several MADS-box subfamilies participate concurrently in responses to diverse abiotic stresses—including drought, salinity, temperature extremes, waterlogging, heavy-metal toxicity, and nutrient fluctuations—as well as in pathogen defense, with the AGL17 -like clade representing a prominent multi-stress hub. For example, OsMADS23 links drought, salinity, and nutrient responses with pathogen-associated regulation ( Yu et al., 2014a ; Aerts et al., 2018 ; Li et al., 2021b ), whereas OsMADS57 promotes cold adaptation while negatively modulating pathogen responses ( Guo et al., 2013 ; Aerts et al., 2018 ). This functional antagonism suggests the existence of physiological trade-offs, in which common upstream signals—such as ROS/Ca 2+ waves and hormone reprogramming—are subsequently channeled into stimulus-specific signaling cascades that generate distinct transcriptional and adaptive outputs ( Gilroy et al., 2016 ).A similar integration logic is evident in the SVP and AGL12 subfamilies, which connect drought, waterlogging, and pathogen responses in a manner consistent with a convergent-input but divergent-output model. In this framework, shared signaling nodes are routed into discrete functional modules, including ABA-dominated regulation of osmotic and ionic homeostasis under drought and salinity; hypoxia- and ethylene-associated acclimation under waterlogging; and SA-, JA-, and ethylene-centered immune responses upon pathogen infection ( Lee et al., 2005 ; Wilson et al., 2017 ; Wang et al., 2018 ). SOC1 and FLC further couple temperature responsiveness with immunity and senescence, exemplified by the opposing regulatory roles of SOC1 / AGL20 under heat versus cold or pathogen challenge ( Lee et al., 2000 ; Li et al., 2008 ; Seo et al., 2009 ; Wang et al., 2019 ). The multi-process involvement of SlMBP8 likewise highlights that stress outcomes are shaped by both stress identity and developmental context ( Yin et al., 2017a ; 2017b ). A defining property that enables such integration is the capacity of MADS-box TFs to coordinate phytohormone crosstalk under stress conditions. During abiotic stress, ABA-inducible members such as OsMADS23 and SVP promote drought tolerance by regulating stomatal behavior, osmotic adjustment, and ABA biosynthesis. These outputs can be further fine-tuned by kinase-mediated phosphorylation, as exemplified by SAPK9-dependent regulation ( Wang et al., 2018 ; Li et al., 2021b ). In contrast, AGL16 negatively modulates salt tolerance by repressing ABA-related pathways and downstream stress-responsive genes ( Zhao et al., 2021 ). During biotic stress, JA- and SA-responsive MADS-box TFs, including GbMADS9 and PpMADS2, activate defense-related metabolic pathways and pathogenesis-related gene expression ( Yang et al., 2016 ; Li et al., 2022 ). Notably, PpMADS2 provides a clear example of multi-hormonal integration by linking BABA-induced SA–NPR1 signaling with ABA-dependent callose deposition ( Wang et al., 2021 ). Collectively, these observations indicate that paralogs within the same subfamily often converge on shared hormonal systems—such as ABA-centered stress responses—while diverging toward JA- or SA-dominated defense strategies. This facilitates context-specific decision-making when plants are exposed to multiple, overlapping stresses ( Supplemental Figure 5 ). Beyond hormonal regulation, MADS-box TFs are embedded within extensive cross-regulatory networks involving other TF families that refine stress-responsive gene expression programs. Regulation of TFs by other TFs represents a key mechanism for integrating stress inputs, as exemplified by AGL16-mediated repression of HsfA6a and MYB102 during drought and salinity responses ( Zhao et al., 2021 ), and by SOC1-mediated modulation of cold tolerance through regulation of CBF and COR ( Michaels and Amasino, 1999 ; Lee et al., 2000 ; Seo et al., 2009 ). In immune signaling, MADS-box TFs can regulate WRKY TF genes to engage downstream defense pathways ( Khong et al., 2015 ). In parallel, interactions with regulators of hormone metabolism and signaling further expand the regulatory reach of MADS-mediated networks. For example, AGL67 partners with SOMNUS to balance gibberellin and ABA signaling during thermoinhibition of germination ( Li et al., 2020 ). Importantly, SEP/AGL2- and AP1-related modules—including CaMADS, AP1–SEP3, and RIN-associated complexes—suggest that stress specificity is frequently shaped by the combinatorial composition of MADS-box complexes, enabling shared signaling inputs to be translated into subfamily- or member-specific target gene programs ( Tan et al., 1997 ; Xie et al., 2014 ). Mechanistically, MADS-box TFs integrate stress information across multiple regulatory layers. Evolutionary diversification of cis -regulatory elements enriches promoters with hormone- and stress-responsive features, conferring transcriptional sensitivity to environmental cues ( Smaczniak et al., 2012 ; Marand et al., 2023 ). Signal transmission to MADS-box proteins is mediated by hormone-dependent cascades, kinase signaling, and dynamic partner exchange, positioning these TFs as central signal transducers rather than primary sensors. Post-translational modifications—including phosphorylation, ubiquitination, and SUMOylation—further modulate protein stability, transcriptional activity, and interaction specificity, as exemplified by SAPK9-mediated phosphorylation of OsMADS23 ( Wang et al., 2018 ; Li et al., 2021b ). However, the extent to which epigenetic regulation and higher-order interactome organization contribute to the temporal and context-dependent modulation of MADS-box TF function remains poorly understood. This regulatory complexity is further compounded by pronounced spatiotemporal specificity, with distinct MADS-box factors operating in defined tissues, cell types, and developmental stages, thereby aligning stress responses with developmental status ( Supplemental Table 1 ). Despite their conserved roles in coordinating developmental transitions and stress responses, lineage-specific diversification has generated distinct MADS-box regulatory architectures across taxa ( Castelán-Muñoz et al., 2019 ; Zhang et al., 2024 ). Although several paralogs, including SOC1 , SVP , OsMADS23 , OsMADS26 , and GbMADS9 , have been identified as multi-stress integrators ( Figure 7 ), critical gaps remain in our understanding of how MADS-box TFs hierarchically resolve overlapping or antagonistic stress signals. In particular, it is unclear how post-translational modifications, epigenetic regulation, interactome dynamics, and spatiotemporal constraints collectively shape stress-specific transcriptional outcomes. Given the growing urgency to develop climate-resilient agricultural systems, comprehensive functional characterization of MADS-box genes in major crops and their wild progenitors is therefore imperative. In this context, integrating pan-genomic and comparative evolutionary frameworks with genome-editing technologies and artificial intelligence (AI)-assisted regulatory network modeling offers a powerful strategy for translating fundamental mechanistic insights into actionable crop-improvement applications ( Ansori et al., 2023 ). In conclusion, MADS-box TFs constitute an evolutionarily refined, multilayered regulatory framework that combines shared regulatory axes with stress-specific branching pathways, thereby equipping plants with the flexibility required to cope with complex and fluctuating environments. Elucidating the organizing principles underlying subfamily-level stress crosstalk, including hormone coordination, combinatorial complex assembly, and spatiotemporal deployment, will be central to advancing climate-resilient breeding strategies and sustaining agricultural productivity under global climate change. Future research directions Despite significant progress in characterizing the roles of MADS-box TFs in stress responses, critical knowledge gaps remain, necessitating innovative approaches to fully unlock their biotechnological potential. Key research frontiers are outlined below. Translational expansion and “bridge-species” validation How can the field overcome its heavy reliance on model plants to accelerate the development of climate-smart crops? Future studies should systematically compare the function, regulation, and network architecture of MADS-box orthologs across stress-resilient wild relatives—referred to as bridge species—and major crops. Such comparisons will facilitate the identification of lineage-specific innovations and superior allelic variants suitable for direct breeding applications. Achieving this goal will require overcoming technical barriers in genetic transformation and establishing high-throughput phenotyping platforms capable of assessing responses to complex environmental stresses in non-model crop systems. Mechanistic integration and signaling specificity How do individual MADS-box TFs dynamically interface with convergent abiotic and biotic stress-signaling pathways? Advanced spatiotemporal multi-omics approaches will be essential to delineate context-dependent interactions between MADS-box factors, core senescence regulators (e.g., ORE1), ethylene biosynthesis cascades (ACS/ACO), and cell-wall-remodeling components. These efforts will help elucidate the hierarchical organization of regulatory networks operating under combinatorial stress conditions. Network plasticity via multi-omics What principles govern the architecture and stress-induced rewiring of MADS-centered interactomes? Integrative epigenomic, metabolomic, and transcriptomic profiling—coupled with machine-learning-driven network inference—should be used to map condition-specific protein–DNA and protein–RNA complexes. These approaches will enable the identification of key regulatory hubs that orchestrate growth–defense trade-offs. Functional diversification vs. conservation To what extent does paralogous redundancy enable evolvable stress resilience, and how is this process regulated by post-translational mechanisms? Multiplexed mutagenesis, combined with comprehensive profiling of post-translational modifications (PTMs) such as phosphorylation and SUMOylation, could disentangle paralog-specific contributions to stress tolerance while minimizing confounding developmental pleiotropy. AI-driven trait integration in breeding How can AI-guided pangenome mining be leveraged to identify MADS-box haplotypes that confer multi-stress resilience without yield penalties, thereby enabling precision breeding of climate-adapted crops? Evolutionarily informed AI models should be developed to predict optimal allelic combinations across ecotypes. Candidate haplotypes can then be validated and engineered using prime editing or synthetic promoter strategies to decouple stress adaptation from developmental trade-offs in elite germplasm. Funding This study was supported by the National Key R&D Program of China (2023YFD1401500); the National Natural Science Foundation of China (32402330); the Project of the Henan Provincial Department of Education (22A180002); the Science and Technology Key Projects of Henan Province (242102111118); the Natural Science Foundation of Henan Province (242300421327); and the Research Start-up Fund for Top-notch Talents and Young Talents of Henan Agricultural University (30500924 and 30501347). Acknowledgments We are grateful to all members of our lab at Henan Agricultural University. No conflict of interest is declared. Author contributions N.L., W.M.Z., Z.Q.F., and X.W. conceived the manuscript. N.L., Z.H.L., and G.X.T. drafted the manuscript. N.L., Z.Q.F., D.W.W., X.W., S.J.Z., H.C., Y.H.H., Y.F.Z., K.C., and Y.Y.Z. revised the manuscript. All authors read and approved the final manuscript. Published: February 16, 2026 Footnotes Supplemental information is available at Plant Communications Online . Contributor Information Na Liu, Email: [email protected]. Wenming Zheng, Email: [email protected]. Zheng Qing Fu, Email: [email protected]. Xu Wang, Email: [email protected]. Supplemental information Document S1. Supplemental Figures 1–5 and Supplemental Table 1 mmc1.pdf (4.9MB, pdf) Document S2. Article plus supplemental information mmc2.pdf (17.6MB, pdf) References Aerts N., de Bruijn S., van Mourik H., Angenent G.C., van Dijk A.D.J. Comparative analysis of binding patterns of MADS-domain proteins in Arabidopsis thaliana. BMC Plant Biol. 2018;18:131. doi: 10.1186/s12870-018-1348-8. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Ahluwalia O., Singh P.C., Bhatia R. A review on drought stress in plants: Implications, mitigation and the role of plant growth promoting rhizobacteria. Res. Environ. Sustain. 2021;5 [ Google Scholar ] Alfatih A., Zhang J., Song Y., Jan S.U., Zhang Z.S., Xia J.Q., Zhang Z.Y., Nazish T., Wu J., Zhao P.X., Xiang C.B. Nitrate-responsive OsMADS27 promotes salt tolerance in rice. Plant Commun. 2023;4 doi: 10.1016/j.xplc.2022.100458. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Allen J., Guo K., Zhang D., Ince M., Jammes F. ABA-glucose ester hydrolyzing enzyme ATBG1 and PHYB antagonistically regulate stomatal development. PLoS One. 2019;14 doi: 10.1371/journal.pone.0218605. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Amorim L.L.B., da Fonseca Dos Santos R., Neto J.P.B., Guida-Santos M., Crovella S., Benko-Iseppon A.M. Transcription factors involved in plant resistance to pathogens. Curr. Protein Pept. Sci. 2017;18:335–351. doi: 10.2174/1389203717666160619185308. [ DOI ] [ PubMed ] [ Google Scholar ] Ansori A.N., Antonius Y., Susilo R.J., Hayaza S., Kharisma V.D., Parikesit A.A., Zainul R., Jakhmola V., Saklani T., Rebezov M., et al. Application of CRISPR-Cas9 genome editing technology in various fields: A review. Narrat. J. 2023;3 doi: 10.52225/narra.v3i2.184. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Arne W., Ming W., Marschal B., Jin H.L. Small RNAs: a new paradigm in plant-microbe interactions. Annu. Rev. Phytopathol. 2014;52:495–516. doi: 10.1146/annurev-phyto-102313-045933. [ DOI ] [ PubMed ] [ Google Scholar ] Arora R., Agarwal P., Ray S., Singh A.K., Singh V.P., Tyagi A.K., Kapoor S. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genom. 2007;8:242. doi: 10.1186/1471-2164-8-242. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Awad K.M., Salih A.M., Khalaf Y., Suhim A.A., Abass M.H. Phytotoxic and genotoxic effect of Aluminum to date palm (Phoenix dactylifera L.) in vitro cultures. J. Genet. Eng. Biotechnol. 2019;17:7. doi: 10.1186/s43141-019-0007-2. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Begcy K., Sandhu J., Walia H. Transient heat stress during early seed development primes germination and seedling establishment in rice. Front. Plant Sci. 2018;9:1768. doi: 10.3389/fpls.2018.01768. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Bhoite R., Onyemaobi O., Halder T., Shankar M., Sharma D. Transcription factors – Insights into abiotic and biotic stress resilience and crop improvement. Curr. Plant Biol. 2025;41 [ Google Scholar ] Cao H., Cui R., Guo H., Xia Q., Zhang J., Liu W., Yang Z.B. Ca2+-dependent cytoplasmic and nuclear phosphorylation of STOP1 by CPK21 and CPK23 confers ALMT1-dependent aluminum resistance. Nat. Commun. 2025;16:5225. doi: 10.1038/s41467-025-60426-9. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Castelán-Muñoz N., Herrera J., Cajero-Sánchez W., Arrizubieta M., Trejo C., García-Ponce B., Sánchez M.d.l.P., Álvarez-Buylla E.R., Garay-Arroyo A. MADS-Box genes are key components of genetic regulatory networks involved in abiotic stress and plastic developmental responses in plants. Front. Plant Sci. 2019;10:853. doi: 10.3389/fpls.2019.00853. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Chang M., Chen H., Liu F., Fu Z.Q. PTI and ETI: Convergent pathways with diverse elicitors. Trends Plant Sci. 2022;27:113–115. doi: 10.1016/j.tplants.2021.11.013. [ DOI ] [ PubMed ] [ Google Scholar ] Chen C., Begcy K., Liu K., Folsom J.J., Wang Z., Zhang C., Walia H. Heat stress yields a unique MADS box transcription factor in determining seed size and thermal sensitivity. Plant Physiol. 2016;171:606–622. doi: 10.1104/pp.15.01992. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Chen H., Xu N., Wu Q., Yu B., Chu Y., Li X., Huang J., Jin L. OsMADS27 regulates the root development in a NO3--Dependent manner and modulates the salt tolerance in rice (Oryza sativa L.) Plant Sci. 2018;277:20–32. doi: 10.1016/j.plantsci.2018.09.004. [ DOI ] [ PubMed ] [ Google Scholar ] Chen L., Zhao Y., Xu S., Zhang Z., Xu Y., Zhang J., Chong K. OsMADS57 together with OsTB1 coordinates transcription of its target OsWRKY94 and D14 to switch its organogenesis to defense for cold adaptation in rice. New Phytol. 2018;218:219–231. doi: 10.1111/nph.14977. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Chen R., Ma J., Luo D., Hou X., Ma F., Zhang Y., Meng Y., Zhang H., Guo W. CaMADS, a MADS-box transcription factor from pepper, plays an important role in the response to cold, salt, and osmotic stress. Plant Sci. 2019;280:164–174. doi: 10.1016/j.plantsci.2018.11.020. [ DOI ] [ PubMed ] [ Google Scholar ] Chern M., Bai W., Sze-To W.H., Canlas P.E., Bartley L.E., Ronald P.C. A rice transient assay system identifies a novel domain in NRR required for interaction with NH1/OsNPR1 and inhibition of NH1-mediated transcriptional activation. Plant Methods. 2012;8:6. doi: 10.1186/1746-4811-8-6. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Chiou T.J., Lin S.I. Signaling network in sensing phosphate availability in plants. Annu. Rev. Plant Biol. 2011;62:185–206. doi: 10.1146/annurev-arplant-042110-103849. [ DOI ] [ PubMed ] [ Google Scholar ] de Bang T.C., Husted S., Laursen K.H., Persson D.P., Schjoerring J.K. The molecular-physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants. New Phytol. 2021;229:2446–2469. doi: 10.1111/nph.17074. [ DOI ] [ PubMed ] [ Google Scholar ] de Folter S., Angenent G.C. Trans meets cis in MADS science. Trends Plant Sci. 2006;11:224–231. doi: 10.1016/j.tplants.2006.03.008. [ DOI ] [ PubMed ] [ Google Scholar ] de Folter S., Immink R.G.H., Kieffer M., Parenicová L., Henz S.R., Weigel D., Busscher M., Kooiker M., Colombo L., Kater M.M., et al. Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell. 2005;17:1424–1433. doi: 10.1105/tpc.105.031831. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Ding L.N., Li Y.T., Wu Y.Z., Li T., Geng R., Cao J., Zhang W., Tan X.L. Plant disease resistance-related signaling pathways: Recent progress and future prospects. Int. J. Mol. Sci. 2022;23 doi: 10.3390/ijms232416200. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Ding S.W., Voinnet O. Antiviral immunity directed by small RNAs. Cell. 2007;130:413–426. doi: 10.1016/j.cell.2007.07.039. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Du B., Haensch R., Alfarraj S., Rennenberg H. Strategies of plants to overcome abiotic and biotic stresses. Biol. Rev. Camb. Phil. Soc. 2024;99:1524–1536. doi: 10.1111/brv.13079. [ DOI ] [ PubMed ] [ Google Scholar ] Egea-Cortines M., Saedler H., Sommer H. Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J. 1999;18:5370–5379. doi: 10.1093/emboj/18.19.5370. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] FAO New standards to curb the global spread of plant pests and diseases. 2019. https://www.fao.org/news/story/en/item/1187738/icode/ Fan J., Deng M., Li B., Fan G. Genome-wide identification of the Paulownia fortunei Aux/IAA gene family and its response to witches' broom caused by Phytoplasma. Int. J. Mol. Sci. 2024;25:2260. doi: 10.3390/ijms25042260. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Fan Q., Tian S.P. Postharvest biological control of rhizopus rot of nectarine fruits by pichia membranefaciens. Plant Dis. 2000;84:1212–1216. doi: 10.1094/PDIS.2000.84.11.1212. [ DOI ] [ PubMed ] [ Google Scholar ] Gan Y., Bernreiter A., Filleur S., Abram B., Forde B.G. Overexpressing the ANR1 MADS-box gene in transgenic plants provides new insights into its role in the nitrate regulation of root development. Plant Cell Physiol. 2012;53:1003–1016. doi: 10.1093/pcp/pcs050. [ DOI ] [ PubMed ] [ Google Scholar ] Gan Y., Filleur S., Rahman A., Gotensparre S., Forde B.G. Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta. 2005;222:730–742. doi: 10.1007/s00425-005-0020-3. [ DOI ] [ PubMed ] [ Google Scholar ] Gramzow L., Theißen G. Phylogenomics of MADS-Box genes in plants - Two opposing life styles in one gene family. Biology. 2013;2:1150–1164. doi: 10.3390/biology2031150. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Guo S., Xu Y., Liu H., Mao Z., Zhang C., Ma Y., Zhang Q., Meng Z., Chong K. The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat. Commun. 2013;4:1566. doi: 10.1038/ncomms2542. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Guo X., Chen G., Cui B., Gao Q., Guo J.E., Li A., Zhang L., Hu Z. Solanum lycopersicum agamous-like MADS-box protein AGL15-like gene, SlMBP11, confers salt stress tolerance. Mol. Breed. 2016;36:125. [ Google Scholar ] Gupta S.K., Rai A.K., Kanwar S.S., Chand D., Singh N.K., Sharma T.R. The single functional blast resistance gene Pi54 activates a complex defence mechanism in rice. J. Exp. Bot. 2012;63:757–772. doi: 10.1093/jxb/err297. [ DOI ] [ PubMed ] [ Google Scholar ] Han J.P., Wan J.N., Guan Z.L., Xu H., Wang Q.F., Wan T. The origin, evolution and diversification of MADS-box transcription factors in green plants. Plant Commun. 2025;6 doi: 10.1016/j.xplc.2025.101462. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Han Y., Liu N., Li C., Wang S., Jia L., Zhang R., Li H., Tan J., Xue H., Zheng W. TaMADS2-3D, a MADS transcription factor gene, regulates phosphate starvation responses in plants. Crop J. 2022;10:243–253. [ Google Scholar ] He S., Creasey Krainer K.M. Pandemics of people and plants: Which is the greater threat to food security? Mol. Plant. 2020;13:933–934. doi: 10.1016/j.molp.2020.06.007. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Henschel K., Kofuji R., Hasebe M., Saedler H., Münster T., Theissen G. Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol. Biol. Evol. 2002;19:801–814. doi: 10.1093/oxfordjournals.molbev.a004137. [ DOI ] [ PubMed ] [ Google Scholar ] Hui L., Khan D., Khokhar A.A., You Z., Lv W., Usman B., Zaman Q.U., Wang H.F. Characterization of MADS-box gene family and its unique response to drought and nickel stresses with melatonin-mediated tolerance in dragon fruit (Selenicereus undatus L.) Plant Stress. 2024;12 [ Google Scholar ] Huo S., Li Y., Li R., Chen R., Xing H., Wang J., Zhao Y., Song X. Genome-wide analysis of the MADS-box gene family in Rhododendron hainanense Merr. and expression analysis under heat and waterlogging stresses. Ind. Crops Prod. 2021;172 [ Google Scholar ] Hussain S., Hussain S., Ali B., Ren X., Chen X., Li Q., Saqib M., Ahmad N. Recent progress in understanding salinity tolerance in plants: Story of Na+/K+ balance and beyond. Plant Physiol. Biochem. 2021;160:239–256. doi: 10.1016/j.plaphy.2021.01.029. [ DOI ] [ PubMed ] [ Google Scholar ] Islam F., Khan M.S.S., Chen H., Chen J. Utilizing effector-triggered immunity (ETI) as a robust priming agent to protect plants from pathogens. Stress Biol. 2024;4:51. doi: 10.1007/s44154-024-00204-7. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Jiang Z., van Zanten M., Sasidharan R. Mechanisms of plant acclimation to multiple abiotic stresses. Commun. Biol. 2025;8:655. doi: 10.1038/s42003-025-08077-w. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Jones J.D.G., Staskawicz B.J., Dangl J.L. The plant immune system: From discovery to deployment. Cell. 2024;187:2095–2116. doi: 10.1016/j.cell.2024.03.045. [ DOI ] [ PubMed ] [ Google Scholar ] Kambale R., Rajagopalan V., Ayyenar B., Muthurajan R. Allelic diversity analysis of OsMADS87, a MADS box transcription factor influencing seed size and thermo- sensitivity in rice. J. Pharm. Innov. 2021;10:2201–2203. [ Google Scholar ] Katiyar-Agarwal S., Jin H. Role of small RNAs in host-microbe interactions. Annu. Rev. Phytopathol. 2010;48:225–246. doi: 10.1146/annurev-phyto-073009-114457. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Kaufmann K., Melzer R., Theissen G. MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene. 2005;347:183–198. doi: 10.1016/j.gene.2004.12.014. [ DOI ] [ PubMed ] [ Google Scholar ] Ke Y., Deng H., Wang S. Advances in understanding broad-spectrum resistance to pathogens in rice. Plant J. 2017;90:738–748. doi: 10.1111/tpj.13438. [ DOI ] [ PubMed ] [ Google Scholar ] Khan M., Rozhon W., Poppenberger B. The role of hormones in the aging of plants - a mini-review. Gerontology. 2014;60:49–55. doi: 10.1159/000354334. [ DOI ] [ PubMed ] [ Google Scholar ] Khong G.N., Pati P.K., Richaud F., Parizot B., Bidzinski P., Mai C.D., Bès M., Bourrié I., Meynard D., Beeckman T., et al. OsMADS26 negatively regulates resistance to pathogens and drought tolerance in rice. Plant Physiol. 2015;169:2935–2949. doi: 10.1104/pp.15.01192. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Kitazawa Y., Iwabuchi N., Maejima K., Sasano M., Matsumoto O., Koinuma H., Tokuda R., Suzuki M., Oshima K., Namba S., Yamaji Y. A phytoplasma effector acts as a ubiquitin-like mediator between floral MADS-box proteins and proteasome shuttle proteins. Plant Cell. 2022;34:1709–1723. doi: 10.1093/plcell/koac062. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Kobayashi Y., Ohyama Y., Kobayashi Y., et al. STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in. Mol. Plant. 2014;7:311–322. doi: 10.1093/mp/sst116. [ DOI ] [ PubMed ] [ Google Scholar ] Koskimäki J.J., Pohjanen J., Kvist J., et al. The meristem-associated endosymbiont Methylorubrum extorquens DSM13060 reprograms development and stress responses of pine seedlings. Tree Physiol. 2022;42:391–410. doi: 10.1093/treephys/tpab102. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Krasnov G.S., Dmitriev A.A., Zyablitsin A.V., Rozhmina T.A., Zhuchenko A.A., Kezimana P., Snezhkina A.V., Fedorova M.S., Novakovskiy R.O., Pushkova E.N., et al. Aluminum responsive genes in Flax (Linum usitatissimum L.) BioMed Res. Int. 2019;2019 doi: 10.1155/2019/5023125. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Kumari P., Kumari R., Sharma B., Prasad S.K., Singh R.K. Abiotic stress response of field crops: Recent approach. Int. J. Curr. Microbiol. Appl. Sci. 2019;8:1761–1769. [ Google Scholar ] Kus J.V., Zaton K., Sarkar R., Cameron R.K. Age-related resistance in Arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. Plant Cell. 2002;14:479–490. doi: 10.1105/tpc.010481. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Lai X., Vega-Léon R., Hugouvieux V., Blanc-Mathieu R., van der Wal F., Jérémy L., Silva C.S., Agnès J., Muino J.M., Nanao M.H., et al. The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors. Nat. Commun. 2021;12:4760. doi: 10.1038/s41467-021-24978-w. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Lee B.H., Henderson D.A., Zhu J.K. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell. 2005;17:3155–3175. doi: 10.1105/tpc.105.035568. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Lee H., Suh S.S., Park E., Cho E., Ahn J.H., Kim S.G., Lee J.S., Kwon Y.M., Lee I. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 2000;14:2366–2376. doi: 10.1101/gad.813600. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Li C., Lei C., Wang K., Tan M., Xu F., Wang J., Zheng Y. MADS2 regulates priming defence in postharvest peach through combined salicylic acid and abscisic acid signaling. J. Exp. Bot. 2022;73:3787–3806. doi: 10.1093/jxb/erac099. [ DOI ] [ PubMed ] [ Google Scholar ] Li D., Liu C., Shen L., Wu Y., Chen H., Robertson M., Helliwell C.A., Ito T., Meyerowitz E., Yu H. A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell. 2008;15:110–120. doi: 10.1016/j.devcel.2008.05.002. [ DOI ] [ PubMed ] [ Google Scholar ] Li P., Zhang Q., He D., Zhou Y., Ni H., Tian D., Chang G., Jing Y., Lin R., Huang J., Hu X. AGAMOUS-LIKE67 cooperates with the histone mark reader EBS to modulate seed germination under high temperature. Plant Physiol. 2020;184:529–545. doi: 10.1104/pp.20.00056. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Li S., Zhang Z., Zhou C., Li S. RNA-dependent RNA polymerase 1 delays the accumulation of viroids in infected plants. Mol. Plant Pathol. 2021;22:1195–1208. doi: 10.1111/mpp.13104. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Li X., Yu B., Wu Q., Min Q., Zeng R., Xie Z., Huang J. OsMADS23 phosphorylated by SAPK9 confers drought and salt tolerance by regulating ABA biosynthesis in rice. PLoS Genet. 2021;17 doi: 10.1371/journal.pgen.1009699. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Li Y., Lu Y.G., Shi Y., Wu L., Xu Y.J., Huang F., Guo X.Y., Zhang Y., Fan J., Zhao J.Q., et al. Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiol. 2014;164:1077–1092. doi: 10.1104/pp.113.230052. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Li Y.F., Zheng Y., Addo-Quaye C., Zhang L., Saini A., Jagadeeswaran G., Axtell M.J., Zhang W., Sunkar R. Transcriptome-wide identification of microRNA targets in rice. Plant J. 2010;62:742–759. doi: 10.1111/j.1365-313X.2010.04187.x. [ DOI ] [ PubMed ] [ Google Scholar ] Lozano R., Angosto T., Gomez P., Payan C., Capel J., Huijser P., Salinas J., Martinez-Zapater J.M. Tomato flower abnormalities induced by low temperatures are associated with changes of expression of MADS-Box genes. Plant Physiol. 1998;117:91–100. doi: 10.1104/pp.117.1.91. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Lu C., Jeong D.H., Kulkarni K., Pillay M., Nobuta K., German R., Thatcher S.R., Maher C., Zhang L., Ware D., et al. Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs) Proc. Natl. Acad. Sci. USA. 2008;105:4951–4956. doi: 10.1073/pnas.0708743105. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Ma J., Yang Y., Luo W., Yang C., Ding P., Liu Y., Qiao L., Chang Z., Geng H., Wang P., et al. Genome-wide identification and analysis of the MADS-box gene family in bread wheat (Triticum aestivum L.) PLoS One. 2017;12 doi: 10.1371/journal.pone.0181443. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] MacLean A.M., Orlovskis Z., Kowitwanich K., Zdziarska A.M., Angenent G.C., Immink R.G.H., Hogenhout S.A. Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. PLoS Biol. 2014;12 doi: 10.1371/journal.pbio.1001835. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Marand A.P., Eveland A.L., Kaufmann K., Springer N.M. cis-Regulatory Elements in Plant Development, Adaptation, and Evolution. Annu. Rev. Plant Biol. 2023;74:111–137. doi: 10.1146/annurev-arplant-070122-030236. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Martinez-Castilla L.P., Alvarez-Buylla E.R. Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny. Proc. Natl. Acad. Sci. USA. 2003;100:13407–13412. doi: 10.1073/pnas.1835864100. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Meraj T.A., Fu J., Raza M.A., Zhu C., Shen Q., Xu D., Wang Q. Transcriptional factors regulate plant stress responses through mediating secondary metabolism. Genes. 2020;11:346. doi: 10.3390/genes11040346. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Michaels S.D., Amasino R.M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell. 1999;11:949–956. doi: 10.1105/tpc.11.5.949. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Minakuchi K., Kameoka H., Yasuno N., Umehara M., Luo L., Kobayashi K., Hanada A., Ueno K., Asami T., Yamaguchi S., Kyozuka J. FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol. 2010;51:1127–1135. doi: 10.1093/pcp/pcq083. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Mthiyane P., Aycan M., Mitsui T. Strategic advancements in rice cultivation: Combating heat dtress through genetic innovation and sustainable practices — A Review. Stresses. 2024;4:452–480. [ Google Scholar ] Müller F., Xu J., Kristensen L., Wolters-Arts M., de Groot P.F.M., Jansma S.Y., Mariani C., Park S., Rieu I. High-temperature-induced defects in Tomato (Solanum lycopersicum) anther and pollen development are associated with reduced expression of B-Class floral patterning genes. PLoS One. 2016;11 doi: 10.1371/journal.pone.0167614. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Nam J., de Pamphilis C.W., Ma H., Nei M. Antiquity and evolution of the MADS-box gene family controlling flower development in plants. Mol. Biol. Evol. 2003;20:1435–1447. doi: 10.1093/molbev/msg152. [ DOI ] [ PubMed ] [ Google Scholar ] Narayan O.P., Kumar P., Yadav B., Dua M., Johri A.K. Sulfur nutrition and its role in plant growth and development. Plant Signal. Behav. 2023;18 doi: 10.1080/15592324.2022.2030082. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Ngou B.P.M., Ahn H.K., Ding P., Jones J.D.G. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature. 2021;592:110–115. doi: 10.1038/s41586-021-03315-7. [ DOI ] [ PubMed ] [ Google Scholar ] Nicaise V. Crop immunity against viruses: outcomes and future challenges. Front. Plant Sci. 2014;5:660. doi: 10.3389/fpls.2014.00660. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Overmyer K., Vuorinen K., Brosché M. Interaction points in plant stress signaling pathways. Physiol. Plant. 2018;162:191–204. doi: 10.1111/ppl.12639. [ DOI ] [ PubMed ] [ Google Scholar ] Pachamuthu K., Hari Sundar V., Narjala A., Singh R.R., Das S., Avik Pal H.C.Y., Shivaprasad P.V. Nitrate-dependent regulation of miR444-OsMADS27 signalling cascade controls root development in rice. J. Exp. Bot. 2022;73:3511–3530. doi: 10.1093/jxb/erac083. [ DOI ] [ PubMed ] [ Google Scholar ] Panchy N., Lehti-Shiu M., Shiu S.H. Evolution of gene duplication in plants. Plant Physiol. 2016;171:2294–2316. doi: 10.1104/pp.16.00523. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Parenicová L., de Folter S., Kieffer M., Horner D.S., Favalli C., Busscher J., Cook H.E., Ingram R.M., Kater M.M., Davies B., et al. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell. 2003;15:1538–1551. doi: 10.1105/tpc.011544. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Peng S., Huang J., Sheehy J.E., Laza R.C., Visperas R.M., Zhong X., Centeno G.S., Khush G.S., Cassman K.G. Rice yields decline with higher night temperature from global warming. Proc. Natl. Acad. Sci. USA. 2004;101:9971–9975. doi: 10.1073/pnas.0403720101. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Postma J.A., Dathe A., Lynch J.P. The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiol. 2014;166:590–602. doi: 10.1104/pp.113.233916. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Pumplin N., Voinnet O. RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat. Rev. Microbiol. 2013;11:745–760. doi: 10.1038/nrmicro3120. [ DOI ] [ PubMed ] [ Google Scholar ] Qiu Y., Köhler C. Endosperm evolution by duplicated and neofunctionalized Type I MADS-Box transcription factors. Mol. Biol. Evol. 2022;39 doi: 10.1093/molbev/msab355. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Qiu Y., Li Z., Köhler C. Ancestral duplication of MADS-box genes in land plants empowered the functional divergence between sporophytes and gametophytes. New Phytol. 2024;244:358–363. doi: 10.1111/nph.20065. [ DOI ] [ PubMed ] [ Google Scholar ] Qiu Y., Li Z., Walther D., Köhler C. Updated phylogeny and protein structure predictions revise the hypothesis on the origin of MADS-box transcription factors in land plants. Mol. Biol. Evol. 2023;40 doi: 10.1093/molbev/msad194. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Ren Q., Jiang H., Xiang W., Nie Y., Xue S., Zhi H., Li K., Gai J. A MADS-box gene is involved in soybean resistance to multiple Soybean mosaic virus strains. Crop J. 2022;10:802–808. [ Google Scholar ] Ruiz-Ferrer V., Voinnet O. Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 2009;60:485–510. doi: 10.1146/annurev.arplant.043008.092111. [ DOI ] [ PubMed ] [ Google Scholar ] Ryan P.R., Yang J. Sensing the toxic aluminum cations in acidic soils. Cell Res. 2024;34:269–270. doi: 10.1038/s41422-024-00935-2. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Savary S., Willocquet L., Pethybridge S.J., Esker P., McRoberts N., Nelson A. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 2019;3:430–439. doi: 10.1038/s41559-018-0793-y. [ DOI ] [ PubMed ] [ Google Scholar ] Schilling S., Kennedy A., Pan S., Jermiin L.S., Melzer R. Genome-wide analysis of MIKC-type MADS-box genes in wheat: pervasive duplications, functional conservation and putative neofunctionalization. New Phytol. 2020;225:511–529. doi: 10.1111/nph.16122. [ DOI ] [ PubMed ] [ Google Scholar ] Seo E., Lee H., Jeon J., Park H., Kim J., Noh Y.S., Lee I. Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell. 2009;21:3185–3197. doi: 10.1105/tpc.108.063883. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Seo Y.S., Chern M., Bartley L.E., Han M., Jung K.H., Lee I., Walia H., Richter T., Xu X., Cao P., et al. Towards establishment of a rice stress response interactome. PLoS Genet. 2011;7 doi: 10.1371/journal.pgen.1002020. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Shetty R., Vidya C.S.N., Prakash N.B., Lux A., Vaculík M. Aluminum toxicity in plants and its possible mitigation in acid soils by biochar: A review. Sci. Total Environ. 2021;765 doi: 10.1016/j.scitotenv.2020.142744. [ DOI ] [ PubMed ] [ Google Scholar ] Shi S.Y., Zhang F.F., Gao S., Xiao K. Expression pattern and function analyses of the MADS thranscription factor genes in wheat (Triticum aestivum L.) under phosphorus-starvation condition. J. Integr. Agric. 2016;15:1703–1715. [ Google Scholar ] Shore P., Sharrocks A.D. The MADS-box family of transcription factors. Eur. J. Biochem. 1995;229:1–13. doi: 10.1111/j.1432-1033.1995.tb20430.x. [ DOI ] [ PubMed ] [ Google Scholar ] Shuai L., Huang H., Liao L., Duan Z., Zhang X., Wang Z., Lei J., Huang W., Chen X., Huang D., et al. Variety-Specific flowering of sugarcane induced by the smut fungus Sporisorium scitamineum. Plants. 2023;12:316. doi: 10.3390/plants12020316. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Gilroy S., Białasek M., Suzuki N., Górecka M., Devireddy A.R., Karpiński S., Mittler R. ROS, calcium, and electric Signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 2016;171:1606–1615. doi: 10.1104/pp.16.00434. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Smaczniak C., Immink R.G.H., Angenent G.C., Kaufmann K. Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development. 2012;139:3081–3098. doi: 10.1242/dev.074674. [ DOI ] [ PubMed ] [ Google Scholar ] Stone S.L., Williams L.A., Farmer L.M., Vierstra R.D., Callis J. KEEP ON GOING, a RING E3 Ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell. 2006;18:3415–3428. doi: 10.1105/tpc.106.046532. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Sunkar R., Girke T., Jain P.K., Zhu J.K. Cloning and characterization of microRNAs from rice. Plant Cell. 2005;17:1397–1411. doi: 10.1105/tpc.105.031682. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Tan B.C., Schwartz S.H., Zeevaart J.A., McCarty D.R. Genetic control of abscisic acid biosynthesis in maize. Proc. Natl. Acad. Sci. USA. 1997;94:12235–12240. doi: 10.1073/pnas.94.22.12235. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Tapia-López R., García-Ponce B., Dubrovsky J.G., Garay-Arroyo A., Pérez-Ruíz R.V., Kim S.H., Acevedo F., Pelaz S., Alvarez-Buylla E.R. An AGAMOUS-related MADS-box gene, XAL1 (AGL12), regulates root meristem cell proliferation and flowering transition in Arabidopsis. Plant Physiol. 2008;146:1182–1192. doi: 10.1104/pp.107.108647. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Teixeira E.I., Fischer G., van Velthuizen H., Walter C., Ewert F. Global hot-spots of heat stress on agricultural crops due to climate change. Agric. For. Meteorol. 2013;170:206–215. [ Google Scholar ] Theissen G., Becker A., Di Rosa A., Kanno A., Kim J.T., Münster T., Winter K.U., Saedler H. A short history of MADS-box genes in plants. Plant Mol. Biol. 2000;42:115–149. [ PubMed ] [ Google Scholar ] Theissen G., Kim J.T., Saedler H. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol. 1996;43:484–516. doi: 10.1007/BF02337521. [ DOI ] [ PubMed ] [ Google Scholar ] Wang B., Cheng X.G. Physiological responses and regulatory pathways of transcription factors in plants under drought, high-salt, and low temperature stresses. J. Plant Nutr. 2017;23:1565–1574. [ Google Scholar ] Wang F., Zhou Z., Zhu L., Gu Y., Guo B., Lv C., Zhu J., Xu R. Genome-wide analysis of the MADS-box gene family involved in salt and waterlogging tolerance in barley (Hordeum vulgare L.) Front. Plant Sci. 2023;14 doi: 10.3389/fpls.2023.1178065. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Wang H., Jiao X., Kong X., Hamera S., Wu Y., Chen X., Fang R., Yan Y. A signaling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol. 2016;170:2365–2377. doi: 10.1104/pp.15.01283. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Wang M., Zheng Q., Shen Q., Guo S. The critical role of potassium in plant stress response. Int. J. Mol. Sci. 2013;14:7370–7390. doi: 10.3390/ijms14047370. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Wang T., Wang F., Deng S., Wang K., Feng D., Xu F., Guo W., Yu J., Wu Y., Wuriyanghan H., et al. Single-cell transcriptomes reveal spatiotemporal heat stress response in maize roots. Nat. Commun. 2025;16:177. doi: 10.1038/s41467-024-55485-3. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Wang Y., Li X., Fan B., Zhu C., Chen Z. Regulation and function of defense-related callose deposition in plants. Int. J. Mol. Sci. 2021;22:2393. doi: 10.3390/ijms22052393. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Wang Z., Shen Y., Yang X., Pan Q., Ma G., Bao M., Zheng B., Duanmu D., Lin R., Larkin R.M., Ning G. Overexpression of particular MADS-box transcription factors in heat-stressed plants induces chloroplast biogenesis in petals. Plant Cell Environ. 2019;42:1545–1560. doi: 10.1111/pce.13472. [ DOI ] [ PubMed ] [ Google Scholar ] Wang Z., Wang F., Hong Y., et al. The flowering repressor SVP confers drought resistance in Arabidopsis by regulating abscisic acid catabolism. Mol. Plant. 2018;11:1184–1197. [ Google Scholar ] Whalen M.C. Host defence in a developmental context. Mol. Plant Pathol. 2005;6:347–360. doi: 10.1111/j.1364-3703.2005.00286.x. [ DOI ] [ PubMed ] [ Google Scholar ] Wildermuth M.C., Dewdney J., Wu G., Ausubel F.M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature. 2001;414:562–565. doi: 10.1038/35107108. [ DOI ] [ PubMed ] [ Google Scholar ] Wilson D.C., Kempthorne C.J., Carella P., Liscombe D.K., Cameron R.K. Age-Related resistance in Arabidopsis thaliana involves the MADS-domain transcription factor SHORT VEGETATIVE PHASE and direct action of salicylic acid on pseudomonas syringae. Mol. Plant Microbe Interact. 2017;30:919–929. doi: 10.1094/MPMI-07-17-0172-R. [ DOI ] [ PubMed ] [ Google Scholar ] Wu J., Zhang Y., Li F., Zhang X., Ye J., Wei T., Li Z., Tao X., Cui F., Wang X., et al. Plant virology in the 21st century in China: Recent advances and future directions. J. Integr. Plant Biol. 2024;66:579–622. doi: 10.1111/jipb.13580. [ DOI ] [ PubMed ] [ Google Scholar ] Wu L., Zhang Q., Zhou H., Ni F., Wu X., Qi Y. Rice microRNA effector complexes and targets. Plant Cell. 2009;21:3421–3435. doi: 10.1105/tpc.109.070938. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Xiao N., Wu Y.Y., Li A.H. Strategy for use of rice blast resistance genes in rice molecular breeding. Rice Sci. 2020;27:263–277. [ Google Scholar ] Xie Q., Hu Z., Zhu Z., Dong T., Zhao Z., Cui B., Chen G. Overexpression of a novel MADS-box gene SlFYFL delays senescence, fruit ripening and abscission in tomato. Sci. Rep. 2014;4:4367. doi: 10.1038/srep04367. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Xu N., Chu Y., Chen H., Li X., Wu Q., Jin L., Wang G., Huang J. Rice transcription factor OsMADS25 modulates root growth and confers salinity tolerance via the ABA-mediated regulatory pathway and ROS scavenging. PLoS Genet. 2018;14 doi: 10.1371/journal.pgen.1007662. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Yan L.Y., Zhang H.J., Zheng Y.Q., Cong Y.Q., Liu C.T., Fan F., Zheng C., Yuan G.L., Pan G., Yuan D.Y., Duan M.J. Transcription factor OsMADS25 improves rice tolerance to cold stress. Yi Chuan. 2021;43:1078–1087. doi: 10.16288/j.yczz.21-217. [ DOI ] [ PubMed ] [ Google Scholar ] Yang F., Xu F., Wang X., Liao Y., Chen Q., Meng X. Characterization and functional analysis of a MADS-box transcription factor gene (GbMADS9) from Ginkgo biloba. Sci. Hortic. 2016;212:104–114. [ Google Scholar ] Yin W., Hu Z., Cui B., Guo X., Hu J., Zhu Z., Chen G. Suppression of the MADS-box gene SlMBP8 accelerates fruit ripening of tomato (Solanum lycopersicum) Plant Physiol. Biochem. 2017;118:235–244. doi: 10.1016/j.plaphy.2017.06.019. [ DOI ] [ PubMed ] [ Google Scholar ] Yin W., Hu Z., Hu J., Zhu Z., Yu X., Cui B., Chen G. Tomato (Solanum lycopersicum) MADS-box transcription factor SlMBP8 regulates drought, salt tolerance and stress-related genes. Plant Growth Regul. 2017;83:55–68. [ Google Scholar ] Yu C., Su S., Xu Y., Zhao Y., Yan A., Huang L., Ali I., Gan Y. The effects of fluctuations in the nutrient supply on the expression of five members of the AGL17 clade of MADS-Box genes in rice. PLoS One. 2014;9 doi: 10.1371/journal.pone.0105597. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Yu L.H., Miao Z.Q., Qi G.F., Wu J., Cai X.T., Mao J.L., Xiang C.B. MADS-Box transcription factor AGL21 regulates lateral root development and responds to multiple external and physiological signals. Mol. Plant. 2014;7:1653–1669. doi: 10.1093/mp/ssu088. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Yuan M., Jiang Z., Bi G., Nomura K., Liu M., Wang Y., Cai B., Zhou J.M., He S.Y., Xin X.F. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature. 2021;592:105–109. doi: 10.1038/s41586-021-03316-6. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Zahra N., Hafeez M.B., Ghaffar A., Kausar A., Zeidi M.A., Siddique K.H.M., Farooq M. Plant photosynthesis under heat stress: Effects and management. Environ. Exp. Bot. 2023;206 [ Google Scholar ] Zavaliev R., Dong X. NPR1, a key immune regulator for plant survival under biotic and abiotic stresses. Mol. Cell. 2024;84:131–141. doi: 10.1016/j.molcel.2023.11.018. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Zhang H., Teng W., Liang J., Liu X., Zhang H., Zhang Z., Zheng X. MADS1, a novel MADS-box protein, is involved in the response of Nicotiana benthamiana to bacterial harpinXoo. J. Exp. Bot. 2016;67:131–141. doi: 10.1093/jxb/erv448. [ DOI ] [ PubMed ] [ Google Scholar ] Zhang J., Martijn v.Z., Rashmi S. Mechanisms of plant acclimation to multiple abiotic stresses. Commun. Biol. 2025;8:655. doi: 10.1038/s42003-025-08077-w. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Zhang J., Jia W., Yang J., Ismail A.M. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res. 2006;97:111–119. [ Google Scholar ] Zhang X., Li L., Yang C., Cheng Y., Han Z., Cai Z., Nian H., Ma Q. GsMAS1 encoding a MADS-box transcription factor enhances the tolerance to aluminum stress in Arabidopsis thaliana. Int. J. Mol. Sci. 2020;21:2004. doi: 10.3390/ijms21062004. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Zhang Y., Cai W., Wang A., Huang X., Zheng X., Liu Q., Cheng X., Wan M., Lv J., Guan D., et al. MADS-box protein AGL8 interacts with chromatin-remodelling component SWC4 to activate thermotolerance and environment-dependent immunity in pepper. J. Exp. Bot. 2023;74:3667–3683. doi: 10.1093/jxb/erad092. [ DOI ] [ PubMed ] [ Google Scholar ] Zhang Y., Zhang J., Guo J., Zhou F., Singh S., Xu X., Xie Q., Yang Z., Huang C.F. F-box protein RAE1 regulates the stability of the aluminum-resistance transcription factor STOP1 in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2019;116:319–327. doi: 10.1073/pnas.1814426116. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Zhang Z., Zou W., Lin P., Wang Z., Chen Y., Yang X., Zhao W., Zhang Y., Wang D., Que Y., Wu Q. Evolution and function of MADS-Box transcription factors in plants. Int. J. Mol. Sci. 2024;25 doi: 10.3390/ijms252413278. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Zhao P.X., Miao Z.Q., Zhang J., Chen S.Y., Liu Q.Q., Xiang C.B. Arabidopsis MADS-box factor AGL16 negatively regulates drought resistance via stomatal density and stomatal movement. J. Exp. Bot. 2020;71:6092–6106. doi: 10.1093/jxb/eraa303. [ DOI ] [ PubMed ] [ Google Scholar ] Zhao P.X., Zhang J., Chen S.Y., Wu J., Xia J.Q., Sun L.Q., Ma S.S., Xiang C.B. Arabidopsis MADS-box factor AGL16 is a negative regulator of plant response to salt stress by downregulating salt-responsive genes. New Phytol. 2021;232:2418–2439. doi: 10.1111/nph.17760. [ DOI ] [ PubMed ] [ Google Scholar ] Zhao S., Chu H., Lu Y., Chen J., Wang X., Tian G., Zhang M., Song P., Zhang Y., Bai G., et al. The TaMADS2-TaTBL21 module enhances wheat resistance to stripe rust by activating TaGKL-mediated immunity. Plant Biotechnol. J. 2025 doi: 10.1111/pbi.70476. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Zheng H., Jin R., Liu Z., Sun C., Shi Y., Grierson D., Zhu C., Li S., Ferguson I., Chen K. Role of the tomato fruit ripening regulator MADS-RIN in resistance to Botrytis cinerea infection. Food Qual. Saf. 2021;5 [ Google Scholar ] Zou L.F., Wang X.P., Xiang Y., Zhang B., Li Y.R., Xiao Y.L., Wang J.S., Walmsley A.R., Chen G.Y. Elucidation of the hrp clusters of Xanthomonas oryzae pv. oryzicola that control the hypersensitive response in nonhost tobacco and pathogenicity in susceptible host rice. Appl. Environ. Microbiol. 2006;72:6212–6224. doi: 10.1128/AEM.00511-06. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ] Zuo D., Hu M., Zhou W., Lei F., Zhao J., Gu L. EcAGL enhances cadmium tolerance in transgenic Arabidopsis thaliana through inhibits cadmium transport and ethylene synthesis pathway. Plant Physiol. Biochem. 2023;201 doi: 10.1016/j.plaphy.2023.107900. [ DOI ] [ PubMed ] [ Google Scholar ] Associated Data This section collects any data citations, data availability statements, or supplementary materials included in this article. Supplementary Materials Document S1. Supplemental Figures 1–5 and Supplemental Table 1 mmc1.pdf (4.9MB, pdf) Document S2. Article plus supplemental information mmc2.pdf (17.6MB, pdf) Articles from Plant Communications are provided here courtesy of Elsevier ACTIONS View on publisher site PDF (5.5 MB) Cite Collections Permalink PERMALINK Copy RESOURCES Similar articles Cited by other articles Links to NCBI Databases Cite Copy Download .nbib .nbib Format: AMA APA MLA NLM Add to Collections Create a new collection Add to an existing collection Name your collection * Choose a collection Unable to load your collection due to an error Please try again Add Cancel Follow NCBI NCBI on X (formerly known as Twitter) NCBI on Facebook NCBI on LinkedIn NCBI on GitHub NCBI RSS feed Connect with NLM NLM on X (formerly known as Twitter) NLM on Facebook NLM on YouTube National Library of Medicine 8600 Rockville Pike Bethesda, MD 20894 Web Policies FOIA HHS Vulnerability Disclosure Help Accessibility Careers NLM NIH HHS USA.gov Back to Top

Related documents

• Force-Induced Control of Circularly Polarized Luminescence With Rotaxane Architecture.#1054380
• Dental school caries and periodontitis risk analysis skillset: survey of carryover to practice.#1054381
• Maternal and child health challenges during and after flooding: a qualitative study in Makassar, Indonesia.#1054382
• Genetic diversity of Camelina sativa: implications for sustainable crop improvement through Genotyping-by-Sequencing (GBS).#1054383
• 'Poverty is the biggest barrier': stakeholder perspectives on social determinants of malaria in Wakiso District, Uganda.#1054384