Flower color as a model system for studies of plant evo-devo

Frontiers in Plant Science

Volumn 4, Issue AUG, 2013, Pages

  Sobel, James M ^a   Streisfeld, Matthew A ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Anthocyanin; Co option; Flower color; Pleiotropy; Predictability; R2R3 MYB

Indexed keywords

EID: 84897626110     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00321     Document Type: Article

References (130)

1. Albert, N. W., Lewis, D. H., Zhang, H., Schwinn, K. E., Jameson, P. E., and Davies, K. M. (2011). Members of an R2R3-MYB transcription factor family in Petunia are developmentally and environmentally regulated to contrsol complex floral and vegetative pigmentation patterning. Plant J. 65, 771-784. doi: 10.1111/j.1365-313X.2010.04465.x
2. Arendt, J., and Reznick, D. (2008). Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23, 26-32. doi: 10.1016/j.tree.2007.09.011
3. Armbruster, W. S. (2002). Can indirect selection and genetic context contribute to trait diversification? A transition-probability study of blossom-colour evolution in two genera. J. Evol. Biol. 15, 468-486. doi: 10.1046/j.1420-9101. 2002.00399.x
4. Baumann, K., Perez-Rodriguez, M., Bradley, D., Venail, J., Bailey, P., Jin, H. L., et al. (2007). Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134, 1691-1701. doi: 10.1242/dev.02836
5. Beardsley, P. M., Schoenig, S. E., Whittall, J. B., and Olmstead, R. G. (2004). Patterns of evolution in Western North American Mimulus (Phrymaceae). Am. J. Bot. 91, 474-489. doi: 10.3732/ajb.91. 3.474
6. Beardsley, P. M., Yen, A., and Olmstead, R. G. (2003). AFLP phylogeny of Mimulus section Erythranthe and the evolution of hummingbird pollination. Evolution 57, 1397-1410.
7. Becker, A., and Theissen, G. (2003). The major clades of MADS-box 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
8. Beeks, R. M. (1962). Variation and hybridization in southern California populations of Diplacus (Scrophulariaceae). El Aliso 5, 83-122.
9. Bradshaw, H. D., Otto, K. G., Frewen, B. E., McKay, J. K., and Schemske, D. W. (1998). Quantitative trait loci affecting differences in floral morphology between two species of mon-keyflower (Mimulus). Genetics 149, 367-382.
10. Bradshaw, H. D., and Schemske, D. W. (2003). Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426, 176-178. doi: 10.1038/ nature02106
11. Bradshaw, H. D., Wilbert, S. M., Otto, K. G., and Schemske, D. W. (1995). Genetic-mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature 376, 762-765. doi: 10.1038/ 376762a0
12. Brockington, S. F., Walker, R. H., Glover, B. J., Soltis, P. S., and Soltis, D. E. (2011). Complex pigment evolution in the Caryophyllales. New Phytol. 190, 854-864. doi: 10.1111/j.1469-8137. 2011.03687.x
13. Broun, P. (2005). Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr. Opin. Plant Biol. 8, 272-279. doi: 10.1016/j.pbi. 2005.03.006
14. Caicedo, A. L., Stinchcombe, J. R., Olsen, K. M., Schmitt, J., and Purugganan, M. D. (2004). Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc. Natl. Acad. Sci. U.S.A. 101, 15670-15675. doi: 10.1073/pnas.0406232101
15. Carroll, S. B. (2005). Evolution at two levels: on genes and form. PLoS Biol. 3:e245. doi: 10.1371/jour-nal.pbio.0030245
16. Carroll, S. B. (2008). Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25-36. doi: 10.1016/j.cell.2008.06.030
17. Chalker-Scott, L. (1999). Environmental significance of anthocyanins in plant stress response. Photochem. Photobiol. 70, 1-9. doi: 10.1111/j.1751-1097.1999.tb01944.x
18. Chan, Y. F., Marks, M. E., Jones, F. C., Villarreal G. Jr., Shapiro, M. D., Brady, S. D., et al. (2010). Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302-305. doi: 10.1126/science.1182213
19. Chang, S. M., Lu, Y. Q., and Rausher, M. D. (2005). Neutral evolution of the nonbinding region of the antho-cyanin regulatory gene Ipmyb1 in Ipomoea. Genetics 170, 1967-1978. doi: 10.1534/genetics.104.034975
20. Coberly, L. C., and Rausher, M. D. (2003). Analysis of a chalcone syn-thase mutant in Ipomoea pur-purea reveals a novel function for flavonoids: amelioration of heat stress. Mol. Ecol. 12, 1113-1124. doi: 10.1046/j.1365-294X.2003.01786.x
21. Coberly, L. C., and Rausher, M. D. (2008). Pleiotropic effects of an allele producing white flowers in Ipomoea purpurea. Evolution 62, 1076-1085. doi: 10.1111/j.1558-5646.2008.00355.x
22. Conte, G. L., Arnegard, M. E., Peichel, C. L., and Schluter, D. (2012). The probability of genetic parallelism and convergence in natural popu lations. Proc. R. Soc. B Biol. Sci. 279, 5039-5047. doi: 10.1098/rspb. 2012.2146
23. Cooley, A. M., Carvallo, G., and Willis, J. H. (2008). Is floral diversification associated with pollinator divergence? Flower shape, flower colour and pollinator preference in chilean Mimulus. Ann. Bot. 101, 641-650. doi: 10.1093/aob/ mcn014
24. Cooley, A. M., Modliszewski, J. L., Rommel, M. L., and Willis, J. H. (2011). Gene duplication in Mimulus underlies parallel floral evolution via independent trans-regulatory changes. Curr. Biol. 21, 700-704. doi: 10.1016/j.cub.2011.03.028
25. Cooley, A. M., and Willis, J. H. (2009). Genetic divergence causes parallel evolution of flower color in Chilean Mimulus. New Phytol. 183, 729-739. doi: 10.1111/j.1469-8137.2009.02858.x
26. Davies, K. M., Albert, N. W., and Schwinn, K. E. (2012). From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning. Funct. Plant Biol. 39, 619-638. doi: 10.1071/ FP12195
27. Des Marais, D. L., and Rausher, M. D. (2008). Escape from adaptive conflict after duplication in an antho-cyanin pathway gene. Nature 454, U762-U785.
28. Dias, A. P., Braun, E. L., McMullen, M. D., and Grotewold, E. (2003). Recently duplicated maize R2R3 Myb genes provide evidence for distinct mechanisms of evolutionary divergence after duplication. Plant Physiol. 131, 610-620. doi: 10.1104/pp.012047
29. Dick, C. A., Buenrostro, J., Butler, T., Carlson, M. L., Kliebenstein, D. J., and Whittall, J. B. (2011). Arctic mustard flower color polymorphism controlled by petal-specific downregulation at the threshold of the anthocyanin biosynthetic pathway. PLoS ONE 6:e18230. doi: 10.1371/journal. pone.0018230
30. Dixon, R. A., Xie, D. Y., and Sharma, S. B. (2005). Proanthocyanidins - a final frontier in flavonoid research? New Phytol. 165, 9-28. doi: 10.1111/j.1469-8137.2004.01217.x
31. Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., and Lepiniec, L. (2010). MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573-581. doi: 10.1016/j.tplants. 2010.06.005
32. Durbin, M. L., Lundy, K. E., Morrell, P. L., Torres-Martinez, C. L., and Clegg, M. T. (2003). Genes that determine flower color: the role of regulatory changes in the evolution of phenotypic adaptations. Mol. Phylogenet. Evol. 29, 507-518. doi: 10.1016/S1055-7903 (03)00196-9
33. Emerson, K. J., Merz, C. R., Catchen, J. M., Hohenlohe, P. A., Cresko, W. A., Bradshaw, W. E., et al. (2010). Resolving postglacial phylo-geography using high-throughput sequencing. Proc. Natl. Acad. Sci. U.S.A. 107, 16196-16200. doi: 10.1073/pnas.1006538107
34. Fehr, C., and Rausher, M. D. (2004). Effects of variation at the flower-colour A locus on mating system parameters in Ipomoea pur-purea. Mol. Ecol. 13, 1839-1847. doi: 10.1111/j.1365-294X.2004.02182.x
35. Feller, A., Machemer, K., Braun, E. L., and Grotewold, E. (2011). Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J. 66, 94-116. doi: 10.1111/j.1365-313X.2010.04459.x
36. Fenster, C. B., Armbruster, W. S., Wilson, P., Dudash, M. R., and Thomson, J. D. (2004). Pollination syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst. 35, 375-403. doi: 10.1146/annurev. ecolsys.34.011802.132347
37. Fitzjohn, R. G., Maddison, W. P., and Otto, S. P. (2009). Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58, 595-611. doi: 10.1093/sysbio/syp067
38. Flagel, L. E., and Wendel, J. F. (2009). Gene duplication and evolutionary novelty in plants. New Phytol. 183, 557-564. doi: 10.1111/j.1469-8137.2009.02923.x
39. Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y. L., and Postlethwait, J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531-1545.
40. Gompel, N., and Prud'Homme, B. (2009). The causes of repeated genetic evolution. Dev. Biol. 332, 36-47. doi: 10.1016/j.ydbio.2009.04.040
41. Gompel, N., Prud'Homme, B., Wittkopp, P. J., Kassner, V. A., and Carroll, S. B. (2005). Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433, 481-487. doi: 10.1038/ nature03235
42. Gonzalez, A., Zhao, M., Leavitt, J. M., and Lloyd, A. M. (2008). Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 53, 814-827. doi: 10.1111/j.1365-313X.2007.03373.x
43. Grant, A. L. (1924). A monograph of the genus Mimulus. Ann. Mo. Bot. Gard. 11, 99-388. doi: 10.2307/2394024
44. Grant, V. (1981). Plant Speciation. New York, NY: Columbia University Press.
45. Grotewold, E. (2006). The Science of Flavonoids. New York, NY: Springer. doi: 10.1007/978-0-387-28822-2
46. Guillaume, F., and Otto, S. P. (2012). Gene functional trade-offs and the evolution of pleiotropy. Genetics 192, 1389-1409. doi: 10.1534/genet-ics.112.143214
47. Haberer, G., Hindemitt, T., Meyers, B. C., and Mayer, K. F. X. (2004). Transcriptional similarities, dissimilarities, and conservation of cis-elements in duplicated genes of arabidopsis. Plant Physiol. 136, 3009-3022. doi: 10.1104/pp.104.046466
48. Habu, Y., Hisatomi, Y., and Lida, S. (1998). Molecular characterization of the mutable flaked allele for flower variegation in the common morning glory. Plant J. 16, 371-376. doi: 10.1046/j.1365-313x.1998.00308.x
49. Hichri, I., Barrieu, F., Bogs, J., Kappel, C., Delrot, S., and Lauvergeat, V. (2011). Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J. Exp. Bot. 62, 2465-2483. doi: 10.1093/jxb/erq442
50. Hiesey, W. M., Nobs, M. A., and Bjorkman, O. (1971). Experimental Studies on the Nature of Species. V. Biosystematics, Genetics, and Physiological Ecology of the Erythranthe Section of Mimulus. Washington, DC: Carnegie Institution of Washington Publication 628.
51. Hoballah, M. E., Gubitz, T., Stuurman, J., Broger, L., Barone, M., Mandel, T., et al. (2007). Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19, 779-790. doi: 10.1105/tpc.106.048694
52. Hoekstra, H. E., and Coyne, J. A. (2007). The locus of evolu tion: evo devo and the genetics of adaptation. Evolution 61, 995-1016. doi: 10.1111/j.1558-5646.2007.00105.x
53. Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A., and Crossland, J. P. (2006). A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313, 101-104. doi: 10.1126/ science.1126121
54. Holton, T. A., and Cornish, E. C. (1995). Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7, 1071-1083.
55. Hopkins, R., and Rausher, M. D. (2011). Identification of two genes causing reinforcement in the Texas wildflower Phlox drum-mondii. Nature 469, 411-414. doi: 10.1038/nature09641
56. Hopkins, R., and Rausher, M. D. (2012). Pollinator-mediated selection on flower color allele drives reinforcement. Science 335, 1090-1092. doi: 10.1126/science.1215198
57. Innan, H., and Kondrashov, F. (2010). The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97-108. doi: 10.1038/nrg2689
58. Jia, L., Clegg, M. T., and Jiang, T. (2003). Excess non-synonymous substitutions suggest that positive selection episodes occurred during the evolution of DNA-binding domains in the Arabidopsis R2R3-MYB gene family. Plant Mol. Biol. 52, 627-642. doi: 10.1023/A:1024875232511
59. Jenner, R. A., and Wills, M. A. (2007). The choice of model organisms in evo-devo. Nat. Rev. Genet. 8, 311-319. doi: 10.1038/nrg2062
60. Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R., and Dean, C. (2000). Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344-347. doi: 10.1126/science.290.5490.344
61. Kay, K. M., Reeves, P. A., Olmstead, R. G., and Schemske, D. W. (2005). Rapid speciation and the evolution of hummingbird pollination in Neotropical Costus subgenus Costus (Costaceae): evidence from nrDNA ITS and ETS sequences. Am. J. Bot. 92, 1899-1910. doi: 10.3732/ajb.92.11.1899
62. Keeling, C. I., Weisshaar, S., Lin, R. P. C., and Bohlmann, J. (2008). Functional plasticity of paralogous diterpene synthases involved in conifer defense. Proc. Natl. Acad. Sci. U.S.A. 105, 1085-1090. doi: 10.1073/pnas.0709466105
63. Koes, R., Verweij, W., and Quattrocchio, F. (2005). Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 10, 236-242. doi: 10.1016/j.tplants.2005.03.002
64. Kopp, A. (2009). Metamodels and phylogenetic replication: a systematic approach to the evolution of developmental pathways. Evolution 63, 2771-2789. doi: 10.1111/j.1558-5646.2009.00761.x
65. Kramer, E. M., Dorit, R. L., and 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.
66. Kramer, E. M., and Irish, V. F. (1999). Evolution of genetic mechanisms controlling petal development. Nature 399, 144-148. doi: 10.1038/20172
67. Levin, D. A. (1985). Reproductive character displacement in Phlox. Evol. 39, 1275-1281. doi: 10.2307/2408784
68. Lowry, D. B., Sheng, C. C., Lasky, J. R., and Willis, J. H. (2012). Five anthocyanin polymorphisms are associated with an R2r3-Myb cluster in Mimulus guttatus (Phrymaceae). Am. J. Bot. 99, 82-91. doi: 10.3732/ajb.1100285
69. Lu, Y. Q., and Rausher, M. D. (2003). Evolutionary rate variation in anthocyanin pathway genes. Mol. Biol. Evol. 20, 1844-1853. doi: 10.1093/molbev/msg197
70. Lynch, M., and Conery, J. S. (2000). The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155. doi: 10.1126/sci-ence.290.5494.1151
71. Lynch, V. J., and Wagner, G. P. (2008). Resurrecting the role of transcription factor change in developmental evolution. Evolution 62, 2131-2154. doi: 10.1111/j.1558-5646.2008.00440.x
72. Maddison, W. P., Midford, P. E., and Otto, S. P. (2007). Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56, 701-710. doi: 10.1080/10635150701607033
73. Manceau, M., Domingues, V. S., Linnen, C. R., Rosenblum, E. B., and Hoekstra, H. E. (2010). Convergence in pigmentation at multiple levels: mutations, genes and function. Philos. Trans. R. Soc. B Biol. Sci. 365, 2439-2450. doi: 10.1098/rstb.2010.0104
74. Martin, A., and Orgogozo, V. (2013). The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67, 1235-1250.
75. Martin, C., Ellis, N., and Rook, F. (2010). Do transcription factors play special roles in adaptive variation? Plant Physiol. 154, 506-511. doi: 10.1104/pp.110.161331
76. Matsui, K., Umemura, Y., and Ohme-Takagi, M. (2008). AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J. 55, 954-967. doi: 10.1111/j.1365-313X.2008.03565.x
77. Mauseth, J. D. (2004). The structure of photosynthetic succulent stems in plants other than cacti. Int. J. Plant Sci. 165, 1-9. doi: 10.1086/380978
78. Medel, R., Botto-Mahan, C., and Kalin-Arroyo, M. (2003). Pollinator-mediated selection on the nectar guide phenotype in the Andean monkey flower, Mimulus luteus. Ecology 84, 1721-1732. doi: 10.1890/01-0688
79. Medel, R., Valiente, A., Botto-Mahan, C., Carvallo, G., Perez, F., Pohl, N., et al. (2007). The influence of insects and hummingbirds on the geographical variation of the flower phenotype in Mimulus luteus. Ecography 30, 812-818. doi: 10.1111/j.2007.0906-7590.05175.x
80. Mendel, G. (1866). Experiments in plant hybridization. Proc. Nat. Hist. Soc. Brünn 4, 3-47.
81. Morita, Y., Saitoh, M., Hoshino, A., Nitasaka, E., and Iida, S. (2006). Isolation of cDNAs for R2R3-MYB, bHLH and WDR transcriptional regulators and identification of c and ca mutations conferring white flowers in the Japanese morning glory. Plant Cell Physiol. 47, 457-470. doi: 10.1093/pcp/pcj012
82. Ohno, S. (1970). Evolution by Gene Duplication. New York, NY: Springer.
83. Orr, H. A. (2000). Adaptation and the cost of complexity. Evolution 54, 13-20. doi: 10.1111/j.0014-3820.2000.tb00002.x
84. Ossowski, S., Schneeberger, K., Lucas-Lledo, J. I., Warthmann, N., Clark, R. M., Shaw, R. G., et al. (2010). The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92-94. doi: 10.1126/science.1180677
85. Otto, S. P. (2004). Two steps forward, one step back: the pleiotropic effects of favoured alleles. Proc. R. Soc. B Biol. Sci. 271, 705-714. doi: 10.1098/rspb.2003.2635
86. Perret, M., Chautems, A., Spichiger, R., Kite, G., and Savolainen, V. (2003). Systematics and evolution of tribe Sinningieae (Gesneriaceae): evidence from phylogenetic analyses of six plastid DNA regions and nuclear ncpGS. Am. J. Bot. 90, 445-460. doi: 10.3732/ajb. 90.3.445
87. Prazmo, W. (1961). Cytogenetic studies on the genus Aquilegia II. Crosses between Aquilegia ecalcarata Maxim. and Aquilegia chrysantha gray. Acta Societatis Botanicorum Poloniae 30, 57-77.
88. Preston, J. C., and Hileman, L. C. (2009). Developmental genetics of floral symmetry evolution. Trends Plant Sci. 14, 147-154. doi: 10.1016/j.tplants.2008.12.005
89. Prud'Homme, B., Gompel, N., and Carroll, S. B. (2007). Emerging principles of regulatory evolution. Proc. Natl. Acad. Sci. U.S.A. 104, 8605-8612. doi: 10.1073/pnas.0700488104
90. Quattrocchio, F., Baudry, A., Lepiniec, L., and Grotewold, E. (2006). "The regulation of flavonoid biosynthesis," in The Science of Favonoids, ed E. Grotewold (New York, NY: Springer), 97-122. doi: 10.1007/978-0-387-28822-2_4
91. Quattrocchio, F., Wing, J., van der Woude, K., Souer, E., de Vetten, N., Mol, J., et al. (1999). Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11, 1433-1444.
92. Rajagopalan, R., Vaucheret, H., Trejo, J., and Bartel, D. P. (2006). A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20, 3407-3425. doi: 10.1101/gad.1476406
93. Ramsay, N. A., and Glover, B. J. (2005). MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci. 10, 63-70. doi: 10.1016/j.tplants.2004.12.011
94. Rausher, M. D. (2008). Evolutionary transitions in flower color. Int. J. Plant Sci. 169, 7-21. doi: 10.1086/523358
95. Rausher, M. D., and Fry, J. D. (1993). Effects of a locus affecting floral pigmentation in Ipomoea purpurea on female fitness components. Genetics 134, 1237-1247.
96. Rebeiz, M., Pool, J. E., Kassner, V. A., Aquadro, C. F., and Carroll, S. B. (2009). Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326, 1663-1667. doi: 10.1126/sci-ence.1178357
97. Rosin, F. M., and 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
98. Schemske, D. W., and Bradshaw, H. D. (1999). Pollinator preference and the evolution of floral traits in mon-keyflowers (Mimulus). Proc. Natl. Acad. Sci. U.S.A. 96, 11910-11915. doi: 10.1073/pnas.96.21.11910
99. Schwinn, K., Venail, J., Shang, Y. J., Mackay, S., Alm, V., Butelli, E., 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
100. Shang, Y. J., Venail, J., Mackay, S., Bailey, P. C., Schwinn, K. E., Jameson, P. E., et al. (2011). The molecular basis for venation patterning of pigmentation and its effect on pollinator attraction in flowers of Antirrhinum. New Phytol. 189, 602-615. doi: 10.1111/j.1469-8137.2010.03498.x
101. Simon, M., Lee, M. M., Lin, Y., Gish, L., and Schiefelbein, J. (2007). Distinct and overlapping roles of single-repeat MYB genes in root epi-dennal patterning. Dev. Biol. 311, 566-578. doi: 10.1016/j.ydbio.2007. 09.001
102. Stern, D. L. (2000). Perspective: evolutionary developmental biology and the problem of variation. Evolution 54, 1079-1091.
103. Stern, D. L. (2011). Evolution, Development, and the Predictable Genome. Greenwood Village, CO: Roberts and Co.
104. Stern, D. L., and Orgogozo, V. (2008). The loci of evolution: how predictable is genetic evolution? Evolution 62, 2155-2177. doi: 10.1111/j.1558-5646.2008.00450.x
105. Stern, D. L., and Orgogozo, V. (2009). Is genetic evolution predictable? Science 323, 746-751. doi: 10.1126/science.1158997
106. Stracke, R., Werber, M., and Weisshaar, B. (2001). The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447-456. doi: 10.1016/S1369-5266(00)00199-0
107. Strauss, S. Y., and Whittall, J. B. (2006). "Non-pollinator agents of selection on floral traits," in Ecology and Evolution of Flowers, eds L. D. Harder and S. C. H. Barrett (Oxford: Oxford University Press), 120-138.
108. Streisfeld, M. A., and Kohn, J. R. (2005). Contrasting patterns of floral and molecular variation across a cline in Mimulus aurantiacus. Evolution 59, 2548-2559.
109. Streisfeld, M. A., and Kohn, J. R. (2007). Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J. Evol. Biol. 20, 122-132. doi: 10.1111/j.1420-9101.2006.01216.x
110. Streisfeld, M. A., Liu, D., and Rausher, M. D. (2011). Predictable pat terns of constraint among anthocyanin-regulating tran- scription factors in Ipomoea. New Phytol. 191, 264-274. doi: 10.1111/j.1469-8137.2011.03671.x
111. Streisfeld, M. A., and Rausher, M. D. (2007). Relaxed constraint and evolutionary rate variation between basic helix-loop-helix floral antho-cyanin regulators in Ipomoea. Mol. Biol. Evol. 24, 2816-2826. doi: 10.1093/molbev/msm216
112. Streisfeld, M. A., and Rausher, M. D. (2009). Altered trans-regulatory 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/mol-bev/msn268
113. Streisfeld, M. A., and Rausher, M. D. (2011). Population genetics, pleiotropy, and the preferential fixation of mutations during adaptive evolution. Evolution 65, 629-642. doi: 10.1111/j.1558-5646.2010.01165.x
114. Streisfeld, M. A., Young, W. N., and Sobel, J. M. (2013). Divergent selection drives genetic differentiation in an R2R3-Myb transcription factor that contributes to incipient speciation in Mimulus aurantiacus. PLoS Genet. 9:e1003385. doi: 10.1371/journal.pgen.1003385
115. Toleno, D. M., Durbin, M. L., Lundy, K. E., and Clegg, M. T. (2010). Extensive evolutionary rate variation in floral color determining genes in the genus Ipomoea. Plant Species Biol. 25, 30-42. doi: 10.1111/j.1442-1984.2009.00256.x
116. True, J. R., and Carroll, S. B. (2002). Gene co-option in physiological and morphological evolution. Annu. Rev. Cell Dev. Biol. 18, 53-80. doi: 10.1146/annurev.cellbio.18.020402. 140619
117. Vargas, P., Carrio, E., Guzman, B., Amat, E., and Guemes, J. (2009). A geographical pattern of Antirrhinum (Scrophulariaceae) speciation since the Pliocene based on plastid and nuclear DNA polymorphisms. J. Biogeogr. 36, 1297-1312. doi: 10.1111/j.1365-2699.2008.02059.x
118. Vickery, R. K. (1995). Speciation by aneuploidy and polyploidy in Mimulus (Scrophulariaceae). Gt. Basin Nat. 55, 174-176.
119. Von Wettberg, E. J., Stanton, M. L., and Whittall, J. B. (2010). How anthocyanin mutants respond to stress: the need to distinguish between stress tolerance and maximal vigour. Evol. Ecol. Res. 12, 457-476.
120. Wagner, A. (2011). The molecular origins of evolutionary innovations. Trends Genet. 27, 397-410. doi: 10.1016/j.tig.2011.06.002
121. Wagner, G. P., and Lynch, V. J. (2008). The gene regulatory logic of transcription factor evolution. Trends Ecol. Evol. 23, 377-385. doi: 10.1016/j.tree.2008.03.006
122. Wessinger, C. A., and Rausher, M. D. (2012). Lessons from flower colour evolution on targets of selection. J. Exp. Bot. 63, 5741-5749. doi: 10.1093/jxb/ers267
123. Whibley, A. C., Langlade, N. B., Andalo, C., Hanna, A. I., Bangham, A., Thebaud, C., et al. (2006). Evolutionary paths underlying flower color variation in Antirrhinum. Science 313, 963-966. doi: 10.1126/science.1129161
124. Whittall, J. B., Voelckel, C., Kliebenstein, D. J., and Hodges, S. A. (2006). 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
125. Wilson, Y., and Hudson, A. (2011). The evolutionary history of Antirrhinum suggests that ancestral phenotype combinations survived repeated hybridizations. Plant J. 66, 1032-1043. doi: 10.1111/j.1365-313X.2011.04563.x
126. Winkel-Shirley, B. (2002). Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 5, 218-223. doi: 10.1016/S1369-5266(02)00256-X
127. Wittkopp, P. J., Stewart, E. E., Arnold, L. L., Neidert, A. H., Haerum, B. K., Thompson, E. M., et al. (2009). Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326, 540-544. doi: 10.1126/science.1176980
128. Wray, G. A. (2007). The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8, 206-216. doi: 10.1038/nrg2063
129. Wu, C. A., Lowry, D. B., Cooley, A. M., Wright, K. M., Lee, Y. W., and Willis, J. H. (2008). Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100, 220-230. doi: 10.1038/sj.hdy.6801018
130. Yuan, Y., Sagawa, J. M., Young, R. C., Christensen, B. J., and Bradshaw, H. D. (2013). Genetic dissection of a major anthocyanin QTL contributing to pollinator-mediated reproductive isolation between sister species of Mimulus. Genetics 194, 255-263. doi: 10.1534/genet-ics.112.146852