Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. 2004 Feb; 166(2): 1011–1023.
PMCID: PMC1470751

Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms.

Abstract

Members of the AGAMOUS (AG) subfamily of MIKC-type MADS-box genes appear to control the development of reproductive organs in both gymnosperms and angiosperms. To understand the evolution of this subfamily in the flowering plants, we have identified 26 new AG-like genes from 15 diverse angiosperm species. Phylogenetic analyses of these genes within a large data set of AG-like sequences show that ancient gene duplications were critical in shaping the evolution of the subfamily. Before the radiation of extant angiosperms, one event produced the ovule-specific D lineage and the well-characterized C lineage, whose members typically promote stamen and carpel identity as well as floral meristem determinacy. Subsequent duplications in the C lineage resulted in independent instances of paralog subfunctionalization and maintained functional redundancy. Most notably, the functional homologs AG from Arabidopsis and PLENA (PLE) from Antirrhinum are shown to be representatives of separate paralogous lineages rather than simple genetic orthologs. The multiple subfunctionalization events that have occurred in this subfamily highlight the potential for gene duplication to lead to dissociation among genetic modules, thereby allowing an increase in morphological diversity.

Full Text

The Full Text of this article is available as a PDF (772K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Alfaro Michael E, Zoller Stefan, Lutzoni François. Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol. 2003 Feb;20(2):255–266. [PubMed]
  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. [PMC free article] [PubMed]
  • Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, Ribas de Pouplana L, Martínez-Castilla L, Yanofsky MF. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci U S A. 2000 May 9;97(10):5328–5333. [PMC free article] [PubMed]
  • Angenent GC, Franken J, Busscher M, van Dijken A, van Went JL, Dons HJ, van Tunen AJ. A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell. 1995 Oct;7(10):1569–1582. [PMC free article] [PubMed]
  • Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000 Dec 14;408(6814):796–815. [PubMed]
  • Bowman JL, Smyth DR, Meyerowitz EM. Genes directing flower development in Arabidopsis. Plant Cell. 1989 Jan;1(1):37–52. [PMC free article] [PubMed]
  • Bowman JL, Smyth DR, Meyerowitz EM. Genetic interactions among floral homeotic genes of Arabidopsis. Development. 1991 May;112(1):1–20. [PubMed]
  • Bradley D, Carpenter R, Sommer H, Hartley N, Coen E. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell. 1993 Jan 15;72(1):85–95. [PubMed]
  • Brunner AM, Rottmann WH, Sheppard LA, Krutovskii K, DiFazio SP, Leonardi S, Strauss SH. Structure and expression of duplicate AGAMOUS orthologues in poplar. Plant Mol Biol. 2000 Nov;44(5):619–634. [PubMed]
  • Carpenter R, Coen ES. Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev. 1990 Sep;4(9):1483–1493. [PubMed]
  • Coen ES, Meyerowitz EM. The war of the whorls: genetic interactions controlling flower development. Nature. 1991 Sep 5;353(6339):31–37. [PubMed]
  • Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, van Tunen AJ. The petunia MADS box gene FBP11 determines ovule identity. Plant Cell. 1995 Nov;7(11):1859–1868. [PMC free article] [PubMed]
  • Davies B, Motte P, Keck E, Saedler H, Sommer H, Schwarz-Sommer Z. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J. 1999 Jul 15;18(14):4023–4034. [PMC free article] [PubMed]
  • Douady Christophe J, Delsuc Frédéric, Boucher Yan, Doolittle W Ford, Douzery Emmanuel J P. Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol Biol Evol. 2003 Feb;20(2):248–254. [PubMed]
  • 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 Oct 1;18(19):5370–5379. [PMC free article] [PubMed]
  • Favaro R, Immink RGH, Ferioli V, Bernasconi B, Byzova M, Angenent GC, Kater M, Colombo L. Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants. Mol Genet Genomics. 2002 Oct;268(2):152–159. [PubMed]
  • Favaro Rebecca, Pinyopich Anusak, Battaglia Raffaella, Kooiker Maarten, Borghi Lorenzo, Ditta Gary, Yanofsky Martin F, Kater Martin M, Colombo Lucia. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell. 2003 Nov;15(11):2603–2611. [PMC free article] [PubMed]
  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999 Apr;151(4):1531–1545. [PMC free article] [PubMed]
  • Gasser CS, Robinson-Beers K. Pistil Development. Plant Cell. 1993 Oct;5(10):1231–1239. [PMC free article] [PubMed]
  • Kyozuka Junko, Shimamoto Ko. Ectopic expression of OsMADS3, a rice ortholog of AGAMOUS, caused a homeotic transformation of lodicules to stamens in transgenic rice plants. Plant Cell Physiol. 2002 Jan;43(1):130–135. [PubMed]
  • Gaut BS, Doebley JF. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6809–6814. [PMC free article] [PubMed]
  • Lamb Rebecca S, Hill Theresa A, Tan Queenie K-G, Irish Vivian F. Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development. 2002 May;129(9):2079–2086. [PubMed]
  • Gustafson-Brown C, Savidge B, Yanofsky MF. Regulation of the arabidopsis floral homeotic gene APETALA1. Cell. 1994 Jan 14;76(1):131–143. [PubMed]
  • Lee MM, Schiefelbein J. Developmentally distinct MYB genes encode functionally equivalent proteins in Arabidopsis. Development. 2001 May;128(9):1539–1546. [PubMed]
  • Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature. 2000 Apr 13;404(6779):766–770. [PubMed]
  • Hasebe M, Wen CK, Kato M, Banks JA. Characterization of MADS homeotic genes in the fern Ceratopteris richardii. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6222–6227. [PMC free article] [PubMed]
  • Litt Amy, Irish Vivian F. Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics. 2003 Oct;165(2):821–833. [PMC free article] [PubMed]
  • Henschel Katrin, Kofuji Rumiko, Hasebe Mitsuyasu, Saedler Heinz, Münster Thomas, Theissen Günter. Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol Biol Evol. 2002 Jun;19(6):801–814. [PubMed]
  • Lopez-Dee ZP, Wittich P, Enrico Pè M, Rigola D, Del Buono I, Gorla MS, Kater MM, Colombo L. OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev Genet. 1999 Sep;25(3):237–244. [PubMed]
  • Honma T, Goto K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature. 2001 Jan 25;409(6819):525–529. [PubMed]
  • Lynch M, Force A. The probability of duplicate gene preservation by subfunctionalization. Genetics. 2000 Jan;154(1):459–473. [PMC free article] [PubMed]
  • Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001 Aug;17(8):754–755. [PubMed]
  • Ma H, Yanofsky MF, Meyerowitz EM. AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 1991 Mar;5(3):484–495. [PubMed]
  • Hughes AL. The evolution of functionally novel proteins after gene duplication. Proc Biol Sci. 1994 May 23;256(1346):119–124. [PubMed]
  • Hughes MK, Hughes AL. Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. Mol Biol Evol. 1993 Nov;10(6):1360–1369. [PubMed]
  • Mandel MA, Bowman JL, Kempin SA, Ma H, Meyerowitz EM, Yanofsky MF. Manipulation of flower structure in transgenic tobacco. Cell. 1992 Oct 2;71(1):133–143. [PubMed]
  • Jager Muriel, Hassanin Alexandre, Manuel Michael, Le Guyader Hervé, Deutsch Jean. MADS-box genes in Ginkgo biloba and the evolution of the AGAMOUS family. Mol Biol Evol. 2003 May;20(5):842–854. [PubMed]
  • Mena M, Ambrose BA, Meeley RB, Briggs SP, Yanofsky MF, Schmidt RJ. Diversification of C-function activity in maize flower development. Science. 1996 Nov 29;274(5292):1537–1540. [PubMed]
  • Johansen Bo, Pedersen Louise B, Skipper Martin, Frederiksen Signe. MADS-box gene evolution-structure and transcription patterns. Mol Phylogenet Evol. 2002 Jun;23(3):458–480. [PubMed]
  • Mizukami Y, Ma H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell. 1992 Oct 2;71(1):119–131. [PubMed]
  • Kang HG, Noh YS, Chung YY, Costa MA, An K, An G. Phenotypic alterations of petal and sepal by ectopic expression of a rice MADS box gene in tobacco. Plant Mol Biol. 1995 Oct;29(1):1–10. [PubMed]
  • Mizukami Y, Huang H, Tudor M, Hu Y, Ma H. Functional domains of the floral regulator AGAMOUS: characterization of the DNA binding domain and analysis of dominant negative mutations. Plant Cell. 1996 May;8(5):831–845. [PMC free article] [PubMed]
  • Kang HG, Jeon JS, Lee S, An G. Identification of class B and class C floral organ identity genes from rice plants. Plant Mol Biol. 1998 Dec;38(6):1021–1029. [PubMed]
  • Münster T, Pahnke J, Di Rosa A, Kim JT, Martin W, Saedler H, Theissen G. Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2415–2420. [PMC free article] [PubMed]
  • Kapoor Meenu, Tsuda Shinzo, Tanaka Yoshikazu, Mayama Tomoko, Okuyama Yohei, Tsuchimoto Suguru, Takatsuji Hiroshi. Role of petunia pMADS3 in determination of floral organ and meristem identity, as revealed by its loss of function. Plant J. 2002 Oct;32(1):115–127. [PubMed]
  • Kater MM, Colombo L, Franken J, Busscher M, Masiero S, Van Lookeren Campagne MM, Angenent GC. Multiple AGAMOUS homologs from cucumber and petunia differ in their ability to induce reproductive organ fate. Plant Cell. 1998 Feb;10(2):171–182. [PMC free article] [PubMed]
  • Muse SV, Gaut BS. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol Biol Evol. 1994 Sep;11(5):715–724. [PubMed]
  • Kempin SA, Mandel MA, Yanofsky MF. Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiol. 1993 Dec;103(4):1041–1046. [PMC free article] [PubMed]
  • Nagasawa Nobuhiro, Miyoshi Masahiro, Sano Yoshio, Satoh Hikaru, Hirano Hiroyuki, Sakai Hajime, Nagato Yasuo. SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development. 2003 Feb;130(4):705–718. [PubMed]
  • Kishino H, Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol. 1989 Aug;29(2):170–179. [PubMed]
  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature. 2000 May 11;405(6783):200–203. [PubMed]
  • Perl-Treves R, Kahana A, Rosenman N, Xiang Y, Silberstein L. Expression of multiple AGAMOUS-like genes in male and female flowers of cucumber (Cucumis sativus L.). Plant Cell Physiol. 1998 Jul;39(7):701–710. [PubMed]
  • Kramer EM, Dorit RL, Irish VF. Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics. 1998 Jun;149(2):765–783. [PMC free article] [PubMed]
  • Pinyopich Anusak, Ditta Gary S, Savidge Beth, Liljegren Sarah J, Baumann Elvira, Wisman Ellen, Yanofsky Martin F. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature. 2003 Jul 3;424(6944):85–88. [PubMed]
  • Krizek BA, Meyerowitz EM. Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4063–4070. [PMC free article] [PubMed]
  • Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E. Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell. 1994 Feb;6(2):163–173. [PMC free article] [PubMed]
  • Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. [PubMed]
  • Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF. Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics. 1995 May;140(1):345–356. [PMC free article] [PubMed]
  • Theissen G. Plant biology. Shattering developments. Nature. 2000 Apr 13;404(6779):711–713. [PubMed]
  • Theissen G, Saedler H. Plant biology. Floral quartets. Nature. 2001 Jan 25;409(6819):469–471. [PubMed]
  • Qiu YL, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature. 1999 Nov 25;402(6760):404–407. [PubMed]
  • Theissen G, Strater T, Fischer A, Saedler H. Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of AGAMOUS-like MADS-box genes from maize. Gene. 1995 Apr 24;156(2):155–166. [PubMed]
  • Theissen G, Kim JT, 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 Nov;43(5):484–516. [PubMed]
  • Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, Saedler H. A short history of MADS-box genes in plants. Plant Mol Biol. 2000 Jan;42(1):115–149. [PubMed]
  • Rutledge R, Regan S, Nicolas O, Fobert P, Côté C, Bosnich W, Kauffeldt C, Sunohara G, Séguin A, Stewart D. Characterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis. Plant J. 1998 Sep;15(5):625–634. [PubMed]
  • Savidge B, Rounsley SD, Yanofsky MF. Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell. 1995 Jun;7(6):721–733. [PMC free article] [PubMed]
  • Tzeng Tsai-Yu, Chen Hsing-Yu, Yang Chang-Hsien. Ectopic expression of carpel-specific MADS box genes from lily and lisianthus causes similar homeotic conversion of sepal and petal in Arabidopsis. Plant Physiol. 2002 Dec;130(4):1827–1836. [PMC free article] [PubMed]
  • Schmidt RJ, Ambrose BA. The blooming of grass flower development. Curr Opin Plant Biol. 1998 Feb;1(1):60–67. [PubMed]
  • Vandenbussche Michiel, Theissen Günter, Van de Peer Yves, Gerats Tom. Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acids Res. 2003 Aug 1;31(15):4401–4409. [PMC free article] [PubMed]
  • 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):729–737. [PMC free article] [PubMed]
  • Shore P, Sharrocks AD. The MADS-box family of transcription factors. Eur J Biochem. 1995 Apr 1;229(1):1–13. [PubMed]
  • Skaer Nick, Pistillo Daniela, Gibert Jean-Michel, Lio Pietro, Wülbeck Corinna, Simpson Pat. Gene duplication at the achaete-scute complex and morphological complexity of the peripheral nervous system in Diptera. Trends Genet. 2002 Aug;18(8):399–405. [PubMed]
  • Winter KU, Becker A, Münster T, Kim JT, Saedler H, Theissen G. MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7342–7347. [PMC free article] [PubMed]
  • Yang AS. Modularity, evolvability, and adaptive radiations: a comparison of the hemi- and holometabolous insects. Evol Dev. 2001 Mar-Apr;3(2):59–72. [PubMed]
  • Suzuki Yoshiyuki, Glazko Galina V, Nei Masatoshi. Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16138–16143. [PMC free article] [PubMed]
  • Yang Yingzhen, Fanning Laura, Jack Thomas. The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J. 2003 Jan;33(1):47–59. [PubMed]
  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature. 1990 Jul 5;346(6279):35–39. [PubMed]
  • Yu D, Kotilainen M, Pöllänen E, Mehto M, Elomaa P, Helariutta Y, Albert VA, Teeri TH. Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae) Plant J. 1999 Jan;17(1):51–62. [PubMed]
  • Zanis Michael J, Soltis Douglas E, Soltis Pamela S, Mathews Sarah, Donoghue Michael J. The root of the angiosperms revisited. Proc Natl Acad Sci U S A. 2002 May 14;99(10):6848–6853. [PMC free article] [PubMed]
  • Tandre K, Albert VA, Sundås A, Engström P. Conifer homologues to genes that control floral development in angiosperms. Plant Mol Biol. 1995 Jan;27(1):69–78. [PubMed]
  • Tandre K, Svenson M, Svensson ME, Engström P. Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J. 1998 Sep;15(5):615–623. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...