The naked and the dead: The ABCs of gymnosperm reproduction and the origin of the angiosperm flower

Seminars in Cell and Developmental Biology

Volumn 21, Issue 1, 2010, Pages 118-128

  Melzer, Rainer ^a   Wang, Yong Qiang ^a   Theißen, Günter ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

ABC model; Floral quartet model; Flower origin; Gymnosperm; MADS box gene

Indexed keywords

MADS DOMAIN PROTEIN; PLANT DNA; VEGETABLE PROTEIN;

ANGIOSPERM; EVOLUTION; FLOWER DEVELOPMENT; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TARGETING; GYMNOSPERM; HOMEOBOX; MOLECULAR MECHANICS; NONHUMAN; PHYLOGENY; PLANT GENE; PLANT REPRODUCTION; PLANT SEED; REVIEW;

GYMNOSPERMAE; MAGNOLIOPHYTA; SPERMATOPHYTA;

EID: 75849156654     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2009.11.015     Document Type: Review

References (73)

1. Friedman W.E. The meaning of Darwin's "Abominable Mystery". Am J Bot 96 (2009) 5-21
2. Frohlich M.W., and Chase M.W. After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450 (2007) 1184-1189
3. Theißen G., and Becker A. Gymnosperm orthologues of class B floral homeotic genes and their impact on understanding flower origin. Crit Rev Plant Sci 23 (2004) 129-148
4. Bateman R.M., Hilton J., and Rudall P.J. Morphological and molecular phylogenetic context of the angiosperms: contrasting the 'top-down' and 'bottom-up' approaches used to infer the likely characteristics of the first flowers. J Exp Bot 57 (2006) 3471-3503
5. Baum D.A., and Hileman L.C. A genetic model for the origin of flowers. In: Ainsworth C. (Ed). Flowering and its manipulations (2006), Blackwell Publishing, Sheffield, UK
6. Theißen G., and Melzer R. Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann Bot-Lond 100 (2007) 603-619
7. Specht C.D., and Bartlett M.E. Flower evolution: the origin and subsequent diversification of the angiosperm flower. Annu Rev Ecol Evol Syst 40 (2009) 217-243
8. Friis E.M., Pedersen K.R., and Crane P.R. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeogr Palaeoclimatol Palaeoecol 232 (2006) 251-293
9. Ronse De Craene L.P. The evolutionary significance of homeosis in flowers: a morphological perspective. Int J Plant Sci 164 (2003) S225-S235
10. Theißen G. The proper place of hopeful monsters in evolutionary biology. Theory Biosci 124 (2006) 349-369
11. Arthur W. The emerging conceptual framework of evolutionary developmental biology. Nature 415 (2002) 757-764
12. Kramer E.M., and Jaramillo M.A. Genetic basis for innovations in floral organ identity. J Exp Zool Part B-Mol Dev Evol 304B (2005) 526-535
13. Theißen G., Becker A., Di Rosa A., Kanno A., Kim J.T., Münster T., et al. A short history of MADS-box genes in plants. Plant Mol Biol 42 (2000) 115-149
14. Coen E.S., and Meyerowitz E.M. The war of the whorls-genetic interactions controlling flower development. Nature 353 (1991) 31-37
15. Theißen G. Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4 (2001) 75-85
16. Egea-Gutierrez-Cortines M., and Davies B. Beyond the ABCs: ternary complex formation in the control of floral organ identity. Trends Plant Sci 5 (2000) 471-476
17. Krizek B.A., and Fletcher J.C. Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6 (2005) 688-698
18. Angenent G.C., and Colombo L. Molecular control of ovule development. Trends Plant Sci 1 (1996) 228-232
19. Theißen G., Kim J.T., and 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 (1996) 484-516
20. Pelaz S., Ditta G.S., Baumann E., Wisman E., and Yanofsky M.F. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405 (2000) 200-203
21. Ditta G., Pinyopich A., Robles P., Pelaz S., and Yanofsky M.F. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14 (2004) 1935-1940
22. Honma T., and Goto K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409 (2001) 525-529
23. Egea-Cortines M., Saedler H., and 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 (1999) 5370-5379
24. Immink R.G., Nougalli-Tonaco I.A., de Folter S., Shchennikova A., van Dijk A.D., Busscher-Lange J., et al. SEPALLATA3: the "glue" for MADS box transcription factor complex formation. Genome Biol 10 (2009) R24
25. Kaufmann K., Muino J.M., Jauregui R., Airoldi C.A., Smaczniak C., Krajewski P., et al. Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7 (2009) 854-875
26. Melzer R., Verelst W., and Theißen G. The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in 'floral quartet'-like complexes in vitro. Nucleic Acids Res 37 (2009) 144-157
27. Melzer R., and Theissen G. Reconstitution of floral quartets in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Res 37 (2009) 2723-2736
28. Ferrario S., Immink R.G.H., Shchennikova A., Busscher-Lange J., and Angenent G.C. The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell 15 (2003) 914-925
29. Leseberg C.H., Eissler C.L., Wang X., Johns M.A., Duvall M.R., and Mao L. Interaction study of MADS-domain proteins in tomato. J Exp Bot 59 (2008) 2253-2265
30. Agrawal G., Abe K., Yamazaki M., Miyao A., and Hirochika H. Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-of-function mutants of the OsMADS1 gene. Plant Mol Biol 59 (2005) 125-135
31. Kater M.M., Dreni L., and Colombo L. Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. J Exp Bot 57 (2006) 3433-3444
32. Kim S., Koh J., Yoo M.J., Kong H.Z., Hu Y., Ma H., et al. Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. Plant J 43 (2005) 724-744
33. Zahn L.M., King H.Z., Leebens-Mack J.H., Kim S., Soltis P.S., Landherr L.L., et al. The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169 (2005) 2209-2223
34. Castillejo C., Romera-Branchat M., and Pelaz S. A new role of the Arabidopsis SEPALLATA3 gene revealed by its constitutive expression. Plant J 43 (2005) 586-596
35. Liu C., Xi W.Y., Shen L.S., Tan C.P., and Yu H. Regulation of floral patterning by flowering time genes. Dev Cell 16 (2009) 711-722
36. Becker A., and Theißen G. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29 (2003) 464-489
37. Rijpkema A.S., Zethof J., Gerats T., and Vandenbussche M. The petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant J (2009)
38. Thompson B.E., Bartling L., Whipple C., Hall D.H., Sakai H., Schmidt R., et al. Bearded-ear encodes a MADS box transcription factor critical for maize floral development. Plant Cell 21 (2009) 2578-2590
39. Ohmori S., Kimizu M., Sugita M., Miyao A., Hirochika H., Uchida E., et al. MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice. Plant Cell (2009) advance online publication doi:10.1105/tpc.109.068742.
40. Doyle J.A. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. Int J Plant Sci 169 (2008) 816-843
41. Doyle J.A., and Donoghue M.J. Seed plant phylogeny and the origin of angiosperms-an experimental cladistic approach. Bot Rev 52 (1986) 321-431
42. Frohlich M.W. Recent developments regarding the evolutionary origin of flowers. Adv Bot Res: Incorporating Adv Plant Pathol 44 (2006) 63-127
43. Friis E.M., Doyle J.A., Endress P.K., and Leng Q. Archaefructus-angiosperm precursor or specialized early angiosperm?. Trends Plant Sci 8 (2003) 369-373
44. Soltis D.E., Soltis P.S., Endress P.K., and Chase M.W. Phylogeny and evolution of angiosperms (2005), Sinauer Associates, Sunderland, MA
45. Tanabe Y., Hasebe M., Sekimoto H., Nishiyama T., Kitani M., Henschel K., et al. Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc Natl Acad Sci USA 102 (2005) 2436-2441
46. Becker A., Winter K.U., Meyer B., Saedler H., and Theißen G. MADS-box gene diversity in seed plants 300 million years ago. Mol Biol Evol 17 (2000) 1425-1434
47. Winter K.U., Saedler H., and Theißen G. On the origin of class B floral homeotic genes: functional substitution and dominant inhibition in Arabidopsis by expression of an orthologue from the gymnosperm Gnetum. Plant J 31 (2002) 457-475
48. Fukui M., Futamura N., Mukai Y., Wang Y.Q., Nagao A., and Shinohara K. Ancestral MADS box genes in sugi, Cryptomeria japonica D. Don (Taxodiaceae), homologous to the B function genes in angiosperms. Plant Cell Physiol 42 (2001) 566-575
49. Jager M., Hassanin A., Manuel M., Le Guyader H., and Deutsch J. MADS-box genes in Ginkgo biloba and the evolution of the AGAMOUS family. Mol Biol Evol 20 (2003) 842-854
50. Mouradov A., Hamdorf B., Teasdale R.D., Kim J.T., Winter K.U., and Theißen G. 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 (1999) 245-252
51. Rutledge R., Regan S., Nicolas O., Fobert P., Cote C., Bosnich W., 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 (1998) 625-634
52. Sundström J., Carlsbecker A., Svensson M.E., Svenson M., Johanson U., Theißen G., 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 (1999) 253-266
53. Tandre K., Albert V.A., Sundas A., and Engström P. Conifer homologs to genes that control floral development in angiosperms. Plant Mol Biol 27 (1995) 69-78
54. Tandre K., Svenson M., Svensson M.E., and Engström P. Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J 15 (1998) 615-623
55. Winter K.U., Becker A., Münster T., Kim J.T., Saedler H., and Theißen G. MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc Natl Acad Sci USA 96 (1999) 7342-7347
56. Zhang P.Y., Tan H.T.W., Pwee K.H., and Kumar P.P. Conservation of class C function of floral organ development during 300 million years of evolution from gymnosperms to angiosperms. Plant J 37 (2004) 566-577
57. Futamura N., Totoki Y., Toyoda A., Igasaki T., Nanjo T., Seki M., et al. Characterization of expressed sequence tags from a full-length enriched cDNA library of Cryptomeria japonica male strobili. BMC Genomics 9 (2008) 383
58. Shindo S., Ito M., Ueda K., Kato M., and Hasebe M. Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants. Evol Dev 1 (1999) 180-190
59. Mouradov A., Glassick T.V., Hamdorf B.A., Murphy L.C., Marla S.S., Yang Y.M., et al. Family of MADS-box genes expressed early in male and female reproductive structures of Monterey pine. Plant Physiol 117 (1998) 55-61
60. Sundström J., and Engström P. Conifer reproductive development involves B-type MADS-box genes with distinct and different activities in male organ primordia. Plant J 31 (2002) 161-169
61. Carlsbecker A., Tandre K., Johanson U., Englund M., and Engström P. The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies). Plant J 40 (2004) 546-557
62. Krizek B.A., and Meyerowitz E.M. The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122 (1996) 11-22
63. Ma H., Yanofsky M.F., and Meyerowitz E.M. AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Gene Dev 5 (1991) 484-495
64. Rudall P.J., Remizowa M.V., Prenner G., Prychid C.J., Tuckett R.E., and Sokoloff D.D. Nonflowers near the base of extant angiosperms? Spatiotemporal arrangement of organs in reproductive units of Hydatellaceae and its bearing on the origin of the flower. Am J Bot 96 (2009) 67-82
65. Meyen S.V. Basic features of gymnosperm systematics and phylogeny as evidenced by the fossil record. Bot Rev 50 (1984) 1-111
66. Mizukami Y., and Ma H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71 (1992) 119-131
67. Battaglia R., Brambilla V., Colombo L., Stuitje A.R., and Kater M.M. Functional analysis of MADS-box genes controlling ovule development in Arabidopsis using the ethanol-inducible alc gene-expression system. Mech Dev 123 (2006) 267-276
68. Kanno A., Saeki H., Kameya T., Saedler H., and Theißen G. Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol Biol 52 (2003) 831-841
69. Erwin D.H., and Davidson E.H. The evolution of hierarchical gene regulatory networks. Nat Rev Genet 10 (2009) 141-148
70. Qiu Y.L., Li L.B., Wang B., Chen Z.D., Dombrovska O., Lee J., et al. A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci 168 (2007) 691-708
71. Henschel K., Kofuji R., Hasebe M., Saedler H., Münster T., and Theißen G. Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol Biol Evol 19 (2002) 801-814
72. Arora R., Agarwal P., Ray S., Singh A.K., Singh V.P., Tyagi A.K., et al. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8 (2007) 242
73. Saitou N., and Nei M. The Neighbor-Joining Method-a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 (1987) 406-425