The genetic basis of a rare flower color polymorphism in Mimulus lewisii provides insight into the repeatability of evolution

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Wu, Carrie A ^a   Streisfeld, Matthew A ^b   Nutter, Laura I ^a,c   Cross, Kaitlyn A ^a  

^a UNIVERSITY OF RICHMOND   (United States)

^b UNIVERSITY OF OREGON   (United States)

^c TC Williams High School   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHOCYANIN;

ARTICLE; CONTROLLED STUDY; FLOWER COLOR; FRAMESHIFT MUTATION; GENE EXPRESSION; GENE FREQUENCY; GENE SEGREGATION; GENETIC POLYMORPHISM; LOSS OF FUNCTION MUTATION; MIDFR GENE; MIMULUS; MIMULUS LEWISII; NONHUMAN; PLANT GENE; PLANT GENETICS; POPULATION GENETICS;

FLOWERS; MIMULUS; MUTATION; PIGMENTATION; POLYMORPHISM, GENETIC;

EID: 84891817078     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081173     Document Type: Article

References (47)

1. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313: 101-104.
2. Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326: 1663-1667.
3. Wittkopp PJ, Stewart EE, Arnold LL, Neidert AH, Haerum BK, et al. (2009) Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326: 540-544.
4. Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD, et al. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327: 302-305.
5. Stern DL (2000) Perspective: Evolutionary developmental biology and the problem of variation. Evolution 54: 1079-1091.
6. Carroll SB (2005) Evolution at two levels: on genes and form. Plos Biology 3: e245.
7. Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution 61: 995-1016.
8. Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nature Reviews Genetics 8: 206-216.
9. Stern DL, Orgogozo V (2008) The loci of evolution: How predictable is genetic evolution? Evolution 62: 2155-2177.
10. Streisfeld MA, Rausher MD (2011) Population genetics, pleiotropy, and the preferential fixation of mutations during adaptive evolution. Evolution 65: 629- 642.
11. Conte GL, Arnegard ME, Peichel CL, Schluter D (2012) The probability of genetic parallelism and convergence in natural populations. Proceedings of the Royal Society B-Biological Sciences 279: 5039-5047.
12. Stern DL, Orgogozo V (2009) Is genetic evolution predictable? Science 323: 746-751.
13. Otto SP (2004) Two steps forward, one step back: the pleiotropic effects of favoured alleles. Proceedings of the Royal Society B-Biological Sciences 271: 705-714.
14. Orr HA (2000) Adaptation and the cost of complexity. Evolution 54: 13-20.
15. Gompel N, Prud'homme B (2009) The causes of repeated genetic evolution. Developmental Biology 332: 36-47.
16. Nosil P, Harmon LJ, Seehausen O (2009) Ecological explanations for (incomplete) speciation. Trends in Ecology & Evolution 24: 145-156.
17. Rausher MD (2008) Evolutionary transitions in floral color. International Journal of Plant Sciences 169: 7-21.
18. Warren J, Mackenzie S (2001) Why are all colour combinations not equally represented as flower-colour polymorphisms? New Phytologist 151: 237-241.
19. Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7: 1071-1083.
20. Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends in Plant Science 10: 236-242.
21. Quattrocchio F, Baudry A, Lepiniec L, Grotewold E (2006) The regulation of flavonoid biosynthesis. In: Grotewold E, editor. The Science of Flavonoids. New York: Springer. pp. 97-122.
22. Hiesey WM, Nobs MA, Bjorkman O (1971) Experimental studies on the nature of species. V. Biosystematics, genetics, and physiological ecology of Erythranthe section of Mimulus. Washington, D. C.: Carnegie Institute.
23. Hickman JC (1993) The Jepson Manual: Higher plants of California. Berkeley, CA: University of California Press.
24. Schemske DW, Bradshaw HD (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus) . Proceedings of the National Academy of Sciences of the United States of America 96: 11910-11915.
25. Beardsley PM, Yen A, Olmstead RG (2003) AFLP phylogeny of Mimulus section Erythranthe and the evolution of hummingbird pollination. Evolution 57: 1397- 1410.
26. Wilbert SM, Schemske DW, Bradshaw HD (1997) Floral anthocyanins from two monkeyflower species with different pollinators. Biochemical Systematics and Ecology 25: 437-443.
27. Harborne JB (1984) Phytochemical Methods. New York: Chapman and Hall.
28. Mol J, Grotewold E, Koes R (1998) How genes paint flowers and seeds. Trends in Plant Science 3: 212-217.
29. Streisfeld M, Rausher M (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.
30. Streisfeld MA, Young WN, Sobel JM (2013) Divergent selection drives genetic differentiation in an R2R3-Myb transcription factor that contributes to incipient speciation in Mimulus aurantiacus. PloS Genetics 9: e1003385.
31. Schwinn K, Venail J, Shang YJ,Mackay S, Alm V, 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.
32. Morita Y, Saitoh M, Hoshino A, Nitasaka E, 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.
33. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetic data analysis. Evolutionary Bioinformatics Online 1: 47-50.
34. Hopkins R, Rausher MD (2011) Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469: 411-415.
35. Habu Y, Hisatomi Y, Lida S (1998) Molecular characterization of the mutable flaked allele for flower variegation in the common morning glory. Plant Journal 16: 371-376.
36. Chang SM, Lu YQ, Rausher MD (2005) Neutral evolution of the nonbinding region of the anthocyanin regulatory gene Ipmyb1 in Ipomoea. Genetics 170: 1967-1978.
37. Dick CA, Buenrostro J, Butler T, Carlson ML, Kliebenstein DJ, et al. (2011) Arctic mustard fower color polymorphism controlled by petal-specific downregulation at the threshold of the anthocyanin biosynthetic pathway. Plos One 6: e18230.
38. Koes RE, Quattrocchio F, Mol JNM (1994) The flavonoid biosynthetic pathway in plants - function and evolution. Bioessays 16: 123-132.
39. Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5: 218-223.
40. Broun P (2005) Transcriptional control of flavonoid biosynthesis: A complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis . Current Opinion in Plant Biology 8: 272-279.
41. Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends in Plant Science 10: 63-70.
42. Coberly LC, Rausher MD (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.
43. Fehr C, Rausher MD (2004) Effects of variation at the flower-colour A locus on mating system parameters in Ipomoea purpurea.Molecular Ecology 13: 1839-1847.
44. Coberly LC, Rausher MD (2008) Pleiotropic effects of an allele producing white flowers in Ipomoea purpurea. Evolution 62: 1076-1085.
45. Dixon RA, Xie DY, Sharma SB (2005) Proanthocyanidins - a final frontier in flavonoid research? New Phytologist 165: 9-28.
46. Martin C, Ellis N, Rook F (2010) Do transcription factors play special roles in adaptive variation? Plant Physiol 154: 506-511.
47. Rausher MD, Fry JD (1993) Effects of a locus affecting floral pigmentation in Ipomoea purpurea on female fitness components. Genetics 134: 1237-1247.