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Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes

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Abstract

The MADS-box encodes a novel type of DNA-binding domain found so far in a diverse group of transcription factors from yeast, animals, and seed plants. Here, our first aim was to evaluate the primary structure of the MADS-box. Compilation of the 107 currently available MADS-domain sequences resulted in a signature which can strictly discriminate between genes possessing or lacking a MADS-domain and allowed a classification of MADS-domain proteins into several distinct subfamilies. A comprehensive phylogenetic analysis of known eukaryotic MADS-box genes, which is the first comprising animal as well as fungal and plant homologs, showed that the vast majority of subfamily members appear on distinct subtrees of phylogenetic trees, suggesting that subfamilies represent monophyletic gene clades and providing the proposed classification scheme with a sound evolutionary basis. A reconstruction of the history of the MADS-box gene subfamilies based on the taxonomic distribution of contemporary subfamily members revealed that each subfamily comprises highly conserved putative orthologs and recent paralogs. Some subfamilies must be very old (1,000 MY or more), while others are more recent. In general, subfamily members tend to share highly similar sequences, expression patterns, and related functions. The defined species distribution, specific function, and strong evolutionary conservation of the members of most subfamilies suggest that the establishment of different subfamilies was followed by rapid fixation and was thus highly advantageous during eukaryotic evolution. These gene subfamilies may have been essential prerequisites for the establishment of several complex eukaryotic body structures, such as muscles in animals and certain reproductive structures in higher plants, and of some signal transduction pathways. Phylogenetic trees indicate that after establishment of different subfamilies, additional gene duplications led to a further increase in the number of MADS-box genes. However, several molecular mechanisms of MADS-box gene diversification were used to a quite different extent during animal and plant evolution. Known plant MADS-domain sequences diverged much faster than those of animals, and gene duplication and sequence diversification were extensively used for the creation of new genes during plant evolution, resulting in a relatively large number of interacting genes. In contrast, the available data on animal genes suggest that increase in gene number was only moderate in the lineage leading to mammals, but in the case of MEF2-like gene products, heterodimerization between different splice variants may have increased the combinatorial possibilities of interactions considerably. These observations demonstrate that in metazoan and plant evolution, increased combinatorial possibilities of MADS-box gene product interactions correlated with the evolution of increasingly complex body plans.

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Abbreviations

accession number:

(acc. no.)

amino acids:

(aa)

Genetics Computer Group:

(GCG)

maximum parsimony method:

(MP)

million years:

(MY)

million years ago:

(MYA)

neighbor-joining algorithm:

(NJ)

References

  • Affolter M, Montagne J, Walldorf U, Groppe J, Kloter U, LaRosa M, Gehring WJ (1994) TheDrosophila SRF homolog is expressed in a subset of tracheal cells and maps within a genomic region required for tracheal development. Development 120:743–753

    CAS  PubMed  Google Scholar 

  • Ainsworth C, Crossley S, Buchanan-Wollaston V, Thangavelu M, Parker J (1995) Male and female flowers of the dioecious plant sorrel show different patterns of MADS box gene expression. Plant Cell 7:1583–1598

    Article  CAS  PubMed  Google Scholar 

  • Ammerer G (1990) Identification, purification, and cloning of a polypeptide (PRTF/GRM) that binds to mating-specific promoter elements in yeast. Genes Div 4:299–312

    CAS  Google Scholar 

  • Angenent GC, Busscher M, Franken J, Mol JNM, van Tunen AJ (1992) Differential expression of two MADS box genes in wild-type and mutant petunia flowers. Plant Cell 4:983–993

    Article  CAS  PubMed  Google Scholar 

  • Angenent GC, Franken J, Busscher M, Colombo L, van Tunen AJ (1993) Petal and stamen formation in petunia is regulated by the homeotic genefbp1. Plant J 4:101–112

    Article  CAS  PubMed  Google Scholar 

  • Angenent GC, Franken J, Busscher M, Weiss D, van Tunen AJ (1994) Co-suppression of the petunia homeotic genefbp2 affects the identity of the generative meristem. Plant J 5:33–44

    Article  CAS  PubMed  Google Scholar 

  • Angenent GC, Busscher M, Franken J, Dons HJM, van Tunen AJ (1995a) Functional interaction between the homeotic genesfbp1 andpMADS1 during petunia floral organogenesis. Plant Cell 7:507–516

    CAS  Google Scholar 

  • Angenent GC, Franken J, Busscher M, van Dijken A, van Went JL, Dons HIM,van Tunen AJ (1995b) A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell 7: 1569–1582

    CAS  Google Scholar 

  • Anthony RG, James PE, Jordan BR (1995) The cDNA sequence of a Cailiflowerapetala-1/squamosa homolog. Plant Physiol 108:441–442

    Article  CAS  PubMed  Google Scholar 

  • Araki I, Satoh N (1995) As-MEF2 is predominantly expressed in mesenchyme and central nervous system in ascidian embryos. (unpublished)

  • Bairoch A (1991) PROSITE: a dictionary of sites and patterns in proteins. Nucleic Acids Res 19:2241–2245

    CAS  PubMed  Google Scholar 

  • Balavoine G, Telford MJ (1995) Identification of planarian homeobox sequences indicates the antiquity of most Hox/homeotic gene subclasses. Proc Natl Acad Sci USA 92:7227–7231

    CAS  PubMed  Google Scholar 

  • Baldauf SL, Palmer JD (1993) Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci USA 90:11558–11562

    CAS  PubMed  Google Scholar 

  • Baudinette SC, Savin KW (1995) Carnation MADS-box genes. (unpublished)

  • Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR (1993) Control of flower development inArabidopsis thaliana byAPETALA1 and interacting genes. Development 119:721–743

    CAS  Google Scholar 

  • Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at theplena locus of Antirrhinum. Cell 72:85–95

    Article  CAS  PubMed  Google Scholar 

  • Cacharrón J, Fischer A, Saedler H, Theißen G (1995) Expression patterns of MADS-box genes as studied byin situ hybridization. Maize Genet Coop Newslett 69:37–38

    Google Scholar 

  • Carroll SB (1995) Homeotic genes and the evolution of arthropods and chordates. Nature 376:479–485

    Article  CAS  PubMed  Google Scholar 

  • Chambers AE, Kotecha S, Towers N, Mohun TJ (1992) Muscle-specific expression of SRF-related genes in the early embryo ofXenopus leavis. EMBO J 11:4981–4991

    CAS  PubMed  Google Scholar 

  • Chung Y-Y, Kim S-R, Finkel D, Yanofsky MF, An G (1994) Early flowering and reduced apical dominance result from ectopic expression of a rice MADS box gene. Plant Mol Biol 26:657–665

    CAS  PubMed  Google Scholar 

  • Chung Y-Y, Kim S-R, Kang H-G, Noh Y-S, Park MC, Finkel D, An G (1995) Characterization of two rice MADS box genes homologous toGLOBOSA. Plant Sci 109:45–56

    CAS  Google Scholar 

  • Colombo L, Franken J, Koetje E, van Went J, Dons HIM, Angenent GC, van Tunen AJ (1995) The petunia MADS box geneFBP11 determines ovule identity. Plant Cell 7:1859–1868

    Article  CAS  PubMed  Google Scholar 

  • Davidson EH, Peterson KJ, Cameron RA (1995) Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270:1319–1325

    CAS  PubMed  Google Scholar 

  • Davies B, Schwarz-Sommer Z (1994) Control of floral organ identity by homeotic MADS-box transcription factors. In: Nover L (ed) Results and problems in cell differentiation 20, Plant promoters and transcription factors. Springer, Berlin, pp 235–258

    Google Scholar 

  • Dayhoff MO (1979) Atlas of protein sequences and structure, vol 5, supplement 3, 1978. National Biomedical Research Foundation, Washington, DC

    Google Scholar 

  • Démolis N, Mallet L, Jacquet M (1994) A 12.5 kb fragment of the yeast chromosome II contains two adjacent genes encoding ribosomal proteins and six putative new genes, one of which encodes a putative transcriptional factor. Yeast 10:1511–1525

    Article  PubMed  Google Scholar 

  • Dodou E, Sparrow DB, Mohun T, Treisman R (1995) MEF2 proteins, including MEF2A, are expressed in both muscle and non-muscle cells. Nucleic Acids Res 23:4267–4274

    CAS  PubMed  Google Scholar 

  • Doyle JJ (1994) Evolution of a plant homeotic multigene family: toward connecting molecular systematics and molecular developmental genetics. Syst Biol 43:307–328

    Google Scholar 

  • Dubois E, Bercy J, Messenguy F (1987) Characterization of two genes,ARGRI andARGRIII, required for specific regulation of arginine metabolism in yeast. Mol Gen Genet 207:142–148

    Article  CAS  PubMed  Google Scholar 

  • Edwards D, Feehan J (1980) Records ofCooksonia-type sporangia from late Wenlock strata in Ireland. Nature 287:41–42

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the boostrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1993) PHYLIP Phylogeny Inference Package 3.5. Department of Genetics, The University of Washington

  • Fischer A, Baum N, Saedler H, Theißen G (1995a) Chromosomal mapping of the MADS-box multigene family inZea mays reveals dispersed distribution of allelic genes as well as transposed copies. Nucleic Acids Res 23:1901–1911

    CAS  Google Scholar 

  • Fischer A, Saedler H, Theissen G (1995b) Restriction fragment length polymorphism-coupled domain-directed differential display: a highly efficient technique for expression analysis of multigene families. Proc Natl Acad Sci USA 92:5331–5335

    CAS  Google Scholar 

  • Fitch WW (1971) Toward defining the course of evolution: minimum change for a specified tree topology. Syst Zool 20:406–416

    Google Scholar 

  • Flanagan CA, Ma H (1994) Spatially and temporally regulated expression of the MADS-box geneAGL2 in wild-type and mutantArabidopsis flowers. Plant Mol Biol 26:581–595

    Article  CAS  PubMed  Google Scholar 

  • Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, Fritchman JL, Weidman JF, Small KV, Sandusky M, Fuhrmann J, Nguyen D, Utterback TR, Saudek DM, Phillips CA, Merrick JM, Tomb J-F, Dougherty BA, Bon KF, Hu P-C, Lucier TS, Peterson SN, Smith HO, Hutchison III CA, Venter JC (1995) The minimal gene complement ofMycoplasma geuitalium. Science 270:397–403

    CAS  PubMed  Google Scholar 

  • Garcia-Maroto F, Salamini F, Rohde W (1993) Molecular cloning and expression patterns of three alleles of theDeficiens-homologous geneSt-Deficiens fromSolanum tuberosum. Plant J 4:771–780

    Article  CAS  PubMed  Google Scholar 

  • Gehring WJ (1992) The homeobox in perspective. Trends Biochem Sci 17:277–280

    Article  CAS  PubMed  Google Scholar 

  • Gehring WJ, Affolter M, Biirglin T (1994) Homeodomain proteins. Annu Rev Biochem 63:487–526

    Article  CAS  PubMed  Google Scholar 

  • Genetics Computer Group (1994) Program Manual for the Wisconsin Package, Version 8, September 1994, Genetics Computer Group, 575 Science Drive, Madison, Wisconsin, USA 53711

    Google Scholar 

  • Gensel PG, Andrews HN (1984) Plant life in the Devonian. Praeger, New York

    Google Scholar 

  • Gogarten JP (1994) Which is the most conserved group of proteins? Homology-orthology, paralogy, xenology, and the fusion of independent lineages. J Mol Evol 39:541–543

    Article  CAS  PubMed  Google Scholar 

  • Gojobori T, Ikeo K (1994) Molecular evolution of serine protease and its inhibitor with special reference to domain evolution. Philos Trans R Soc Lond Biol 344:411–415

    CAS  PubMed  Google Scholar 

  • Goto K, Meyerowitz EM (1994) Function and regulation of theArabidopsis floral homeotic genePISTILLATA. Genes Dev 8:1548–1560

    CAS  PubMed  Google Scholar 

  • Hansen G, Estruch JJ, Sommer H, Spena A (1993) NTGLO: a tobacco homologue of theGLOBOSA floral homeotic gene ofAntirrhinum majus: cDNA sequence and expression pattern. Mol Gen Genet 239:310–312

    CAS  PubMed  Google Scholar 

  • Hardenack S, Ye D, Saedler H, Grant S (1994) Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant white campion. Plant Cell 6:1775–1787

    Article  CAS  PubMed  Google Scholar 

  • Hartland WB, Cox AV, Llewellyn PG, Pickton CAG, Smith AG, Walters R (1982) A geologic time scale. Cambridge University Press, Cambridge

    Google Scholar 

  • Heard J, Dunn K (1995) Symbiotic induction of a MADS-box gene during development of alfalfa root nodules. Proc Natl Acad Sci USA 92:5273–5277

    CAS  PubMed  Google Scholar 

  • Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 7:1271–1282

    Article  CAS  PubMed  Google Scholar 

  • Hill CS, Wynne J, Treisman R (1995) The Rho family GTPases RhoA, Racl, and CDC42Hs regulate transcriptional activation by SRF. Cell 81:1159–1170

    Article  CAS  PubMed  Google Scholar 

  • Hobson GM, Krahe R, Garcia E, Siciliano MJ, Funanage VL (1995) Regional chromosomal assignments for four members of the MADS domain transcription enhancer factor 2 (MEF2) gene family to human chromosomes 15826, 19p12, 5gl4, and lgl2-q23. Genomics 29:704–711

    CAS  PubMed  Google Scholar 

  • Holland PWH (1992) Homeobox genes in vertebrate evolution. Bioessays 14:267–273

    Article  CAS  PubMed  Google Scholar 

  • Huang H, Mizukami Y, Hu Y, Ma H (1993) Isolation and characterization of the binding sequences for the product of theArabidopsis floral homeotic geneAGAMOUS. Nucleic Acids Res 21:4769–4776

    CAS  PubMed  Google Scholar 

  • Huang H, Tudor M, Weiss CA, Hu Y, Ma H (1995) TheArabidopsis MADS-box geneAGL3 is widely expressed and encodes a sequence-specific DNA-binding protein. Plant Mol Biol 28:549–567

    Article  CAS  PubMed  Google Scholar 

  • Huijser P, Klein J, Lönnig W-E, Meijer H. Saedler H, Sommer H (1992) Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box genesquamosa inAntirrhinum majus. EMBO J 11:1239–1249

    CAS  PubMed  Google Scholar 

  • Ingram GC, Goodrich J, Wilkinson MD, Simon R, Haughn OW, Coen ES (1995) Parallels betweenUNUSUAL FLORAL ORGANS andFIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. Plant Cell 7:1501–1510

    Article  CAS  PubMed  Google Scholar 

  • Irish VF, Yamamoto YT (1995) Conservation of floral homeotic gene function between Arabidopsis and Antirrhinum. Plant Cell 7:1635–1644

    Article  CAS  PubMed  Google Scholar 

  • Jack T, Brockman LL, Meyerowitz EM (1992) The homeotic geneAPETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683–697

    Article  CAS  PubMed  Google Scholar 

  • Jack T, Fox GL, Meyerowitz EM (1994) Arabidopsis homeotic geneAPETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell 76:703–716

    Article  CAS  PubMed  Google Scholar 

  • Jarvis EE, Clark KL, Sprague GF (1989) The yeast transcription activator PRTF, a homolog of the mammalian serum response factor, is encoded by theMCM1 gene. Genes Dev 3:936–945

    CAS  PubMed  Google Scholar 

  • Jofuku KD, den Boer BGW, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic geneAPETALA2. Plant Cell 6:1211–1225

    Article  CAS  PubMed  Google Scholar 

  • Johnson AD (1995) Molecular mechanisms of cell-type determination in budding yeast. Curr Opin Gen Dev 5:552–558

    CAS  Google Scholar 

  • Kang S-G, Hannapel DJ (1995) Nucleotide sequences of novel potato (Solanum tuberosum L.)MADS-box cDNAs and their expression in vegetative organs. Gene 166:329–330

    Article  CAS  PubMed  Google Scholar 

  • Kang H-G, Noh Y-S, Chung Y-Y, Costa MA, An K, An G (1995) Phenotypic alterations of petal and sepal by ectopic expression of a rice MADS box gene in tobacco. Plant Mol Biol 29:1–10

    Article  CAS  PubMed  Google Scholar 

  • Kappen C, Ruddle FH (1993) Evolution of a regulatory gene family:HOM/HOX genes. Curr Opin Genet Dev 3:931–938

    Article  CAS  PubMed  Google Scholar 

  • Kappen C, Schughart K, Ruddle FH (1989) Two steps in the evolution of Antennapedia-class vertebrate homeobox genes. Proc Natl Acad Sci USA 86:5459–5463

    CAS  PubMed  Google Scholar 

  • Kappen C, Schughart K, Ruddle FH (1993) Early evolutionary origin of major homeodomatn sequence classes. Genomics 18:54–70

    Article  CAS  PubMed  Google Scholar 

  • Karunanandaa B, Kao T-H ( 1995) Characterization of a flower specific cDNA ofPetunia inflata encoding a putative homolog of Agamous protein. (unpublished)

  • Kaushal S, Schneider JW, Nadal-Ginard B. Mahdavi V (1994) Activation of the myogenic lineage by MEF2A, a factor that induces and cooperates with MyoD. Science 266:1236–1240

    CAS  PubMed  Google Scholar 

  • Kempin SA, Mandel MA, Yanofsky MF (1993) Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic geneNAG1. Plant Physiol 103:1041–1046

    Article  CAS  PubMed  Google Scholar 

  • Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of thecauliflower phenotype inArabidopsis. Science 267:522–525

    CAS  PubMed  Google Scholar 

  • Kim YS, Lee HS, Hoon LS, Yoo OJ, Jung WI, Liu JR (1995) The cDNA sequence of two MADS box genes inPanax ginseng (GenBank Z46612 for GAG2, Z46613 for GAGI) (PGR95-060). Plant Physiol 109:339

    Google Scholar 

  • Knoll AH (1992) The early evolution of eukaryotes: a geological perspective. Science 256:622–627

    CAS  PubMed  Google Scholar 

  • Kobel HR, Du Pasquier L (1986) Genetics of polyploidXenopus. Trends Genet 2:310–315

    Article  Google Scholar 

  • Krause MW, Dichoso D, Park M, Fire A, Ahnn J (1995) Zygotic CeMEF-2 expression is not required for myogenesis in C. elegans. (unpublished)

  • Kush A, Brunelle A, Shevell D, Chua N-H (1993) The cDNA sequence of two MADS box proteins inPetunia. Plant Physiol 102:1051–1052

    Article  CAS  PubMed  Google Scholar 

  • Laudet V, Stehelin D, Clevers H (1993) Ancestry and diversity of the HMG box superfamily. Nucleic Acids Res 21:2493–2501

    CAS  PubMed  Google Scholar 

  • Lee I, Aukerman MJ, Gore SL, Lohman KN, Michaels SD, Weaver LM, John MC, Feldmann KA, Amasino RM (1994) Isolation ofLuminidependens: a gene involved in the control of flowering time in Arabidopsis. Plant Cell 6:75–83

    CAS  PubMed  Google Scholar 

  • Leifer D, Krainc D, Yu Y-T, McDermott J, Breitbart RE, Heng J, Neve RL, Kosofsky B, Nadal-Ginard B, Lipton SA (1993) MEF2C, a MADS/MEF2-family transcription factor expressed in a laminar distribution in cerebral cortex. Proc Natl Acad Sci USA 90:1546–1550

    CAS  PubMed  Google Scholar 

  • Li W-H, Graur D (1991) Fundamentals of molecular evolution. Sinauer, Sunderland, MA

    Google Scholar 

  • Lilly B, Galewsky S, Firulli AB, Schulz RA, Olson EN (1994) D-MEF2; a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages duringDrosophila embryogenesis. Proc Natl Acad Sci USA 91:5662–5666

    CAS  PubMed  Google Scholar 

  • Lilly B, Zhao B, Ranganayakulu G, Paterson BM, Schulz RA, Olson EN (1995) Requirement of MADS domain transcription factor D-MEF2 for muscle formation inDrosophila. Science 267:688–693

    CAS  PubMed  Google Scholar 

  • Litman GW, Rast JP, Shamblott MJ, Haire RN, Hulst M, Roess W, Litman RT, Hinds-Frey KR, Zilch A, Amemiya CT (1993) Phylogenetic diversification of immunoglobulin genes and the antibody repertoire. Mol Biol Evol 10:60–72

    CAS  PubMed  Google Scholar 

  • Lönnig W-E, Saedler H (1994) The homeoticMacho mutant ofAntirrhinum majus reverts to wild-type or mutates to the homeoticplena phenotype. Mol Gen Genet 245:636–643

    Article  PubMed  Google Scholar 

  • Lu Z-X, Wu M, Loh C-S, Yeong C-Y, Goh C-J (1993) Nucleotide sequence of a flower-specific MADS box cDNA clone from orchid. Plant Mol Biol 23:901–904

    Article  CAS  PubMed  Google Scholar 

  • Ma H (1994) The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev 8:745–756

    CAS  PubMed  Google Scholar 

  • Ma H, Yanofsky MIT, Meyerowitz EM (1991)AGL1-AGL6, anArabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5:484–495

    CAS  PubMed  Google Scholar 

  • Mandel MA, Bowman JL, Kempin SA, Ma H, Meyerowitz EM, Yanofsky MF (1992a) Manipulation of flower structure in transgenic tobacco. Cell 71:133–143

    Article  CAS  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992b) Molecular characterization of theArabidopsis floral homeotic geneAPETALA1. Nature 360:273–277

    CAS  Google Scholar 

  • Mandel T, Lutziger I, Kuhlemeier C (1994) A ubiquitously expressed MADS-box gene fromNicotiana tabacum. Plant Mol Biol 25:319–321

    Article  CAS  PubMed  Google Scholar 

  • Mandel MA, Yanofsky MF (1995) The ArabidopsisAGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated byAPETALA1. Plant Cell 7:1763–1771

    Article  CAS  PubMed  Google Scholar 

  • Martin W, Lydiate D, Brinkmann H, Forkmann G, Saedler H, Cerff R (1993a) Molecular phylogenies in angiosperm evolution. Mol Biol Evol 10:140–162

    CAS  Google Scholar 

  • Martin JF, Schwarz JJ, Olson EN (1993b) Myocyte enhancer factor (MEF) 2C: a tissue-restricted member of the MEF-2 family of transcription factors. Proc Natl Acad Sci USA 90:5282–5286

    CAS  Google Scholar 

  • Martin JF, Miano JM, Hustad CM, Copeland NG, Jenkins NA, Olson EN (1994) AMef2 gene that generates a muscle-specific isoform via alternative mRNA splicing. Mol Cell Biol 14:1647–1656

    CAS  PubMed  Google Scholar 

  • McDermott JC, Cardoso MC, Yu Y-T, Andres V, Leifer D, Krainc D, Lipton SA, Nadal-Ginard B (1993) hMEF2C gene encodes skeletal muscle- and brain-specific transcription factors. Mol Cell Biol 13: 2564–2577

    CAS  PubMed  Google Scholar 

  • McGinnis W, Kuziora M (1994) The molecular architects of body design. Sci Am 270:36–42

    Google Scholar 

  • Mena M, Mandel MA, Lerner DR, Yanofsky MF, Schmidt RJ (1995) A characterization of the MADS-box gene family in maize. Plant J 8:845–854

    CAS  PubMed  Google Scholar 

  • Menzel G, Apel K, Melzer S (1995) Isolation and analysis of SaMADS C, the APETALA 1 cDNA homolog from mustard. Plant Physiol 108:853–854

    Article  CAS  PubMed  Google Scholar 

  • Meyerowitz EM (1994a) Flower development and evolution: new answers and new questions. Proc Natl Acad Sci USA 91:5735–5737

    CAS  Google Scholar 

  • Meyerowitz EM (1994b) The genetics of flower development. Sci Am 271:40–47

    Google Scholar 

  • Miller HG, Kocher TD, Loy B (1995) New MADS box domains inAsparagus officinalis L. Sex Plant Reprod 8:318–320

    Article  Google Scholar 

  • Mizukami Y, Ma H (1995) Separation of AG function in floral meristem determinacy from that in reproductive organ identity by expressing antisenseAG RNA. Plant Mol Biol 28:767–784

    Article  CAS  PubMed  Google Scholar 

  • Mohun TJ, Chambers AE, Towers N, Taylor MV (1991) Expression of genes encoding the transcription factor SRF during early development ofXenopus laevis: identification of a CArG box-binding activity as SRF. EMBO J 10:933–940

    CAS  PubMed  Google Scholar 

  • Montag K, Salamini F, Thompson RD (1995)ZEMa, a member of a novel group of MADS box genes, is alternatively spliced in maize endosperm. Nucleic Acids Res 23:2168–2177

    CAS  PubMed  Google Scholar 

  • Norman C, Runswick M, Pollock R, Treisman R (1988) Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55:989–1003

    Article  CAS  PubMed  Google Scholar 

  • Nurrish SJ, Treisman R (1995) DNA binding specificity determinants in MADS-box transcription factors. Mol Cell Biol 15:4076–4085

    CAS  PubMed  Google Scholar 

  • Okada K, Shimura Y (1994) Genetic analyses of signalling in flower development usingArabidopsis. Plant Mol Biol 26:1357–1377

    Article  CAS  PubMed  Google Scholar 

  • Olson EN, Perry M, Schulz RA (1995) Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev Biol 172:2–14

    Article  CAS  PubMed  Google Scholar 

  • Pabo CO, Sauer RT (1992) Transcription factors: structural families and principles of DNA recognition. Annu Rev Biochem 61:1053–1095

    Article  CAS  PubMed  Google Scholar 

  • Passmore S, Maine GT, Elble R, Christ C, Tye B-K (1988)Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of MATα cells. J Mol Biol 204:593–606

    Article  CAS  PubMed  Google Scholar 

  • Pellegrini L, Tan S, Richmond TJ (1995) Structure of serum response factor core bound to DNA. Nature 376:490–498

    Article  CAS  PubMed  Google Scholar 

  • Pendleton JW, Nagai BK, Murtha MT, Ruddle FH (1993) Expansion of theHox gene family and the evolution of chordates. Proc Natl Acad Sci USA 90:6300–6304

    CAS  PubMed  Google Scholar 

  • Philippe H, Chenuil A, Adoutte A (1994) Can the Cambrian explosion be inferred through molecular phylogeny? Dev Suppl: 15–25

  • Pnueli L, Abu-Abeid M, Zamir D, Nacken W, Schwarz-Sommer Z, Lifschitz E (1991) The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes fromAntirrhinum andArabidopsis. Plant J 1:255–266

    CAS  PubMed  Google Scholar 

  • Pnueli L, Hareven D, Broday L, Hurwitz C, Lifschitz E (1994a) TheTM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6:175–186

    CAS  Google Scholar 

  • Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E (1994b) Isolation of the tomatoAGAMOUS geneTAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6:163–173

    CAS  Google Scholar 

  • Pollock R, Treisman R (1991) Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev 5: 2327–2341

    CAS  PubMed  Google Scholar 

  • Pu WT, Struhl K (1991) Highly conserved residues in the bZIP domain of yeast GCN4 are not essential for DNA binding. Mol Cell Biol 11:4918–4926

    CAS  PubMed  Google Scholar 

  • Purugganan MD, Wessler SR (1994) Molecular evolution of the plantR regulatory gene family. Genetics 138:849–854

    CAS  PubMed  Google Scholar 

  • Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140:345–356

    CAS  PubMed  Google Scholar 

  • Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) TheCONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–857

    Article  CAS  PubMed  Google Scholar 

  • Reiser L, Modrusan Z, Margossian L, Samach A, Ohad N, Haughn GW, Fischer RL (1995) TheBELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83:735–742

    Article  CAS  PubMed  Google Scholar 

  • Riley DE, Krieger JN (1995) Molecular and phylogenetic analysis of PCR-amplified cyclin-dependent kinase (CDK) family sequences from representatives of the earliest available lineages of eukaryotes. J Mol Evol 41:407–413

    Article  CAS  PubMed  Google Scholar 

  • Rounsley SD, Ditta GS, Yanofsky MF (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7:1259–1269

    Article  CAS  PubMed  Google Scholar 

  • Saedler H, Huijser P (1993) Molecular biology of flower development inAntirrhinum majus (snapdragon). Gene 135:239–243

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sakai H, Medrano LJ, Meyerowitz EM (1995) Role of SUPERMAN in maintainingArabidopsis floral whorl boundaries. Nature 378:199–203

    Article  CAS  PubMed  Google Scholar 

  • Savard L, Li P, Strauss SH, Chase MW, Michaud M], Bousquet J (1994) Chloroplast and nuclear gene sequences indicate Late Pennsylvania time for the last common ancestor of extant seed plants. Proc Natl Acad Sci 91:5163–5167

    CAS  PubMed  Google Scholar 

  • Savidge B, Rounsley SD, Yanofsky MF (1995) Temporal relationship between transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7:721–733

    Article  CAS  PubMed  Google Scholar 

  • Schena M, Davis RW (1994) Structure of homeobox-leucine zipper genes suggests a model for the evolution of gene families. Proc Natl Acad Sci USA 91:8393–8397

    CAS  PubMed  Google Scholar 

  • Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF (1993) Identification and molecular characterization ofZAG1, the maize homolog of the Arabidopsis floral homeotic geneAGAMOUS. Plant Cell 5:729–737

    Article  CAS  PubMed  Google Scholar 

  • Schubert FR, Nieselt-Struwe K, Gross P (1993) The Antennapedia-type homeobox genes have evolved from three precursors separated early in metazoan evolution. Proc Natl Acad Sci USA 90:143–147

    CAS  PubMed  Google Scholar 

  • Schughart K, Kappen C, Ruddle FH (1989) Duplication of large genomic regions during the evolution of vertebrate homeobox genes. Proc Natl Acad Sci USA 86:7067–7071

    CAS  PubMed  Google Scholar 

  • Schwarz-Sommer Z, Huijser P. Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes inAntirrhinum majus. Science 250:931–936

    CAS  Google Scholar 

  • Schwarz-Sommer Z, Hue I, Huijser P, Flor PJ, Hansen R, Tetens F, Lönnig W-E, Saedler H, Sommer H (1992) Characterization of theAntirrhinum floral homeotic MADS-box genedeficiens; evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J 11:251–263

    CAS  PubMed  Google Scholar 

  • Scott MP (1993) A rational nomenclature for vertebrate homeobox (HOX) genes. Nucleic Acids Res 21:1687–1688

    CAS  PubMed  Google Scholar 

  • Shiraishi H, Okada K, Shimura Y (1993) Nucleotide sequences recognized by the AGAMOUS MADS domain ofArabidopsis thaliana in vitro. Plant J 4:385–398

    Article  CAS  PubMed  Google Scholar 

  • Shore P, Sharrocks AD (1995) The MADS-box family of transcription factors. Eur J Biochem 229:1–13

    Article  CAS  PubMed  Google Scholar 

  • Sommer H, Beltrán J-P, Huijser P, Pape H, Lönnig W-E, Saedler H, Schwarz-Sommer Z (1990)Deficiens, a homeotic gene involved in the control of flower morphogenesis inAntirrhinum majus: the protein shows homology to transcription factors. EMBO J 9:605–613

    CAS  PubMed  Google Scholar 

  • Strauss SH, Rottmann WH, Brunner AM, Sheppard LA (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breeding 1:5–26

    CAS  Google Scholar 

  • Tandre K, Albert VA, Sundas A, Engström P (1995) Conifer homologues to genes that control floral development in angiosperms. Plant Mol Biol 27:69–78

    Article  CAS  PubMed  Google Scholar 

  • Theißen G, Saedler H (1995) MADS-box genes in plant ontogeny and phylogeny: Haeckel's ‘biogenefc law’ revisited. Curr Opin Genet Dev 5:628–639

    PubMed  Google Scholar 

  • Theißen G, Strater T, Fischer A, Saedler H (1995) Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs ofAGAMOUS-likeMADS-box genes from maize. Gene 156:155–166

    PubMed  Google Scholar 

  • Treisman R (1990) The SRE: a growth factor responsive transcriptional regulator. Semin Cancer Biol 1:47–58

    CAS  PubMed  Google Scholar 

  • Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig W-E, Saedler H, Sommer H, Schwarz-Sommer Z (1992)GLOBOSA: a homeotic gene which interacts withDEFICIENS in the control ofAntirrhinum floral organogenesis. EMBO J 11:4693–4704

    PubMed  Google Scholar 

  • Tsuchimoto S, van der Krol AR, Chua N-H (1993) Ectopic expression ofpMADS3 in transgenic petunia phenocopies the petuniablind mutant. Plant Cell 5:843–853

    Article  CAS  PubMed  Google Scholar 

  • van der Krol AR, Chua N-H (1993) Flower development in petunia. Plant Cell 5:1195–1203

    Google Scholar 

  • van der Krol AR, Brunelle A, Tsuchimoto S, Chua N-H (1993) Functional analysis of petunia floral homeotic MADS box genepMADS1. Genes Dev 7:1214–1228

    PubMed  Google Scholar 

  • Watanabe Y, Irie K, Matsumoto K (1995) YeastRLM1 encodes a serum response factor-like protein that may function downstream of the Mpkl (Slt2) mitogen-activated protein kinase pathway. Mol Cell Biol 15:5740–5749

    CAS  PubMed  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    Article  CAS  PubMed  Google Scholar 

  • Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992)LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859

    Article  CAS  PubMed  Google Scholar 

  • Wolfe KH, Gouy M, Yang Y-W, Sharp PM, Li W-H (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205

    CAS  PubMed  Google Scholar 

  • Wolffe AP (1994) Structural and functional properties of the evolutionary ancient Y-box family of nucleic acid binding proteins. Bioessays 16:245–251

    Article  CAS  PubMed  Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by theArabidopsis homeotic geneagamous resembles transcription factors. Nature 346:35–39

    Article  CAS  PubMed  Google Scholar 

  • Yu Y-T, Breitbart RE, Smoot LB, Youngsook L, Mahdavi V, Nadal-Ginard B (1992) Human myocyte-specific enhancer factor 2 comprises a group of tissue-restricted MADS box transcription factors. Genes Dev 6:1783–1798

    CAS  PubMed  Google Scholar 

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  1. Max-Planck-Institut für Züchtungsforschung, Abteilung Molekular Pflanzengenetik, Carl-von-Linné-Weg 10, D-50829, Köln, Germany

    Günter Theißen, Jan T. Kim & Heinz Saedler

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  1. Günter Theißen
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  2. Jan T. Kim
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  3. Heinz Saedler
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Correspondence to: G. Theißen

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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 43, 484–516 (1996). https://doi.org/10.1007/BF02337521

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