The major clades of MADS-box genes and their role in the development and evolution of flowering plants

Molecular Phylogenetics and Evolution

Volumn 29, Issue 3, 2003, Pages 464-489

  Becker, Annette ^a   Theißen, Günter ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ARABIDOPSIS; BRASSICACEAE; FUNGI; GYMNOSPERMAE; LILIOPSIDA; MAGNOLIOPHYTA; SPERMATOPHYTA;

EID: 0345581665     PISSN: 10557903     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1055-7903(03)00207-0     Document Type: Article

References (153)

1. Albert, V.A., Gustafsson, M.H.G., Di Laurenzio, L., 1998. Ontogenetic systematics, molecular developmental genetics, and the angiosperm petal. In: Soltis, D.E., Soltis, P.S., Doyle, J.J. (Eds.), Molecular Systematics of Plants II. Kluwer Academic Publishers, Boston, USA, pp. 349-374.
2. Allen, K.D., 2002. Assaying gene content in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 9568-9572.
3. Alvarez-Buylla, E.R., Liljegren, S.J., Pelaz, S., Gold, S.E., Burgeff, C., Ditta, G.S., Vergara-Silva, F., Yanofsky, M.F., 2000a. MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J. 24, 457-466.
4. Alvarez-Buylla, E.R., Pelaz, S., Liljegren, S.J., Gold, S.E., Burgeff, C., Ditta, G.S., De Pouplana, L.R., Martinez-Castilla, L., Yanofsky, M.F., 2000b. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl. Acad. Sci. USA 97, 5328-5333.
5. Ambrose, B.A., Lerner, D.R., Ciceri, P., Padilla, C.M., Yanofsky, M.F., Schmidt, R.F., 2000. Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell. 5, 569-579.
6. Ampomah-Dwamena, C., Morris, B.A., Sutherland, P., Veit, B., Yao, J.-L., 2002. Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol. 130, 605-617.
7. Ando, S., Sato, Y., Kamachi, S., Sakai, S., 2001. Isolation of a MADS-box gene (ERAF17) and correlation of its expression with the induction of formation of female flowers by ethylene in cucumber plants (Cucumis sativus L.). Planta 213, 943-952.
8. Angenent, G.C., Colombo, L., 1996. Molecular control of ovule development. Trends Plant Sci. 1, 228-232.
9. Angenent, G.C., Franken, J., Busscher, M., Weiss, D., van Tunen, A.J., 1994. Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J. 5, 33-44.
10. The Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
11. Barkman, T.J., Chenery, G., McNeal, J.R., Lyons-Weiler, J., Ellisens, W.J., Moore, G., Wolfe, A.D., dePamphilis, C.W., 2000. Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. Proc. Natl. Acad. Sci. USA 97, 13166-13171.
12. Becker, A., Winter, K.-U., Meyer, B., Saedler, H., Theißen, G., 2000. MADS-box gene diversity in seed plants 300 million years ago. Mol. Biol. Evol. 17, 1425-1434.
13. Becker, A., Kaufmann, K., Freialdenhoven, A., Vincent, C., Li, M.-A., Saedler, H., Theißen, G., 2002. A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Mol. Genet. Genomics 266, 942-950.
14. Berbel, A., Navarro, C., Ferrándiz, C., Canas, L.A., Madueno, F., Beltran, J.-P., 2001. Analysis of PEAM4, the pea AP1 functional homologue, supports a model for AP1-like genes controlling both floral meristem and floral organ identity in different plant species. Plant J. 25, 441-451.
15. Borner, R., Kampmann, G., Chandler, J., Gleißner, R., Wisman, E., Apel, K., Melzer, S., 2000. A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24, 591-599.
16. Bowe, L.M., Coat, G., dePamphilis, C.W., 2000. Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. Proc. Natl. Acad. Sci. USA 97, 4092-4097.
17. Bradley, D., Carpenter, R., Sommer, H., Hartley, N., Coen, E., 1993. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72, 85-95.
18. Burgeff, C., Liljegren, S.J., Tapia-López, R., Yanofsky, M.F., Alvarez-Buylla, E.R., 2002. MADS-box gene expression in lateral primordia, meristems and differentiated tissues of Arabidopsis thaliana roots. Planta 214, 365-372.
19. Cacharrón, J., Saedler, H., Theißen, G., 1999. Expression of the 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.
20. Carmona, M.-J., Ortega, N., Garcia-Maroto, F., 1998. Isolation and molecular characterization of a new vegetative MADS-box gene from Solanum tuberosum L. Planta 207, 181-188.
21. Chaw, S.-M., Zharkikh, A., Sung, H.-M., Lau, T.-C., Li, W.-H., 1997. Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNA sequences. Mol. Biol. Evol. 14, 56-68.
22. Chaw, S.-M., Parkinson, C.L., Cheng, Y., Vincent, T.M., Palmer, J.D., 2000. Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc. Natl. Acad. Sci. USA 97, 4086-4091.
23. Cho, S., Jang, S., Chae, S., Chung, K.M., Moon, Y., An, G., Jang, S.K., 1999. Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol. Biol. 40, 419-429.
24. Chung, Y.-Y., Kim, S.-R., Finkel, D., Yanofsky, M.F., 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.
25. Davies, B., Motte, P., Keck, E., Saedler, H., Sommer, H., Schwarz-Sommer, Z., 1999. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J. 18, 4023-4034.
26. De Bodt, S., Raes, J., Florquin, K., Rombauts, S., Rouzé, P., Theißen, G., Van de Peer, Y., 2003. Genome-wide structural annotation and evolutionary analysis of the type I MADS-box genes in plants. J. Mol. Evol. 56, 573-586.
27. Doyle, J.J., 1994. Evolution of a plant homeotic multigene family: towards connecting molecular systematics and molecular developmental genetics. Syst. Biol. 43, 307-328.
28. Drinnan, A.N., Crane, P.R., Hoot, S.B., 1994. Patterns of floral evolution in the early diversification of non-magnoliid dicotyledons (eudicots). Plant Syst. Evol. 8, 93-122.
29. 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 Anthirrinum majus. EMBO J. 18, 5370-5379.
30. Fan, H.Y., Hu, Y., Tudor, M., Ma, H., 1997. 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.
31. Fernandez, D., Heck, G.R., Perry, S.E., Patterson, S.E., Bleecker, A.B., Fang, S.C., 2000. The embryo MADS domain factor AGL15 acts postembryonically: inhibition of perianth senescence and abscission via constitutive expression. Plant Cell 12, 183-197.
32. Ferrándiz, C., Gu, Q., Martienssen, R., Yanofsky, M.F., 2000. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127, 725-734.
33. Fischer, A., Baum, N., Saedler, H., Theißen, G., 1995a. Chromosomal mapping of the MADS-box multigene family in Zea mays reveals dispersed distribution of allelic genes as well as transposed copies. Nucleic Acids Res. 23, 1901-1911.
34. Fischer, A., Saedler, H., Theißen, G., 1995b. Restriction fragment length polymorphism-coupled domain-directed differential display: a highly efficient technique for expression analysis of multigene families. Proc. Natl. Acad. Sci. USA 92, 5331-5335.
35. Flanagan, C.A., Ma, H., 1994. Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant Arabidopsis flowers. Plant Mol. Biol. 26, 581-595.
36. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.-I., Postlethwait, J., 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531-1545.
37. Frohlich, M.W., Parker, D.S., 2000. The mostly male theory of flower evolutionary origins: from genes to fossils. Syst. Bot. 25, 155-170.
38. Fukui, M., Futamura, N., Mukai, Y., Wang, Y., Nagao, A., Shinohara, K., 2001. Ancestral MADS box genes in Sugi, Cryptomeria japonica D. Don (Taxodiaceae), homologous to the B function genes in angiosperms. Plant Cell Physiol. 42, 566-575.
39. Garcia-Maroto, F., Ortega, N., Lozano, R., Carmona, M.J., 2000. Characterization of the potato MADS-box gene STMADS16 and expression analysis in tobacco transgenic plants. Plant Mol. Biol. 42, 499-513.
40. Goff, S.A., Ricke, D., Lan, T.H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., Hadley, D., Hutchison, D., Martin, C., Katagiri, F., Lange, B.M., Moughamer, T., Xia, Y., Budworth, P., Zhong, J., Miguel, T., Paszkowski, U., Zhang, S., Colbert, M., Sun, W.L., Chen, L., Cooper, B., Park, S., Wood, T.C., Mao, L., Quail, P., Wing, R., Dean, R., Yu, Y., Zharkikh, A., Shen, R., Sahasrabudhe, S., Thomas, A., Cannings, R., Gutin, A., Pruss, D., Reid, J., Tavtigian, S., Mitchell, J., Eldredge, G., Scholl, T., Miller, R.M., Bhatnagar, S., Adey, N., Rubano, T., Tusneem, N., Robinson, R., Feldhaus, J., Macalma, T., Oliphant, A., Briggs, S., 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92-100.
41. Goremykin, V., Bobrova, V., Pahnke, J., Troitsky, A., Antonov, A., Martin, W., 1996. Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbc L data do not support Gnetalean affinities of angiosperms. Mol. Biol. Evol. 13, 383-396.
42. Goremykin, V., Hansmann, S., Martin, W.F., 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, 337-351.
43. Goto, K., Meyerowitz, E.M., 1994. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8, 1548-1560.
44. Graham, S.W., Olmstead, R.G., 2000. Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. Am. J. Bot. 87, 1712-1730.
45. Gu, Q., Ferrándiz, C., Yanofsky, M.F., Martienssen, R., 1998. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 1509-1517.
46. Hartmann, U., Höhmann, S., Nettesheim, K., Wisman, E., Saedler, H., Huijser, P., 2000. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351-360.
47. Haughn, G.W., Somerville, C.R., 1988. Genetic control of morphogenesis in Arabidopsis. Dev. Genet. 9, 73-89.
48. Hasebe, M., Banks, J.A., 1997. Evolution of MADS gene family in plants. In: Iwatsuki, K., Raven, R.H. (Eds.), Evolution and Diversification of Land Plants. Springer-Verlag, Tokyo, Japan, pp. 179-197.
49. Hasebe, M., Kofuji, R., Ito, M., Kato, M., Iwatsuki, K., Ueda, K., 1992. Phylogeny of gymnosperms inferred from rbcL gene sequences. Bot. Mag. Tokyo 105, 673-679.
50. Hasebe, M., Wen, C.-K., Kato, M., Banks, J.A., 1998. Characterization of MADS homeotic genes in the fern Ceratopteris richardii. Proc. Natl. Acad. Sci. USA 95, 6222-6227.
51. Heard, J., Caspi, M., Dunn, K., 1997. Evolutionary diversity of symbolically induced nodule MADS box genes: characterization of nmhC5, a member of a novel subfamily. Mol. Plant-Microbe Interact. 10, 665-676.
52. Heck, G., Perry, S.E., Nichols, K.W., Fernandez, D.E., 1995. AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 7, 1271-1282.
53. Henschel, K., Kofuji, R., Hasebe, M., Saedler, H., Münster, T., Theißen, G., 2002. Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol. Biol. Evol. 19, 801-814.
54. Heuer, S., Lörz, H., Dresselhaus, T., 2000. The MADS box gene ZmMADS2 is specifically expressed in maize pollen and during maize pollen tube growth. Sex. Plant Reprod. 13, 21-27.
55. Heuer, S., Hansen, S., Bantin, J., Brettschneider, R., Kranz, E., Lörz, 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.
56. Hohe, A., Rensing, S.A., Mildner, M., Lang, D., Reski, R., 2002. Day length and temperature strongly influence sexual reproduction and expression of a novel MADS-box gene in the moss Physcomitrella patens. Plant Biol. 4, 595-602.
57. Honma, T., Goto, K., 2001. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409, 525-529.
58. Huang, H., Tudor, M., Weiss, C.A., Hu, Y., Ma, H., 1995. The Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein. Plant Mol. Biol. 28, 549-567.
59. Huijser, P., Klein, J., Lönnig, W.-E., Meijer, H., Saedler, H., Sommer, H., 1992. 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.
60. Immink, R.G.H., Hannapel, D.J., Ferrario, S., Busscher, M., Franken, J., Lockeren Campagne, M.M., Angenent, G.C., 1999. A petunia MADS-box gene involved in the transition from vegetative to reproductive development. Development 126, 5117-5126.
61. Jack, T., Brockmann, L.L., Meyerowitz, E.M., 1992. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68, 683-697.
62. Jeon, J.-S., Jang, S., Lee, S., Nam, J., Kim, C., Lee, S.-H., Chung, Y.-Y., Kim, S.-R., Lee, Y.H., Cho, Y.-G., An, G., 2000. leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell 12, 871-884.
63. Kang, H.-G., An, G., 1997. Isolation and characterization of a rice MADS box gene belonging to the AGL2 gene family. Mol. Cells 7, 45-51.
64. Kang, H.-G., Jeon, J.-S., Lee, S., An, G., 1998. Identification of class B and class C floral organ identity genes from rice. Plant Mol. Biol. 38, 1021-1029.
65. Karol, K.G., McCourt, R.M., Cimino, M.T., Delwiche, C.F., 2001. The closest living relatives of land plants. Science 294, 2351-2353.
66. Kempin, S.A., Savidge, B., Yanofsky, M.F., 1995. Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267, 522-525.
67. Kenrick, P., Crane, P.R., 1997. The origin and early evolution of plants on land. Nature 389, 33-39.
68. Kim, S., Mizuno, K., Fujimura, T., 2002. Isolation of MADS-box genes from sweet potatoe (Ipomoea batatas (L.) Lam.) expressed specifically in vegetative tissue. Plant Cell. Physiol. 43, 314-322.
69. Kofuji, R., Yamaguchi, K., 1997. Isolation and phylogenetic analysis of MADS genes from the fern Ceratopteris richardii. J. Phytogeogr. Taxon. 45, 83-91.
70. Koonin, E.V., Wolf, Y.I., Karev, G.P., 2002. The structure of the protein universe and genome evolution. Nature 420, 218-223.
71. Kotilainen, M., Elomaa, P., Uimari, A., Albert, V.A., Yu, D., Teeri, T.H., 2000. GRCD1, an AGL2-like MADS-box gene, participates in the C function during stamen development in Gerbera hybrida. Plant Cell 12, 1893-1902.
72. Kramer, E.M., Irish, V.F., 1999. Evolution of genetic mechanisms controlling petal development. Nature 399, 144-148.
73. Kramer, E.M., Irish, V.F., 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 (6 Suppl.), S29-S40.
74. Kramer, E.M., Dorit, R.L., Irish, V.F., 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.
75. Krogan, N.T., Ashton, N.W., 2000. Ancestry of plant MADS-box genes revealed by bryophyte (Physcomitrella patens) homologues. New Phytol. 147, 505-517.
76. Kuzoff, R.K., Gasser, C.S., 2000. Recent progress in reconstructing angiosperm phylogeny. Trends Plant Sci. 5, 330-336.
77. Lawton-Rauh, A.L., Alvarez-Buylla, E.R., Purugganan, M.D., 2000. Molecular evolution of flower development. Trends Ecol. Evol. 15, 144-149.
78. Lee, H., Suh, S.-S., Park, E., Cho, E., Ahn, J.H., Kim, S.-G., Lee, J.S., Kwon, Y.M., Lee, I., 2000. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366-2376.
79. Liljegren, S.J., Ditta, G.S., Eshed, Y., Savidge, B., Bowman, J.L., Yanofsky, M.F., 2000. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766-770.
80. Lopez-Dee, Z.P., Wittich, P., Pè, M.E., Rigola, D., Buono, I.D., Sari Gorla, M., Kater, M.M., Colombo, L., 1999. OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev. Genet. 25, 237-244.
81. Ma, H., dePamphilis, C., 2000. The ABCs of floral evolution. Cell 101, 5-8.
82. Ma, H., Yanofsky, M.F., Meyerowitz, E.M., 1991. AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5, 484-495.
83. Mandel, M.A., Yanofsky, M.F., 1998. The Arabidopsis AGL9 MADS box gene is expressed in young flower primordia. Sex Plant Reprod. 11, 22-28.
84. Mandel, M.A., Gustafson-Brown, C., Savidge, B., Yanofsky, M.F., 1992. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360, 273-277.
85. Mathews, S., Donoghue, M.J., 1999. The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286, 947-950.
86. Mao, L., Begum, D., Chuang, H.-W., Budiman, M.A., Szymkowiak, E.J., Irish, E.E., Wing, R.A., 2000. JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature 406, 910-913.
87. Mena, M., Mandel, M.A., Lerner, D.R., Yanofsky, M.F., Schmidt, R.J., 1995. A characterization of the MADS-box gene family in maize. Plant J. 8, 845-854.
88. Menzel, G., Apel, K., Melzer, S., 1996. Identification of two MADS box genes that are expressed in the apical meristem of the long-day plant Sinapis alba in transition to flowering. Plant J. 9, 399-408.
89. Michaels, S.D., Amasino, R.M., 1999. Flowering Locus C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956.
90. Mouradov, A., Glassick, T.V., Hamdorf, B.A., Murphy, L.C., Marla, S.S., Yang, Y., Teasdale, R., 1998. Family of MADS-box genes expressed in early male and female reproductive structures of Monterey Pine. Plant Physiol. 117, 55-61.
91. Mouradov, A., Hamdorf, B., Teasdale, R.D., Kim, J.T., Winter, K.-U., Theißen, G., 1999. A DEF/GLO-like MADS-box gene from a gymnosperm: Pinus radiata contains an ortholog of angiosperm B class floral homeotic genes. Dev. Genet. 25, 245-252.
92. Münster, T., Pahnke, J., Di Rosa, A., Kim, J.T., 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. Proc. Natl. Acad. Sci. USA 94, 2415-2420.
93. Münster, T., Wingen, L.U., 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 genes of grasses. Gene 262, 1-13.
94. Münster, T., Deleu, W., Wingen, L.U., Ouzunova, M., Cacharrón, J., Faigl, W., Werth, S., Kim, J.T.T., Saedler, H., Theißen, G., 2002a. Maize MADS-box genes galore. Maydica 47, 287-301.
95. Münster, T., Faigl, W., Saedler, H., Theißen, G., 2002b. Evolutionary aspects of MADS-box genes in the eusporangiate fern Ophioglossum. Plant Biol. 4, 474-483.
96. Nesi, N., Debeaujon, I., Jond, C., Stewart, A.J., Jenkins, G.I., Caboche, M., Lepiniec, L., 2002. The TRANSPARANT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14, 2463-2479.
97. Niklas, K.J., 2000. The evolution of plant body plans - a biomechanical perspective. Ann. Botany 85, 411-438.
98. Ng, M., Yanofsky, M., 2001. Function and evolution of the plant MADS-box gene family. Nat. Rev. Gen. 2, 186-195.
99. Onouchi, H., Igeno, M.I., Périlleux, C., Graves, K., Coupland, G., 2000. Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-times genes. Plant Cell 12, 885-900.
100. Parkinson, C.L., Adams, K.L., Palmer, J.D., 1999. Multigene analyses identify the three earliest lineages of extant flowering plants. Curr. Biol. 9, 1485-1488.
101. Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E., Yanofsky, M.F., 2000. B and C organ identity functions require SEPALLATA MADS-box genes. Nature 405, 200-203.
102. Pelucchi, N., Fornara, F., Favalli, C., Masiero, S., Lago, C., Pé, E., Colombo, L., Kater, M.M., 2002. Comparative analysis of rice MADS-box genes expressed during flower development. Sex Plant Reprod. 15, 113-122.
103. Perry, S.E., Nichols, K.W., Fernandez, D.E., 1996. The MADS domain protein AGL15 localizes to the nucleus during early stages of seed development. Plant Cell 8, 1977-1989.
104. Pnueli, L., Abu-Abeid, M., Zamir, D., Nacken, W., Schwarz-Sommer, Z., Lifschitz, E., 1991. The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. Plant J. 1, 255-266.
105. Pnueli, L., Hareven, D., Broday, L., Hurwitz, C., Lifschitz, E., 1994. The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6, 175-186.
106. Prakash, A.P., Kumar, P.P., 2002. PkMADS1 is a novel MADS box gene regulating adventitious shoot induction and vegetative shoot development in Paulownia kawakamii. Plant J. 29, 141-151.
107. Prince, V.E., Pickett, F.B., 2002. Splitting pairs: the diverging fates of duplicate genes. Nat. Rev. Genet. 3, 827-837.
108. Pryer, K.M., Schneider, H., Smith, A.R., Cranfill, R., Wolf, P.G., Hunt, J.S., Sipes, S.D., 2001. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409, 618-622.
109. Purugganan, M.D., 1997. The MADS-box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J. Mol. Biol. 45, 392-396.
110. Purugganan, M.D., Rounsley, S.D., Schmidt, R.J., Yanofsky, M.F., 1995. Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140, 345-356.
111. Qiu, Y.-L., Lee, J., Bernasconi-Quadroni, F., Soltis, D.E., Soltis, P.S., Zanis, M., Zimmer, E.A., Chen, Z., Savolainen, V., Chase, M.W., 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402, 404-407.
112. Ratcliffe, O.J., Nadzan, G.C., Reuber, T.L., Riechmann, J.L., 2001. Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol. 126, 122-132.
113. Riechmann, J.L., Meyerowitz, E.M., 1997. MADS domain proteins in plant development. Biol. Chem. 378, 1079-1101.
114. Rounsley, S.D., Ditta, G.S., Yanofsky, M.F., 1995. Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7, 1259-1269.
115. Rutledge, R., Regan, S., Nicolas, O., Fobert, P., Cote, C., Bosnich, W., Kauffeldt, C., Sunohara, G., Seguin, A., Stewart, D., 1998. 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.
116. Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
117. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F., Coupland, G., 2000. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1616.
118. Samigullin, T.K., Martin, W.F., Troitsky, A.V., Antonov, A.S., 1999. Molecular data from the chloroplast rpoC gene suggest a deep and distinct dichotomy of contemporary spermatophytes into two monophyla: gymnosperms (including Gnetales) and angiosperms. J. Mol. Evol. 49, 310-315.
119. Savard, L., Li, P., Strauss, S.H., Chase, M.W., Michaud, M., Bousquet, J., 1994. 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.
120. Savidge, B., Rounsley, S.D., Yanofsky, M.F., 1995. Temporal relationships between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7, 721-733.
121. Schmidt, R.J., Veit, B., Mandel, M.A., Mena, M., Hake, S., Yanofsky, M.F., 1993. Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 5, 729-737.
122. Schmitz, J., Franzen, R., Ngyuen, T.H., Garcia-Maroto, F., Pozzi, C., Salamini, F., Rohde, W., 2000. Cloning, mapping and expression analysis of barley MADS-box genes. Plant Mol. Biol. 42, 899-913.
123. 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, 931-936.
124. Scortecci, K., Michaels, S.D., Amasino, R.M., 2001. Identification of a MADS-box gene, FLOWERING LOCUS M that represses flowering. Plant J. 26, 229-236.
125. Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, W.J., Peacock, W.J., Dennis, E.S., 1999. The FLF MADS-box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11, 444-458.
126. Sheldon, C.C., Rouse, D.T., Finnegan, E.J., Peacock, W.J., Dennis, E.S., 2000. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc. Natl. Acad. Sci. USA 97, 3753-3758.
127. Shore, P., Sharrocks, A.D., 1995. The MADS-box family of transcription factors. Eur. J. Biochem. 229, 1-13.
128. Soltis, P.S., Soltis, D.E., Chase, M.W., 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402, 402-404.
129. Soltis, D.E., Soltis, P.S., Albert, V.A., Oppenheimer, D.G., dePamphilis, C.W., Ma, H., Frohlich, M.W., Theißen, G., 2002. Missing links: the genetic architecture of flower and floral diversification. Trends Plant Sci. 7, 22-31.
130. Sundström, J., Carlsbecker, A., Svensson, M.E., Svenson, M., Johanson, U., Theißen, G., Engström, P., 1999. 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. 25, 253-266.
131. Tandre, K., Albert, V.A., Sundas, A., Engström, P., 1995. Conifer homologues to genes that control floral development in angiosperms. Plant Mol. Biol. 27, 69-78.
132. Tandre, K., Svenson, M., Svensson, M.E., Engström, P., 1998. Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J. 15, 615-623.
133. Taylor, S.A., Hofer, J.M.I., Murfet, I.C., Sollinger, J.D., Singer, S.R., Knox, M.R., Ellis, T.H.N., 2002. PROLIFERATING INFLORESCENCE MERISTEM, a MADS-box gene that regulates floral meristem identity in pea. Plant Physiol. 129, 1150-1159.
134. Theißen, G., 2000. Shattering developments. Nature 404, 711-713.
135. Theißen, G., 2001. Development of floral organ identity: stories from the MADS house. Curr. Opin. Plant Biol. 4, 75-85.
136. Theißen, G., Saedler, H., 1995. MADS-box genes in plant ontogeny and phylogeny: Haeckel's 'biogenetic law' revisited. Curr. Opin. Genet. Dev. 5, 628-639.
137. Theißen, G., Saedler, H., 1999. The golden decade of molecular floral development (1990-1999): a cheerful obituary. Dev. Genet. 25, 181-193.
138. Theißen, G., Saedler, H., 2001. Floral quartets. Nature 409, 469-471.
139. 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.
140. Theißen, G., Kim, J., 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, 484-516.
141. Theißen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T., Münster, T., Winter, K.-U., Saedler, H., 2000. A short history of MADS-box genes in plants. Plant Mol. Biol. 42, 115-149.
142. Vrebalov, J., Ruezinsky, D., Padmanabhan, V., White, R., Medrano, D., Drake, R., Schuch, W., Giovannoni, J., 2002. A MADS-box gene necessary for fruit ripening at the tomato Ripining-Inhibitor (Rin) locus. Science 296, 343-346.
143. Walden, A.R., Wang, D.Y., Walter, C., Gardner, R.C., 1998. A large family of TM3 MADS-box cDNAs in Pinus radiata includes two members with deletions of the conserved K domain. Plant Sci. 138, 167-176.
144. Weigel, D., Meyerowitz, E.M., 1994. The ABCs of floral homeotic genes. Cell 78, 203-209.
145. Winter, K.-U., Becker, A., Münster, T., Kim, J.T., 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.
146. Winter, K.-U., Saedler, H., Theißen, G., 2002a. On the origin of class B floral homeotic genes: functional substitution and dominant inhibition in Arabidopsis by expression of an ortholog from the gymnosperm Gnetum. Plant J. 31, 457-475.
147. Winter, K.-U., Weiser, C., Kaufmann, K., Bohne, A., Kirchner, C., Kanno, A., Saedler, H., Theißen, G., 2002b. Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. Mol. Biol. Evol. 19, 587-596.
148. Wolfe, K.H., Gouy, M., Yang, Y.-W., Sharp, P.M., Li, W.-H., 1989. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc. Natl. Acad. Sci. USA 86, 6201-6205.
149. Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldman, K.A., Meyerowitz, E.M., 1990. The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346, 35-39.
150. Yu, J., Hu, S., Wang, J., Wong, G.K., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X., Cao, M., Liu, J., Sun, J., Tang, J., Chen, Y., Huang, X., Lin, W., Ye, C., Tong, W., Cong, L., Geng, J., Han, Y., Li, L., Li, W., Hu, G., Huang, X., Li, W., Li, J., Liu, Z., Li, L., Liu, J., Qi, Q., Liu, J., Li, L., Li, T., Wang, X., Lu, H., Wu, T., Zhu, M., Ni, P., Han, H., Dong, W., Ren, X., Feng, X., Cui, P., Li, X., Wang, H., Xu, X., Zhai, W., Xu, Z., Zhang, J., He, S., Zhang, J., Xu, J., Zhang, K., Zheng, X., Dong, J., Zeng, W., Tao, L., Ye, J., Tan, J., Ren, X., Chen, X., He, J., Liu, D., Tian, W., Tian, C., Xia, H., Bao, Q., Li, G., Gao, H., Cao, T., Wang, J., Zhao, W., Li, P., Chen, W., Wang, X., Zhang, Y., Hu, J., Wang, J., Liu, S., Yang, J., Zhang, G., Xiong, Y., Li, Z., Mao, L., Zhou, C., Zhu, Z., Chen, R., Hao, B., Zheng, W., Chen, S., Guo, W., Li, G., Liu, S., Tao, M., Wang, J., Zhu, L., Yuan, L., Yang, H., 2002a. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296, 79-91.
151. Yu, H., Xu, Y., Tan, E.L., Kumar, P.P., 2002b. AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc. Natl. Acad. Sci. USA 99, 16336-16341.
152. Zhang, H., Forde, E.G., 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409.
153. Zachgo, S., Saedler, H., Schwarz-Sommer, Z., 1997. Pollen-specific expression of DEFH125, a MADS-box transcription factor in Antirrhinum with unusual features. Plant J. 11, 1043-1050.