MADS-box genes are a family of transcription factors found in plants, animals and fungi and are characterized by a conserved MADS domain. MADS-box genes have been found in all major plant lineages studied to date including green algae, mosses, ferns, gymnosperms and angiosperms. In Arabidopsis, MADS-box genes can be divided into three groups: Type I and Type II MADS box genes and MADS-like genes. Type II MADS box genes in plants can be further subdivided into the MIKCC and MIKC* types (reviewed in (Becker and Theissen, 2003)). Type I MADS-box genes contain a conserved MADS-box gene, but lack the relatively conserved I and K and highly divergent C domains found in the Type II MIKC type MADS-box genes.

Among the TYPE II MIKC genes in Arabidopsis, there have been approximately 19 genes that have been functionally characterized. These genes include many of the so called floral MADS-box genes (Theissen et al., 2000). These genes, along with other genes that have been less well characterized but are hypothesized to preferentially affect floral organ development, includes AGAMOUS (AG), AGL6, AGL13, APETALA1 (AP1), APETALA3 (AP3), CAULIFLOWER (CAL), PISTILLATA (PI), SEEDSTICK (STK), SEPALLATA1,2,3,4 (SEP1,2,3,4), SHATTERPROOF1 and 2 (SHP1, 2) and TRANSPARENT TESTA16 (TT16). Additionally, several genes with either identified or hypothesized function regulating floral timing and inflorescence development have been identified including AGL24, AGL27, FLOWERING LOCUS C (FLC) (also known as FLOWERING LOCUS F (FLF)), FLC1, FLC2, FLOWERING LOCUS M (FLM) (also known as MADS AFFECTING FLOWERING1 (MAF1), FRUITFUL (FUL), SHORT VEGETATIVE PHASE (SVP) and SUPRESSOR OF CONSTANS (SOC1). Lastly, there are the non-floral genes, a group that mostly have currently unknown function, but that exhibit diverse expression that likely reflects roles in floral, root, seed, seedling, stem and leaf development. These genes include AGL12, AGL14, AGL15, AGL16, AGL17, AGL18, AGL19, AGL21 and ANR1.

Of the Type I MADS-box genes, PHERES1 (PHE1, formerly AGL37), has been investigated. It is a master regulator of paternally expressed imprinted genes, as well as of non-imprinted key regulators of endosperm development. It was shown that the CArG-box-like DNA-binding motifs that are bound by PHE1 have been distributed by RC/Helitron transposable elements. This provides an example of the molecular domestication of these elements which, by distributing PHE1 binding sites throughout the genome, have facilitated the recruitment of crucial endosperm regulators into a single transcriptional network (Batista et al., 2019).

In maize a number of MADs box genes have been studied.  The maize ZAG1 gene encodes a protein that is homologous to the AGAMOUS (AG) gene which specifies stamen and carpel identity in Arabidopsis (Schmidt et al., 1993). Several other ZAG1 homologs were also identified based on library screening (Mena et al., 1995). Bearded ear 1 (bde1) was cloned and found to encode zea agamous3 (zag3). bde zag1 double mutants have a severe ear phenotype, not observed in either single mutant, in which floral meristems are converted to branch-like meristems, indicating that bde and zag1 redundantly promote floral meristem identity (Thompson et al., 2009).

A genome wide analysis of the maize genome revealed 98 expressed MADS box genes that could be divided into five subfamilies: MIKC-type, Mα, Mβ, Mγ, and Mδ (Zhao et al., 2021). 211 different proteins were reported from these 98 genes.

Zea mays mads16 (Zmm16)/sterile tassel silky ear1 (sts1) encodes a PISTILLATA/GLOBOSA ortholog and has been implicated in the zygomorphy and sex determination pathways during maize flower development (Bartlett et al., 2015).

ZmTMM1 is a truncated MIKC-type MADS-box transcription factor lacking K- and C-domains, expressed preferentially in the lateral root branching zone and induced by the localized supply of nitrate (Liu et al., 2020).

Pod corn, known since pre-Columbian times, is the result of a dominant gain-of-function mutation at the Tunicate (Tu) locus. The pod corn trait is caused by a cis-regulatory mutation and duplication of the ZMM19 MADS-box gene. Although the WT locus contains a single-copy gene that is expressed in vegetative organs only, mutation and duplication of ZMM19 in Tu lead to ectopic expression of the gene in the inflorescences, thus conferring vegetative traits to reproductive organs (Wingen et al., 2012).

Last updated June 2023 by John Gray

References:

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Becker A, Theissen G. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol. 2003 Dec;29(3):464-89. doi: 10.1016/s1055-7903(03)00207-0. PMID: 14615187.

Mena M, Mandel MA, Lerner DR, Yanofsky MF, Schmidt RJ. A characterization of the MADS-box gene family in maize. Plant J. 1995 Dec;8(6):845-54. doi: 10.1046/j.1365-313x.1995.8060845.x. PMID: 8580958.

Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF. Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell. 1993 Jul;5(7):729-37. doi: 10.1105/tpc.5.7.729. PMID: 8103379; PMCID: PMC160311.

Zhao D, Chen Z, Xu L, Zhang L, Zou Q. Genome-Wide Analysis of the MADS-Box Gene Family in Maize: Gene Structure, Evolution, and Relationships. Genes (Basel). 2021 Dec 7;12(12):1956. doi: 10.3390/genes12121956. PMID: 34946905; PMCID: PMC8701013.

Liu Y, Jia Z, Li X, Wang Z, Chen F, Mi G, Forde B, Takahashi H, Yuan L. Involvement of a truncated MADS-box transcription factor ZmTMM1 in root nitrate foraging. J Exp Bot. 2020 Jul 25;71(15):4547-4561. doi: 10.1093/jxb/eraa116. PMID: 32133500; PMCID: PMC7382388.

Bartlett ME, Williams SK, Taylor Z, DeBlasio S, Goldshmidt A, Hall DH, Schmidt RJ, Jackson DP, Whipple CJ. The Maize PI/GLO Ortholog Zmm16/sterile tassel silky ear1 Interacts with the Zygomorphy and Sex Determination Pathways in Flower Development. Plant Cell. 2015 Nov;27(11):3081-98. doi: 10.1105/tpc.15.00679. Epub 2015 Oct 30. PMID: 26518212; PMCID: PMC4682306.

Thompson BE, Bartling L, Whipple C, Hall DH, Sakai H, Schmidt R, Hake S. bearded-ear encodes a MADS box transcription factor critical for maize floral development. Plant Cell. 2009 Sep;21(9):2578-90. doi: 10.1105/tpc.109.067751. Epub 2009 Sep 11. PMID: 19749152; PMCID: PMC2768933.

Batista RA, Moreno-Romero J, Qiu Y, van Boven J, Santos-González J, Figueiredo DD, Köhler C. The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons. Elife. 2019 Dec 2;8:e50541. doi: 10.7554/eLife.50541. PMID: 31789592; PMCID: PMC6914339.

Wingen LU, Münster T, Faigl W, Deleu W, Sommer H, Saedler H, Theißen G. Molecular genetic basis of pod corn (Tunicate maize). Proc Natl Acad Sci U S A. 2012 May 1;109(18):7115-20. doi: 10.1073/pnas.1111670109. Epub 2012 Apr 18. PMID: 22517751; PMCID: PMC3344968.