The development of multicellular eukaryotes, according to their body plan, is often directed by members of multigene families that encode transcription factors. MADS (for MINICHROMOSOME MAINTENANCE1, AGAMOUS, DEFICIENS and SERUM RESPONSE FACTOR)-box genes form one of those families controlling nearly all major aspects of plant development. Knowing the complete complement of MADS-box genes in sequenced plant genomes will allow a better understanding of the evolutionary patterns of these genes and the association of their evolution with the evolution of plant morphologies. Here, we have applied a combination of automatic and manual annotations to identify the complete set of MADS-box genes in 17 plant genomes. Furthermore, three plant genomes were reanalyzed and published datasets were used for four genomes such that more than 2,600 genes from?24 species were classified into the two types of MADS-box genes, Type I and Type II. Our results extend previous studies, highlighting the remarkably different evolutionary patterns of Type I and Type II genes and provide a basis for further studies on the evolution and function of MADS-box genes.
References
[1]
Gramzow, L.; Ritz, M.S.; Theissen, G. On the origin of MADS-domain transcription factors. Trends Genet. 2010, 26, 149–153, doi:10.1016/j.tig.2010.01.004.
[2]
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, 29, 464–489, doi:10.1016/S1055-7903(03)00207-0.
[3]
Messenguy, F.; Dubois, E. Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 2003, 316, 1–21, doi:10.1016/S0378-1119(03)00747-9.
[4]
Schwarz-Sommer, Z.; Huijser, P.; Nacken, W.; Saedler, H.; Sommer, H. Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 1990, 250, 931–936.
[5]
Theissen, G.; Becker, A.; di Rosa, A.; Kanno, A.; Kim, J.T.; Munster, T.; Winter, K.U.; Saedler, H. A short history of MADS-box genes in plants. Plant Mol. Biol. 2000, 42, 115–149, doi:10.1023/A:1006332105728.
[6]
Gramzow, L.; Barker, E.; Schulz, C.; Ambrose, B.; Ashton, N.; Theissen, G.; Litt, A. Selaginella Genome Analysis—Entering the “Homoplasy Heaven” of the MADS World. Front. Plant Sci. 2012, 3, 214.
[7]
Gramzow, L.; Theissen, G. A hitchhiker’s guide to the MADS world of plants. Genome Biol. 2010, 11, 214, doi:10.1186/gb-2010-11-6-214.
[8]
Arora, R.; Agarwal, P.; Ray, S.; Singh, A.K.; Singh, V.P.; Tyagi, A.K.; Kapoor, S. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 2007, 8, 242, doi:10.1186/1471-2164-8-242.
[9]
Parenicova, L.; de Folter, S.; Kieffer, M.; Horner, D.S.; Favalli, C.; Busscher, J.; Cook, H.E.; Ingram, R.M.; Kater, M.M.; Davies, B.; et al. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 2003, 15, 1538–1551, doi:10.1105/tpc.011544.
[10]
Alvarez-Buylla, E.R.; Pelaz, S.; Liljegren, S.J.; Gold, S.E.; Burgeff, C.; Ditta, G.S.; de Pouplana, L.R.; Martinez-Castilla, L.; Yanofsky, M.F. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl. Acad. Sci. USA 2000, 97, 5328–5333, doi:10.1073/pnas.97.10.5328.
[11]
Henschel, K.; Kofuji, R.; Hasebe, M.; Saedler, H.; Munster, T.; Theissen, G. Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol. Biol. Evol. 2002, 19, 801–814, doi:10.1093/oxfordjournals.molbev.a004137.
[12]
Bemer, M.; Wolters-Arts, M.; Grossniklaus, U.; Angenent, G.C. The MADS domain protein DIANA acts together with AGAMOUS-LIKE80 to specify the central cell in Arabidopsis ovules. Plant Cell 2008, 20, 2088–2101, doi:10.1105/tpc.108.058958.
[13]
Colombo, M.; Masiero, S.; Vanzulli, S.; Lardelli, P.; Kater, M.M.; Colombo, L. AGL23, a type I MADS-box gene that controls female gametophyte and embryo development in Arabidopsis. Plant J. 2008, 54, 1037–1048, doi:10.1111/j.1365-313X.2008.03485.x.
[14]
Kang, I.H.; Steffen, J.G.; Portereiko, M.F.; Lloyd, A.; Drews, G.N. The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 2008, 20, 635–647, doi:10.1105/tpc.107.055137.
[15]
Steffen, J.G.; Kang, I.H.; Portereiko, M.F.; Lloyd, A.; Drews, G.N. AGL61 interacts with AGL80 and is required for central cell development in Arabidopsis. Plant Physiol. 2008, 148, 259–268, doi:10.1104/pp.108.119404.
[16]
Mandel, M.A.; Gustafson-Brown, C.; Savidge, B.; Yanofsky, M.F. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 1992, 360, 273–277, doi:10.1038/360273a0.
[17]
Pelaz, S.; Tapia-Lopez, R.; Alvarez-Buylla, E.R.; Yanofsky, M.F. Conversion of leaves into petals in Arabidopsis. Curr. Biol. 2001, 11, 182–184.
[18]
Trobner, W.; Ramirez, L.; Motte, P.; Hue, I.; Huijser, P.; Lonnig, W.E.; Saedler, H.; Sommer, H.; Schwarz-Sommer, Z. GLOBOSA—A homeotic gene which interacts with DEFICIENS in the control of antirrhinum floral organogenesis. EMBO J. 1992, 11, 4693–4704.
[19]
Yanofsky, M.F.; Ma, H.; Bowman, J.L.; Drews, G.N.; Feldmann, K.A.; Meyerowitz, E.M. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 1990, 346, 35–39, doi:10.1038/346035a0.
[20]
Theissen, G.; Kim, J.T.; Saedler, H. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol. 1996, 43, 484–516, doi:10.1007/BF02337521.
[21]
Leseberg, C.H.; Li, A.; Kang, H.; Duvall, M.; Mao, L. Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene 2006, 378, 84–94, doi:10.1016/j.gene.2006.05.022.
[22]
Barker, E.I.; Ashton, N.W. A parsimonious model of lineage-specific expansion of MADS-box genes in Physcomitrella patens. Plant Cell Rep. 2013, 32, 1161–1177, doi:10.1007/s00299-013-1411-8.
[23]
Shu, Y.; Yu, D.; Wang, D.; Guo, D.; Guo, C. Genome-wide survey and expression analysis of the MADS-box gene family in soybean. Mol. Biol. Rep. 2013, 40, 3901–3911, doi:10.1007/s11033-012-2438-6.
[24]
Hu, L.; Liu, S. Genome-wide analysis of the MADS-box gene family in cucumber. Genome 2012, 55, 245–256, doi:10.1139/g2012-009.
Majoros, W.H.; Pertea, M.; Salzberg, S.L. TigrScan and GlimmerHMM: Two open source ab initio eukaryotic gene-finders. Bioinformatics 2004, 20, 2878–2879, doi:10.1093/bioinformatics/bth315.
[28]
Nam, J.; Kim, J.; Lee, S.; An, G.; Ma, H.; Nei, M. Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms. Proc. Natl. Acad. Sci. USA 2004, 101, 1910–1915, doi:10.1073/pnas.0308430100.
[29]
Phytozome. Available online: http://www.phytozome.net (accessed on 29 April 2013).
[30]
Marchler-Bauer, A.; Anderson, J.B.; Derbyshire, M.K.; DeWeese-Scott, C.; Gonzales, N.R.; Gwadz, M.; Hao, L.N.; He, S.Q.; Hurwitz, D.I.; Jackson, J.D.; et al. CDD: A conserved domain database for interactive domain family analysis. Nucleic Acids Res. 2007, 35, D237–D240, doi:10.1093/nar/gkl951.
[31]
Salamov, A.A.; Solovyev, V.V. Ab initio gene finding in Drosophila genomic DNA. Genome Res. 2000, 10, 516–522, doi:10.1101/gr.10.4.516.
[32]
Chenna, R.; Sugawara, H.; Koike, T.; Lopez, R.; Gibson, T.J.; Higgins, D.G.; Thompson, J.D. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003, 31, 3497–3500, doi:10.1093/nar/gkg500.
[33]
Katoh, K.; Misawa, K.; Kuma, K.; Miyata, T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30, 3059–3066, doi:10.1093/nar/gkf436.
[34]
Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22, 2688–2690, doi:10.1093/bioinformatics/btl446.
[35]
Ming, R.; Hou, S.; Feng, Y.; Yu, Q.; Dionne-Laporte, A.; Saw, J.H.; Senin, P.; Wang, W.; Ly, B.V.; Lewis, K.L.; et al. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 2008, 452, 991–996, doi:10.1038/nature06856.
[36]
Prochnik, S.; Marri, P.R.; Desany, B.; Rabinowicz, P.D.; Kodira, C.; Mohiuddin, M.; Rodriguez, F.; Fauquet, C.; Tohme, J.; Harkins, T.; et al. The Cassava Genome: Current Progress, Future Directions. Trop. Plant Biol. 2012, 5, 88–94, doi:10.1007/s12042-011-9088-z.
[37]
Chan, A.P.; Crabtree, J.; Zhao, Q.; Lorenzi, H.; Orvis, J.; Puiu, D.; Melake-Berhan, A.; Jones, K.M.; Redman, J.; Chen, G.; et al. Draft genome sequence of the oilseed species Ricinus communis. Nat. Biotechnol. 2010, 28, 951–956, doi:10.1038/nbt.1674.
[38]
Wang, Z.; Hobson, N.; Galindo, L.; Zhu, S.; Shi, D.; McDill, J.; Yang, L.; Hawkins, S.; Neutelings, G.; Datla, R.; et al. The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. Plant J. 2012, 72, 461–473, doi:10.1111/j.1365-313X.2012.05093.x.
[39]
Tuskan, G.A.; Difazio, S.; Jansson, S.; Bohlmann, J.; Grigoriev, I.; Hellsten, U.; Putnam, N.; Ralph, S.; Rombauts, S.; Salamov, A.; et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313, 1596–1604, doi:10.1126/science.1128691.
[40]
Cannon, S.B.; Sterck, L.; Rombauts, S.; Sato, S.; Cheung, F.; Gouzy, J.; Wang, X.; Mudge, J.; Vasdewani, J.; Schiex, T.; et al. Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proc. Natl. Acad. Sci. USA 2006, 103, 14959–14964, doi:10.1073/pnas.0603228103.
Huang, S.; Li, R.; Zhang, Z.; Li, L.; Gu, X.; Fan, W.; Lucas, W.J.; Wang, X.; Xie, B.; Ni, P.; et al. The genome of the cucumber, Cucumis sativus L. Nat. Genet. 2009, 41, 1275–1281, doi:10.1038/ng.475.
[43]
Verde, I.; Abbott, A.G.; Scalabrin, S.; Jung, S.; Shu, S.; Marroni, F.; Zhebentyayeva, T.; Dettori, M.T.; Grimwood, J.; Cattonaro, F.; et al. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat. Genet. 2013, 45, 487–494, doi:10.1038/ng.2586.
[44]
Velasco, R.; Zharkikh, A.; Affourtit, J.; Dhingra, A.; Cestaro, A.; Kalyanaraman, A.; Fontana, P.; Bhatnagar, S.K.; Troggio, M.; Pruss, D.; et al. The genome of the domesticated apple (Malus x domestica Borkh.). Nat. Genet. 2010, 42, 833–839, doi:10.1038/ng.654.
[45]
The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408, 796–815, doi:10.1038/35048692.
[46]
Hu, T.T.; Pattyn, P.; Bakker, E.G.; Cao, J.; Cheng, J.F.; Clark, R.M.; Fahlgren, N.; Fawcett, J.A.; Grimwood, J.; Gundlach, H.; et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 2011, 43, 476–481, doi:10.1038/ng.807.
Zhang, G.; Liu, X.; Quan, Z.; Cheng, S.; Xu, X.; Pan, S.; Xie, M.; Zeng, P.; Yue, Z.; Wang, W.; et al. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat. Biotechnol. 2012, 30, 549–554, doi:10.1038/nbt.2195.
[54]
Goff, S.A.; Ricke, D.; Lan, T.H.; Presting, G.; Wang, R.L.; Dunn, M.; Glazebrook, J.; Sessions, A.; Oeller, P.; Varma, H.; et al. A draft sequence of the rice genome (Oryza sativa L. ssp japonica). Science 2000, 296, 92–100.
[55]
International Brachypodium Initiative. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 2010, 463, 763–768, doi:10.1038/nature08747.
[56]
D'Hont, A.; Denoeud, F.; Aury, J.M.; Baurens, F.C.; Carreel, F.; Garsmeur, O.; Noel, B.; Bocs, S.; Droc, G.; Rouard, M.; et al. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 2012, 488, 213–217, doi:10.1038/nature11241.
[57]
Banks, J.A.; Nishiyama, T.; Hasebe, M.; Bowman, J.L.; Gribskov, M.; dePamphilis, C.; Albert, V.A.; Aono, N.; Aoyama, T.; Ambrose, B.A.; et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 2011, 332, 960–963, doi:10.1126/science.1203810.
[58]
Rensing, S.A.; Lang, D.; Zimmer, A.D.; Terry, A.; Salamov, A.; Shapiro, H.; Nishiyama, T.; Perroud, P.F.; Lindquist, E.A.; Kamisugi, Y.; et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 2008, 319, 64–69, doi:10.1126/science.1150646.
[59]
Fawcett, J.A.; Maere, S.; van de Peer, Y. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl. Acad. Sci. USA 2009, 106, 5737–5742, doi:10.1073/pnas.0900906106.
[60]
Koch, M.A.; Haubold, B.; Mitchell-Olds, T. Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 2000, 17, 1483–1498, doi:10.1093/oxfordjournals.molbev.a026248.
Freeling, M. Bias in plant gene content following different sorts of duplication: Tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 2009, 60, 433–453, doi:10.1146/annurev.arplant.043008.092122.
[63]
Edger, P.P.; Pires, J.C. Gene and genome duplications: The impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res. 2009, 17, 699–717, doi:10.1007/s10577-009-9055-9.
[64]
Melzer, R.; Theissen, G. Reconstitution of 'floral quartets’ in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Res. 2009, 37, 2723–2736, doi:10.1093/nar/gkp129.
[65]
De Folter, S.; Immink, R.G.; Kieffer, M.; Parenicova, L.; Henz, S.R.; Weigel, D.; Busscher, M.; Kooiker, M.; Colombo, L.; Kater, M.M.; et al. Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 2005, 17, 1424–1433, doi:10.1105/tpc.105.031831.
[66]
Kaufmann, K.; Melzer, R.; Theissen, G. MIKC-type MADS-domain proteins: Structural modularity, protein interactions and network evolution in land plants. Gene 2005, 347, 183–198, doi:10.1016/j.gene.2004.12.014.
[67]
Freeling, M.; Lyons, E.; Pedersen, B.; Alam, M.; Ming, R.; Lisch, D. Many or most genes in Arabidopsis transposed after the origin of the order Brassicales. Genome Res. 2008, 18, 1924–1937, doi:10.1101/gr.081026.108.
[68]
Masiero, S.; Colombo, L.; Grini, P.E.; Schnittger, A.; Kater, M.M. The emerging importance of type I MADS box transcription factors for plant reproduction. Plant Cell 2011, 23, 865–872, doi:10.1105/tpc.110.081737.
[69]
Walia, H.; Josefsson, C.; Dilkes, B.; Kirkbride, R.; Harada, J.; Comai, L. Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility. Curr. Biol. 2009, 19, 1128–1132, doi:10.1016/j.cub.2009.05.068.
[70]
De Bodt, S.; Raes, J.; Van de Peer, Y.; Theissen, G. And then there were many: MADS goes genomic. Trends Plant Sci. 2003, 8, 475–483, doi:10.1016/j.tplants.2003.09.006.
[71]
Wang, Y.; Wang, X.; Tang, H.; Tan, X.; Ficklin, S.P.; Feltus, F.A.; Paterson, A.H. Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLoS One 2011, 6, e28150.