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Review

Research Progress on the Regulation of Plant Floral Organ Development by the MADS-box Gene Family

by
Qiufei Wu
1,2,
Yi Wu
2,
Rui Li
1,2,
Hongxing Cao
1,2,
Zongming Li
1,2,
Qihong Li
1,2 and
Lixia Zhou
1,2,*
1
State Key Laboratory of Tropical Crop Breeding, Chinese Academy of Tropical Agricultural Sciences, Sanya 572024, China
2
Coconut Research Institute, Chinese Academy of Tropical Agricultural Sciences, Wenchang 571339, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2025, 26(18), 8946; https://doi.org/10.3390/ijms26188946
Submission received: 8 August 2025 / Revised: 2 September 2025 / Accepted: 4 September 2025 / Published: 14 September 2025
(This article belongs to the Section Molecular Biology)
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Abstract

The initiation, development, and morphological construction of floral organs constitute a highly intricate process, involving numerous factors and their interactions. MADS-box genes are key regulators of developmental processes and are consequently the most extensively studied gene family in floral organ research. By synthesizing current understanding of the regulatory roles of MADS-box genes in the initiation, differentiation, and morphogenesis of floral organ, this review provides novel insights into the floral development program and the general transcriptional regulatory mechanisms of this gene family. It also offers a reference for further in-depth exploration of this gene family and the refinement of theories governing floral development regulation.

1. Introduction

Floral organs are essential for the reproduction in angiosperms and represent one of the most morphologically diverse organ systems in plants. In response to varying in growth environments and reproductive strategies, these organs have evolved into a wide array of forms that enhance reproductive success. While some plants, such as those in the Orchidaceae family and Snapdragons, exhibit highly specialized and unique floral morphologies, the majority of angiosperms possess a typical four-whorled structure, consisting from the outside inward of sepals, petals, stamens, and carpels. Floral organs serve as vital indicators for studying plant evolution and classification and have consistently been a focal point of research. Since the cloning of the first MADS-box gene associated with floral development from the model plant Arabidopsis thaliana, studies on the regulation of floral development and related genes have advanced significantly. Molecular-level research has revealed that the initiation, differentiation, and formation of floral organs are governed by a coordinated mechanism involving the transcriptional regulation and interaction of various genes, within which the MADS-box gene family plays a pivotal regulatory role [1].
MADS-box genes encode transcription factors that are ubiquitously present in all eukaryotes [2], influencing the morphogenesis and growth of various plant organs, such as roots and fruits [3,4]. The in-depth study of MADS-box genes has been propelled by their crucial functions in floral organs. The term “MADS” is derived from the initial letters of four genes: Minichromosome maintenance gene (MCM1) in yeast, AGAMOUS (AG) in Arabidopsis thaliana, DEFICIENS (DEF) in snapdragon, and the human SerumResponse Factor (SRF). The above four genes all contain a highly conserved region known as the MADS-box domain, located near the N-terminus. This domain consists of approximately 180 base pairs and encodes a DNA-binding motif that recognizes similar target DNA sequences [5]. To date, research on the functions of MADS-box genes in plants has been extensive, with numerous MADS-box genes identified and their functions validated in model plants such as Arabidopsis thaliana, snapdragon, petunia, rice, and maize [6]. However, the expression patterns of MADS-box genes are not entirely consistent across different plant species, necessitating further research to explore the model systems of floral organ development in various plants through the functional analysis of homologous genes. This article summarizes recent advances in the regulation of floral organ initiation and development by MADS-box genes, elucidates the regulatory network mechanisms underlying floral development, and provides a foundation for further exploration of MADS-box homologous genes and protein function analysis. This will contribute to refining the regulatory network of floral development and investigating the model systems of floral development in different plant species.

2. Classification and Structure of MADS-box Genes

Early phylogenetic analyses classified MADS-box genes into distinct subfamilies according to their functions. Subsequent comparative genomic studies, primarily using Arabidopsis thaliana sequences, established the phylogenetic relationships among major evolutionary branches of this gene family and confirmed that a single ancestral duplication event gave rise to two lineages (Type I and Type II) in plants, animals, and fungi [7]. In plants, Type I genes are phylogenetically clustered with SRF-like genes from animals. Structurally, Type I genes typically contain only 1–2 exons and encode proteins featuring a conserved core MADS-domain and a highly variable Carboxy-terminal domain [8]. Owing to these structural characteristics and their functional importance, Type I genes have attracted growing research interest [9]. For example, several Type I genes cloned from Arabidopsis thaliana, including AGL23, AGL28, AGL61, AGL62, AGL37, and AGL80, play crucial roles in endosperm development and are essential for female gametophytes and embryo formation [10,11]. Similarly, in Moso bamboo, six Type I genes have been implicated in inflorescence development, with PeMADS5 promoting early flowering when heterologously expressed in Arabidopsis thaliana [12].
In angiosperms, the majority of MADS-box genes identified belong to the Type II lineage. Type II genes are further divided into two branches: MEF2-type, primarily found in animals and fungi, and MIKC-type, which is unique to plants. MIKC-type genes typically consist of six introns and seven exons, encoding proteins composed of four domains: the MADS-domain, I-domain (intervening domain), K-domain (keratin-like domain), and C-terminal domain (Figure 1). The K-domain is a characteristic feature of MIKC-type genes, while the C-terminal domain is the least conserved region, with variations in its structure potentially leading to functional differences among MADS-box proteins. Research indicates that the I and K domains are involved in protein–protein interactions of MADS-box transcription factors, while the C-terminal domain, acting as a transcriptional activation domain, may play a role in stabilizing these interactions [13,14]. The MIKC-type is further subdivided into MIKCC-type and MIKC*-type, with the MIKCC-type constituting the majority and encompassing all known plant MADS-box genes with characterized expression patterns or mutant phenotypes [15] (Table 1).

3. Regulation of Floral Organ Development by the MADS-box Gene Family

From cytological and anatomical perspectives, floral development initiates with the transformation of meristematic cells, a process driven by both endogenous and environmental factors. This transformation initiates flowering, during which cells transition from the shoot apical meristem (SAM) to the inflorescence meristem (IM) [16]. The IM then generates floral meristems at its periphery, which subsequently differentiate into distinct floral organ whorls. In monocots, the IM first produces spikelet meristems, which then differentiate into floral meristems [2,17]. This developmental cascade is tightly regulated by a complex network of factors, including flowering integrators (FT, SOC1), floral meristem identity genes (AP1, LFY, CAL, FUL, AGL24), and floral organ identity genes (ABCDE-class genes), alongside other regulatory elements. The morphological patterning of floral organs is orchestrated by multiple signaling pathways and gene families, with key determinants shaping phenotypic variation. As central regulators, MADS-box genes exhibit differential expression levels that specify distinct morphological structures. These genes encode transcription factors that modulate floral architecture through DNA binding or protein–protein interactions. Additionally, the responsiveness of downstream target genes further contributes to the diversity of floral organ phenotypes.

3.1. Role of MADS-box Genes in Floral Initiation

The initiation of flowering is a process driven by signal transduction and the transformation of plant cell identity. To date, six major flowering signaling pathways have been characterized: the photoperiod pathway, vernalization pathway, autonomous pathway, gibberellin pathway, temperature-sensitive pathway, and age pathway [2]. These pathways perceive and relay flowering signals, ultimately regulating two antagonistic classes of MADS-box genes that control flowering onset. One class consists of strong flowering repressors, including FLOWERING LOCUS C (FLC) and SHORT VEGETATIVE PHASE (SVP), while the other comprises flowering integrators and floral meristem identity genes, which promote floral bud differentiation. The vernalization, autonomous, and temperature-sensitive pathways primarily suppress FLC and SVP expression through post-transcriptional regulation and epigenetic modifications (e.g., histone methylation), thereby alleviating their repression of flowering. Notably, FLC, a MADS-box transcription factor, directly inhibits the transcription of flowering integrators FT and SOC1 to delay flowering [18,19]. Prior to flowering, FLC exhibits high baseline transcriptional levels. Upon receiving flowering initiation signals, FRI, histone acetyltransferases, the histone methyltransferase COMPASS-like, and other chromatin modifiers are part of a FRI-containing supercomplex enriched in a region around the FLC transcription start site (TSS) to promote the expression of FLC antisense mRNA, leading to a reduction in sense mRNA expression. Concurrently, chromatin-modifying complexes alter the chromatin state of the FLC locus through histone modifications, further repressing FLC expression [20,21]. In the temperature-sensitive pathway, high temperatures promote the expression of FT while suppressing SVP, which interacts with FLC to negatively regulate the transcriptional activity of flowering integrators [22], thereby influencing flowering. However, the precise molecular mechanisms remain unclear. Interestingly, SVP and the floral meristem identity gene AGL24 are paralogous genes within the SVP/AGAMOUS-LIKE lineage of the MADS-box gene family. While SVP inhibits floral organ formation, AGL24 acts as a flowering activator [23]. In the monocot wheat, the SVP ortholog TaVRT2, along with TaVRN1, functions as a flowering initiator in the vernalization pathway. The TaVRT2 protein can directly bind to the promoter of TaVRN1, mediating a positive feedback loop [24,25], which differs from the regulation of SVP in dicots. Therefore, further research is needed to elucidate the regulatory roles of SVP and its orthologs in floral organ formation. In the photoperiod, gibberellin, and age pathways, signals directly or indirectly activate the expression of genes such as FT, SOC1, AP1, and AGL24 to initiate flowering [26,27,28].

3.2. Regulation of Cell Differentiation by MADS-box Genes

The six major flowering signaling pathways converge on two central integrators: FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1). While FT is not a MADS-box gene, it encodes a mobile protein that translocates over long distances to the shoot apex. There, it activates the downstream floral meristem identity gene AP1, initiating floral meristem formation at specific positions on the inflorescence meristem [29]. SOC1 serves as a hub that integrates flowering signals from multiple pathways. It forms a self-regulatory feedback loop with AGL24 through reciprocal promoter binding. Furthermore, the SOC1-AGL24 heterodimer cooperatively upregulates LEAFY (LFY) expression [30], a critical regulator of floral development. Within the shoot apical meristem (SAM), the concerted upregulation of SOC1 and other factors drives the transition from vegetative growth to inflorescence meristem identity [31].
The formation of floral meristems requires the decisive action of floral meristem identity genes (AP1, LFY, CAL, FUL, AGL24), all of which, except LFY, are MADS-box genes. APETALA1 (AP1) and CAULIFLOWER (CAL) are paralogous genes whose high expression determines the differentiation of floral meristems. In Arabidopsis, the ap1-cal double mutant exhibits prolific shoot proliferation at single flower positions, a phenomenon known as the “cauliflower phenotype,” where the inflorescence meristem fails to differentiate into floral meristems [32]. Although FRUITFULL (FUL) is expressed only in the inflorescence meristem and not in the floral meristem, it plays a crucial role in the initiation and differentiation of floral meristems. In Arabidopsis, FUL and AP1 exhibit functional redundancy in determining floral meristem identity [33].
MADS-box transcription factors play a pivotal role in orchestrating floral development by regulating stage-specific transitions between meristem identities. They achieve this by dynamically modulating the expression of identity genes, thereby establishing new developmental programs while repressing previous ones. The shift from vegetative growth to inflorescence meristem (IM) identity is governed by flowering integrators, which assimilate signals from multiple pathways to initiate this transition. Subsequently, integrators such as SOC1 activate floral meristem identity genes, promoting the formation of floral meristems on the flanks of the IM while simultaneously suppressing IM identity genes [34]. Research has demonstrated that SOC1, AGL24, and AGL15 interact with chromatin complexes to suppress premature activation of the floral organ identity gene SEP3, thereby preventing the early differentiation of floral meristem cells [35]. Once the floral meristem is established, AP1 gradually downregulates earlier developmental programs, including its own activators such as SOC1 [36]. Furthermore, AP1 upregulates LFY, and together, these genes play a crucial role in floral organ specification. AP1 also forms dimers with SEP3, an E-class protein of the MADS-box gene family, to activate genes responsible for floral organ identity [37].

3.3. Regulation of Floral Organ Formation by MADS-box Genes

Under the regulation of floral organ identity genes (ABCDE-class genes), cells of the floral meristem sequentially form different floral organs from the outer to the inner whorls along the flanks of the primordia. With the exception of the A-class gene AP2, which belongs to the AP2/ERF family, all floral organ identity genes are MADS-box genes. For most of these genes, their expression domains reflect their functional domains. A-class genes are expressed in sepals and petals, where they independently regulate sepal formation and synergistically regulate petal development with B-class genes. B-class and C-class genes are co-expressed in stamens to regulate their development and differentiation, while C-class and D-class genes regulate the formation of carpels and ovules. A-class and C-class genes exhibit antagonistic interactions, mutually restricting their expression domains within the floral primordia, thereby defining the boundaries of floral organs [37]. When A-class genes are mutated, C-class genes are expressed in the first and second whorls (sepals and petals), and vice versa, a phenomenon explained by the classic “ABC model of floral development” (Figure 2A). This model has been used to analyze the correspondence between the floral structures of monocots and the floral organs of dicots, providing evidence that the lemma and palea are homologous to sepals, and the lodicules are homologous to petals [38]. Ectopic expression of these genes can lead to alterations in floral organ structure, as seen in the triple mutants of Arabidopsis. In nature, floral organ structures vary widely. For example, in monocots such as lilies, the petaloid sepals in the first whorl result from the ectopic expression of B-class genes in the outer three whorls (Figure 2B), and reducing the expression of B-class genes affects the formation of floral perianth characteristics [39]. In some basal eudicots, such as those in the Ranunculaceae, B-class genes are expressed only in certain petals [36] (Figure 2C). With further research into floral development across different plants, the more complex ABCDE model has gained widespread acceptance (Figure 3). Studies on petunias introduced the D-class genes FLORAL BINDING PROTEIN7 (FBP7) and FLORAL BINDING PROTEIN11 (FBP11), with their homologs in Arabidopsis being SEEDSTICK (STK) and SHATTERPROOF (SHP), which are responsible for ovule determination and formation [40,41]. Meanwhile, E-class genes, such as SEPALLATA (SEP), are expressed throughout the floral meristem and are essential for the proper formation of all floral organs. SEP proteins can form multimeric complexes with A, B, and C-class proteins, maintaining their normal functions [42,43].
The expression levels of MADS-box genes regulate the morphological formation of floral organs, with biochemical regulation involving the binding of transcription factor-encoded proteins to target DNA sequences or interactions with other proteins. MADS-box transcription factors regulate complex gene networks in plants, requiring high specificity to target different genes. All MADS-box transcription factors recognize the CArG (CC[A/T]6GG) motif on DNA as dimers. Specifically, MIKCC-type MADS-box proteins can bind DNA at two sites as dimers and then form tetramers, causing DNA looping and structural changes to either inhibit or activate target gene expression. This regulatory mechanism is unique to plants [8]. For example, B-class gene proteins such as AP3 and PI bind DNA exclusively as heterodimers and maintain their transcription through a self-regulatory feedback loop involving their own promoters [44]. Yeast two-hybrid experiments have shown that the heterodimers formed by B-class orthologs DEF and GLO exhibit strong DNA-binding activity. Meanwhile, E-class gene-encoded proteins function as cofactors by forming complexes that help activate ABC genes and interact with their homo- or heterodimeric proteins to form tetramers, regulating floral organ formation. This is the basis of the tetramer model of regulation [45] (Figure 2A). Different MADS-box proteins vary in their ability to activate target gene transcription. For instance, the AP3-PI heterodimer binds to the CArG-box in the AP3 promoter but cannot activate transcription unless it forms a trimer with AP1 or SEP3 proteins, which then activates the AP3 gene promoter [46].

3.4. Research Progress on ABCDE-Class Genes

3.4.1. A-Class Genes

In Arabidopsis, class A genes include AP1 and AP2. Among these, only AP1 contains a conserved MADS domain and encodes a MADS-box transcription factor. AP1 is specifically expressed in floral tissues, not only in the first whorl (sepals) and the second whorl (petals), but also plays a critical role in establishing floral meristem identity during early flower differentiation [47,48,49]. In situ hybridization analyses reveal that AP1 expression is initiated in floral primordia and gradually intensifies as the primordia develop. Although not strictly essential for floral meristem formation, its expression is sufficient to convert an inflorescence into a flower [50]. The ap1 mutant in Arabidopsis produces leaf-like bracts in place of sepals and exhibits an almost complete loss of petals [51]. Furthermore, primary ap1 flowers often show partial conversion of floral organs into ectopic secondary inflorescences [52]. These observations demonstrate that AP1 regulates both floral meristem identity and the development of the first- and second-whorl floral organs. Besides AP1, the Arabidopsis genome contains three other AP1-subfamily members: CAULIFLOWER (CAL), FRUITFULL (FUL), and AGL79. Among them, CAL and FUL are paralogs of AP1, and all three genes cluster phylogenetically within a group named after SQUA, the snapdragon ortholog of AP1 [52]. Double mutants of ap1 and cal exhibit a “cauliflower” phenotype, in which positions normally occupied by individual flowers are replaced by proliferating masses of inflorescence meristems [53]. This phenotype is enhanced in the AP1 CAL FUL triple mutant, indicating a synergistic role among these genes [54]. The mutant analyses confirm that AP1, CAL, and FUL collectively act as floral meristem identity genes. In dicot plants, AP1, CAL, and FUL together fulfill the functions of class A genes [55], whereas in monocots, only FUL is associated with class A gene functions [56].
As the only gene in the ABCDE model that does not belong to the MADS-box family, AP2 possesses a unique AP2/ERF-type domain and encodes a transcription factor within the AP2/ERF family. The AP2 domain, comprising approximately 60–70 amino acids, is highly conserved and forms an amphipathic α-helix. It mediates protein–protein interactions, contains nuclear localization signals, and functions in transcriptional regulation [57]. AP2/ERF transcription factors can be categorized into three subfamilies based on the number of AP2 domains. Proteins with two AP2 domains belong to the AP2 subfamily, which is further divided into two groups: the AP2 group and the ANT (AINTEGUMENTA) group. Most members of this subfamily are involved in plant developmental processes, including floral organ morphogenesis, inflorescence meristem formation, and ovule and seed development. In Arabidopsis, the AP2 group includes five genes: AP2, TOE1, TOE2, SHLAFMUTZE (SMZ), and SCHNARCHZAPFEN (SNZ). The ANT group consists of ANT, AIL1, AIL5, AIL6, AIL7, AtBBM/AIL2, PLETHORA1 (PLT1), and PLETHORA2 (PLT2)/AIL4 [58]. AP2 is a key transcription factor required for establishing floral meristem identity, determining floral organ identity, and regulating the expression of homeotic genes. It is expressed in both floral and non-floral tissues, with distinct temporal and spatial patterns [59]. Weak AP2 mutants exhibit homeotic transformations—sepals become leaf-like and petals develop as stamen-like structures [60]—while strong ap2 mutants show a conversion of first-whorl organs into carpels and a reduction in organ number in the second and third whorls [61]. These phenotypes confirm that AP2 plays a critical role in regulating floral development in the first two whorls, and its loss leads to ectopic expression of AG, consistent with the ABC model. Studies of other AP2 subfamily genes in Arabidopsis indicate that TOE1 and TOE2 act as floral repressors [62], SMZ and SNZ are involved in flowering time control [63], and ANT is essential for ovule and female gametophyte development, partially overlapping in function with AP2 [64,65,66]. In petunias, the gene with the highest homology to Arabidopsis AP2 is PhAp2A, which exhibits similar spatiotemporal expression and functional characteristics. In snapdragons, LIP1 and LIP2 serve as functional equivalents of AP2 and contribute to sepal, petal, and ovule development. However, unlike AP2, they do not repress the expression of C-class genes in floral organs.

3.4.2. B-Class Genes

Arabidopsis thaliana possesses two class B floral organ identity genes, AP3 and PI, which belong to the DEF and GLO clades, respectively—named after their orthologs in Antirrhinum majus [67]. Mutations in these genes result in the replacement of petals (second whorl) by sepals and the transformation of stamens (third whorl) into carpel-like structures [67]. These findings demonstrate that class B genes are not only essential for specifying petal identity but also play a critical role in plant sex determination by promoting stamen development and suppressing carpel formation. Evolutionary studies indicate that the function of class B genes in specifying reproductive organ identity is highly conserved across angiosperms and even among seed plants more broadly [68]. However, gene duplication events during angiosperm evolution have given rise to distinct DEF and GLO lineages, leading to partial subfunctionalization and neofunctionalization. Notably, the encoded proteins have evolved from ancestral homodimers into obligate heterodimers. In orchids, the expression of class B genes extends into the first whorl of floral organs, contributing to their characteristic petaloid perianth. The remarkable diversity and specialized morphology of orchid flowers may also reflect evolutionary innovations within the class B gene family [45].

3.4.3. C- and D-Class Genes

The AG gene, a canonical class C gene in Arabidopsis thaliana, plays a central role in regulating the development of stamens, carpels, ovules, and fruits, and is crucial for floral organ formation and differentiation. Studies on the Arabidopsis ag mutant show that while sepals and petals develop normally, the stamens in the third whorl are transformed into petals, and the fourth whorl produces a new ag flower instead of carpels—consistent with predictions from the floral organ development model. Additionally, AG represses the expression of AP1 in the third and fourth whorls, although AP1 does not reciprocally inhibit AG. Instead, AG expression is suppressed in the first and second whorls by AP2 and five other genes in Arabidopsis [69]. Takeda et al. (2022) identified a new repressor of AG, RABBITEARS (RBE), which is involved in petal development and, like ANT, suppresses AG expression in the second whorl [70]. Class D genes are responsible for specifying ovule identity during floral morphogenesis. Pinyopich et al. (2003) demonstrated that SHP1, SHP2, and STK all contribute to ovule development [71]. Single and double mutants of these genes developed normal ovules, whereas triple mutants exhibited a transformation of ovules into leaf-like or carpel-like structures. Ectopic expression of any one of these three genes resulted in the formation of sepal–ovule chimeric structures. In addition to their role in ovules, SHP1 and SHP2 also regulate carpel development [72].

3.4.4. E-Class Genes

Class E genes encode a group of functionally essential transcription factors that are required for the development of all types of floral organs. Their protein products interact with class A, B, C, and D floral homeotic proteins to form multimeric MADS-box complexes, which are critical for normal plant growth and floral organ differentiation [73]. In Arabidopsis thaliana, four SEP genes (SEP1, SEP2, SEP3, and SEP4) have been identified. The sep1/2/3 triple mutant exhibits homeotic transformations in which petals, stamens, and carpels are converted into sepal-like organs—a phenotype resembling that of class B and C double mutants [44]. Notably, the expression of class A, B, and C genes remains unchanged in these mutants. These results confirm that class E genes are necessary for maintaining floral organ and meristem identity and exhibit partial functional redundancy.

3.5. Regulation of Downstream Target Genes by MADS-box Genes

In recent years, research on the regulation of downstream target genes by MADS-box transcription factors has advanced rapidly, revealing their role in inducing floral organ formation through the activation of these targets. The first identified target gene of MADS-box proteins was NAC-LIKE ACTIVATED BY AP3/PI (NAP). NAP encodes a plant-specific NAC family protein and is induced by AP3-PI during petal and stamen development, controlling the transition from cell division to elongation [74]. Additionally, the expression of NAP-like genes increases during floral organ formation, fruit maturation, and senescence, suggesting their interaction with MADS-box genes in regulating the transition from flower to fruit development [75]. The restriction of boundaries between stamens and carpels requires the SUPERMAN (SUP) gene, which is regulated by AP3, PI, and AG genes at the boundaries of these floral whorls. Although the regulatory mechanism remains unclear, studies propose that SUP also inhibits the expression of B-class genes AP3 and PI in the fourth whorl (carpels) and balances cell proliferation between the third and fourth whorls [76]. The AG protein can bind to a CArG-box-like sequence in the 3′UTR of the SPOROCYTELESS (SPL) gene, activating SPL transcription. Thus, SPL, as a direct target of AG, encodes a transcription factor that regulates ovule patterning and early microsporogenesis [77]. In rice, the E-class protein OsMADS8 targets OsTGA10, a gene encoding a bZIP transcription factor that is preferentially expressed during stamen development. Mutations in OsTGA10 result in male sterility, highlighting its critical role in tapetum development through interactions with known tapetum-related genes [78] (Figure 4). The VvMADS39 protein interacts with VvAGAMOUS in table grape, and their dimer is essential for integument development by activating and sustaining VvINO expression. Furthermore, the synergistic cooperation between VvMADS39 and associated proteins plays a crucial role in maintaining floral meristem identity, as well as supporting ovule and fruit development [79]. Investigating downstream target genes of MADS-box transcription factors provides a more comprehensive understanding of the floral development regulatory network. For example, microarray technology has identified 47 target genes of AP3 and PI, with 11 being primarily or exclusively expressed in flowers. In Aquilegia, 7049 direct target genes of AP3-3 have been identified [80]. The types and functions of downstream target genes of MADS-box transcription factors are crucial for comprehensively understanding the mechanisms of floral organ development and diversification. With advancements in biotechnology, from yeast two-hybrid systems to chromatin immunoprecipitation, the discovery of more target genes of MADS-box transcription factors will further refine the regulatory network of floral development.

4. Conclusions and Prospectives

In 1991, Coen and Meyerowitz conducted a landmark study on floral organ mutants in Arabidopsis thaliana and Antirrhinum majus, proposing the ABC model of floral organ development—a major milestone in plant developmental biology [81]. Most genes in this model (e.g., AP1, AP2, AP3, PI, and AG) belong to the MADS-box family of transcription factors. Their work revealed that behind the complex morphology of flowers lies a highly conserved “genetic toolkit” encoded by MADS-box genes. According to the ABC model, sepals are specified by class A genes alone; petals by the combined activity of class A and B genes; stamens by class B and C genes together; and carpels by class C genes alone. This framework provided a critical foundation for subsequent molecular studies on floral organ identity [82]. Further research has demonstrated that MADS-box proteins form specific homo- or heterodimers, which then assemble into higher-order quartet complexes. These complexes bind directly to CArG box motifs in the regulatory sequences of target genes [83]. This mechanism functions as a “molecular switch”, precisely activating or repressing downstream gene expression and thus elucidating the biochemical basis of the ABC model.
Over the decades of research on floral organ development, scientists have explored the intrinsic mechanisms underlying floral structure formation at the cellular, molecular, and genetic levels. While gene expression studies do not supersede morphological or anatomical approaches, the vast amount of genetic data has helped address questions hidden beneath phenotypic observations. Research at the genetic level has established a foundational framework for understanding the regulatory network of floral development (Figure 4), which continues to be refined with the discovery of additional regulatory nodes. Among these nodes, the MADS-box gene family has garnered significant attention as a major regulatory factor. With advancements in sequencing technologies and bioinformatics, an increasing number of plant species have been studied in depth through genomic or transcriptomic sequencing, revealing the roles of numerous members of the MADS-box gene family in floral organ development across different species. For example, overexpression of the BpAP1 gene in European white birch leads to early flowering [84]. In the Phalaenopsis orchid, the B-class gene PhalPI plays a crucial role in regulating the development of lateral petals and the labellum [85]. Studies on the dichogamy of Cyclocarya paliurus flowers show that CpAG interacts with gibberellins (GA) to break bud dormancy and regulate floral initiation through the GA pathway [86]. In chrysanthemum, ectopic expression of the sunflower C-class gene HAM59 results in male sterility and floral structure transformation, with stamens in disk florets converting into petal-like structures, creating a double-flower phenotype [87]. These studies represent only the tip of the iceberg regarding the MADS-box gene family, with many members yet to be explored. Future research will undoubtedly deepen our understanding of the complex regulation of floral organ development and enhance our comprehension of the higher-order functions of the MADS-box gene family. A key focus will be elucidating how MADS-box transcription factors form protein complexes and regulate target gene activity through epigenetic modifications, which will be a critical area of investigation in the study of the MADS-box gene family moving forward.
Through comparative genomic analysis of Arabidopsis thaliana, the phylogenetic relationships among the major evolutionary branches of the MADS-box gene family have been confirmed [7]. Determining these genes in different plant species will further aid in evaluating plant evolutionary relationships. MADS-box B- and C-class genes have been cloned from Conifers [88,89] and Gnetales [90], with studies indicating that these genes were present in the last common ancestor of angiosperms and gymnosperms. Their homologous genes were likely expressed in reproductive structures before the divergence of these two groups [38]. Although the homology of reproductive organs between gymnosperms and angiosperms remains unclear, MADS-box genes in gymnosperms will serve as powerful tools for further research into evolutionary systematics. Additionally, MADS-box genes have been identified in more distantly related plants such as mosses and ferns [54]. While these genes are not orthologous to those involved in floral structures, analyzing the functions of MADS-box genes across diverse plant groups is essential for constructing a comprehensive plant evolutionary tree. Although many MADS-box genes primarily function in reproductive development, some members of this family also play significant roles in vegetative growth and fruit development. For example, the JOINTLESS gene in tomatoes is associated with the abscission of leaves, flowers, and fruits [91]. In Arabidopsis, the Arabidopsis nitrate regulated 1 (ANR1) gene controls nitrate regulation to modulate root growth [92]. MADS-box genes are widely expressed in the roots, stems, leaves, and embryos of angiosperms. By integrating these expression patterns and gene functions, we can elucidate the comprehensive role of MADS-box genes in plant morphological evolution and development.
In-depth research on MADS-box genes extends far beyond theoretical exploration, offering significant practical implications and widespread application value. In molecular breeding for crop improvement, many MADS-box genes (e.g., SOC1, FLC, SVP) function as key integrators within the floral transition pathway [93]. Modulating these genes through gene editing or conventional breeding allows the development of early- or late-flowering varieties adapted to specific environmental conditions, thereby helping address challenges posed by climate change or specific market requirements [94]. In the improvement of floral organ and fruit traits, direct regulation of class B or class C genes can modify floral architecture. For example, manipulating class B genes may lead to double-flowered phenotypes (with increased petal number) or facilitate the production of male sterile lines [95], while tuning class C gene activity can influence fruit development and seed formation [96,97]. Such approaches represent core technologies in the ornamental horticulture industry for creating novel floral morphologies and extending blooming periods. In studies of seed and fruit development, genes within the AG subfamily play direct roles in regulating carpel and fruit formation. Elucidating their mechanisms offers pathways to improve traits such as fruit size, fruit set rate, ripening timing, and seed characteristics, including the development of seedless varieties [98]. Moreover, MADS-box genes provide an excellent model system for investigating major evolutionary events, such as the origin of flowers and the radiation of angiosperms [99]. Comparative analyses of MADS-box gene function and expression across species can reveal fundamental mechanisms of plant evolution [100]. Furthermore, deciphering how MADS-box genes integrate environmental signals, such as vernalization and photoperiod, to control flowering time is essential for predicting plant phenological responses to global warming and for designing resilient crop varieties capable of thriving under future climate conditions [101].
Despite the significant progress achieved to date, research on the MADS-box gene family continues to hold promising and expansive prospects. Future studies will increasingly focus on elucidating the complex interaction networks between MADS-box genes and other transcription factors, epigenetic regulators (such as DNA methylation and histone modification), hormone signaling pathways (e.g., gibberellins and auxins), and non-coding RNAs [102,103,104]. Such integrated approaches will provide a more systematic understanding of the regulatory mechanisms controlling floral development. The application of single-cell sequencing and spatial transcriptomics will enable the mapping of MADS-box gene expression profiles and their dynamic changes at cellular resolution [105]. These technologies are expected to precisely uncover the roles of MADS-box genes in floral meristem initiation and the specification of floral organ primordia, potentially revealing novel cell types and more detailed regulatory mechanisms. While current knowledge is largely derived from a limited set of model plants, future research should expand functional investigations to economically important or evolutionarily significant species, such as orchids, cereal crops, and forest trees, to identify novel, species-specific genes and functions [106,107,108]. This expansion will open new avenues for precision breeding and trait engineering. Furthermore, synthetic biology approaches may allow the reprogramming of MADS-box gene expression combinations and regulatory circuits, potentially enabling the design of novel floral structures in heterologous systems. Such achievements would not only demonstrate considerable commercial value but also represent the ultimate test of our foundational knowledge of floral development.

Author Contributions

Conceptualization, L.Z.; methodology and data analysis, Q.W., Z.L., R.L., H.C. and Q.L.; writing—original draft preparation, L.Z., Y.W., and Q.W.; writing—review and editing, L.Z.; supervision. All authors have read and agreed to the published version of the manuscript.

Funding

This research work was financially supported by the Project of State Key Laboratory of Tropical Crop Breeding (No. NKLTCB-HZ06, No. SKLTCBQN202507) and the National Natural Science Foundation of China (No. 32460412).

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Classification and structure of MADS-box proteins. I-domain means intervening domain, K-domain means keratin-like domain, and C-domain means C-terminal domain.
Figure 1. Classification and structure of MADS-box proteins. I-domain means intervening domain, K-domain means keratin-like domain, and C-domain means C-terminal domain.
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Figure 2. Floral organ development models. (A): Interpreted floral development models at different levels. “The ABC (D) E model” was at gene level. Sepals: A-class genes alone specified; Petals: A-and B-class genes combined to specified; Stamens: B-and C-class genes combined to specified; Carpels: C-class genes alone specified; Ovules: D-class genes specified (partially involved C-class genes); E-class genes were required to co-regulate the formation of floral organs. “The quartet model” was at protein level. Tetramers were formed by homodimer or heterodimer. Sepals: AP1-SEP-AP1-SEP; Petals: AP3-PI-SEP-AP1; Stamens: AP3-PI-SEP-AG; Carpels: AG-SEP-AG-SEP; Ovules: AG-SEP-SHP-STK. (B): Petaloid sepals in Liliaceae of monocotyledon resulted as B-class genes which covered the first three whorls. (C): B-class genes were expressed only in parts of the petals in some Ranunculus. AP2 gene was not a MADS-box gene; the other ABCDE genes were all MADS-box genes. AP1: APETALA1, AP2: APETALA2, AP3: APETALA3, PI: PISTILLATA; AG: AGAMOUS, STK: SEEDSTICK, SHP1: SHATTERPROOF1, SHP2: SHATTERPROOF2, SEP: SEPALLATA.
Figure 2. Floral organ development models. (A): Interpreted floral development models at different levels. “The ABC (D) E model” was at gene level. Sepals: A-class genes alone specified; Petals: A-and B-class genes combined to specified; Stamens: B-and C-class genes combined to specified; Carpels: C-class genes alone specified; Ovules: D-class genes specified (partially involved C-class genes); E-class genes were required to co-regulate the formation of floral organs. “The quartet model” was at protein level. Tetramers were formed by homodimer or heterodimer. Sepals: AP1-SEP-AP1-SEP; Petals: AP3-PI-SEP-AP1; Stamens: AP3-PI-SEP-AG; Carpels: AG-SEP-AG-SEP; Ovules: AG-SEP-SHP-STK. (B): Petaloid sepals in Liliaceae of monocotyledon resulted as B-class genes which covered the first three whorls. (C): B-class genes were expressed only in parts of the petals in some Ranunculus. AP2 gene was not a MADS-box gene; the other ABCDE genes were all MADS-box genes. AP1: APETALA1, AP2: APETALA2, AP3: APETALA3, PI: PISTILLATA; AG: AGAMOUS, STK: SEEDSTICK, SHP1: SHATTERPROOF1, SHP2: SHATTERPROOF2, SEP: SEPALLATA.
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Figure 3. ABCDE model of floral development (A) and floral quartet model (B). AP1: APETALA1, AP2: APETALA2, AP3: APETALA3, PI: PISTILLATA; AG: AGAMOUS, STK: SEEDSTICK, SHP1: SHATTERPROOF1, SHP2: SHATTERPROOF2, SEP: SEPALLATA.
Figure 3. ABCDE model of floral development (A) and floral quartet model (B). AP1: APETALA1, AP2: APETALA2, AP3: APETALA3, PI: PISTILLATA; AG: AGAMOUS, STK: SEEDSTICK, SHP1: SHATTERPROOF1, SHP2: SHATTERPROOF2, SEP: SEPALLATA.
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Figure 4. Relative MADS-box genes regulate floral development network, floral development processes, and related genes. → indicated acceleration; ─┤ inhibition; ─ represent this regulatory path has been studied; …… represent an unspecified regulatory path; * meant the gene was not a MADS-box gene. Genes unmarked were all MADS-box genes. AP1: APETALA1, AP2: APETALA2, AP3: APETALA3, PI: PISTILLATA; AG: AGAMOUS, STK: SEEDSTICK, SHP1: SHATTERPROOF1, SHP2: SHATTERPROOF2, SEP: SEPALLATA.
Figure 4. Relative MADS-box genes regulate floral development network, floral development processes, and related genes. → indicated acceleration; ─┤ inhibition; ─ represent this regulatory path has been studied; …… represent an unspecified regulatory path; * meant the gene was not a MADS-box gene. Genes unmarked were all MADS-box genes. AP1: APETALA1, AP2: APETALA2, AP3: APETALA3, PI: PISTILLATA; AG: AGAMOUS, STK: SEEDSTICK, SHP1: SHATTERPROOF1, SHP2: SHATTERPROOF2, SEP: SEPALLATA.
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Table 1. MADS-box genes and their functions.
Table 1. MADS-box genes and their functions.
GeneFunctionExpression PatternHomologous Gene
FLCControl of flowering time, flowering suppressorExcept shoot apex, widely expressed before flowering, download expression caused floweringCereal plants have no FLC homologous genes
SVPControl of flowering time, flowering suppressorApical meristem of inflorescence, buds, leaves before floweringBarley: BM1, BM9, HvVRT2; Wheat: TaVRT2
SOC1Control of flowering timeShoot apical meristem, leaves, flower budsBrassica: LF, MF1, MF2
CALFloral meristem identityFloral meristemParalogs of AP1
FULControl of flowering time, floral meri stemidentity, fruit developmentInflorescence meristem, ovules, cauline leavesParalogs of AP1
AGL24Control of flowering time, flowering activatorFloral meristemParalogs of SVP
AP1Floral meristem identity, A-class homeotic gene, regulated sepals and petalsThroughout floral meristem, whorls 1 and whorls 2 of floral organsSnapdragon: SQUA, DEFH28; Rice: OsMADS14, OsMADS15, OsMADS18
AP3B-class homeotic gene, regulated petals and stamensWhorls 2 and whorls 3 of floral organsSnapdragon: DEF, Petunia: PhGLO1/2, Rice: OsMADS16, Maize: Si1
PIB-class homeotic gene, regulated petals and stamensWhorls 2 and whorls 3 of floral organsSnapdragon: GLO; Petunia: pMADS1,GP; Rice: OsMADS2, OsMADS4
AGC-class homeotic gene, regulated stamens and carpelsWhorls 3 and whorls 4 of floral organsSnapdragon: FAR, Petunia: pMADS3, Rice: OsMADS3, Maize: ZAG1
SHP1/2D-class homeotic gene, fruit development and dehiscenceOvules, valve margin, fruit dehiscence zoneSnapdragon: PLE; Petunia: FBP6
STKD-class homeotic gene, regulated ovules developmentOvulesPetunia: FBP7, FBP11, Rice: OsMADS13, OsMADS21
SEP1/2/3/4E-class homeotic gene, co-regulated floral development, activated B-and C class genesSEP1/2: all whorls of floral organs; SEP3: whorls 2 and whorls 3; SEP4: whorls 1Petunia: FBP2, Tomato: TM5, Rice: OsMADS1
Only those MADS-box genes related to floral development were mainly listed. Unless otherwise stated, the genes mentioned were from Arabidopsis.
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Wu, Q.; Wu, Y.; Li, R.; Cao, H.; Li, Z.; Li, Q.; Zhou, L. Research Progress on the Regulation of Plant Floral Organ Development by the MADS-box Gene Family. Int. J. Mol. Sci. 2025, 26, 8946. https://doi.org/10.3390/ijms26188946

AMA Style

Wu Q, Wu Y, Li R, Cao H, Li Z, Li Q, Zhou L. Research Progress on the Regulation of Plant Floral Organ Development by the MADS-box Gene Family. International Journal of Molecular Sciences. 2025; 26(18):8946. https://doi.org/10.3390/ijms26188946

Chicago/Turabian Style

Wu, Qiufei, Yi Wu, Rui Li, Hongxing Cao, Zongming Li, Qihong Li, and Lixia Zhou. 2025. "Research Progress on the Regulation of Plant Floral Organ Development by the MADS-box Gene Family" International Journal of Molecular Sciences 26, no. 18: 8946. https://doi.org/10.3390/ijms26188946

APA Style

Wu, Q., Wu, Y., Li, R., Cao, H., Li, Z., Li, Q., & Zhou, L. (2025). Research Progress on the Regulation of Plant Floral Organ Development by the MADS-box Gene Family. International Journal of Molecular Sciences, 26(18), 8946. https://doi.org/10.3390/ijms26188946

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