Aquilegia as a model system for the evolution and ecology of petals

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1539, 2010, Pages 477-490

  Kramer, Elena M ^a   Hodges, Scott A ^b  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adaptation; Aquilegia; Nectar spur; Petal evolution; Ranunculaceae; Speciation

Indexed keywords

ADAPTATION; DATABASE; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; HERB; MORPHOLOGY; NATURAL SELECTION; NECTAR; SPECIATION (BIOLOGY); VIRUS;

AQUILEGIA; MAGNOLIOPHYTA; RANUNCULACEAE;

EID: 76749155010     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0230     Document Type: Review

References (114)

1. Abouheif, E., Akam, M., Dickinson, W. J., Holland, P. W. H., Meyer, A., Patel, N. H., Raff, R. A., Roth, V. L. & Wray, G. A. 1997 Homology and developmental genes. Trends Genet. 13, 432-433. (doi:10.1016/S0168-9525(97) 01271-7)
2. Abzhanov, A., Extavour, C. G., Groover, A., Hodges, S. A., Hoekstra, H. E., Kramer, E. M. & Monteiro, A. 2008 Are we there yet? Tracking the development of new model systems. Trends Genet. 24, 353-360. (doi:10.1016/j.tig.2008.04.002)
3. APG 2003 An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141, 399-436. (doi:10.1046/j.1095-8339.2003.t01-1-00158.x) (Pubitemid 36463424)
4. Baum, D. A. & Whitlock, B. A. 1999 Genetic clues to petal evolution. Curr. Biol. 9, 525-527.
5. Becker, A. & Theissen, G. 2003 The major clades of MADSbox genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29, 464-489. (doi:10.1016/S1055-7903(03)00207-0) (Pubitemid 37491891)
6. Bernardello, G. 2007 A systematic survey of floral nectaries. In Nectaries and nectar (eds S. W. Nicolson, M. Nepi & E. Pacini), pp. 19-128. Dordrecht, The Netherlands: Springer.
7. Bierhorst, D. W. 1971 Morphology of vascular plants. New York, NY: Macmillan.
8. Bowman, J. L. 1997 Evolutionary conservation of angiosperm flower development at the molecular and genetic levels. J. Biosci. 22, 515-527. (doi:10.1007/BF02703197)
9. Bowman, J. L., Smyth, D. R. & Meyerowitz, E. M. 1989 Genes directing flower development in Arabidopsis. Plant Cell 1, 37-52. (doi:10.1105/tpc.1.1.37)
10. Brunet, J. 2009 Pollinators of the Rocky Mountain columbine: temporal variation, functional groups and associations with floral traits. Ann. Bot. 103, 1567-1578. (doi:10.1093/aob/mcp096)
11. Burch-Smith, T. M., Anderson, J. C., Martin, G. B. & Dinesh-Kumar, S. P. 2004 Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J. 39, 734-746. (doi:10.1111/j.1365-313X.2004. 02158.x) (Pubitemid 39218781)
12. Chase, V. C. & Raven, P. H. 1975 Evolutionary and ecological relationships between Aquilegia formosa and Aquilegia pubescens (Ranunculaceae), 2 perennial plants. Evolution 29, 474-486. (doi:10.2307/2407260)
13. Coen, E. S. & Meyerowitz, E. M. 1991 The war of the whorls: genetic interactions controlling flower development. Nature 353, 31-37. (doi:10.1038/353031a0)
14. Darwin, C. 1862 The various contrivances by which orchids are fetilized by insects. London, UK: John Murray.
15. Davies, B., Cartolano, M. & Schwarz-Sommer, Z. 2006 Flower development: the Antirrhinum perspective. Adv. Bot. Res. 44, 279-321. (doi:10.1016/S0065-2296(06)44007-6) (Pubitemid 44691711)
16. Drews, G. N., Bowman, J. L. & Meyerowitz, E. M. 1991 Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETELA2 product. Cell 65, 991-1002. (doi:10.1016/0092-8674(91)90551-9)
17. Eames, A. J. 1961 Morphology of the angiosperms. New York, NY: McGraw-Hill.
18. Endress, P. K. 1994 Diversity and evolutionary biology of tropical flowers. Cambridge, UK: Cambridge University Press.
19. Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y.-L. & Postlethwait, J. 1999 Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531-1545.
20. Fulton, M. & Hodges, S. A. 1999 Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc. R. Soc. Lond. B 266, 2247-2252. (doi:10.1098/rspb.1999.0915)
21. Gaudin, V., Lunness, P. A., Fobert, P. R., Towers, M., Riou- Khamlichi, C., Murray, J. A. H., Coen, E. & Doonan, J. H. 2000 The expression of D-cyclin genes defines distinct development zones in snapdragon apical meristems and is locally regulated by the Cycliodea gene. Plant Phys. 122, 1137-1148. (doi:10.1104/pp.122.4.1137)
22. Geuten, K., Becker, A., Kaufmann, K., Caris, P., Janssens, S., Viaene, T., Theissen, G. & Smets, E. 2006 Petaloidy and petal identity MADS-box genes in the balsaminoid genera Impatiens and Marcgravia. Plant J. 47, 501-518.
23. Glover, B., Perez-Rodrigues, M. & Martin, C. 1998 Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development 125, 3497-3508.
24. Goethe, J. W. V. 1790 Versuch die Metamorphose der Pflanzen zu erklaren. Gotha, Germany: C. W. Ettinger.
25. Golz, J. F., Keck, E. J. & Hudson, A. 2002 Spontaneous mutations in KNOX genes give rise to a novel floral structure in Antirrhinum. Curr. Biol. 12, 515-522. (doi:10.1016/S0960-9822(02)00721-2) (Pubitemid 34271364)
26. Goto, K. & Meyerowitz, E. M. 1994 Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8, 1548-1560. (doi:10.1101/gad.8.13.1548)
27. Gottlieb, L. D. 1984 Genetics and morphological evolution in plants. Am. Nat. 123, 681-709.
28. Gould, B. & Kramer, E. M. 2007 Virus-induced gene silencing as a tool for functional analyses in the emerging model plant Aquilegia (columbine, Ranunculaceae). Plant Meth. 3, 6. (doi:10.1186/1746-4811-3-6) (Pubitemid 46986305)
29. Grant, V. 1952 Isolation and hybridization between Aquilegia formosa and A. pubescens. Aliso 2, 341-360.
30. Grant, V. 1976 Isolation between Aquilegia formosa and Aquilegia pubescens-reply and reconsideration. Evolution 30, 625-628. (doi:10.2307/ 2407586)
31. Hiepko, P. 1965 Vergleichend-morphologische und entwicklungsgeschichliche Untersuchungen uber das Perianth bei den Polycarpicae. Bot. Jahrb. Syst. 84, 359-426.
32. Hileman, L. C. & Irish, V. F. 2009 More is better: the uses of developmental genetic data to reconstruct perianth evolution. Am. J. Bot. 96, 83-95. (doi:10.3732/ajb.0800066)
33. Hodges, S. A. 1997a Floral nectar spurs and diversification. Int. J. Plant Sci. 158, S81-S88. (doi:10.1086/297508) (Pubitemid 28069477)
34. Hodges, S. A. 1997b Rapid radiation due to a key innovation in columbines. In Molecular evolution and adaptive radiation (eds T. J. Givnish & K. J. Sytsma), pp. 391-405. Cambridge, UK: Cambridge University Press.
35. Hodges, S. A. & Arnold, M. L. 1994a Columbines-a geographically widespread species flock. Proc. Natl Acad. Sci. USA 91, 5129-5132. (doi:10.1073/pnas.91.11.5129) (Pubitemid 24177806)
36. Hodges, S. A. & Arnold, M. L. 1994b Floral and ecological isolation between Aquilegia formosa and Aquilegia pubescens. Proc. Natl Acad. Sci. USA 91, 2493-2496. (doi:10.1073/pnas.91.7.2493)
37. Hodges, S. A. & Arnold, M. L. 1995 Spurring plant diversification: are floral nectar spurs a key innovation? Proc. R. Soc. Lond. B 262, 343-348. (doi:10.1098/rspb.1995.0215) (Pubitemid 26023715)
38. Hodges, S. A. & Derieg, N. J. 2009 Adaptive radiations: from field to genomic studies. Proc. Natl Acad. Sci. USA 106, 9947-9954. (doi:10.1073/pnas. 0901594106)
39. Hodges, S. A. & Whittall, J. B. 2008 One-sided evolution or two? A reply to Ennos. Heredity 100, 541-542. (doi:10.1038/hdy.2008.12) (Pubitemid 351733265)
40. Hodges, S. A., Whittall, J. B., Fulton, M. & Yang, J. Y. 2002 Genetics of floral traits influencing reproductive isolation between Aquilegia formosa and Aquilegia pubescens. Am. Nat. 159, S51-S60.
41. Hodges, S. A., Fulton, M., Yang, J. Y. & Whittall, J. B. 2004 Verne Grant and evolutionary studies of Aquilegia. New Phytol. 161, 113-120. (doi:10.1046/j.1469-8137.2003.00950.x) (Pubitemid 38047052)
42. Hoekstra, H. E. & Coyne, J. A. 2007 The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995-1016. (doi:10.1111/j.1558- 5646.2007.00105.x) (Pubitemid 46699436)
43. Hoot, S. B., Magallon, S. & Crane, P. R. 1999 Phylogeny of basal eudicots based on three molecular data sets: atpB, rbcL and 18S nuclear ribosomal DNA sequences. Ann. Mo. Bot. Gard. 86, 1-32. (doi:10.2307/2666215)
44. Irish, V. 2008 The Arabidopsis petal: a model for plant organogenesis. Trends Plant Sci. 13, 430-436. (doi:10.1016/j.tplants.2008.05.006)
45. Irish, V. 2009 Evolution of petal identity. J. Exp. Bot. 60, 2517-2527. (doi:10.1093/jxb/erp159)
46. Jack, T., Brockman, 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. (doi:10.1016/0092-8674(92)90144-2)
47. Jaramillo, M. A. & Kramer, E. M. 2004 APETALA3 and PISTILLATA homologs exhibit novel expression patterns in the unique perianth in Aristolochia (Aristolochiaceae). Evol. Dev. 6, 449-458. (doi:10.1111/j.1525- 142X.2004.04053.x) (Pubitemid 39554260)
48. Jaramillo, M. A. & Kramer, E. M. 2007 The role of developmental genetics in understanding homology and morphological evolution in plants. Int. J. Plant Sci. 168, 61-72. (doi:10.1086/509078) (Pubitemid 46095311)
49. Kay, K. M., Voelckel, C., Yang, J. Y., Hufford, K. M., Kaska, D. D. & Hodges, S. A. 2006a Floral characters and species diversification. In Ecology and evolution of flowers (eds L. Harder & C. H. Spencer), pp. 311-325. Oxford, UK: Oxford University Press.
50. Kay, K. M., Whittall, J. B. & Hodges, S. A. 2006b A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol. Biol. 6. (doi:10.1186/1471-2148-6-36) (Pubitemid 43987020)
51. Keck, E., McSteen, P., Carpenter, R. & Coen, E. 2003 Separation of genetic functions controlling organ identity in flowers. EMBO 22, 1058-1066.
52. Kim, S., Yoo, M., Albert, V. A., Farris, J. S., Soltis, P. S. & Soltis, D. E. 2004 Phylogeny and diversification of B-function genes in angiosperms: evolutionary and functional implications of a 260-million year old duplication. Am. J. Bot. 91, 2102-2118. (doi:10.3732/ajb.91.12.2102)
53. Kramer, E. M. 2006 Floral patterning and control of floral organ formation. In Flowering and its manipulation, vol.20 (ed. C. Ainsworth), pp. 49-70. Oxford, UK: Blackwell Publishing.
54. Kramer, E. M. 2009 Aquilegia: a new model for plant development, ecology, and evolution. Annu. Rev. Plant Biol. 60, 261-277. (doi:10.1146/annurev. arplant.043008.092051)
55. 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, S29-S40. (doi:10.1086/317576)
56. Kramer, E. M. & Jaramillo, M. A. 2005 The genetic basis for innovations in floral organ identity. J. Exp. Zool. (Mol. Dev. Evol.) 304B, 526-535.
57. Kramer, E. M. & Zimmer, E. A. 2006 Gene duplication and floral developmental genetics of basal eudicots. In Advances in botanical research: develomental genetics of the flower, vol.44 (eds D. E. Soltis, P. S. Soltis & J. Leebens-Mack), pp. 354-385. London, UK: Academic Press.
58. 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.
59. Kramer, E. M., Di Stilio, V. S. & Schluter, P. 2003 Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. Int. J. Plant Sci. 164, 1-11. (doi:10.1086/344694)
60. Kramer, E. M., Jaramillo, M. A. & Di Stilio, V. S. 2004 Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS-box genes in angiosperms. Genetics 166, 1011-1023. (doi:10.1534/genetics.166.2.1011) (Pubitemid 38391758)
61. Kramer, E. M., Su, H.-J., Wu, J. M. & Hu, J. M. 2006 A simplified explanation for the frameshift mutation that created a novel C-terminal motif in the APETALA3 gene lineage. BMC Evol. Biol. 6, 30. (doi:10.1186/1471-2148-6-30) (Pubitemid 44104968)
62. Kramer, E. M., Holappa, L., Gould, B., Jaramillo, M. A., Setnikov, D. & Santiago, P. 2007 Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia (Ranunculaceae). Plant Cell 19, 750-766. (doi:10.1105/tpc.107.050385) (Pubitemid 46953225)
63. Krizek, B. A., Prost, V. & Macias, A. 2000 AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. Plant Cell 12, 1357-1366. (doi:10.1105/tpc.12.8.1357) (Pubitemid 30704888)
64. Lamb, R. S. & Irish, V. F. 2003 Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc. Natl Acad. Sci. USA 100, 6558-6563. (doi:10.1073/pnas.0631708100) (Pubitemid 36666619)
65. Lee, J. Y., Baum, S. F., Oh, S. H., Jiang, C. Z., Chen, J. C. & Bowman, J. L. 2005 Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132, 5021-5032. (doi:10.1242/dev.02067) (Pubitemid 41764013)
66. Litt, A. 2007 An evaluation of A-function: evidence from the APETALA1 and APETALA2 gene lineages. Int. J. Plant Sci. 168, 73-91. (doi:10.1086/509662) (Pubitemid 46095312)
67. Litt, A. & Irish, V. F. 2003 Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165, 821-833.
68. Liu, Y., Nakayama, N., Schiff, M., Litt, A., Irish, V. F. & Dinesh-Kumar, S. P. 2004 Virus induced gene silencing of a DEFICIENS ortholog in Nicotiana benthamiana. Plant Mol. Biol. 54, 701-711. (doi:10.1023/B:PLAN. 0000040899.53378.83)
69. Mara, C. & Irish, V. 2008 Two GATA transcription factors are downstream effectors of floral homeotic gene action in Arabidopsis. Plant Phys. 147, 707-718. (doi:10.1104/pp.107.115634) (Pubitemid 352844317)
70. Martin, C. & Gerats, T. 1993 Control of pigment biosynthesis genes during petal development. Plant Cell 5, 1253-1264. (doi:10.1105/tpc.5.10.1253) (Pubitemid 2001861)
71. Martin, C., Bhatt, K., Baumann, E., Jin, H., Zachgo, S., Roberts, K., Schwarz-Sommer, Z., Glover, B. & Perez- Rodrigues, M. 2002 The mechanics of cell fate determination in petals. Phil. Trans. R. Soc. Lond. B 357, 809-813. (doi:10.1098/rstb.2002.1089) (Pubitemid 34735688)
72. Miikeda, O., Kita, K., Handa, T. & Yukawa, T. 2006 Phylogenetic relationships of Clematis (Ranunculaceae) based on chloroplast and nuclear DNA sequences. Bot. J. Linn. Soc. 152, 153-168.
73. Miller, R. B. 1981 Hawkmoths and the geographic patterns of floral variation in Aquilegia caerulea. Evolution 35, 763-774. (doi:10.2307/2408246)
74. Noda, K., Glover, B. J., Linstead, P. & Martin, C. 1994 Flower color intensity depends on specialized cell-shape controlled by a Myb-related transcription factor. Nature 369, 661-664. (doi:10.1038/369661a0) (Pubitemid 24199471)
75. Okamuro, J. K., Caster, B., Villarroel, R., van Montagu, M. & Jofuku, K. D. 1997 The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc. Natl Acad. Sci. 94, 7076-7081. (doi:10.1073/pnas.94.13.7076) (Pubitemid 27281993)
76. Orr, H. A. & Coyne, J. A. 1992 The genetics of adaptation- a reassesment. Am. Nat. 140, 725-742.
77. Park, J. -H., Ishikawa, Y.,Yoshida, R.,Kanno, A.&Kameya, T. 2003 Expression of AODEF, a B-functional MADS-box gene, in stamens and inner tepals of the dioecious species Asparagus officinalis L. Plant Mol. Biol. 51, 867-875. (doi:10.1023/A:1023097202885) (Pubitemid 36573166)
78. Park, J.-H., Ishikawa, Y., Ochiai, H., Kanno, A. & Kameya, T. 2004 Two GLOBOSA-like genes are expressed in second and third whorls of homochlamydeous flowers in Asparagus offinalis L. Plant Cell Phys. 45, 325-332. (doi:10.1093/pcp/pch040) (Pubitemid 38473461)
79. Piwarzyk, E., Yang, Y. & Jack, T. 2007 Conserved C-terminal motifs of the Arabidopsis proteins APETALA3 and PISTILLATA are dispensable for floral organ identity function. Plant Phys. 145, 1495-1505. (doi:10.1104/pp.107.105346) (Pubitemid 350276769)
80. Prantl, K. 1887 Beitrage zur Morphologie und Systematik der Ranunculacean. Bot. Jahrb. Syst. 9, 225-273.
81. Prazmo,W. 1961 Cytogenetic studies on the genus Aquilegia II. Crosses between Aquilegia ecalcarata Maxim. and Aquilegia chrysantha Gray. Acta Soc. Bot. Pol. 30, 57-77.
82. Prazmo,W. 1965 Cytogenetic studies on the genus Aquilegia. III. Inheritance of the traits distinguishing different complexes in the genus Aquilegia. Acta Soc. Bot. Pol. 34, 403-437.
83. Preston, J. C. & Hileman, L. C. 2009 Developmental genetics of floral symmetry evolution. Trends Plant Sci. 14, 147-154. (doi:10.1016/j.tplants.2008. 12.005)
84. Rasmussen, D. E., Kramer, E. M. & Zimmer, E. A. 2009 One size fits all? Molecular evidence for a commonly inherited petal identity program in the Ranunculales. Am. J. Bot. 96, 1-14.
85. Rausher, M. D. 2008 Evolutionary transitions in floral color. Int. J. Plant Sci. 169, 7-21. (doi:10.1086/523358) (Pubitemid 351230619)
86. Ro, K. E. & McPheron, B. A. 1997 Molecular phylogeny of the Aquilegia group (Ranunculaceae) based on internal transcribed spacers and 5.8S nuclear ribosmal DNA. Biochem. Syst. Ecol. 25, 445-461. (doi:10.1016/S0305-1978(97) 00029-X) (Pubitemid 27327914)
87. Rosin, F. M. & Kramer, E. M. 2009 Old dogs, new tricks: regulatory evolution in conserved genetic modules leads to novel morphologies in plants. Dev. Biol. 332, 25-35 (doi:10.1016/j.ydbio.2009.05.542)
88. Sablowski, R. W. M. & Meyerowitz, E. M. 1998 A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92, 93-103. (doi:10.1016/S0092-8674(00)80902-2) (Pubitemid 28053301)
89. Schwinn, K. et al. 2006 A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18, 831-851. (doi:10.1105/tpc.105.039255) (Pubitemid 43956139)
90. Smith, G. H. 1928 Vascular anatomy of ranalian flowers. Bot. Gaz. 82, 85, 1-29. 152-177.
91. Stellari, G. M., Jaramillo, M. A. & Kramer, E. M. 2004 Evolution of the APETALA3 and PISTILLATA lineages of MADS-box containing genes in basal angiosperms. Mol. Biol. Evol. 21, 506-519. (doi:10.1093/molbev/msh044) (Pubitemid 38339667)
92. Streisfeld, M. A. & Rausher, M. D. 2009 Altered transregulatory control of gene expression in multiple anthocyanin genes contributes to adaptive flower color evolution in Mimulus aurantiacus. Mol. Biol. Evol. 26, 433-444. (doi:10.1093/molbev/msn268)
93. Takhtajan, A. 1991 Evolutionary trends in flowering plants. New York, NY: Columbia University Press.
94. Tamura, M. 1965 Morphology, ecology, and phylogeny of the Ranunculaceae IV. Sci. Rep. Osaka Univ. 14, 53-71.
95. Tamura, M. 1993 Ranunculaceae. In The families and genera of vascular plants. 2. Flowering plants. Dicotyledons. Magnoliid, Hamamelid and Caryophyllid families, vol.2 (eds K. Kubitzki, J. G. Rohwer & V. Bittrich), pp. 563-583. Berlin, Germany: Springer.
96. Taylor, R. J. 1984 Floral anthocyanins of Aquilegia and their relationship to distribution and pollination biology of the species. Bull. Torrey Bot. Club 111, 462-468. (doi:10.2307/2995896)
97. Tucker, S. C. & Hodges, S. A. 2005 Floral ontogeny of Aquilegia, Semiaquilegia, and Isopyrum (Ranunculaceae). Int. J. Plant Sci. 166, 557-574. (doi:10.1086/429848)
98. Vandenbussche, M., Theissen, G., Van de Peer, Y. & Gerats, T. 2003 Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucl. Acids Res. 31, 4401-4409. (doi:10.1093/nar/gkg642) (Pubitemid 37441800)
99. Walker-Larsen, J. & Harder, L. D. 2000 The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention. Am. J. Bot. 87, 1367-1384. (doi:10.2307/2656866)
100. Wang, Z. et al. 2008 Genetic control of floral zygomorphy in pea (Pisum sativum L.). Proc. Natl Acad. Sci. USA 105, 10 414-10 419. (doi:10.1073/pnas. 0803291105)
101. Wasserthal, L. T. 1997 The pollinators of the Malagasy star orchids Angraecum sesquipedale, A. sororium and A. compactum and the evolution of extremely long spurs by pollinator shift. Bot. Acta 110, 343-359.
102. Weigel, D. 1995 The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell 7, 388-389. (doi:10.1105/tpc.7.4.388)
103. Whibley, A. C., Langlade, N. B., Andalo, C., Hanna, A. I., Bangham, A., Thebaud, C. & Coen, E. 2006 Evolutionary paths underlying flower color variation in Antirrhinum. Science 313, 963-966. (doi:10.1126/science.1129161) (Pubitemid 44267386)
104. Whitney, H. M., Chittka, L., Bruce, T. J. A. & Glover, B. J. 2009 Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr. Biol. 19, 948-953. (doi:10.1016/j.cub.2009.04.051)
105. Whittall, J. B. & Hodges, S. A. 2007 Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447, 706-710. (doi:10.1038/nature05857) (Pubitemid 46889728)
106. Whittall, J. B., Medina-Marino, A., Zimmer, E. A. & Hodges, S. A. 2006a Generating single-copy nuclear gene data for a recent adaptive radiation. Mol. Phylogenet. Evol. 39, 124-134. (doi:10.1016/j.ympev.2005.10.010)
107. Whittall, J. B., Voelckel, C., Kliebenstein, D. J. & Hodges, S. A. 2006b Convergence, constraint and the role of gene expression during adaptive radiation: floral anthocyanins in Aquilegia. Mol. Ecol. 15, 4645-4657. (doi:10.1111/j.1365-294X.2006.03114.x) (Pubitemid 44749576)
108. Worsdell, W. C. 1903 The origin of the perianth of flowers, with special reference to the Ranunculaceae. New Phyt. 2, 42-48.
109. Xu, L., Chen, H., Hu, X. H., Zhang, R. M., Zhang, Z. & Luo, Z. W. 2006 Average gene length is highly conserved in prokaryotes and eukaryotes and diverges only between the two kingdoms. Mol. Biol. Evol. 23, 1107-1108. (doi:10.1093/molbev/msk019) (Pubitemid 43781585)
110. Yang, J. Y., Counterman, B. A., Eckert, C. G. & Hodges, S. A. 2005 Cross-species amplification of microsatellite loci in Aquilegia and Semiaquilegia (Ranunculaceae). Mol. Ecol. Notes 5, 317-320. (doi:10.1111/j.1471- 8286.2005.00913.x) (Pubitemid 40772361)
111. Zachgo, S., de Andrade Silva, E., Motte, P., Trobner, W., Saedler, H. & Schwarz-Sommer, Z. 1995 Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant. Development 121, 2861-2875.
112. Zahn, L. M., Kong, H., Leebens-Mack, J. H., Kim, S., Soltis, P. S., Landherr, L. L., Soltis, D. E., Depamphilis, C. W. & Ma, H. 2005a The evolution of the SEPALLATA subfamily of MADS-Box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169, 2209-2223. (doi:10.1534/genetics.104.037770) (Pubitemid 40695631)
113. Zahn, L. M., Leebens-Mack, J., dePamphilis, C.W., Ma, H. & Theissen, G. 2005b To B or not to B a flower: the role of DEFICIENS and GLOBOSA orthologs in the evolution of the angiosperms. J. Hered. 96, 225-240. (doi:10.1093/jhered/ esi033) (Pubitemid 40434677)
114. Zanis, M., Soltis, P. S., Qiu, Y.-L., Zimmer, E. A. & Soltis, D. E. 2003 Phylogenetic analyses and perianth evolution in basal angiosperms. Ann. Mo. Bot. Gard. 90, 129-150. (doi:10.2307/3298579)