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Molecular aspects of flower development in grasses

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Abstract

The grass family (Poaceae) of the monocotyledons includes about 10,000 species and represents one of the most important taxa among angiosperms. Their flower morphology is remarkably different from those of other monocotyledons and higher eudicots. The peculiar floral structure of grasses is the floret, which contains carpels and stamens, like eudicots, but lacks petals and sepals. The reproductive organs are surrounded by two lodicules, which correspond to eudicot petals, and by a palea and lemma, whose correspondence to eudicot organs remains controversial. The molecular and genetic analysis of floral morphogenesis and organ specification, primarily performed in eudicot model species, led to the ABCDE model of flower development. Several genes required for floral development in grasses correspond to class A, B, C, D, and E genes of eudicots, but others appear to have unique and diversified functions. In this paper, we outline the present knowledge on the evolution and diversification of grass genes encoding MIKC-type MADS-box transcription factors, based on information derived from studies in rice, maize, and wheat. Moreover, we review recent advances in studying the genes involved in the control of flower development and the extent of structural and functional conservation of these genes between grasses and eudicots.

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References

  • Agrawal GK, Abe K, Yamazaki M, Miyao A, Hirochika H (2005) Conservation of E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-of-function mutants of the OsMADS1 gene. Plant Mol Biol 59:125–135

    Article  PubMed  CAS  Google Scholar 

  • Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analysis of the Silky1 gene reveals conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569–579

    Article  PubMed  CAS  Google Scholar 

  • Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:24

    Article  CAS  Google Scholar 

  • Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489

    Article  PubMed  CAS  Google Scholar 

  • Bell CD, Soltis DE, Soltis PS (2005) The age of the angiosperms: a molecular timescale without a clock. Evolution 59:1245–1258

    PubMed  CAS  Google Scholar 

  • Bell CD, Soltis DE, Soltis PS (2010) The age and diversification of the angiosperms re-revisited. Am J Bot 97:1296–1303

    Article  PubMed  Google Scholar 

  • Bertioli DJ, Moretzsohn MC, Madsen LH, Sandal N, Leal-Bertioli SCM, Guimaraes PM, Hougaard BK, Fredslund J, Schauser L, Nielsen AM, Sato S, Tabata S, Cannon SB, Stougaard J (2009) An analysis of Arachis with Lotus and Medicago sheds new light on the structure, stability and evolution of legume genomes. BMC Genomics 10:45

    Article  PubMed  CAS  Google Scholar 

  • Bolot S, Abrouk M, Masood-Quraishi U, Stein N, Messing J, Feuillet C, Salse J (2009) The “inner circle” of the cereal genomes. Curr Opin Plant Biol 12:119–125

    Article  PubMed  CAS  Google Scholar 

  • Bommert P, Satoh-Nagasawa N, Jackson D, Hirano HY (2005) Genetics and evolution of inflorescence and flower development in grasses. Plant Cell Physiol 46:69–78

    Article  PubMed  CAS  Google Scholar 

  • Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438

    Article  PubMed  CAS  Google Scholar 

  • Bowman JL, Smyth DR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387–2396

    PubMed  CAS  Google Scholar 

  • Bowman JL, Sakai H, Jack T, Weigel D, Mayer U, Meyerowitz EM (1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114:599–615

    PubMed  CAS  Google Scholar 

  • Bremer K (2002) Gondwanan evolution of the grass alliance of families (Poales). Evolution 56:1374–1387

    PubMed  CAS  Google Scholar 

  • Cacharrón J, Saedler H, Theissen G (1999) Expression of MADS box genes ZMM8 and ZMM14 during inflorescence development of Zea mays discriminates between the upper and the lower floret of each spikelet. Dev Genes Evol 209:411–420

    Article  Google Scholar 

  • Causier B, Schwarz-Sommer Z, Davies B (2010) Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 21:73–79

    Article  PubMed  CAS  Google Scholar 

  • Chung YY, Kim SR, 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

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  PubMed  CAS  Google Scholar 

  • Columbus JT (1999) An expanded circumscription of Bouteloma (Gramineae: Chloridoideae): new combinations and names. Aliso 18:61–65

    Google Scholar 

  • Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, dePamphilis CW (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749

    Article  PubMed  CAS  Google Scholar 

  • Cui R, Han J, Zhao S, Su K, Wu F, Du X, Xu Q, Chong K, Theissen G, Meng Z (2010) Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). Plant J 61:767–781

    Article  PubMed  CAS  Google Scholar 

  • de Martino G, Pan I, Emmanuel E, Levy A, Irish VF (2006) Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18:1833–1845

    Article  PubMed  CAS  Google Scholar 

  • Dinneny JR, Yadegari R, Fischer RL, Yanofsky MF, Weigel D (2004) The role of JAGGED in shaping lateral organs. Development 131:1101–1110

    Article  PubMed  CAS  Google Scholar 

  • Dinneny JR, Weigel D, Yanofsky MF (2006) NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis. Development 133:1645–1655

    Article  PubMed  CAS  Google Scholar 

  • Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940

    Article  PubMed  CAS  Google Scholar 

  • Doust A (2007) Architectural evolution and its implications for domestication in grasses. Ann Bot 100:941–950

    Article  PubMed  Google Scholar 

  • Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk PB, An G, Colombo L, Kater MM (2007) The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant J 52:690–699

    Article  PubMed  CAS  Google Scholar 

  • Dreni L, Pilatone A, Yun D, Erreni S, Pajoro A, Caporali E, Zhang D, Kater MM (2011) Functional analysis of all AGAMOUS subfamily members in rice reveals their roles in reproductive organ identity determination and meristem determinacy. Plant Cell. doi:10.1105/tpc.111.087007

  • Dwivedi S, Perotti E, Ortiz R (2008) Towards molecular breeding of reproductive traits in cereal crops. Plant Biotech J 6:529–559

    Article  CAS  Google Scholar 

  • Favaro R, Immink R, Ferioli V, Bernasconi B, Byzova M, Angenent G, Kater M, Colombo L (2002) Ovule-specific MADS-box proteins have conserved protein–protein interactions in monocot and dicot plants. Mol Genet Genomics 268:152–159

    Article  PubMed  CAS  Google Scholar 

  • Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15:2603–2611

    Article  PubMed  CAS  Google Scholar 

  • Fawcett JA, Maere S, Van de Peer Y (2009) Plants with double genomes might have had a better chance to survive the cretaceous- tertiary extinction event. Proc Natl Acad Sci USA 106:5737–5742

    Article  PubMed  CAS  Google Scholar 

  • Ferrario S, Immink RG, Shchennikova A, Busscher-Lange J, Angenent GC (2003) The MADS box gene FBP2 is required for SEPALLATA function in Petunia. Plant Cell 15:914–925

    Article  PubMed  CAS  Google Scholar 

  • Ferrario S, Immink RG, Angenent GC (2004) Conservation and diversity in flower land. Curr Opin Plant Biol 7:84–91

    Article  PubMed  Google Scholar 

  • Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Zool 19:99–113

    Article  PubMed  CAS  Google Scholar 

  • Fladung M, Bossinger G, Roeb GW, Salamini F (1991) Correlated alterations in leaf and flower morphology and rate of leaf photosynthesis in a midribless (mbl) mutant of Panicum maximum Jacq. Planta 184:356–361

    Article  Google Scholar 

  • Fornara F, Parenicova L, Falasca G, Pelucchi N, Masiero S, Ciannamea S, Lopez-Dee Z, Altamura MM, Colombo L, Kater MM (2004) Functional characterization of OsMADS18, a member of AP1/SQUA subfamily of MADS box genes. Plant Physiol 135:2207–2219

    Article  PubMed  CAS  Google Scholar 

  • Fourquin C, Vinauger-Douard M, Fogliani B, Dumas C, Scutt CP (2005) Evidence that CRABS CLAW and TOUSLED have conserved their role in carpel development since the ancestor of the extant angiosperms. Proc Natl Acad Sci USA 102:4649–4654

    Article  PubMed  CAS  Google Scholar 

  • Fu D, Szucs P, Yan L, Helguera M, Skinner JS, von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletion within the first intron VRN-1 are associated with spring growth habit in barley and wheat. Mol Genet Genomics 273:54–65

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Liang W, Yin C, Ji S, Wang H, Su X, Guo C, Kong H, Xue H, Zhang D (2010) The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development. Plant Physiol 153:728–740

    Article  PubMed  CAS  Google Scholar 

  • Gaut BS (2001) Patterns of chromosomal duplication in maize and their implications for comparative maps of the grasses. Genome Res 11:55–66

    Article  PubMed  CAS  Google Scholar 

  • Gaut BS, Doebley JF (1997) DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci USA 94:6809–6814

    Article  PubMed  CAS  Google Scholar 

  • Goff S, Ricke D, Lan T, Presting G, Wang R, Dunn M et al (2002) A draft sequene of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  PubMed  CAS  Google Scholar 

  • Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1556

    Article  PubMed  CAS  Google Scholar 

  • GrassPhylogenyWorking Group (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Missouri Bot Gard 88:373–457

    Article  Google Scholar 

  • Gu Q, Ferrandiz C, Yanofsky MF, Matienssen R (1998) The FRUITFULL MADS-box gene mediates cell differenziation during Arabidopsis fruit development. Development 125:1509–1517

    PubMed  CAS  Google Scholar 

  • Hama E, Takumi S, Ogihara Y, Murai K (2004) Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218:712–720

    Article  PubMed  CAS  Google Scholar 

  • Hay RKM, Ellis RP (1998) The control of flowering in wheat and barley: what recent advances in molecular genetics can reveal. Ann Bot 82:541–554

    Article  CAS  Google Scholar 

  • Heuer S, Hansen S, Bantin J, Brettschneider R, Kranz E, Lorz H, Dresselhaus T (2001) The maize MADS box gene ZmMADS3 affects node number and spikelet development and is co-expressed with ZmMADS1 during flower development in egg cells, and early embryogenesis. Plant Physiol 127:33–45

    Article  PubMed  CAS  Google Scholar 

  • Honma T, Goto K (2000) The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 127:2021–2030

    PubMed  CAS  Google Scholar 

  • Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529

    Article  PubMed  CAS  Google Scholar 

  • Horigome A, Nagasawa N, Ikeda K, Ito M, Ito JI, Nagato Y (2009) Rice OPEN BEAK is a negative regulator of class 1 knox genes and a posite regulator of class B floral homeotic gene. Plant J 58:724–736

    Article  PubMed  CAS  Google Scholar 

  • Ikeda K, Nagasawa N, Nagato Y (2005) ABERRANT PANICLE ORGANIZATION 1 temporally regulates meristem identity in rice. Dev Biol 282:349–360

    Article  PubMed  CAS  Google Scholar 

  • Ikeda K, Ito M, Nagasawa N, Kyozuka J, Nagato Y (2007) Rice ABERRANT PANICLE ORGANIZATION 1, encoding an F-box protein, regulates meristem fate. Plant J 51:1030–1040

    Article  PubMed  CAS  Google Scholar 

  • Immink RGH, Tonaco I, de Folter S, Shchennikova A, van Dijk A, Busscher-Lange J, Borst JW, Angenent GC (2009) SEPALLATA3: the glue for MADS box transcription factor complex formation. Genome Biol 10:24

    Article  CAS  Google Scholar 

  • Immink RGH, Kaufmann K, Angement GC (2010) The “ABC” of MADS domain protein behaviour and interactions. Semin Cell Dev Biol 21:87–93

    Article  PubMed  CAS  Google Scholar 

  • Irish V (2006) Duplication, diversification, and comparative genetics of angiosperm MADS-box genes. In: Soltis DE, Soltis PS, Leebens-Mack J (eds) Developmental genetics of the flower, advances in botanical research 44. Academic Press, San Diego, London, pp 130–151

    Google Scholar 

  • Ishikawa M, Ohmori Y, Tanaka W, Hirabayashi C, Murai K, Ogihara Y, Yamaguchi T, Hirano HY (2009) The spatial expression patterns of DROOPING LEAF orthologs suggest a conserved function in grasses. Genes Genet Syst 84:137–146

    Article  PubMed  CAS  Google Scholar 

  • Jack T, Brochman LL, Meyerowitz EM (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683–697

    Article  PubMed  CAS  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  PubMed  CAS  Google Scholar 

  • Jansen RK, Kaittanis C, Saski C, Lee SB, Tomkins J, Alverson AJ, Daniell H (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6:32

    Article  PubMed  CAS  Google Scholar 

  • Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Muller KF et al (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104:19369–19374

    Article  PubMed  CAS  Google Scholar 

  • Jeon JS, Jang S, Lee S, Nam J, Kim C, Lee SH, Chung YY, Kim SR, Lee YH, Cho YG, An G (2000) Leafy hull sterile 1 is a homeotic mutation in a rice MADS-box gene affecting rice flower development. Plant Cell 12:871–884

    Article  PubMed  CAS  Google Scholar 

  • Judziewicz EJL, Clark G, Londono X, Stern MJ (1999) American bamboos. Smithsonian Institution Press, Washington

    Google Scholar 

  • Kang HG, Jeon JS, Lee S, An G (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol Biol 38:1021–1029

    Article  PubMed  CAS  Google Scholar 

  • Kater MM, Dreni L, Colombo L (2006) Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. J Exp Bot 57:3433–3444

    Article  PubMed  CAS  Google Scholar 

  • Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205

    Article  PubMed  CAS  Google Scholar 

  • Kellogg EA (2007) Floral displays: genetic control of grass inflorescences. Curr Opin Plant Biol 10:26–31

    Article  PubMed  CAS  Google Scholar 

  • Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidospis. Science 267:522–525

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Yoo MJ, Albert VA, Farris JS, Soltis PS, Soltis DE (2004) Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implication of a 260-million-year-old duplication. Am J Bot 91:2102–2118

    Article  PubMed  CAS  Google Scholar 

  • Komatsu M, Chujo A, Nagato Y, Shimamoto K, Kyozuka J (2003) FRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikelets. Development 130:3841–3850

    Article  PubMed  CAS  Google Scholar 

  • Kramer EM, Zimmer EA (2006) Gene duplication and floral developmental genetics of basal eudicots. In: Soltis DE, Soltis PS, Leebens-Mack J (eds) Developmental genetics of the flower, advances in botanical research 44. Academic Press, San Diego, pp 354–376

    Google Scholar 

  • Kramer EM, Dorit RL, Irish VF (1998) Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149:765–783

    PubMed  CAS  Google Scholar 

  • Kramer EM, Jaramillo MA, Di Stilio VS (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166:1011–1023

    Article  PubMed  CAS  Google Scholar 

  • Kramer EM, Su H, Wu C, Hu J (2006) A simplified explanation for the frameshift mutation that created a novel C-terminal motif in the APETALA3 lineage. BMC Evol Biol 6:30

    Article  PubMed  CAS  Google Scholar 

  • Krizek BA, Lewis MW, Fletcher JC (2006) RABBIT EARS is a second-whorl repressor of AGAMOUS that maintains spatial boundaries in Arabidopsis flowers. Plant J 45:369–383

    Article  PubMed  CAS  Google Scholar 

  • Kyozuka J, Shimamoto K (2002) Ectopic expression of OsMADS3, a rice ortholog of AGAMOUS, caused a homeotic transformation of lodicules to stamens in transgenic rice plants. Plant Cell Physiol 43:130–135

    Article  PubMed  CAS  Google Scholar 

  • Kyozuka J, Kobayashi T, Morita M, Shimamoto K (2000) Spatially and temporally regulated expression of rice MADS-box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol 41:710–718

    PubMed  CAS  Google Scholar 

  • Lamb RS, Hill TA, Tan QKG, Irish VF (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129:2079–2086

    PubMed  CAS  Google Scholar 

  • Laudencia-Chingcuanco D, Hake S (2002) The indeterminate floral apex1 gene regulates meristem determinacy and identity in the maize inflorescence. Development 129:2629–2638

    PubMed  CAS  Google Scholar 

  • Lee I, Wolfe DS, Nilsson O, Weigel D (1997) A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS. Curr Biol 7:95–104

    Article  PubMed  Google Scholar 

  • Lee S, Kim J, Son JS, Nam J, Jeong DH, Lee K, Jang S, Yoo J, Lee J, Lee D-Y, Kang HG, An G (2003a) Systematic reverse genetic screening of T-DNA tagged genes in rice for functional genomic analyses: MADS-box genes as a test case. Plant Cell Physiol 44:1403–1411

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Jeon JS, An K, Moon YH, Lee S, Chung YY, An G (2003b) Alteration of floral organ identity in rice through ectopic expression of OsMADS16. Planta 217:904–911

    Article  PubMed  CAS  Google Scholar 

  • Levin JZ, Meyerowitz EM (1995) UFO: An Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7:529–548

    Article  PubMed  CAS  Google Scholar 

  • Li H, Liang W, Jia R, Yin C, Zong J, Kong H, Zhang D (2009) The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice. Cell Res 20:299–313

    Article  PubMed  CAS  Google Scholar 

  • Li H, Liang W, Hu Y, Zhu L, Yin C, Xu J, Dreni L, Kater MM, Zhang D (2011a) Rice MADS6 interacts with the floral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13 and DROOPING LEAF in specifying floral organ identities and meristem fate. Plant Cell. doi:10.1105/tpc.111.087262

  • Li H, Liang W, Yin C, Zhu L, Zhang D (2011b) Genetic interaction of OsMADS3, DROOPING LEAF and OsMADS13 in specifying rice floral organ identities and meristem determinacy. Plant Physiol 156:263–274

    Article  PubMed  CAS  Google Scholar 

  • Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770

    Article  PubMed  CAS  Google Scholar 

  • Lim J, Moon YH, An G, Jang SK (2000) Two rice MADS domain proteins interact with OsMADS1. Plant Mol Biol 44:513–527

    Article  PubMed  CAS  Google Scholar 

  • Litt A (2007) An evaluation of A-function: evidence from the APETALA1 and APETALA2 gene lineages. Int J Plant Sci 168:73–91

    Article  CAS  Google Scholar 

  • Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833

    PubMed  CAS  Google Scholar 

  • Litt A, Kramer MK (2010) The ABC model and the diversification of floral organ identity. Semin Cell Dev Biol 21:129–137

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Mara C (2010) Regulatory mechanisms for floral homeotic gene expression. Semin Cell Dev Biol 21:80–86

    Article  PubMed  CAS  Google Scholar 

  • Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Dee ZP, Wittich P, Pè ME, Rigola D, Del Buono I, Sari-Gorla M, Kater MM, Colombo L (1999) OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev Genet 25:237–244

    Article  PubMed  CAS  Google Scholar 

  • Luo Q, Zhou K, Zhao X, Zeng Q, Xia H, Zhai W, Xu J, Wu X, Yang H, Zhu L (2005) Identification and fine mapping of a mutant gene for palealess spikelet in rice. Planta 221:222–230

    Article  PubMed  CAS  Google Scholar 

  • Magallon SA, Sanderson MJ (2005) Angiosperm divergence times: the effect of genes, codon positions, and time constraints. Evolution 59:1653–1670

    Article  PubMed  CAS  Google Scholar 

  • Malcomber ST, Kellogg EA (2004) Heterogenous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses. Plant Cell 16:1692–1706

    Article  PubMed  CAS  Google Scholar 

  • Malcomber ST, Kellogg EA (2005) SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 10:427–435

    Article  PubMed  CAS  Google Scholar 

  • Malcomber ST, Kellogg EA (2006) Evolution of unisexual flowers in grasses (Poaceae) and the putative sex determination gene, TASSEL-SEED2 (TS2). New Phytol 170:885–899

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277

    Article  PubMed  CAS  Google Scholar 

  • Marchant AD, Briggs BG (2007) Ecdeiocoleaceae and Joinvilleaceae, sisters of Poaceae (Poales): evidence from rbcL and matK data. Telopea 11(4):437–450

    Google Scholar 

  • Melzer R, Verelst W, Theissen G (2009) The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in “floral quartet”-like complexes in vitro. Nucl Acids Res 37:144–157

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mena M, Ambrose BA, Meeley RB, Briggs SP, Yanofsky MF, Schmidt RJ (1996) Diversification of C-function activity in maize flower development. Science 274:1537–1540

    Article  PubMed  CAS  Google Scholar 

  • Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KLT et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996

    Article  PubMed  CAS  Google Scholar 

  • Moon YH, Kang HG, Jung JY, Jeo JS, Sung SK, An G (1999) Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol 120:1193–1204

    Article  PubMed  CAS  Google Scholar 

  • Mouradov A, Glassick TV, Hamdorf BA, Murphy LC, Marla SS, Yang Y, Teasdale RD (1998) Family of MADS-box genes expressed early in male and female reproductive structures of Monterey Pine. Plant Physiol 117:55–61

    Article  PubMed  CAS  Google Scholar 

  • Muller BM, Saedler H, Zachgo S (2001) The MADS-box gene DEFH28 from Antirrhinum is involved in the regulation of floral meristem identity and fruit development. Plant J 28:169–179

    Article  PubMed  CAS  Google Scholar 

  • Munster T, Wingen LU, Faigl W, Werth S, Saedler H, Theissen G (2001) Characterization of three Globosa-like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function gene of grasses. Gene 262:1–13

    Article  PubMed  CAS  Google Scholar 

  • Munster T, Deleu W, Wingen LU, Ouzunova M, Cacharron J, Faigl W, Werth S, Kim JTT, Saedler H, Theissen G (2002) Maize MADS-box genes galore. Maydica 47:287–301

    Google Scholar 

  • Murai K, Takumi S, Koga H, Ogihara Y (2002) Pistillody, homeotic transformation of stamens into pistil-like structures, caused by nuclear-cytoplasm interaction in wheat. Plant J 29:169–181

    Article  PubMed  Google Scholar 

  • Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130:705–718

    Article  PubMed  CAS  Google Scholar 

  • Navaud O, Dabos P, Carnus E, Tremousaygue D, Herve C (2007) TCP transcription factors predate the emergence of land plants. J Mol Evol 65:23–33

    Article  PubMed  CAS  Google Scholar 

  • Ohmori S, Kimizu M, Sugita M, Miyao A, Hirochita H, Uchida E, Nagato Y, Yoshida H (2009) MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene regulates floral organ identity and meristem fate in rice. Plant Cell 21:3008–3025

    Article  PubMed  CAS  Google Scholar 

  • Ohno CK, Reddy GV, Heisler MG, Meyerowitz EM (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 131:1111–1122

    Article  PubMed  CAS  Google Scholar 

  • Paolacci AR, Tanazarella OA, Porceddu E, Varotto S, Ciaffi M (2007) Molecular and phylogenetic analysis of MADS-box genes of MIKC type and chromosome location of SEP-like genes in wheat (Triticum aestivum L.). Mol Genet Genomics 278:689–708

    Article  PubMed  CAS  Google Scholar 

  • Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395:561–566

    Article  PubMed  CAS  Google Scholar 

  • Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular and phylogenetic analysis of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538–1551

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Van de Peer Y, Vandepoele K (2005) Ancient duplication of cereal genomes. New Phytol 165:658–661

    Article  PubMed  CAS  Google Scholar 

  • Pelaz S, Ditta GS, Bauman E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    Article  PubMed  CAS  Google Scholar 

  • Pelaz S, Tapia-Lopez R, Alvarez-Buylla ER, Yanofsky MF (2001) Conversion of leaves into petals in Arabidopsis. Curr Biol 11:182–184

    Article  PubMed  CAS  Google Scholar 

  • Pelucchi N, Fornara F, Favalli C, Masiero S, Lago C, Pè ME, Colombo L, Kater MM (2002) Comparative analysis of rice MADS-box genes expressed during flower development. Sex Plant Reprod 15:113–122

    Article  CAS  Google Scholar 

  • Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424:85–88

    Article  PubMed  CAS  Google Scholar 

  • Prasad K, Vijayraghavan U (2003) Double-stranded RNA interference of a rice PI/GLO paralog, OsMADS2, uncover its second-whorl-specific function in floral organ patterning. Genetics 165:2301–2305

    PubMed  CAS  Google Scholar 

  • Prasad K, Sriram P, Kumar SC, Kushalappa K, Vijayraghavan U (2001) Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass organs analogous to sepals. Dev Genes Evol 211:281–290

    Article  PubMed  CAS  Google Scholar 

  • Prasad K, Parameswaran S, Vijayraghavan U (2005) OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J 43:915–928

    Article  PubMed  CAS  Google Scholar 

  • Preston JC, Kellogg EA (2006) Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in Grasses (Poaceae). Genetics 174:421–437

    Article  PubMed  CAS  Google Scholar 

  • Preston JC, Kellogg EA (2007) Conservation and divergence of APETALA1/FRUITFULL-like gene function in grasses: evidence from gene expression analyses. Plant J 52:69–81

    Article  PubMed  CAS  Google Scholar 

  • Preston JC, Christensen A, Malcomber ST, Kellogg EA (2009) MADS-box gene expression and implications for developmental origins of the grass spikelet. Am J Bot 96:1419–1429

    Article  PubMed  CAS  Google Scholar 

  • Rao SA, Mengesha MH, Reddy CR (1988) Characteristics, inheritance, and allelic relationships of midribless mutants in pearl millet. J Hered 79:18–20

    Google Scholar 

  • Reinheimer R, Kellogg EA (2009) Evolution of AGL6-like MADS box genes in grasses (Poaceae): ovule expression is ancient and palea expression is new. Plant Cell 21:2591–2605

    Article  PubMed  CAS  Google Scholar 

  • Rijpkema AS, Royaert S, Zethof J, van der Weerden G, Gerats T, Vandenbussche M (2006) Analysis of the Petunia TM6 MADS-box gene reveals functional divergence within the DEF/AP3 lineage. Plant Cell 18:1819–1832

    Article  PubMed  CAS  Google Scholar 

  • Rijpkema AS, Zethof J, Gerats T, Vandenbussche M (2009) The Petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant J 60:1–9

    Article  PubMed  CAS  Google Scholar 

  • Rijpkema AS, Vandenbussche M, Koes R, Heijmans K, Gerats T (2010) Variation on a theme: changes in floral ABCs in angiosperms. Semin Cell Dev Biol 21:100–107

    Article  PubMed  CAS  Google Scholar 

  • Rudall PJ, Stuppy W, Cunnif J, Kellogg EA, Briggs BG (2005) Evolution of reproductive structures in grasses (Poaceae) inferred by sister-group comparison with their putative closest relatives, Ecdeiocoleaceae. Am J Bot 92:1432–1443

    Article  PubMed  Google Scholar 

  • Sajo MG, Longhi-Wagner HM, Rudall PJ (2008) Reproductive morphology of the early-divergent grass Streptochaeta and its bearing on the homologies of the grass spikelet. Plant System Evol 275:245–255

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sakai H, Krizek BA, Jacobsen SE, Meyerowitz EM (2000) Regulation of SUP expression identifies multiple regulators involved in Arabidopsis floral meristem development. Plant Cell 12:1607–1618

    Article  PubMed  CAS  Google Scholar 

  • Salse J, Bolot S, Throude M, Jouffe V, Piegu B, Masood B, Calcagno T, Cooke R, Delseny M, Feuillet C (2008) Identification and characterization of conserved duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20:11–24

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Ken JG, Clark LG, Kellogg EA, Kay EE (2007) Reinstatement and emendation of subfamily Micrairoideae (Poaceae). System Bot 32:71–80

    Article  Google Scholar 

  • Schmidt RJ, Ambrose BA (1998) The blooming of grass flower development. Curr Opin Plant Biol 1:60–67

    Article  PubMed  CAS  Google Scholar 

  • Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF (1993) Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 5:729–737

    Article  PubMed  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schluter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  PubMed  CAS  Google Scholar 

  • Seok HY, Park HY, Park JI, Lee YM, Lee SY, An G, Moon YH (2010) Rice ternary MADS protein complexes containing class B MADS heterodimer. Biochem Biophys Res Commun 401:598–604

    Article  PubMed  CAS  Google Scholar 

  • Shan H, Zhang N, Liu C, Xu G, Zhang J, Chen Z, Kong H (2007) Patterns of gene duplication and functional diversification during the evolution of the AP1/SQUA subfamily of plant MADS-box genes. Mol Phylogenet Evol 44:26–41

    Article  PubMed  CAS  Google Scholar 

  • Shindo S, Ito M, Ueda K, Kato M, Hasebe M (1999) Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol Dev 1:180–190

    Article  PubMed  CAS  Google Scholar 

  • Shitsukawa N, Tahira C, Kassai KI, Hirabayashi C, Shimizu T, Takumi S, Mochida K, Kawaura K, Ogihara Y, Murai K (2007) Genetic and epigenetic alteration among three homoeologous genes of a class E MADS box gene in hexaploid wheat. Plant Cell 19:1723–1737

    Article  PubMed  CAS  Google Scholar 

  • Soderstrom TR (1981) Some evolutionary trends in the Bambusoideae (Poaceae). Ann Missouri Bot Gard 68:15–47

    Article  Google Scholar 

  • Soltis DE, Chanderbali AS, Kim S, Buzgo M, Soltis PS (2007) The ABC model and its applicability to basal angiosperms. Ann Bot 100:155–163

    Article  PubMed  CAS  Google Scholar 

  • Soltis DE, Bell CD, Kim S, Soltis PS (2008) Origin and early evolution of angiosperms. Ann NY Acad Sci 1133:3–25

    Article  PubMed  CAS  Google Scholar 

  • Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, DePamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Am J Bot 96:336–348

    Article  PubMed  Google Scholar 

  • Sonnhammer ELL, Koonin EV (2002) Orthology, paralogy and proposed classification for paralog subtypes. Trends Genet 18:619–620

    Article  PubMed  CAS  Google Scholar 

  • Stellari GM, Jaramillo MA, Kramer EM (2004) Evolution of the APETALA3 and PISTILLATA lineages of MADS-box-containing genes in the basal angiosperms. Mol Biol Evol 21:506–519

    Article  PubMed  CAS  Google Scholar 

  • Swigonova Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14:1916–1923

    Article  PubMed  CAS  Google Scholar 

  • Takeda S, Matsumoto N, Okada K (2004) RABBIT EARS, encoding a SUPERMAN-like zinc finger protein, regulates petal development in Arabidopsis thaliana. Development 131:425–434

    Article  PubMed  CAS  Google Scholar 

  • Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH (2008) Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18:1944–1954

    Article  PubMed  CAS  Google Scholar 

  • The International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Article  CAS  Google Scholar 

  • Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, Melzer R (2007) Molecular mechanisms underliyng origin and diversification of the angiosperm flower. Ann Bot 100:603–619

    Article  PubMed  Google Scholar 

  • Theissen G, Saedler H (2001) Plant biology: floral quartets. Nature 409:469–471

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149

    Article  PubMed  CAS  Google Scholar 

  • Thompson BE, Hake S (2009) Translational biology: from Arabidopsis flowers to grass inflorescence architecture. Plant Physiol 149:38–45

    Article  PubMed  CAS  Google Scholar 

  • Thompson BE, Bartling L, Whipple C, Hall DH, Sakai H, Schmidt R, Hake S (2009) Bearded-ear encodes a MADS box transcription factor critical for maize floral development. Plant Cell 21:2578–2590

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. and Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Tzeng TY, Hsiao CC, Chi PJ, Yang CH (2003) Two lily SEPALLATA-like genes cause different effects on floral formation and floral transition in Arabidopsis. Plant Physiol 133:1091–1101

    Article  PubMed  CAS  Google Scholar 

  • Van de Peer Y, Fawcett JA, Proost S, Sterck L, Vadepoele K (2009) The flowering world: a tale of duplications. Trends Plant Sci 14:680–688

    Article  PubMed  CAS  Google Scholar 

  • Vandenbussche M, Theissen G, Van de Peer Y, Gerats T (2003) Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucl Acids Res 31:4401–4409

    Article  PubMed  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M et al (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326

    Article  PubMed  CAS  Google Scholar 

  • Veron AS, Kuafmannn K, Bornberg-Bauer E (2007) Evidence of interaction network evolution by whole-genome duplications: a case study in MADS-box proteins. Mol Biol Evol 24:670–678

    Article  PubMed  CAS  Google Scholar 

  • Vollbrecht E, Springer PS, Goh L, Buckler ES, Martienssen R (2005) Architecture of floral branch systems in maize and related grasses. Nature 436:1119–1126

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Sablowski RWM, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584

    Article  PubMed  CAS  Google Scholar 

  • Weigel D, Meyerowitz EM (1993) Activation of floral homeotic genes in Arabidopsis. Science 261:1723–1726

    Article  PubMed  CAS  Google Scholar 

  • Whipple C, Schmidt RJ (2006) Genetics of grass flower development. In: Soltis DE, Soltis PS, Leebens-Mack J (eds) Developmental genetics of the flower, advances in botanical research 44. Academic Press, San Diego, pp 353–384

    Google Scholar 

  • Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ (2004) Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 131:6083–6091

    Article  PubMed  CAS  Google Scholar 

  • Whipple CJ, Zanis MJ, Kellogg EA, Scmidt RJ (2007) Conservation of B class gene expression in the second whorl of a basal grass and outgroups links the origin of lodicules and petals. Proc Natl Acad Sci USA 104:1081–1086

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson MD, Haughn GW (1995) UNUSUAL FLORAL ORGANS Controls Meristem Identity and Organ Primordia Fate in Arabidopsis. Plant Cell 7:1485–1499

    Article  PubMed  CAS  Google Scholar 

  • Winter KU, Becker A, Münster T, Kim JT, Saedler H, Theissen G (1999) MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc Natl Acad Sci USA 96:7342–7347

    Article  PubMed  CAS  Google Scholar 

  • Xu G, Kong H (2007) Duplication and divergence of floral MADS-box genes in grasses: evidence for generation and modification of novel regulators. Int J Plant Biol 49:927–939

    Article  CAS  Google Scholar 

  • Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500–509

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano HY (2006) Functional diversification of the two C-class genes OsMADS3 and OsMADS58 in Oryza sativa. Plant Cell 18:15–28

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  PubMed  CAS  Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldman KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346:35–39

    Article  PubMed  CAS  Google Scholar 

  • Yao SG, Ohmori S, Kimizu M, Yoshida H (2008) Unequal genetic redundancy of rice PISTILLATA orthologs, OsMADS2 and OsMADS4, in lodicules and stamen development. Plant Cell Physiol 49:853–857

    Article  PubMed  CAS  Google Scholar 

  • Yoshida H, Itoh J, Ohmori S, Miyoshi K, Origome A, Uchida E, Kimizu M, Matsumura Y, Kusaba M, Satoh H, Nagato Y (2007) Superwoman1-cleistogamy, a hopeful allele for gene containment in GM rice. Plant Biotech J 5:835–846

    Article  CAS  Google Scholar 

  • Yuan Z, Gao S, Xue DW, Luo D, Li LT, Ding SY, Yao X, Wilson ZA, Qian Q, Zhang DB (2009) RETARDED PALEA1 controls palea development and floral zygomorphy in rice. Plant Physiol 149:235–244

    Article  PubMed  CAS  Google Scholar 

  • Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS et al (2005) The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209–2223

    Article  PubMed  CAS  Google Scholar 

  • Zahn LM, Leebens-Mack JH, Arrington JM, Hu Y, Landherr LL, dePamphilis CW, Becker A, Theissen G, Ma H (2006) Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol Dev 8:30–45

    Article  PubMed  CAS  Google Scholar 

  • Zanis MJ (2007) Grass spikelet genetics and duplicate gene comparisons. Int J Plant Sci 168:93–110

    Article  CAS  Google Scholar 

  • Zhao XY, Cheng ZJ, Zhang XS (2006) Overexpression of TaMADS1, a SEPALLATA-like gene in wheat, causes early flowering and the abnormal development of floral organs in Arabidopsis. Planta 223:698–707

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y, Li X, Chen W, Peng X, Cheng X, Zhu S, Cheng B (2010) Whole-genome survey and characterization of MADS-box gene family in maize and sorghum. Plant Cell Tissue Organ Cult 105:159–173

    Article  Google Scholar 

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  1. Dipartimento di Agrobiologia e Agrochimica, Università della Tuscia, Via San Camillo De Lellis, 01100, Viterbo, Italy

    Mario Ciaffi, Anna Rita Paolacci, Oronzo Antonio Tanzarella & Enrico Porceddu

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  1. Mario Ciaffi
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Ciaffi, M., Paolacci, A.R., Tanzarella, O.A. et al. Molecular aspects of flower development in grasses. Sex Plant Reprod 24, 247–282 (2011). https://doi.org/10.1007/s00497-011-0175-y

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