Function and evolution of the plant MADS-box gene family

Nature Reviews Genetics

Volumn 2, Issue 3, 2001, Pages 186-195

  Ng, Medard ^a,b   Yanofsky, Martin F ^b  

^a EXELIXIS INC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNOLIOPHYTA;

DNA BINDING PROTEIN; MADS DOMAIN PROTEIN; PLANT DNA; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ANIMAL; GENE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR EVOLUTION; MORPHOGENESIS; PHYLOGENY; PLANT; REGULATOR GENE; REGULATORY SEQUENCE; REVIEW;

ANIMALS; DNA, PLANT; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, PLANT; GENES, REGULATOR; MADS DOMAIN PROTEINS; MORPHOGENESIS; PHYLOGENY; PLANT PROTEINS; PLANTS; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSCRIPTION FACTORS;

EID: 0035289981     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/35056041     Document Type: Review

References (142)

1. 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).
2. Meyerowitz, E. M. Plants and the logic of development. Genetics 145, 5-9 (1997).
3. Meyerowitz, E. M. Plants, animals and the logic of development. Trends Genet. 15, M65-M68 (1999).
4. Riechmann, J. L. & Meyerowitz, E. M. MADS domain proteins in plant development. Biol. Chem. 378, 1079-1101 (1997).
5. Doyle, J. J. Evolution of a plant homeotic multigene family: towards connecting molecular systematics and molecular developmental genetics. Syst. Biol. 43, 307-328 (1994).
6. Theissen, G., Kim, J. T. & Saedler, H. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol. 43, 484-516 (1996).
7. Purugganan, M. D., Rounsley, S. D., Schmidt, R. J. & Yanofsky, M. F. Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140, 345-356 (1995).
8. Purugganan, M. D. 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).
9. Alvarez-Buylla, E. R. et al. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl Acad. Sci. USA 97, 5328-5333 (2000).
10. Alvarez-Buylla, E. R. et al. MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J. 24, 457-466 (2000).
11. Doebley, J. & Wang, R. L. Genetics and the evolution of plant form: an example from maize. Cold Spring Harb. Syrnp. Quant. Biol. 62, 361-367 (1997).
12. Wang, R. L., Stec, A., Hey, J., Lukens, L. & Doebley, J. The limits of selection during maize domestication. Nature 398, 236-239 (1998).
13. Weatherbee, S. D. & Carroll, S. Selector genes and limb identity in arthropods and vertebrates. Cell 97, 283-286 (1999).
14. Hill, T. A., Day, C. D., Zondlo, S. C., Thackeray, A. G. & Irish, V. F. Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development 125, 1711-1721 (1998).
15. Parcy, F., Nilsson, O., Busch, M. A., Lee, I. & Weigel, D. A genetic framework for floral patterning. Nature 395, 561-566 (1998).
16. Tilly, J. J., Allen, D. W. & 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).
17. Busch, M. A., Bomblies, K. & Weigel, D. Activation of a floral homeotic gene in Arabidopsis. Science 285, 585-587 (1999).
18. Honma, T. & Goto, K. The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 127, 2021-2030 (2000).
19. Vision, T. J., Brown, D. G. & Tanksley, S. D. The origins of genomic duplications in Arabidopsis. Science 290, 2114-2117 (2000).
20. Un, X. et al. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402, 761-768 (1999).
21. Mayer, K. et al. Sequence and analysis of chromosome 4 of the plant Arabidopsis thaliana. Nature 402, 769-777 (1999).
22. European Union Chromosome 3 Arabidopsis Genome Sequencing Consortium, The Institute for Genomic Research & Kazasa DNA Research Institute. Sequence and analysis of chromosome 3 of the plant Arabidopsis thaliana. Nature 408, 820-823 (2000).
23. Kazasa DNA Research Institute, The Cold Spring Harbor and Washington University Sequencing Consortium, The European Union Arabidopsis Genome Sequencing Consortium & Institute of Plant Genetics and Crop Plant Reserach (IPK). Sequence and analysis of chromosome 5 of the plant Arabidopsis thaliana. Nature 408, 823-826 (2000).
24. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 798-815 (2000).
25. Theologis, A. et al. Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature 408, 816-820 (2000).
26. Meyerowitz, E. M. Arabidopsis, a useful weed. Cell 56, 263-269 (1989).
27. Bechtold, D., Ellis, J. & Pelletier, G. C. In planta Agrobacterium mediated gone transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. Paris 316, 1194-1199 (1993).
28. Wisman, E., Cardon, G. H., Fransz, P. & Saedler, H. The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant mol. Biol. 37, 989-999 (1998).
29. Speulman, E. et al. A two-component enhancer - inhibitor transposon mutagenesis system for functional analysis of the Arabidopsis genome. Plant Cell 11, 1853-1866 (1999).
30. Pelaz, S., Ditta, G. S., Baumann, E., Wisman, E. & Yanofsky, M. F. B and C floral organ identity functions require SEPALATA MADS-box genes. Nature 405, 200-203 (2000). Single mutants of three closely related MADS-box genes SEP1, 2, 3 show little or no alteration in floral morphology, but sep1, 2, 3 triple mutant flowers resemble mutants in B-and C-class genes. The expression patterns of the ABC genes are not altered, suggesting that SEP1, 2, 3 define a new class of floral homeotic genes.
31. Wilson, K., Long, D., Swinburne, J. & Coupland, G. A dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8, 659-671 (1996).
32. Weigel, D. et al. Activation tagging in Arabidopsis. Plant Physiol. 122, 1003-1013 (2000).
33. Simpson, G. G., Gendall, A. R. & Dean, C. When to switch to flowering. Annu. Rev. Cell Dev. Biol. 15, 519-550 (1999).
34. Devlin, P. F., & Kay, S. A. Flower arranging in Arabidopsis. Science 288, 1600-1602 (2000).
35. Samach, A. & Coupland, G. The measurement and the control of flowering in plants. Bioessays 22, 38-47 (2000).
36. Kowalski, S. P., Lan, T. H., Feldmann, K. A. & Paterson, A. H. QTL mapping of naturally-occurring variation in flowering time of Arabidopsis thaliana. Mol. Gen. Genet. 245, 548-555 (1994).
37. Michaels, S. D. & Amasino, R. M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956 (1999).
38. Sheldon, C. C. et al. The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11, 445-458 (1999).
39. Putterill, J., Robson, F., Lee, K., Simon, R. & Coupland, G. The CONSTANS gene ol Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847-857 (1995).
40. Jacobsen, S. E., Binkowski, K. A. & Olszewski, N. E. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc. Natl Acad. Sci. USA 93, 9292-9296 (1996).
41. Blázquez, M. A., Green, R., Nilsson, O., Sussman, M. R. & Weigel, D. Gibberelins promote flowering of Arabidopsis by activating the LFY promoter. Plant Cell 10, 791-800 (1998).
42. Lee, H. et al.The AGAMOUS-like 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366-2376 (2000). A gain-of-function allele of SOC1 was identified as a suppressor of the late-flowering phenotype of frigida (fri) mutants. SOC1 is regulated by all three flowering-time pathways.
43. Onouchi, H., Igeño, M. I., Périlleux, C., Graves, K. & Coupland, G. Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12, 885-900 (2000).
44. Samach, A. et al. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1616 (2000). SOC1, a previously uncharacterized MADS-box gene, was identified as one of four CO target genes. Both SOC1 and FLOWERING LOCUS T (FT) are shown to be positively regulated by CO and negatively regulated by FLC.
45. Ruiz-Garcia, L. et al. Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell 9, 1921-1934 (1997).
46. Mandel, M. A., Gustafson-Brown, C., Savidge, B. & Yanofsky, M. F. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360, 273-277 (1992).
47. Weigel, D., Alvarez, J., Smyth, D. R. Yanofsky, M. F. & Meyerowitz, E. M. LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843-859 (1992).
48. Nilsson, O., Lee, I. & Blázquez, M. A. Flowering-time genes modulate the response to LEAFY activity. Genetics 150, 403-410 (1998).
49. Liljegren, S. J., Gustafson-Brown, C., Pinyopich, A., Ditta, G. S. & Yanofsky, M. F. Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11, 1007-1018 (1999).
50. Bowman, J. L., Alvarez, J., Weigel, D., Meyerowitz, E. M. & Smyth. D. R. Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119, 721-743 (1993).
51. Kempin, S. A., Savidge, B. & Yanofsky, M. F. Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267, 522-525 (1995).
52. Mandel, M. A. & Yanofsky, M. F. The Arabidopsis AGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell 7, 1763-1771 (1995).
53. Ferrándiz, C., Gu, Q., Martienssen, R. & Yanofsky, M. F. Redundant regulation of meristem identity and plant architecture by FRUITFUL, APETALA1 and CAULIFLOWER. Development 127, 725-734 (2000).
54. Hartmann, U. et al. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351-360 (2000).
55. Lee, I., Bleecker, A. & Amasino, R. Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol. Gen. Genet. 237, 171-176 (1993).
56. Smith, L. B. & King, G. J. The distribution of BoCAL - a alleles in Brassica oleracea is consistent with a genetic model for curd development and domestication of the cauliflower. Mol. Breed. 6, 603-613 (2000).
57. Lowman, A. C. & Purugganan, M. D. Duplication of the Brassica oleracea APETALA1 floral homeotic gene and the evolution of domesticated cauliflower. J. Hered. 90, 514-520 (1999).
58. Coen, E. S. & Meyerowitz, E. M. The war of the whorls: genetic interactions controlling flower development. Nature 353, 31-37 (1991).
59. Weigel, D. & Meyerowitz, E. The ABCs of floral homeotic genes. Cell 78, 203-209 (1994).
60. Yanofsky, M. F. Floral meristems to floral organs: genes controlling early events in Arabidopsis flower development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 167-188 (1995).
61. Yanofsky, M. F. et al. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346, 35-39 (1990).
62. Jack, T., Brockman, L. L. & Meyerowitz, E. M. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68, 683-697 (1992).
63. Goto, K. & Meyerowitz, E. M. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8, 1548-1560 (1994).
64. Jofuku, D. K., den Boer, B. G. W., Van Montagu, M. & Okamuro, J. K. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6, 1211-1225 (1994).
65. Huijser, P. et al. 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).
66. Schwarz-Sommer, Z. et al. Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J. 11, 251-263 (1992).
67. Chung, Y.-Y. et al. Characterization of two rice MADS box genes homologous to GLOBOSA. Plant Sci. 109, 45-56 (1995).
68. Kang, H.-G., Jeon, J.-S., Lee, S. & An, G. Identification of class B and class C floral organ identity genes from rice plants. Plant Mol. Biol. 38, 1021-1029 (1998).
69. Kramer, E. M., Dorit, R. L. & Irish, V. F. 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).
70. Kramer, E. M. & Irish, V. F. Evolution of genetic mechanisms controlling petal development. Nature 399, 144-148 (1999). The expression patterns of AP3-and PI-like sequences (B-class genes) in basal eudicots are conserved in stamens but not in petals. The authors suggest that the ABC model is not conserved in all eudicots (see also reference 71).
71. Ambrose, B. A. et al. Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell 5, 569-579 (2000). These authors examined the si1 mutants in maize. They found evidence that si1 encodes a functional AP3 orthologue and the results show that the ABC model of flower development is conserved between monocots and eudicots. The conclusions made by these authors contrast with those made in reference 70.
72. Baum, D. A. The evolution of plant development. Curr. Opin. Plant Biol. 1, 79-86 (1998).
73. Baum, D. A. & Whitlock, B. A. Plant development: genetic clues to petal evolution. Clin Biol. 15, R525-R527 (1999).
74. Ma, H. & dePamphilis, C. The ABCs of floral evolution. Cell 101, 5-8 (2000).
75. Theissen, G. et al. A short history of MADS-box genes in plants. Plant Mol. Biol. 42, 115-149 (2000).
76. Qiu, Y.-L. et al. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402, 404-407 (1999).
77. Soltis, P. S., Soltis, D. E. & Chase, M. W. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402, 402-404 (1999). References 76 and 77 present phylogenetic trees of several gymnosperms and angiosperms on the basis of the sequence alignment of mitochondrial, plastid and nuclear genes. One of the conclusions of these studies is that Gnetales are closely related to gymnosperms (see also references 112, 115, 116).
78. Stebbins, G. L. Natural selection and the differentiation of angiosperm families. Evolution 5, 299-324 (1951).
79. Clifford, H. T. in Grass Systematics and Evolution (eds Soderstrom, T. R., Hilu, K. W., Campbell, C. S. & Barkworth, M. E.) 21-30 (Smithsonian Institution Press, Washington DC, 1987).
80. Bell, A. D. Plant Form - An Illustrated Guide to Flowering Plant Morphology (Oxford Univ. Press, New York, 1991).
81. Bowman, J. L. Evolutionary conservation of angiosperm flower development at the molecular and genetic levels. J. Biosci. 22, 515-527 (1997).
82. Nagato, Y. in Apomixis: Exploiting Hybrid Vigor in Rice (ed. Khush, G. S.) 43-46 (International Rice Research Institute, Los Baños, Philippines, 1994).
83. Colombo, L. et al. BRANCHED SILKLESS mediates the transition from spikelet to floral meristem during Zea mays ear development. Plant J. 16, 355-363 (1998).
84. Márquez-Guzmán, J., Engleman, M., Martínez-Mena, A., Martínez, E. & Ramos, C. H. Anatomía reproductiva de Lacandonia schismática (Lacandoniaceae). Ann. Missouri Bot. Gard. 76, 124-127 (1989).
85. Jack, T., Fox, G. L. & Meyerowitz, E. M. Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell 76, 703-716 (1994).
86. Krizek, B. A. & Meyerowitz, E. M. The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122, 11-22 (1996).
87. Bowman, J. L., Smyth, D. R. & Meyerowitz, E. M. Genes directing flower development in Arabidopsis. Plant Cell 1, 37-52 (1989).
88. Gustafson-Brown, C., Savidge, B. & Yanofsky, M. F. Regulation of the Arabidopsis floral homeotic gene APETALA1. Cell 76, 131-143 (1994).
89. 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).
90. Davies, B. et al. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J. 18, 4023-4034 (1999).
91. Schmidt, R. J. et al. Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 5, 729-737 (1993).
92. Mena, M. et al. Diversification of C-function activity in maize flower development. Science 274, 1537-1540 (1996).
93. Flanagan, C. A. & Ma, H. Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant Arabidopsis flowers. Plant Mol. Biol. 26, 581-595 (1994).
94. Savidge, B., Rounsley, S. D. & Yanofsky, M. F. Temporal relationship between the transcription of two Arabidopsis MADS-box genes and the floral organ identity genes. Plant Cell 7, 721-733 (1995).
95. Mandel, M. A. & Yanofsky, M. F. The Arabidopsis AGL9 MADS box gene is expressed in young flower primordia. Sex. Plant Reprod. 11, 22-28 (1998).
96. Davies, B., Egea-Cortines, M., de Andrade Silva, E., Saedler, H. & Sommer, H. Multiple interactions amongst floral homeotic MADS box proteins. EMBO J. 15, 4330-4343 (1996).
97. Egea-Cortines, M., Saedler, H. & Sommer, H. 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, 5370-5379 (1999).
98. Angenent, G. C., Franken, J., Busscher, M., Weiss, D. & van Tunen, A. J. Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J. 5, 33-44 (1994).
99. Pnueli, L., Hareven, D., Broday, L., Hurwitz, C. & Lifschitz, E. The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6, 175-186 (1994).
100. 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).
101. Mouradov, A. et al. Family of MADS-box genes expressed early in male and female reproductive structures of monterey pine. Plant Physiol. 1217, 55-62 (1998).
102. Ma, H., Yanofsky, M. F. & Meyerowitz, E. M. AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5, 484-495 (1991).
103. Liljegren, S. J. et al. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766-770 (2000). References 103 and 105 show that three MADS-box genes, FUL, SHP1 and SHP2 specify cell fate in the Arabidopsis fruit SHP1, 2 are critical for differentiation of the dehiscence zone. Differentiation of the valves requires the activity of FUL, which negatively regulates SHP1, 2 expression.
104. Gu, Q., Ferrándiz, C., Yanofsky, M. F. & Martienssen, R. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 1509-1517 (1998).
105. Ferrándiz, C., Liljegren, S. J. & Yanofsky, M. F. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289, 436-438 (2000).
106. Mao, L. et al. JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature 406, 910-913 (2000).
107. Zhang, H. & Forde, B. G. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409 (1998).
108. Tandre, K., Albert, V. A., Sundas, A. & Engstrom, P. Conifer homologues to genes that control floral development in angiosperms. Plant Mol. Biol. 27, 69-78 (1995).
109. Rutledge, R. et al. 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).
110. Mouradov, A. et al. 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 (1999).
111. Sundström, J. et al. 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 (1999).
112. Winter, K.-U. et al. 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). This paper describes phylogenetic studies of B-function MADS-box gene orthologues in gymnosperms and angiosperms, and concludes that Gnetales are more closely related to gymnosperms than to angiosperms (see also references 69, 70, 108, 109).
113. Crane, P. R., Friis, E. M. & Pedersen, K. R. The origin and early diversification of angiosperms. Nature 374, 27-33 (1995).
114. Frohlich, M. W. MADS about Gnetales. Proc. Natl Acad. Sci. USA 96, 8811-6813 (2000).
115. Bowe, L. M., Coat, G. & dePamphilis, C. W. 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, 4092-1097 (2000).
116. Chaw, S. M., Parkinson, C. L., Cheng, Y., Vincent, T. M. & Palmer, J. D. Seed plant phytogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc. Natl Acad. Sci. USA 97, 4086-4091 (2000). References 115 and 116 present the phylogenetic trees of mitochondrial, plastid and nuclear genes from gymnosperms and angiosperms. The authors conclude that Gnetales are closely related to gymnosperma (see also references 69, 70, 105).
117. Krogan, N. T. & Ashton, N. W. An cestry of plant MADS-box genes revealed by bryophyte (Physcomitrella patens) homologues. New Phytol. 147, 505-517 (2000).
118. Svensson, M. E., Johannesson, H. & Engström, P. The LAMB1 gene from the clubmoss, Lycopodium annotinum, is a divergent MADS-box gene, expressed specifically in sporogenic structures. Gene 253, 31-43 (2000).
119. Kofuji, R. & Yamaguchi, K. Isolation and phylogenetic analysis of MADS genes from the fern Ceratopteris richardii. J. Phytogeogr. Taxon 45, 83-91 (1997).
120. Münster, T. et al. 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).
121. Hasebe, M., Wen, C.-K., Kato, M. & Banks, J. A. Characterization of MADS homeotic genes in the fern Ceratopteris richardii. Proc. Natl Acad. Sci. USA 95, 6222-6227 (1998).
122. Riechmann, J. L. et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 209, 2105-2110 (2000).
123. Schaefer, D. G. & Zrÿd, J.-P. Efficient gene targeting in the moss Physcomitrella patens. Plant J. 11, 1195-1206 (1997). Gene targeting can be carried out efficiently in a moss species, thus opening up the possibility of determining the function of genes that may be crucial in plant evolution.
124. Rong, Y. S. & Golic, K. G. Gene targeting by homologous recombination in Drosophila. Science 288, 2013-2018 (2000).
125. Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157-161 (1999).
126. Krumlauf, R. Hox genes in vertebrate development. Cell 78, 191-201 (1994).
127. Lawrence, P. A. & Morata, G. Homeobox genes: their function in Drosophila segmentation and pattern formation. Cell 78, 181-189 (1994).
128. Manak, J. R. & Scott, M. P. A class act: conservation of homeodomain protein functions. Development Suppl. 61-71 (1994).
129. Mann, R. S. Why are Hox genes clustered? Bioessays 19, 661-664 (1997).
130. Averof, M. & Akam, M. Hox genes and the diversification of insect and crustacean body plans. Nature 376, 420-423 (1995).
131. Averof, M. & Patel, N. H. Crustacean appendage evolution associated with changes in Hox genes expression. Nature 388, 682-686 (1997).
132. Grenier, J. K., Garber, T. L., Warren, R., Whitington, P. M. & Carroll, S. Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Curr. Biol. 7, 547-553 (1997).
133. Cohn, M. J. & Tickle, C. Developmental basis of limblessness and axial patterning in snakes. Nature 399, 474-179 (1999).
134. Weatherbee, S. D., Halder, G., Kim, J., Hudson, A. & Carroll, S. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev. 12, 1474-1482 (1998).
135. Weatherbee, S. D. et al. Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Curr. Biol. 9, 109-115 (1999).
136. Carroll, S. B. Endless forms: the evolution of gene regulation and morphological diversity. Cell 101, 577-580 (2000).
137. Ryoo, H. D. & Mann, R. S. The control of trunk Hox specificity and activity by Extradenticle. Genes Dev. 13, 1704-1716 (1999).
138. Ryoo, H. D., Marty, T., Casares, F., Affolter, M. & Mann, R. S. Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex. Development 126, 5137-5148 (1999).
139. Abu-Shaar, M., Ryoo, H. D. & Mann, R. S. Control of the nuclear localization of Extradenticle by competing nuclear import and export signals. Genes Dev. 13, 935-945 (1999).
140. Schwarz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H. & Sommer, H. Genetic control of flower development: homeotic genes in Antirrhinum majus. Science 250, 931-936 (1990).
141. Tröbner, W. et al. GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J. 11, 4693-4704 (1992).
142. Smyth, D. R., Bowman, J. L. & Meyerowitz, E. M. Early flower development in Arabidopsis. Plant Cell 2, 755-776 (1990).