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A short history of MADS-box genes in plants

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Abstract

Evolutionary developmental genetics (evodevotics) is a novel scientific endeavor which assumes that changes in developmental control genes are a major aspect of evolutionary changes in morphology. Understanding the phylogeny of developmental control genes may thus help us to understand the evolution of plant and animal form. The principles of evodevotics are exemplified by outlining the role of MADS-box genes in the evolution of plant reproductive structures. In extant eudicotyledonous flowering plants, MADS-box genes act as homeotic selector genes determining floral organ identity and as floral meristem identity genes. By reviewing current knowledge about MADS-box genes in ferns, gymnosperms and different types of angiosperms, we demonstrate that the phylogeny of MADS-box genes was strongly correlated with the origin and evolution of plant reproductive structures such as ovules and flowers. It seems likely, therefore, that changes in MADS-box gene structure, expression and function have been a major cause for innovations in reproductive development during land plant evolution, such as seed, flower and fruit formation.

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References

  1. Abouheif E, Akam M, Dickinson WJ, Holland PWH, Meyer A, Patel NH, Raff RA, Roth VL, Wray GA: Homology and developmental genes. Trends Genet 13: 432–433 (1997).

    Google Scholar 

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

    Google Scholar 

  3. Albert VA, Gustafsson MHG, Di Laurenzio L: Ontogenetic systematics, molecular developmental genetics, and the angiosperm petal. In: Soltis DE, Soltis PS, Doyle JJ (eds), Molecular Systematics of Plants II, pp. 349–374. Kluwer Academic Publishers, Boston, MA (1998).

    Google Scholar 

  4. Angenent GC, Colombo L: Molecular control of ovule development. Trends Plant Sci 1: 228–232 (1996).

    Google Scholar 

  5. Arber EAN, Parkin J: Studies on the evolution of the angiosperms: the relationship of the angiosperms to the Gnetales. Ann Bot 22: 489–515 (1908).

    Google Scholar 

  6. Baum DA: The evolution of plant development. Curr Opin Plant Biol 1: 79–86 (1998).

    Google Scholar 

  7. Beck CB: Origin and Evolution of Gymnosperms. Columbia University Press, New York (1988).

    Google Scholar 

  8. Bowman JL, Smyth DR: Patterns of petal and stamen reduction in Australian species of Lepidium L. (Brassicaceae). Int J Plant Sci 159: 65–74 (1998).

    Google Scholar 

  9. 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 72: 85–95 (1993).

    Google Scholar 

  10. Cacharró n J: MADS-Box-Gene in Zea mays: Vergleichende Expressionsuntersuchungen an Modellen paraloger und orthologer Genpaare. Ph.D. thesis, Mathematisch-Naturwissenschaftliche Fakultät der Universität zu Köln, Germany (1998).

    Google Scholar 

  11. Cacharró n J, Fischer A, Saedler H, Theissen G: Expression patterns of MADS-box genes in maize as studied by in situ hybridization. Maize Genet Coop Newsl 69: 37–38 (1995).

    Google Scholar 

  12. Cacharró n J, Saedler H, Theissen G: Expression of the MADS-box genes ZMM8 andZMM14 during inflorescence development of Zea mays discriminates between the upper and the lower floret of each spikelet. Dev Genes Evol 209: 411–420 (1999).

    Google Scholar 

  13. Carmona MJ, Ortega N, Garcia-Maroto F: Isolation and molecular characterization of a new vegetative MADS-box gene from Solanum tuberosum L. Planta 207: 181–188 (1998).

    Google Scholar 

  14. Chasan R: Ceratopteris: a model plant for the 90s. Plant Cell 4: 113–115 (1992).

    Google Scholar 

  15. Chaw S-M, Zharkikh A, Sung H-M, Lau T-C, Li W-H: Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNA sequences. Mol Biol Evol 14: 56–68 (1997).

    Google Scholar 

  16. Cheng PC, Greyson RI, Walden DB: Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am J Bot 70: 450–462 (1983).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  19. Clifford HT: Spikelet and floral morphology. In: Soderstrom TR, Hilu KW, Campbell CS, Barkworth ME (eds), Grass Systematics and Evolution, pp. 21–30. Smithsonian Institution Press, Smithsonian Institution, Washington, DC (1987).

    Google Scholar 

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

    Google Scholar 

  21. Crane PR, Friis EM, Pedersen KR: The origin and early diversification of angiosperms. Nature 374: 27–33 (1995).

    Google Scholar 

  22. Di Rosa A: Molekularbiologische Untersuchungen zum Ursprung homöotischer Gene in Pflanzen am Beispiel der MADS-Box-Genfamilie aus dem Farn Ceratopteris richardii. PhD thesis, Mathematisch-Naturwissenschaftliche Fakultät der Universität zu Köln, Germany (1998).

    Google Scholar 

  23. Doebley J, Lukens L: Transcriptional regulators and the evolution of plant form. Plant Cell 10: 1075–1082 (1998).

    Google Scholar 

  24. Doyle JA: Origin of the angiosperm flower: a phylogenetic perspective. Plant Syst Evol (Suppl) 8: 7–29 (1994).

    Google Scholar 

  25. Doyle JA: Seed plant phylogeny and the relationships of Gnetales. Int J Plant Sci 157 (Suppl): S3–S39 (1996).

    Google Scholar 

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

    Google Scholar 

  27. Doyle JJ: Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3: 473–478 (1998).

    Google Scholar 

  28. Endress PK: Evolution and floral diversity: the phylogenetic surroundings of Arabidopsis and Antirrhinum. Int J Plant Sci 153: S106–S122 (1992).

    Google Scholar 

  29. Endress PK: Floral structure and evolution of primitive angiosperms: recent advances. Plant Syst Evol 192: 79–97 (1994).

    Google Scholar 

  30. Fan H-Y, Hu Y, Tudor M, Ma H: Specific interactions between the K domains of AG and AGLs, members of the MADS domain family of DNA binding proteins. Plant J 12: 999–1010 (1997).

    Google Scholar 

  31. Fischer A, Baum N, Saedler H, Theissen G: Chromosomal mapping of the MADS-box multigene family in Zea mays reveals dispersed distribution of allelic genes as well as transposed copies. Nucl Acids Res 23: 1901–1911 (1995).

    Google Scholar 

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

    Google Scholar 

  33. Gandolfo MA, Nixon KC, Crepet WL, Stevenson DW, Friis EM: Oldest known fossils of monocotyledons. Nature 394: 532–533 (1998).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  36. Gifford EM, Foster AS: Morphology and Evolution of Vascular Plants, 3rd ed. Freeman, New York (1988).

    Google Scholar 

  37. Gilbert SF, Opitz JM, Raff RA: Resynthesizing evolutionary and developmental biology. Dev Biol 173: 357–372 (1996).

    Google Scholar 

  38. Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G: A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386: 44–51 (1997).

    Google Scholar 

  39. Goremykin V, Bobrova V, Pahnke J, Troitsky A, Antonov A, Martin W: Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support Gnetalean affinities of angiosperms. Mol Biol Evol 13: 383–396 (1996).

    Google Scholar 

  40. Goremykin VV, Hansmann S, Martin WF: 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: 337–351 (1997).

    Google Scholar 

  41. Gould SJ: Ontogeny and phylogeny - revisited and reunited. BioEssays 14: 275–279 (1992).

    Google Scholar 

  42. Greco R, Stagi L, Colombo L, Angenent GC, Sari-Gorla M, Pè ME: MADS box genes expressed in developing inflorescences of rice and sorghum. Mol Gen Genet 253: 615–623 (1997).

    Google Scholar 

  43. Gu Q, Ferrándiz C, Yanofsky MF, Martienssen R: The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125: 1509–1517 (1998).

    Google Scholar 

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

    Google Scholar 

  45. Hasebe M, Banks JA: Evolution of MADS gene family in plants. In: Iwatsuki K, Raven PH (eds), Evolution and Diversification of Land Plants, pp. 179–197. Springer-Verlag, Tokyo (1997).

    Google Scholar 

  46. Hasebe M, Wen C-K, Kato M, Banks JA: Characterization of MADS homeotic genes in the fern Ceratopteris richardii. Proc Natl Acad Sci USA 95: 6222–6227 (1998).

    Google Scholar 

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

    Google Scholar 

  48. Hill TA, Day CD, Zondlo SC, Thackeray AG, Irish VF: Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development 125: 1711–1721 (1998).

    Google Scholar 

  49. Huang H, Tudor M, Weiss CA, Hu Y, Ma H: The Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein. Plant Mol Biol 28: 549–567 (1995).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  52. Jofuku KD, den Boer BGW, Van Montagu M, Okamuro JK: Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6: 1211–1225 (1994).

    Google Scholar 

  53. Kang H-G, An G: Isolation and characterization of a rice MADS box gene belonging to the AGL2 gene family. Mol Cell 7: 45–51 (1997).

    Google Scholar 

  54. Kang H-G, Jeon J-S, Lee S, An G: Identification of class B and class C floral organ identity genes from rice. Plant Mol Biol 38: 1021–1029 (1998).

    Google Scholar 

  55. Kang H-G, Noh Y-S, Chung Y-Y, 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 29: 1–10 (1995).

    Google Scholar 

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

    Google Scholar 

  57. Kenrick P, Crane PR: The origin and early evolution of plants on land. Nature 389: 33–39 (1997).

    Google Scholar 

  58. Kofuji R, Yamaguchi K: Isolation and phylogenetic analysis of MADS genes from the fern Ceratopteris richardii. J Phytogeogr Taxon 45: 83–91 (1997).

    Google Scholar 

  59. Kramer EM, Irish VF: Evolution of genetic mechanisms controlling petal development. Nature 399: 144–148 (1999).

    Google Scholar 

  60. 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 149: 765–783 (1998).

    Google Scholar 

  61. Krüger J, Aichinger C, Kahmann R, Bölker M: A MADSbox homologue in Ustilago maydis regulates the expression of pheromone-inducible genes but is nonessential. Genetics 147: 1643–1652 (1997).

    Google Scholar 

  62. Kyozuka J, Harcourt R, Peacock WJ, Dennis ES: Eucalyptus has functional equivalents of the Arabidopsis AP1 gene. Plant Mol Biol 35: 573–584 (1997).

    Google Scholar 

  63. Liljegren SJ, Ferrándiz C, Alvarez-Buylla ER, Pelaz S, Yanofsky MF: Arabidopsis MADS-box genes involved in fruit dehiscence. Flowering Newsl 25: 9–19 (1998).

    Google Scholar 

  64. Liu J-J, Podila GK: Characterization of a MADS box gene (Accession No. Y09611) from immature female cone of red pine (PGR 97-032). Plant Physiol 113: 665 (1997).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  67. Maes T, Van de Steene N, Van Montagu M, Gerats T: The AP2-like genes of Petunia hybrida. Flowering Newsl 25: 35–40 (1998).

    Google Scholar 

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

    Google Scholar 

  69. Martin WF: Is something wrong with the tree of life? BioEssays 18: 523–527 (1996).

    Google Scholar 

  70. McGinnis W, Kuziora M: The molecular architects of body design. Scient Am 270 (2): 36–42 (1994).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  73. Meyerowitz EM: Plants and the logic of development. Genetics 145: 5–9 (1997).

    Google Scholar 

  74. Meyerowitz EM: Genetic and molecular mechanisms of pattern formation in Arabidopsis flower development. J Plant Res 111: 233–242 (1998).

    Google Scholar 

  75. Mizukami Y, Ma H: Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71: 119–131 (1992).

    Google Scholar 

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

    Google Scholar 

  77. Monod J: Le hasard et la nécessité. Éditions du Seuil, Paris (1970).

    Google Scholar 

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

    Google Scholar 

  79. Montag K, Salamini F, Thompson RD: The ZEM2 family of maize MADS box genes possess features of transposable elements. Maydica 41: 241–254 (1996).

    Google Scholar 

  80. Motte P, Wilkinson M, Schwarz-Sommer Z: Floral meristem identity and the A function in Antirrhinum. Flowering Newsl 25: 41–43 (1998).

    Google Scholar 

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

    Google Scholar 

  82. Mouradov A, Glassick T, Teasdale R: Isolation and characterization of a new MADS-box cDNA from Pinus radiata (Accession No. U76726) (PGR 97-027). Plant Physiol 113: 664 (1997).

    Google Scholar 

  83. Mouradov A, Glassick T, Vivian-Smith A, Teasdale R: Isolation of a MADS box gene family from Pinus radiata (accession No. U42399 and U42400) (PGR 96-002). Plant Physiol 110: 1047 (1996).

    Google Scholar 

  84. Mouradov A, Hamdorf B, Teasdale RD, Kim J, Winter KU, Theissen G: A DEF/GLO-like MADS-box gene from a gymnosperm: Pinus radiata contains an orthologue of angiosperm B class floral homeotic genes. Dev Genet (in press) (1999).

  85. 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 USA 94: 2415–2420 (1997).

    Google Scholar 

  86. Murai K, Murai R, Ogihara Y: Wheat MADS box genes, a multigene family dispersed throughout the genome. Genes Genet Syst 72: 317–321 (1997).

    Google Scholar 

  87. Mushegian AR, Koonin EV: Sequence analysis of eukaryotic developmental proteins: ancient and novel domains. Genetics 144: 817–828 (1996).

    Google Scholar 

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

    Google Scholar 

  89. Okamoto H, Silverthorne J, Wada M: Spatial patterns of phytochrome expression in young leaves of the fern Adiantum capillus-veneris. Plant Cell Physiol 38: 1397–1402 (1997).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  92. 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 39: 701–710 (1998).

    Google Scholar 

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

    Google Scholar 

  94. Pichersky E, Soltis D, Soltis P: Defective chlorophyll a/bbinding protein genes in the genome of a homosporous fern. Proc Natl Acad Sci USA 87: 195–199 (1990).

    Google Scholar 

  95. Pryer KM, Smith AR, Skog JE: Phylogenetic relationships of extant ferns based on evidence from morphology and rbcL sequences. Am Fern J 85: 205–282 (1995).

    Google Scholar 

  96. Purugganan MD: The MADS-box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J Mol Evol 45: 392–396 (1997).

    Google Scholar 

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

    Google Scholar 

  98. Purugganan MD, Suddith JI: Molecular population-genetics of the Arabidopsis cauliflower regulatory gene: nonneutral evolution and naturally occuring variation in floral homeotic function. Proc Natl Acad Sci USA 95: 8130–8134 (1998).

    Google Scholar 

  99. Purugganan MD, Suddith JI: Molecular population genetics of floral homeotic loci: departures from the equilibriumneutral model at the APETALA3 and PISTILLATA genes of Arabidopsis thaliana. Genetics 151: 839–848 (1999).

    Google Scholar 

  100. Qiu Y-L, Cho Y, Cox JC, Palmer JD: The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394: 671–674 (1998).

    Google Scholar 

  101. Raff RA: The Shape of Life. Genes, Development, and the Evolution of Animal Form. University of Chicago Press, Chicago, IL (1996).

    Google Scholar 

  102. Reeves PA, Olmstead RG: Evolution of novel morphological and reproductive traits in a clade containing Antirrhinum majus (Scrophulariaceae). Am J Bot 85: 1047–1056 (1998).

    Google Scholar 

  103. Riechmann JL, Meyerowitz EM: MADS domain proteins in plant development. Biol Chem 378: 1079–1101 (1997).

    Google Scholar 

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

    Google Scholar 

  105. Rutledge R, Regan S, Nicolas O, Fobert P, Coté 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 15: 625–634 (1998).

    Google Scholar 

  106. Sablowski RWM, Meyerowitz EM: A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92: 93–103 (1998).

    Google Scholar 

  107. Samach A, Kohalmi SE, Motte P, Datla R, Haughn GW: Divergence of function and regulation of class B floral organ identity genes. Plant Cell 9: 559–570 (1997).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  110. 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 5: 729–737 (1993).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  113. Sieburth LE, Meyerowitz EM: Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9: 355–365 (1997).

    Google Scholar 

  114. Slack JMW, Holland PWH, Graham CF: The zootype and the phylotypic stage. Nature 361: 490–492 (1993).

    Google Scholar 

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

    Google Scholar 

  116. Sundström J, Carlsbecker A, Svensson M, Svenson M, Urban J, Theissen G, Engström P: MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms. Dev Genet (in press).

  117. Stewart WN, Rothwell GW: Paleobotany and the Evolution of Plants, 2nd ed. Cambridge University Press, Cambridge, UK (1993).

    Google Scholar 

  118. Tandre K: Molecular approaches to the developmental biology of Norway spruce, Picea abies. Acta Universitatis Upsaliensis, Uppsala, Sweden (1997).

    Google Scholar 

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

    Google Scholar 

  120. 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 15: 615–623 (1998).

    Google Scholar 

  121. Taylor TN, Taylor EL: The Biology and Evolution of Fossil Plants. Prentice Hall, Englewood Cliffs, NJ (1993).

    Google Scholar 

  122. Theissen G, Cacharró n J, Fischer A, Saedler H: MADS-box genes in the evolution of maize (Zea mays ssp. mays). In: Hong JC, Kim MJ (eds), Proceedings of the 2nd Korea-Germany Joint Symposium in Plant Biotechnology, pp. 1–12. Gyeongsang National University of Korea, Chinju, Korea (1994).

    Google Scholar 

  123. Theissen G, Kim J, Saedler H: Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43: 484–516 (1996).

    Google Scholar 

  124. Theissen G, Saedler H: MADS-box genes in plant ontogeny and phylogeny: Haeckel's 'biogenetic law' revisited. Curr Opin Genet Dev 5: 628–639 (1995).

    Google Scholar 

  125. Theissen G, Saedler H: Molecular architects of plant body plans. Prog Bot 59: 227–256 (1998).

    Google Scholar 

  126. 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 156: 155–166 (1995).

    Google Scholar 

  127. Tilly JJ, Allen DW, Jack T: The CArG boxes in the promoter of the Arabidopsis floral organ identity gene APETALA3 mediate diverse regulatory effects. Development 125: 1647–1657 (1998).

    Google Scholar 

  128. Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig WE, Saedler H, Sommer H, Schwarz-Sommer Z: GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11: 4693–4704 (1992).

    Google Scholar 

  129. van Tunen AJ, Eikelboom W, Angenent GC: Floral organogenesis in Tulipa. Flowering Newsl 16: 33–37 (1993).

    Google Scholar 

  130. Veuthey A-L, Bittar G: Phylogenetic relationships of fungi, plantae, and animalia inferred from homologous comparison of ribosomal proteins. J Mol Evol 47: 81–92 (1998).

    Google Scholar 

  131. Weigel D, Meyerowitz EM: Genetic hierarchy controlling flower development. In: Bernfeld M (ed), Molecular Basis of Morphogenesis, pp. 91–105. John Wiley, New York (1993).

    Google Scholar 

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

    Google Scholar 

  133. Winter K-U: Charakterisierung von MADS-Box-Genen der Gymnosperme Gnetum gnemon L. Diploma thesis, Universität Bonn, Germany (1997).

    Google Scholar 

  134. Winter K-U, 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 USA 96: 7342–7347 (1999).

    Google Scholar 

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

    Google Scholar 

  136. Yabana N, Yamamoto M: Schizosaccharomyces pombe map1C encodes a MADS-box-family protein required for cell-type-specific gene expression. Mol Cell Biol 16: 3420–3428 (1996).

    Google Scholar 

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

    Google Scholar 

  138. 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 17: 51–62 (1999).

    Google Scholar 

  139. Zachgo S, de Andra Silva E, Motte P, Tröbner W, Saedler H, Schwarz-Sommer Z: Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant. Development 121: 2861–2875 (1995).

    Google Scholar 

  140. Zachgo S, Saedler H, Schwarz-Sommer Z: Pollen-specific expression of DEFH125, a MADS-box transcription factor in Antirrhinum with unusual features. Plant J 11: 1043–1050 (1997).

    Google Scholar 

  141. Zhang H, Forde BG: An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407–409 (1998).

    Google Scholar 

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

    Günter Theissen, Annette Becker, Alexandra Di Rosa, Akira Kanno, Jan T. Kim, Thomas Münster, Kai-Uwe Winter & Heinz Saedler

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  1. Günter Theissen
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  2. Annette Becker
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  3. Alexandra Di Rosa
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Theissen, G., Becker, A., Di Rosa, A. et al. A short history of MADS-box genes in plants. Plant Mol Biol 42, 115–149 (2000). https://doi.org/10.1023/A:1006332105728

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