Flower color polymorphisms: Causes and evolutionary implications;Polimorfismos de color floral: Causas e implicaciones evolutivas

Ecosistemas

Volumn 23, Issue 3, 2014, Pages 36-47

  Narbona, Eduardo ^a   Buide, Ma Luisa ^a   Casimiro Soriguer, Inés ^a,b   del Valle, José C ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Anthocyanin biosynthetic pathway; Floral pigments; Intra individual variation; Pleiotropy; Speciation

Indexed keywords

EID: 84947422818     PISSN: None     EISSN: 16972473     Source Type: Journal    
DOI: 10.7818/ECOS.2014.23-3.06     Document Type: Article

References (157)

1. Agati, G., Biricolti, S., Guidi, L., Ferrini, F., Fini, A., Tattini, M. 2011. The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. Journal of Plant Physiology 168:204-212.
2. Andersen, Ø.M., Jordheim, M. 2006. The anthocyanins. En: Andersen, Ø.M., Markham, K.R. (eds.), Flavonoids: Chemistry, Biochemistry and Applications, pp. 471-551. CRC Press, Boca Raton, EEUU.
3. Arista, M., Talavera, M., Berjano, R., Ortiz, P.L. 2013. Abiotic factors may explain the geographical distribution of flower colour morphs and the maintenance of colour polymorphism in the scarlet pimpernel. Journal of Ecology 101:1613-1622.
4. Aristóteles (aprox. 350 a. C.). Historia animalium. Traducción de obra original al inglés publicada en 1910 por D'Arcy Wentworth Thompson “The works of Aristotle translated into English”. Volume IV. Oxford University Press, Londres, UK.
5. Ashman, T.-L., Majetic C.J. 2006. Genetic constraints on floral evolution: a review and evaluation of patterns. Heredity 96:343-352.
6. Bhuiyan, N.H., Selvaraj, G., Wei, Y., King, J. 2009. Role of lignification in plant defense. Plant Signaling and Behavior 4:158-159.
7. Boerjan, W., Ralph, J., Baucher, M. 2003. Lignin biosynthesis. Annual Review of Plant Biology 54:519-546.
8. Bradshaw, H.D., Schemske, D.W. 2003. Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176-178.
9. Brockington, S.F., Walker, R.H., Glover, B.J., Soltis, P.S., Soltis, D.E. 2011. Complex pigment evolution in the Caryophyllales. New Phytologist 190:854-864.
10. Burdon, J.J., Marshall, D.R., Brown, A.H.D. 1983. Demographic and genetic changes in populations of Echium plantagineum. Journal of Ecology 71:667-679
11. Campbell, D.R., Bischoff, M., Lord, J.M., Robertson, A.W. 2012. Where have all the blue flowers gone: pollinator responses and selection on flower colour in New Zealand Wahlenbergia albomarginata. Journal of Evolutionary Biology 25:352-364.
12. Carlson, J.E., Holsinger, K.E. 2013. Direct and indirect selection on floral pigmentation by pollinators and seed predators in a color polymorphic South African shrub. Oecologia 171:905-919.
13. Casimiro-Soriguer, I., Buide, M.L., Narbona, E. 2013. The roles of female and hermaphroditic flowers in the gynodioecious-gynomonoecious Silene littorea: insights into the phenology of sex expression. Plant Biology 15:941-947.
14. Chang, S.M., Lu, Y.Q., Rausher, M.D. 2005. Neutral evolution of the nonbinding region of the anthocyanin regulatory gene Ipmyb1 in Ipomoea. Genetics 170:1967-1978.
15. Chen, S., Xiang, Y., Deng, J., Liu, Y., Li, S. 2013. Simultaneous analysis of anthocyanin and non-anthocyanin flavonoid in various tissues of different Lotus (Nelumbo) cultivars by HPLC-DAD-ESI-MSn. PLoS ONE 8:e62291.
16. Chittka, L., Raine, N.E. 2006. Recognition of flowers by pollinators. Current Opinion in Plant Biology 9:428-435.
17. Chong, J., Poutaraud, A., Hugueney, P. 2009. Metabolism and roles of stilbenes in plants. Plant Science 177:143-155.
18. Clegg, M.T., Durbin, M.L. 2000. Flower color variation: A model for the experimental study of evolution. Proceedings of the National Academy of Sciences 97:7016-7023.
19. Coberly, L.C., Rausher, M.D. 2003. Analysis of a chalcone synthase mutant in Ipomoea purpurea reveals a novel function for flavonoids: amelioration of heat stress. Molecular Ecology 12:1113-1124.
20. Coberly, L.C., Rausher, M.D. 2008. Pleiotropic effects of an allele producing white flowers in Ipomoea purpurea. Evolution 62:1076-1085.
21. Coley, P.D. 1986. Costs and benefits of defense by tannins in a neotropical tree. Oecologia 70:238-241.
22. Coley, P.D., Aide, T.M. 1989. Red coloration of tropical young leaves: a possible antifungal defence? Journal of Tropical Ecology 5:293-300.
23. Conner, J.K. 2006. Ecological genetics of floral evolution. En: Harder, L.D., Barrett S.C.H. (eds.), Ecology and evolution of flowers, pp. 260-277. Oxford University Press, Oxford, UK.
24. Davies, K.M. 2009. Modifying anthocyanin production in flowers. En: Gould, K., Davies, K., Winefield, C. (eds.), Anthocyanins: Biosynthesis, Functions and Applications, pp. 49-84. Springer Science and Business, New York, EEUU.
25. Davies, K.M., Albert, N.W., Schwinn, K.E. 2012. From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning. Functional Plant Biology 39:619-638.
26. De Jager, M.L., Ellis, A.G. 2014. Floral polymorphism and the fitness implications of attracting pollinating and florivorous insects. Annals of Botany 113:213-222.
27. Des Marais, D.L., Rausher, M.D. 2010. Parallel evolution at multiple levels in the origin of hummingbird pollinated flowers in Ipomoea. Evolution 64:2044-2054.
28. Dick, C.A., Buenrostro, J., Butler, T., Carlson, M.L., Kliebenstein, D.J., 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.
29. Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., Lepiniec, L. 2010. MYB transcription factors in Arabidopsis. Trends in Plant Science 15:573-581.
30. Dyer, A.G., Spaethe, J., Prack, S. 2008. Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. Journal of Comparative Physiology A: Chemistry 194:617-627.
31. Eckhart, V.M., Rushing, N.S., Hart, G.M., Hansen, J. 2006. Frequency-dependent pollinator foraging in polymorphic Clarkia xantiana ssp. xantiana populations: implications for flower colour evolution and pollinator interactions. Oikos 112:412-421.
32. Ellis, A.G., Johnson, S.D. 2009. The evolution of floral variation without pollinator shifts in Gorteria diffusa (Asteraceae). American Journal of Botany 96:793-801.
33. Ellis, T.H., Hofer, J.M., Timmerman-Vaughan, G.M., Coyne, C.J., Hellens, R.P. 2011. Mendel, 150 years on. Trends in Plant Science 16:590-596.
34. Epling, C., Dobzhansky, T. 1942. Genetics of natural populations. VI. Micro-geographic races in Linanthus parryae. Genetics 27:317-332.
35. Epling, C., Lewis, H., Ball, F.M. 1960. The breeding group and seed storage: a study in population dynamics. Evolution 14:238-255.
36. Falcone Ferreyra, M.L., Rius, S.P., Casati, P. 2012. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Frontiers in Plant Science 3:222.
37. Fenster, C.B., Armbruster, W.S., Wilson, P., Dudash, M.R., Thomson, J.D. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35:375-403.
38. Forkmann, G. 1991. Flavonoids as flower pigments: the formation of the natural spectrum and its extension by genetic engineering. Plant Breeding 106:1-26.
39. Foster-Hartnett, D., Danesh, D., Peñuela, S., Sharapova, N., Endre, G., Vandenbosch, K.A., Young, N.D., Samac, D.A. 2007. Molecular and cytological responses of Medicago truncatula to Erysiphe pisi. Molecular Plant Pathology 8:307-319.
40. Fournier-Level, A., Le Cunff, L., Gomez, C., Doligez, A., Ageorges, A., Roux, C., Bertrand, Y., Souquet, J.M., Cheynier, V., This, P. 2009. Quantitative genetic bases of anthocyanin variation in grape (Vitis vinifera L. ssp. sativa) berry: a quantitative trait locus to quantitative trait nucleotide integrated study. Genetics 183:1127-1139.
41. Frey, F.M. 2004. Opposing natural selection from herbivores and pathogens may maintain floral color variation in Claytonia virginica (Portulacaceae). Evolution 58:2426-2437.
42. Fulkerson, J.R., Whittall, J.B., Carlson, M.L. 2012. Reproductive ecology and severe pollen limitation in the polychromic tundra plant, Parrya nudicaulis (Brassicaceae). PLoS ONE 7:e32790.
43. Glover, B.J. 2007. Understanding flowers and flowering: an integrated approach. Oxford University Press, New York, EEUU.
44. Glover, B.J., Martin, C. 1998. The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus. Heredity 80:77-8-784.
45. Glover, B.J., Walker, R.H., Moyroud, E., Brockington, S.F. 2013. How to spot a flower. New Phytologist 197:687-689.
46. Gómez, J.M. 2000. Phenotypic selection and response to selection in Lobularia maritima: importance of direct and correlational components of natural selection. Journal of Evolutionary Biology 13:689-699.
47. Gorton, H.L., Vogelmann, T.C. 1996. Effects of epidermal cell shape and pigmentation on optical properties of Antirrhinum petals at visible and ultraviolet wavelengths. Plant Physiology 112:879-888.
48. Gould, K.S. 2004. Nature's Swiss army knife: the diverse protective roles of anthocyanins in leaves. Journal of Biomedicine and Biotechnology 5:314-320.
49. Grant, V. 1949. Pollination systems as isolating mechanisms in Angiosperms. Evolution 3:82-97.
50. Grotewold, E. 2006. The genetics and biochemistry of floral pigments. Annual Review of Plant Biology 57:761-80.
51. Guzmán, B., Narbona, E., Vargas, P. 2011. Similar reproductive success of the two petal colour polymorphisms of Cistus ladanifer (Cistaceae). Plant Biosystems 145:931-937.
52. Habu, Y., Hisatomi, Y., Lida, S. 1998. Molecular characterization of the mutable flaked allele for flower variegation in the common morning glory. The Plant Journal 16:371-376.
53. Hansen, D.M., Oleson, J.M., Mione, T., Johnson, S.D., Muller, C.B. 2007. Coloured nectar: distribution, ecology, and evolution of an enigmatic floral trait. Biological Reviews 82:83-111.
54. Harder L.D., Johnson, S.D. 2009. Darwin's beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytologist 183:530-545.
55. Havaux, M., Kloppstech, K. 2001. The protective functions of carotenoid and flavonoids pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213:953-966.
56. He, Q., Shen, Y., Wang, M., Huang, M., Yang, R., Zhu, S., Wang, L., Xu, Y., Wu, R. 2011. Natural variation in petal color in Lycoris longituba revealed by anthocyanin components. PLoS ONE 6:e22098.
57. Hichri, I., Barrieu, F., Bogs, J., Kappel, C., Delrot, S., Lauvergeat, V. 2011. Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. Journal of Experimental Botany 62:2465-2483.
58. Higgins, V.J. 1978. The effect of some pterocarpanoid phytoalexins on germ tube elongation of Stemphylium botryosum. Phytopathology 68:339-345.
59. Hoballah, M.E., Gübitz, T., Stuurman, J., Broger, L., Barone, M., Mandel, T., Dell'Olivo, A., Arnold, M., Kuhlemeier, C. 2007. Single gene-mediated shift in pollinator attraction in Petunia. The Plant Cell 19:779-790.
60. 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. The American Naturalist 159: S51-S60.
61. Hopkins, R. 2013. Reinforcement in plants. New Phytologist 197:1095-1103.
62. Hopkins, R., Rausher, M.D. 2011. Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469:411-414.
63. Hopkins, R., Rausher, M.D. 2012. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335:1090-1092.
64. Hughes, N.M. 2011. Winter leaf reddening in 'evergreen' species. New Phytologist 190:573-581.
65. Hughes, N.M., Smith, W.K. 2007. Attenuation of incident light in Galax urceolata (Diapensiaceae): Concerted influence of adaxial and abaxial anthocyanic layers on photoprotection. American Journal of Botany 94:784-790.
66. Irwin, R.E., Strauss, S.Y. 2005. Flower color microevolution in wild radish: evolutionary response to pollinator-mediated selection. American Naturalist 165:225-237.
67. Irwin, R.E., Strauss, S.Y., Storz, S., Emerson, A., Guibert, G. 2003. The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84:1733-1743.
68. Johnson, E.T., Berhow, M.A., Dowd, P.F. 2008. Colored and white sectors from star-patterned petunia flowers display differential resistance to corn earworm and cabbage looper larvae. Journal of Chemical Ecology 34:757-765.
69. Kelber, A., Vorobyev, M., Osorio, D. 2003. Animal colour vision-behavioural tests and physiological concepts. Biological Reviews 78:81-118.
70. Kevan, P., Giurfa, M., Chittka, L. 1996. Why are there so many and so few white flowers?. Trends in Plant Science 1:280-284.
71. Kingsolver, J.G., Hoekstra, H.E., Hoekstra, J.M., Berrigan, D., Vignieri, S.N., Hill, C.E., Hoang, A., Gibert, P., Beerli, P. 2001. The strength of phenotypic selection in natural populations. The American Naturalist 157:245-261.
72. Knight, T.A. 1799. An account of some experiments on the fecundation of vegetables. Philosophical Transactions of the Royal Society of London 89:195-204.
73. Kusano, M., Tohge, T., Fukushima, A., Kobayashi, M., Hayashi,N., Otsuki, H., Kondou, Y., Goto, H., Kawashima, M., Matsuda, F., Niida, R., Matsui, M., Saito, K., Fernie, A.R. 2011. Metabolomics reveals comprehensive reprogramming involving two independent metabolic responses of Arabidopsis to UV-B light. The Plant Journal 67:354-369.
74. Kytridis, V-P., Manetas, Y. 2006. Mesophyll versus epidermal anthocyanins as potential in vivo antioxidants: evidence linking the putative antioxidant role to the proximity of oxyradical source. Journal of Experimental Botany 57:2203-2210.
75. Lacey, E., Herr, D. 2005. Phenotypic plasticity, parental effects, and parental care in plants? I. An examination of spike reflectance in Plantago lanceolata (Plantaginaceae). American Journal of Botany 92:920-930.
76. Lee, D.W. 2007. Nature's palette. University of Chicago Press, London, UK.
77. Lee, D.W., O'Keefe, J., Holbrook, N.M., Field, T.S. 2003. Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA. Ecological Reseach 18:677-694.
78. Levin, D.A. 1985. Reproductive character displacement in Phlox. Evolution 39:1275-1281.
79. Levin, D.A., Brack, E.T. 1995. Natural selection against white petals in Phlox. Evolution 49:1017-1022.
80. Mahajan, M., Ahuja, P.S., Yadav, S.K. 2011. Post-transcriptional silencing of flavonol synthase mRNA in tobacco leads to fruits with arrested seed set. PLoS ONE 6:e28315.
81. Majetic, C.J., Raguso, R.A., Tonsor, S.J., Ashman, T-L. 2007. Flower color-flower scent associations in polymorphic Hesperis matronalis (Brassicaceae). Phytochemistry 68:865-874.
82. Mayer, M.S., Soltis, P.S., Soltis, D.E. 1994. The evolution of the Streptanthus glandulosus complex (Cruciferae): genetic divergence and gene flow in serpentine endemics. American Journal of Botany 81:1288-1299.
83. McCall, A.C., Barr, C.M. 2012. Why do florivores prefer hermaphrodites over females in Nemophila menziesii (Boraginaceae)?. Oecologia 170:147-157.
84. McCall, A.C., Murphy, S.J., Venner, C., Brown, M. 2013. Florivores prefer white versus pink petal color morphs in wild radish, Raphanus sativus. Oecologia 172:189-195.
85. Mendel, G. 1866. Versuche über Plflanzenhybriden. Lectura del 8 de febrero y 8 de marzo en la Sociedad de Historia Natural de Brünn. Traduccion al inglés en http://www.mendelweb.org/MWarchive.html.
86. Méndez, M., Jones, D.G., Manetas, Y. 1999. Enhanced UV-B radiation under field conditions increases anthocyanin and reduces the risk of photoinhibition but does not affect growth in the carnivorous plant Pinguicula vulgaris. New Phytologist 144:275-282.
87. Merzlyak, M.N., Chivkunova, O.B. 2000. Light-stress-induced pigment change and evidence for anthocyanin photoprotection in apples. Journal of Photochemistry and Photobiology B: Biology 55:155-163.
88. Miller, R., Owens, S. J., Rørslett, B. 2011. Plants and colour: Flowers and pollination. Optics and Laser Technology 43:282-294.
89. Misyura, M., Colasanti, J., Rothstein, S.J. 2013. Physiological and genetic analysis of Arabidopsis thaliana anthocyanin biosynthesis mutants under chronic adverse environmental conditions. Journal of Experimental Botany 64:229-240.
90. Mølgaard, P. 1989. Temperature relations of yellow and white flowered Papaver radicatum in North Greenland. Arctic and Alpine Research 21: 83-90.
91. Oigiangbe, N.O., Onigbinde, A.O. 1996. The association between some physico-chemical characteristics and susceptibility of cowpea (Vigna unguiculata (L.) Walp) to Callosobruchus maculatus (F.). Journal of Stored Products Research 32:7-11.
92. Ojeda, D.I., Santos-Guerra, A., Oliva-Tejera, F., Valido, A., Xue, X., Marrero, A., Caujapé-Castells, J., Cronk, Q. 2013. Bird-pollinated Macaronesian Lotus (Leguminosae) evolved within a group of entomophilous ancestors with post-anthesis flower color change. Perspectives in Plant Ecology, Evolution and Systematics 15:193-204.
93. Ollerton, J., Grace, J., Smith, K. 2007. Adaptive floral colour change in Erysimum scoparium (Brassicaceae) and pollinator behaviour of Anthophora alluadii on Tenerife (Hymenoptera: Apidae). Entomologia Generalis 29:252-268.
94. Ono, E., Fukuchi-Mizutani, M., Nakamura, N., Fukul, Y., Yonekura-Sakakibara, K., Yamaguchi, M., Nakayama, T., Tanaka, T., Kusumi, T., Tanaka, Y. 2006. Yellow flowers generated by expression of the aurone biosynthetic pathway. Proceedings of National Academy of Sciences USA 103:11075-11080.
95. Ortiz-Barrientos, D. 2013. The color genes of speciation in plants. Genetics 194:39-42.
96. Pacini, E., Hesse, M. 2005. Pollenkitt - Its composition, forms and functions. Flora 200:399-415.
97. Petroni, K., Tonelli, C. 2011. Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Science 181:219-229.
98. Pollak, P.E., Vogt, T., Mo, Y., Taylor, L.P. 1993. Chalcone synthase and flavonol accumulation in stigmas and anthers of Petunia hybrida. Plant Physiology 102:925-932.
99. Pollastri, S., Tattini, M. 2011. Flavonols: old compounds for old roles. Annals of Botany 108:1225-1233.
100. Quattrocchio, F., Wing, J.F., Leppen, H.T., Mol, J.N., Koes, R.E. 1993. Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. The Plant Cell 5:1497-1512.
101. Queenborough, S.A., Metz, M.R., Valencia, R., Wright, S.J. 2013. Demographic consequences of chromatic leaf defence in tropical tree communities: do red young leaves increase growth and survival? Annals of Botany 112:677-684.
102. Quintana, A., Albrechtová, J., Griesbach, R.J., Freyre, R. 2007. Anatomical and biochemical studies of anthocyanidins in flowers of Anagallis monelli L. (Primulaceae) hybrids. Scientia Horticulturae 112:413-421.
103. Ramsay, N.A., Glover, B.J. 2005. MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends in Plant Science 10:63-70.
104. Rausher, M.D. 2008. Evolutionary transitions in floral color. International Journal of Plant Sciences 169:7-21.
105. Reid, J.B., Ross, J.J. 2011. Mendel's genes: Toward a full molecular characterization. Genetics 189:3-10.
106. Renoult, J.P., Valido, A., Jordano, P., Schaefer, H.M. 2014. Adaptation of flower and fruit colours to multiple, distinct mutualists. New Phytologist 201:678-686.
107. Rodríguez Navarro, M.L., Barone Tosco, R., Hernández Romero, F., Fariña B., Rodríguez López, M. 2010. Algunas plantas de Tenerife con flores albinas o parcialmente albinas. Quercus 288:42-43.
108. Sasaki, K., Takahashi, T. 2002. A flavonoid from Brassica rapa flower as the UV-absorbing nectar guide. Phytochemistry 61:339-343.
109. Schaefer, H.M., Ruxton, G.D. 2011. Plant-animal communication. Oxford University Press, New York, EEUU.
110. Schemske, D.W., Bierzychudek, P. 2001. Evolution of flower color in the desert annual Linanthus parryae: Wright revisited. Evolution 55:1269-1282.
111. Schemske, D.W., Bierzychudek, P. 2007. Spatial differentiation for flower color in the desert annual Linanthus parryae: was Wright right? Evolution 61:2528-2543.
112. Schenke, D., Boettcher, C., Scheel, D. 2011. Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production. Plant, Cell and Environment 34:1849-1864.
113. Schiestl, F.P., Johnson, S.D. 2013. Pollinator-mediated evolution of floral signals. Trends in Ecology and Evolution 28:307-315.
114. Schmitzer, V., Veberic, R., Osterc, G., Stampar, F. 2009. Changes in the phenolic concentration during flower development of rose 'KORcrisett'. Journal of the American Society for Horticultural Science 134:491-496.
115. Schwinn, K., Venail, J., Shang, Y., Mackay, S., Alm, V., Butelli, E., Oyama, R., Bailey, P., Davies, K., Martin, C. 2006. A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. The Plant Cell 18:831-851.
116. Shang, Y., Venail, J., Mackay, S., Bailey, P.C., Schwinn, K.E., Jameson, P.E., Martin, C.R., Davies, K.M. 2011. The molecular basis for venation patterning of pigmentation and its effect on pollinator attraction in flowers of Antirrhinum. New Phytologist 189:602-615.
117. Shimada, S., Otsuki, H., Sakuta, M. 2007. Transcriptional control of anthocyanin biosynthetic genes in the Caryophyllales. Journal of Experimental Botany 58:957-967.
118. Shipunov, A., Kosenko, Y., Volkova, P. 2011. Floral polymorphism in common primrose (Primula vulgaris Huds., Primulaceae) of the Northeastern Black Sea coast. Plant Systematics and Evolution 296:167-178.
119. Skipp, R.A., Bailey, J.A. 1977. The fungitoxicity of isoflavonoid phytoalexins measured using different types of bioassay. Physiological Plant Pathology 11:101-112.
120. Smith, S.D., Rausher, M.D. 2011. Gene loss and parallel evolution contribute to species difference in flower color. Molecular Biology and Evolution 28:2799-2810.
121. Sobel, J.M., Streisfeld, M.A. 2013. Flower color as a model system for studies of plant evo-devo. Frontiers in Plant Science 4:e321.
122. Sprengel, C.K. 1793. Das entdeckte Geheimniss der Natur im Bau und in der Befruchtung der Blumen. Traducción al ingles por Haase, P. 1996. En: Harder, L.D., Barrett S.C.H. (eds.), Ecology and evolution of flowers, pp. 3-43. Oxford University Press, Oxford, UK.
123. Stanton, M.L. 1987. Reproductive biology of petal color variants in wild populations of Raphanus sativus: I. Pollinator response to color morphs. American Journal of Botany 74:178-187.
124. Stanton, M.L., Snow, A.A., Handel, S.N., Bereczky, J. 1989. The impact of a flower-color polymorphism on mating patterns in experimental populations of wild radish (Raphanus raphanistrum L.). Evolution 43:335-346.
125. Stapleton, A.E., Walbot, V. 1994. Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiology 105:881-889.
126. Steyn, W.J. 2009. Prevalence and functions of anthocyanins in fruits. En: Gould, K., Davies, K., Winefield, C. (eds.), Anthocyanins: Biosynthesis, Functions and Applications, pp. 86-105. Springer Science and Business, New York, EEUU.
127. Steyn, W.J., Wand, S.J.E., Holcroft, D.M., Jacobs, G. 2002. Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytologist 155:349-361.
128. Strauss, S., Whittall, J.B. 2006. Non-pollinator agents of selection on floral traits. En: Harder, L.D., Barrett S.C.H. (eds.), Ecology and evolution of flowers, pp. 120-138. Oxford University Press, Oxford, UK.
129. Streisfeld, M.A., Kohn, J.R. 2005. Contrasting patterns of floral and molecular variation across a cline in Mimulus aurantiacus. Evolution 59:2548-2559.
130. Streisfeld, M.A., Kohn, J.R. 2007. Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. Journal of Evolutionary Biology 20: 122-132.
131. Streisfeld, M.A., Rausher, M.D. 2009. Altered trans-regulatory control of gene expression in multiple anthocyanin genes contributes to adaptive flower color evolution in Mimulus aurantiacus. Molecular Biology and Evolution 26:433-444.
132. Streisfeld, M.A., Rausher, M.D. 2011. Population genetics, pleiotropy and the preferential fixation of mutations during adaptive evolution. Evolution 65:629-642.
133. Streisfeld, M.A., Young, W.N., Sobel, J.M. 2013. Divergent selection drives genetic differentiation in an R2R3-MYB transcription factor that contributes to incipient speciation in Mimulus aurantiacus. PLoS Genetics 9:e1003385.
134. Takahashi, A., Takeda, K., Ohnishi, T. 1991. Light-induced anthocyanin reduces the extent of damage to DNA in UV-irradiated Centaurea cyanus cells in culture. Plant Cell Physiology 32:541-547.
135. Tanaka, Y., Sasaki, N., Ohmiya, A. 2008. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. The Plant Journal 54:733-749.
136. Vignolini, S., Davey, M.P., Bateman, R.M., Rudall, P.J., Moyroud, E., Tratt, J., Malmgren, S., Steiner U., Glover, B.J. 2012. The mirror crack'd: both pigment and structure contribute to the glossy blue appearance of the mirror orchid, Ophrys speculum. New Phytologist 196:1038-1047.
137. von Wettberg, E.J., Stanton, M.L., Whittall, J.B. 2010. How anthocyanin mutants respond to stress: the need to distinguish between stress tolerance and maximal vigour. Evolutionary Ecology Research 12:457-476.
138. Wang, H., Conchou, L., Bessière, J.M., Cazals, G., Schatz, B., Imbert, E. 2013. Flower color polymorphism in Iris lutescens (Iridaceae): Biochemical analyses in light of plant-insect interactions. Phytochemistry 94:123-134.
139. Warren, J., Mackenzie, S. 2001. Why are all colour combinations not equally represented as flower-colour polymorphisms? New Phytologist 151: 237-241.
140. Waser, N.M., Price, M.V. 1981. Pollinator choice and stabilizing selection for flower color in Delphinium nelsonii. Evolution 35:376-390.
141. Wasson, A.P., Pellerone, F.I., Mathesius, U. 2006. Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by Rhizobia. The Plant Cell 18:1617-1629.
142. Weiss, M.R. 1995. Floral color change: a widespread functional convergence. American Journal of Botany 82:167-185.
143. Wessinger, C.A., Rausher, M.D. 2012. Lessons from flower colour evolution on targets of selection. Journal of Experimental Botany 63:5741-5749.
144. Wheldale, M. 1916. The anthocyanin pigments of plants. Cambridge University Press, Cambridge, UK.
145. Whibley, A., Langlade, N.B., Andalo, C., Hanna, A.I., Bangham, A., Thébaud, C., Coen, E. 2006. Evolutionary paths underlying flower color variation in Antirrhinum. Science 313:963-966.
146. Whitney, H.M., Bennett, K.V., Dorling, M., Sandbach, L., Prince, D., Chittka, L., Glover, B.J. 2011. Why do so many petals have conical epidermal cells?. Annals of Botany 108:609-616.
147. Whittall, J.B., Carlson, M. 2009. Plant defense: A pre-adaptation for pollinator shifts. New Phytologist 182:5-8.
148. Whittall, J.B., Voelckel, C., Kliebenstein, D.J., Hodges, S.A. 2006. Convergence, constraint and the role of gene expression during adaptive radiation: floral anthocyanins in Aquilegia. Molecular Ecology 15:4645-4657.
149. Winkel-Shirley, B. 2002. Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5:218-223.
150. Wright, S. 1943. An analysis of local variability of flower color in Linanthus parryae. Genetics 28:139-156.
151. Wright, S. 1978. Evolution and the genetics of populations. Volumen 4. Variability between and among natural populations. University of Chicago Press, Chicago, EEUU.
152. Wu, C.A., Streisfeld, M.A., Nutter, L.I., Cross, K.A. 2013. The genetic basis of a rare flower color polymorphism in Mimulus lewisii provides insight into the repeatability of evolution. PLos ONE 8:e81173.
153. Wu, J., Carver, B.F., Goad, C.L. 1999. Kernel color variability of hard white and hard red winter wheat. Crop Science 39:634-638.
154. Yuan, Y.W., Byers, K.J., Bradshaw, H.D. 2013. The genetic control of flower-pollinator specificity. Current Opinion in Plant Biology 16:422-428.
155. Zhang, J., Subramanian, S., Stacey, G., Yu, O. 2009. Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. The Plant Journal 57:171-183.
156. Zhang, Y.J., Yang, Q.Y., Lee, D.W., Goldstein, G., Cao, K.F. 2013. Extended leaf senescence promotes carbon gain and nutrient resorption: importance of maintaining winter photosynthesis in subtropical forests. Oecologia 173:721-730.
157. Zhu, M., Zheng, X., Shu, Q., Li, H., Zhong, P., Zhang, H., Xu, Y., Wang, L., Wang, L. 2012. Relationship between the composition of flavonoids and flower colors variation in tropical water lily (Nymphaea) cultivars. PloS ONE 7:e34335.