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Tropical Plant Biology

, Volume 12, Issue 1, pp 1–11 | Cite as

When Bs Are Better than As: the Relationship between B-Class MADS-Box Gene Duplications and the Diversification of Perianth Morphology

  • Helena Augusto Gioppato
  • Marcelo Carnier DornelasEmail author
Article

Abstract

Flowering plants (angiosperms) are the most species-rich and structurally diverse group of living plants. This evolutionary success is in great part due to morphological novelties characteristic to angiosperms such as the flower. The molecular mechanisms that allowed flowers to be formed and diversified are still unknown but certainly key roles are played by particular members of the MADS-box gene family. They encode transcriptional factors fundamental to several developmental processes, including the organization of floral structure in angiosperms. Studies concerning the evolution of the MADS-box gene family in flowering plants have uncovered several duplication events, followed by functional diversification of members of this gene family belonging to the so called ABC model. According to the literature, some of these duplication events involved B-class MADS-box genes and contributed to the diversification of angiosperm flower morphologies. In this review, we focus on examples of B-class gene duplications and their implications for flower structure and adaptation.

Keywords

Evolution Evo-devo Evolutionary novelty Flower adaptation Flower development MADS-box 

Abbreviations

AP1

APPETALA 1

AP2

APETALA 2

AP3

APETALA 3

AG

AGAMOUS

CAL

CAULIFLOWER

FUL

FRUITFULL

AGL-79

AGAMOUS LIKE 79

PI

PISTILLATA

STK

SEEDSTICK

SHP

SHATTERPROOF

SEP

SEPALLATA

TM6

TOMATO 6

GOA

GORDITA

TT16

TRANSPARENT TESTA 16

SI1

SILKY 1

SPW1

SUPERWOMAN 1

RNAi

RNA interference

FBP1

PI paralog (Petunia hybrida)

PMADS2

PI paralog (Petunia hybrida)

MADS2

PI orthologue (Oryza sativa)

MADS4

PI orthologue (Oryza sativa)

ZMM16

PI orthologue (Zea mays)

ZMM18

PI orthologue (Zea mays)

ZMM29

PI orthologue (Zea mays)

GP

GREEN PETAL

GGM13

MADS-box (Gnetum gnemom)

ZMM17

MADS-box (Zea mays)

DEFH21

MADS-box (Antirrhinum majus)

FBP24

MADS-box (Petunia hybrida)

References

  1. Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569–579Google Scholar
  2. Angenent GC, Colombo L (1996) Molecular control of ovule development. Trends Plant Sci 1:228–232Google Scholar
  3. Bartlett ME, Specht CD (2010) Evidence for the involvement of GLOBOSA-like gene duplications and expression divergence in the evolution of floral morphology in the Zingiberales. New Phytol 187:521–541Google Scholar
  4. 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 29:464–489Google Scholar
  5. Becker A, Kaufmann K, Freialdenhoven A, Vincent C, Li MA, Saedler H, Theissen G (2001) A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Mol Gen Genomics 266:942–950Google Scholar
  6. Broholm SK, Pöllänen E, Ruokolainen S, Tähtiharju S, Kotilainen M, Albert VA, Elomaa P, Teeri TH (2010) Functional characterization of B class MADS-box transcription factors in Gerbera hybrida. J Exp Bot 61:75–85Google Scholar
  7. Buzgo M, Soltis PS, Soltis DE (2004) Floral developmental morphology of Amborella trichopoda (Amborellaceae). Int J Plant Sci 165:925–947Google Scholar
  8. Buzgo M, Soltis PS, Kim S, Soltis DE (2005) The making of the flower. Biologist 52:149–154Google Scholar
  9. Cameron KM (2004) Utility of plastid psaB gene sequences for investigating intrafamilial relationships within Orchidaceae. Mol Phylogenet Evol 31:1157–1180Google Scholar
  10. Chanderbali AS, Yoo M-J, Zahn LM, Brockington SF, Wall PK, Gitzendanner MA, Albert VA, Leebens-Mack J, Altman NS, Ma H, dePamphilis CW, Soltis DE, Soltis PS (2010) Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower. Proc Natl Acad Sci U S A 107:22570–22575Google Scholar
  11. Chang YY, Kao NH, Li JY, Hsu WH, Liang YL, Wu JW, Yang CH (2010) Characterization of the possible roles for B class MADS box genes in regulation of perianth formation in orchid. Plant Physiol 152:837–853Google Scholar
  12. Christenhusz MJM, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261:201–217Google Scholar
  13. Chung YY, Kim SR, Kang HG, Noh YS, Park MC, Finkel D, An G (1995) Characterization of two rice MADS box genes homologous to GLOBOSA. Plant Sci 109:45–56Google Scholar
  14. Clark JW, Donoghue PCJ (2018) Whole-genome duplication and plant macroevolution. Trends Plant Sci 23:933–945Google Scholar
  15. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37Google Scholar
  16. Cozzolino S, Widmer A (2005) Orchid diversity: an evolutionary consequence of deception? Trends Ecol Evol 20:487–494Google Scholar
  17. De Folter S, Shchennikova AV, Franken J, Busscher M, Baskar R, Grossniklaus U, … Immink RGH (2006) A Bsister MADS-box gene involved in ovule and seed development in petunia and Arabidopsis. Plant J, 47(6):934–946.  https://doi.org/10.1111/j.1365-313X.2006.02846.x
  18. de Martino G (2006) Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell Onl 18(8):1833–1845.  https://doi.org/10.1105/tpc.106.042978 Google Scholar
  19. Dezar CA, Tioni MF, Gonzalez DH, Chan RL (2003) Identification of three MADS-box genes expressed in sunflower capitulum. J Exp Bot 54(387):1637–1639.  https://doi.org/10.1093/jxb/erg163 Google Scholar
  20. 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.  https://doi.org/10.1016/j.cub.2004.10.028 Google Scholar
  21. Dornelas MC, Dornelas O (2005) From leaf to flower: revisiting Goethe’s concepts on the ¨metamorphosis¨ of plants. Braz J Plant Physiol 17:335–343Google Scholar
  22. Dressler RL (1993) Phylogeny and classification of the orchid family. Timber Press inc 70:84.  https://doi.org/10.1086/418905 Google Scholar
  23. Egea-Cortines M, Saedler H, Sommer H (1999) 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 18(19):5370–5379.  https://doi.org/10.1093/emboj/18.19.5370 Google Scholar
  24. Erdmann R, Gramzow L, Melzer R, Theissen G, Becker A (2010) GORDITA (AGL63) is a young paralog of the Arabidopsis thaliana BsisterMADS box gene ABS (TT16) that has undergone neofunctionalization. Plant J 63(6):914–924.  https://doi.org/10.1111/j.1365-313X.2010.04290.x Google Scholar
  25. Ferrario S, Immink RGH, Angenent GC (2004) Conservation and diversity in flower land. Curr Opin Plant Biol 7(1):84–91.  https://doi.org/10.1016/j.pbi.2003.11.003 Google Scholar
  26. Fornara F (2004) Functional characterization of OsMADS18, a member of the AP1/SQUA subfamily of MADS box genes. Plant Physiol 135(4):2207–2219.  https://doi.org/10.1104/pp.104.045039 Google Scholar
  27. Galimba KD, Martínez-Gómez J, Di Stilio VS (2018) Gene duplication and transference of function in the paleoAP3 lineage of floral organ identity genes. Front Plant Sci 9:334Google Scholar
  28. Geuten K, Irish V (2010) Hidden variability of floral homeotic B genes in Solanaceae provides a molecular basis for the evolution of novel functions. Plant Cell 22:2562–2578Google Scholar
  29. Geuten K, Viaene T, Irish VF (2011) Robustness and evolvability in the B-system of flower development. Ann Bot 107:1545–1556Google Scholar
  30. Gong P, Ao X, Liu G, Cheng F, He C (2017) Duplication and whorl-specific down-regulation of the obligate AP3-PI heterodimer genes explain the origin of Paeonia lactiflora plants with spontaneous corolla mutation. Plant Cell Physiol 58:411–425Google Scholar
  31. Goremykin VV, Hansmann S, Martin WF (1997) Evolutionary analysis of 58 proteins encoded in six completely sequenced chloroplast genomes: revised molecular estimates of two seed plant divergence times. Plant Syst Evol 206(1–4):337–351.  https://doi.org/10.1007/BF00987956 Google Scholar
  32. Gramzow L, Barker E, Schulz C, Ambrose B, Ashton N, Theissen G, Litt A (2012) Selaginella genome analysis - entering the "homoplasy heaven" of the MADS world. Front Plant Sci 14:214Google Scholar
  33. Hernández-Hernández T, Martínez-Castilla LP, Alvarez-Buylla ER (2007) Functional diversification of B MADS-box homeotic regulators of flower development: adaptive evolution in protein-protein interaction domains after major gene duplication events. Mol Biol Evol 24(2):465–481.  https://doi.org/10.1093/molbev/msl182 Google Scholar
  34. Honma T, Goto K (2000) The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development (Cambridge, England) 127(10):2021–2030Google Scholar
  35. Immink RG, Ferrario S, Busscher-Lange J, Kooiker M, Busscher M, Angenent GC (2003) Analysis of the petunia MADS-box transcription factor family. Mol Gen Genomics 268:598–606Google Scholar
  36. Irish VF (1999) Petal and stamen development. Curr Top Dev Biol 41:133–161Google Scholar
  37. Irish V (2017) The ABC model of floral development. Current Biology 27 (17):R887–R890Google Scholar
  38. Kellogg EA (2001) Update on evolution evolutionary history of the grasses. Plant Physiol 125:1198–1205.  https://doi.org/10.1104/pp.125.3.1198 Google Scholar
  39. 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 implications of a 260-million-year-old duplication. Am J Bot 91:2102–2118Google Scholar
  40. Kim S, Koh J, Ma H, Hu Y, Endress PK, Hauser BA, Buzgo M, Soltis PS, Soltis DE (2005a) Sequence and expression studies of A-, B-, and E-class MADS-box homologues in Eupomatia (Eupomatiaceae): support for the Bracteate origin of the calyptra. Int J Plant Sci 166(2):185–198.  https://doi.org/10.1086/427479 Google Scholar
  41. Kim S, Koh J, Yoo MJ, Kong H, Hu Y, Ma H, Soltis PS, Soltis DE (2005b) Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. Plant J 43:724–744Google Scholar
  42. Kim SY, Yun PY, Fukuda T, Ochiai T, Yokoyama J, Kameya T, Kanno A (2007) Expression of a DEFICIENS-like gene correlates with the differentiation between sepal and petal in the orchid, Habenaria radiata (Orchidaceae). Plant Sci 172(2):319–326.  https://doi.org/10.1016/j.plantsci.2006.09.009 Google Scholar
  43. Kirchoff BK (1988) Inflorescence and flower development in Costus scaber (Costaceae). Can J Bot 66:339–345.  https://doi.org/10.1139/b88-054 Google Scholar
  44. Kirchoff BK (1998) Inflorescence and flower development in the Hedychieae (Zingiberaceae): Scaphochlamys kunstleri (Baker) Holtt. Int J 159(2):261–274Google Scholar
  45. Kirchoff BK, Lagomarsino LP, Newman WH, Bartlett ME, Specht CD (2009) Early floral development of Heliconia latispatha (Heliconiaceae), a key taxon for understanding the evolution of flower development in the Zingiberales. Am J Bot 96(3):580–593.  https://doi.org/10.3732/ajb.0800305 Google Scholar
  46. Koshimizu S, Kofuji R, Sasaki-Sekimoto Y, Kikkawa M, Shimojima M, Ohta H, Shigenobu S, Kabeya Y, Hiwatashi Y, Tamada Y, Murata T, Hasebe M (2018) Physcomitrella MADS-box genes regulate water supply and sperm movement for fertilization. Nat Plants 4:36–45Google Scholar
  47. Kramer EM, Irish VF (2000) Evolution of the petal and stamen developmental programs: evidence from comparative studies of the lower eudicots and basal angiosperms. Int J Plant Sci 161(S6):S29–S40.  https://doi.org/10.1086/317576 Google Scholar
  48. 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(2):765–783Google Scholar
  49. Kress WJ, Prince LM, Hahn WJ, Zimmer EA (2001) Unraveling the evolutionary radiation of the families of the Zingiberales using morphological and molecular evidence. Syst Biol 50(6):926–944Google Scholar
  50. Kress WJ, Prince LM, Williams KJ (2002) The phylogeny and a new classification of the gingers (Zingiberaceae): evidence from molecular data. Am J Bot 89(10):1682–1696.  https://doi.org/10.3732/ajb.89.10.1682 Google Scholar
  51. Krizek B a, Meyerowitz EM (1996) The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development (Cambridge, England) 122(1):11–22Google Scholar
  52. Krogan NT, Hogan K, Long JA (2012) APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139(22):4180–4190Google Scholar
  53. Lamb RS, Irish VF (2003) Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc Natl Acad Sci 100(11):6558–6563Google Scholar
  54. Lee S, Jeon JS, An K, Moon YH, Lee S, Chung YY, An G (2003) Alteration of floral organ identity in rice through ectopic expression of OsMADS16. Planta 217(6):904–911Google Scholar
  55. Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833Google Scholar
  56. Mapes G, Rothwell GW (1991) Structure and relationships of primitive conifers. Neues Jahrb Geol Palaontol Abh 183:269–287Google Scholar
  57. Martinez-Castilla LP, Alvarez-Buylla ER (2003) Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny. Proc Natl Acad Sci 100(23):13407–13412.  https://doi.org/10.1073/pnas.1835864100 Google Scholar
  58. Masiero S, Imbriano C, Ravasio F, Favaro R, Pelucchi N, Gorla MS, Mantovani R, Colombo L, Kater MM (2002) Ternary complex formation between MADS-box transcription factors and the histone fold protein NF-YB. J Biol Chem 277(29):26429–26435.  https://doi.org/10.1074/jbc.M202546200 Google Scholar
  59. McCarthy EW, Mohamed A, Litt A (2015) Functional divergence of APETALA1 and FRUITFULL is due to changes in both regulation and coding sequence. Front Plant Sci 6:1076Google Scholar
  60. McGonigle B, Bouhidel K, Irish VF (1996) Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes Dev 10:1812–1821.  https://doi.org/10.1101/gad.10.14.1812 Google Scholar
  61. Melzer R, Wang YQ, Theissen G (2010) The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower. Semin Cell Dev Biol 21(1):118–128.  https://doi.org/10.1016/j.semcdb.2009.11.015 Google Scholar
  62. Melzer R, Härter A, Rümpler F, Kim S, Soltis PS, Soltis DE, Theissen G (2014) DEF- and GLO-like proteins may have lost most of their interaction partners during angiosperm evolution. Ann Bot 114:1431–1443Google Scholar
  63. Mondragón-Palomino M, Theissen G (2008) MADS about the evolution of orchid flowers. Trends Plant Sci 13(2):51–59.  https://doi.org/10.1016/j.tplants.2007.11.007 Google Scholar
  64. Munster T, Pahnke J, Di Rosa A, Kim JT, Martin W, Saedler H, Theissen G (1997) Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Evolution 94(March):2415–2420.  https://doi.org/10.1073/pnas.94.6.2415 Google Scholar
  65. Münster T, Wingen LU, Faigl W, Werth S, Heinz-Saedler GT (2001) Characterization of three GLOBOSA -like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses. Gene 262:1–13Google Scholar
  66. Nagasawa N (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130(4):705–718.  https://doi.org/10.1111/j.2041-6962.1992.tb00659.x Google Scholar
  67. Nam J, DePamphilis CW, Ma H, Nei M (2003) Antiquity and evolution of the MADS-box gene family controlling flower development in plants. Mol Biol Evol 20(9):1435–1447.  https://doi.org/10.1093/molbev/msg152 Google Scholar
  68. Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L (2002) The transparent TESTA16 Locus Encodes the Arabidopsis Bsister MADS domain protein and is required for proper development and pigmentation of the seed coat. 14(October):2463–2479.  https://doi.org/10.1105/tpc.004127.Beeckman
  69. Pabón-Mora N, Ambrose BA, Litt A (2012) Poppy APETALA1/FRUITFULL orthologs control flowering time, branching, perianth identity, and fruit development. Plant Physiol 158:1685–1704Google Scholar
  70. Pabón-Mora N, Sharma B, Holappa LD, Kramer EM, Litt A (2013) The Aquilegia FRUITFULL-like genes play key roles in leaf morphogenesis and inflorescence development. Plant J 74:197–212Google Scholar
  71. Parenicova L (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell Onl 15(7):1538–1551.  https://doi.org/10.1105/tpc.011544 Google Scholar
  72. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405(6783):200–203.  https://doi.org/10.1038/35012103 Google Scholar
  73. Prasad K, Ambrose BA (2010) Shaping up the fruit, (July), 899–902.  https://doi.org/10.1111/j.1365-313X.2010.04139.x.www.landesbioscience.com Google Scholar
  74. Prasad K, Zhang X, Tobón E, Ambrose BA (2010) The Arabidopsis B-sister MADS-box protein, GORDITA, represses fruit growth and contributes to integument development. Plant J 62(2):203–214.  https://doi.org/10.1111/j.1365-313X.2010.04139.x Google Scholar
  75. Purugganan MD (1997) The MADS-box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J Mol Evol 45:392–396.  https://doi.org/10.1002/(SICI)1521-1878(199903)21:3<265::AID-BIES14>3.0.CO;2-J
  76. 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(1):345–356.  https://doi.org/10.1016/S0169-5347(99)01816-9 Google Scholar
  77. Riechmann JL, Meyerowitz EM (1997) Determination of floral organ identity by Arabidopsis MADS domain homeotic proteins AP1, AP3, PI, and AG is independent of their DNA-binding specificity. Mol Biol Cell 8(7):1243–1259.  https://doi.org/10.1091/mbc.8.7.1243 Google Scholar
  78. Rijpkema AS, Royaert S, Zethof J, Weerden G, Gerats T, Vandenbussche M (2006) Analysis of the Petunia TM6 MADS box gene reveals functional divergence within the DEF / AP3 lineage. Gene 18:1819–1832Google Scholar
  79. Roque E, Fares MA, Yenush L, Rochina MC, Wen J, Mysore KS, Gómez-Mena C, Beltrán JP, Cañas LA (2016) Evolution by gene duplication of Medicago truncatula PISTILLATA-like transcription factors. J Exp Bot 67:1805–1817Google Scholar
  80. Rudall PJ, Bateman RM (2002) Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots. Biol Rev Camb Philos Soc 77:403–441Google Scholar
  81. Rudall PJ, Bateman RM (2004) Evolution of zygomorphy in monocot flowers: iterative patterns and developmental constraints. New Phytol 162:25–44Google Scholar
  82. Sakai S, Kawakita A, Ooi K, Inoue T (2013) Variation in the strength of association among pollination systems and floral traits: evolutionary changes in the floral traits of Bornean gingers (Zingiberaceae). Am J Bot 100(3):546–555.  https://doi.org/10.3732/ajb.1200359 Google Scholar
  83. Salse J, Bolot S, Throude M, Jouffe V, Piegu B, Quraishi UM, Calcagno T, Cooke R, Delseny M, Feuillet C (2008) Identification and characterization of shared duplications between Rice and wheat provide new insight into grass genome evolution. Plant Cell Onl 20(1):11–24.  https://doi.org/10.1105/tpc.107.056309 Google Scholar
  84. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250(4983):931–936.  https://doi.org/10.1126/science.250.4983.931 Google Scholar
  85. Shulga OA, Shchennikova AV, Angenent GC, Skryabin KG (2008) MADS-box genes controlling inflorescence morphogenesis in sunflower. Russ J Dev Biol 39(1):2–5.  https://doi.org/10.1007/s11174-008-1002-8 Google Scholar
  86. Smyth DR (2018) Evolution and genetic control of the floral ground plan. New Phytol 220:70–86Google Scholar
  87. Soltis PS, Soltis DE (2004) The origin and diversification of angiosperms. Am J Bot 91(10):1614–1626.  https://doi.org/10.3732/ajb.91.10.1614 Google Scholar
  88. Soltis PS, Soltis DE, Kim S, Chanderbali A, Buzgo M (2006) Expression of floral regulators in basal angiosperms and the origin and evolution of ABC function. Adv Bot Res 44:483–506.  https://doi.org/10.1016/S0065-2296(06)44012-X Google Scholar
  89. Soltis DE, Ma H, Frohlich MW, Soltis PS, Albert VA, Oppenheimer DG, Altman NS, dePamphilis C, Leebens-Mack J (2007) The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression. Trends Plant Sci 12(8):358–367.  https://doi.org/10.1016/j.tplants.2007.06.012 Google Scholar
  90. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, de Pamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Am J Bot 96(1):336–348.  https://doi.org/10.3732/ajb.0800079 Google Scholar
  91. 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 21:506–519Google Scholar
  92. Sundström J, Engström P (2002) Conifer reproductive development involves B-type MADS-box genes with distinct and different activities in male organ primordia. Plant J 31(2):161–169.  https://doi.org/10.1046/j.1365-313X.2002.01343.x Google Scholar
  93. Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4(1):75–85.  https://doi.org/10.1016/S1369-5266(00)00139-4 Google Scholar
  94. Theissen G, Melzer R (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Annals of Botany 100 (3):603–619Google Scholar
  95. Theissen G, Kim JT, Saedler H (1996) 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(5):484–516.  https://doi.org/10.1007/BF02337521 Google Scholar
  96. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, … Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol, 42(1):115–49.  https://doi.org/10.1023/A:1006332105728
  97. Theissen G, Melzer R, Rümpler F (2016) MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143:3259–3271Google Scholar
  98. Tomlinson PB (1961) Phylogeny of the Scitamineae-Morphological and Anatomical Considerations. 16(2):192–213Google Scholar
  99. Trobner, W., Ramirez, L., Motte, P., Hue, I., Huijser, P., Lonnig, W., …, Schwarz-sommer, Z. (1992). GLOBOSA: a homeotic gene which interacts with DEFICIENS organogenesis in the control of Antirrhinum floral organogenesis. The EMBO JournalGoogle Scholar
  100. Tsai WC, Kuoh CS, Chuang MH, Chen WH, Chen HH (2004) Four DEF-like MADS box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant Cell Physiol 45:831–844Google Scholar
  101. Tsai WC, Lee PF, Chen HI, Hsiao YY, Wei WJ, Pan ZJ, Chuang MH, Kuoh CS, Chen WM, Chen HH (2005) PeMADS6, a GLOBOSA/PISTILLATA-like gene in Phalaenopsis equestris involved in petaloid formation, and correlated with flower longevity and ovary development. Plant Cell Physiol 46:1125–1139Google Scholar
  102. Vandenbussche M, Zethof J, Royaert S, Weterings K, Gerats T (2004) The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. Plant Cell 16:741–754Google Scholar
  103. Viaene T, Vekemans D, Irish VF, Geeraerts A, Huysmans S, Janssens S, Smets E, Geuten K (2009) Pistillata - DUplications as a mode for floral diversification in (basal) Asterids. Mol Biol Evol 26:2627–2645Google Scholar
  104. Wei RX, Ge S (2011) Evolutionary history and complementary selective relaxation of the duplicated PI Genes in grasses. J Integr Plant Biol 53 (8):682–693Google Scholar
  105. Whipple CJ, Zanis MJ, Kellogg EA, Schmidt 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 U S A 104:1081–1086Google Scholar
  106. Winter K, Weiser C, Kaufmann K, Bohne A, Kirchner C, Kanno A, Saedler H (2002) Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. Mol Biol Evol 19:587–596Google Scholar
  107. Xu Y, Teo LL, Zhou J, Kumar PP, Yu H (2006) Floral organ identity genes of the orchid Dendrobium crumenatum. Plant J 46:54–68Google Scholar
  108. Yadav SR, Prasad K, Vijayraghavan U (2007) Divergent regulatory OsMADS2 functions control size, shape and differentiation of the highly derived rice floret second-whorl organ. Genetics 176:283–294Google Scholar
  109. Yamada K, Saraike T, Shitsukawa N, Hirabayashi C, Takumi S, Murai K (2009) Class D and B sister MADS-box genes are associated with ectopic ovule formation in the pistil-like stamens of alloplasmic wheat ( Triticum aestivum L .). Plant Mol Biol 71:1–14Google Scholar
  110. Yao SG, Ohmori S, Kimizu M, Yoshida H (2008) Unequal genetic redundancy of rice PISTILLATA orthologs, OsMADS2 and OsMADS4, in lodicule and stamen development. Plant Cell Physiol 49:853–857Google Scholar
  111. Yu D, Kotilainen M, Pöllänen E, Mehto M, Elomaa P, Helariutta Y, Albert VA, Teeri TH (1999) Organ identity genes and modified patterns of flower development in Gerbera hybrida (Asteraceae). Plant J 17:51–62Google Scholar
  112. Yu J et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38Google Scholar
  113. Zahn LM, Leebens-Mack J, DePamphilis CW, Ma H, Theissen G (2005) To B or not to B a flower: the role of DEFICIENS and GLOBOSA orthologs in the evolution of the angiosperms. J Heredity 96:225–240Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Biologia, Departamento de Biologia VegetalUniversidade Estadual de Campinas (UNICAMP)CampinasBrazil

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