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Cited by 91Plant Gene Expression AnalysisGenetic Mapping and Diversity in Plants and AnimalsEvolution and Genetic Dynamics

Divergent selection drives genetic differentiation in an R2R3-MYB transcription factor that contributes to incipient speciation in Mimulus aurantiacus

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Streisfeld, Matthew A., Young, Wambui N., Sobel, James M.·2013·PLoS Genetics
DOI 10.1371/journal.pgen.1003385PMC PMC3605050
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Abstract

Identifying the molecular genetic basis of traits contributing to speciation is of crucial importance for understanding the ecological and evolutionary mechanisms that generate biodiversity. Despite several examples describing putative "speciation genes," it is often uncertain to what extent these genetic changes have contributed to gene flow reductions in nature. Therefore, considerable interest lies in characterizing the molecular basis of traits that actively confer reproductive isolation during the early stages of speciation, as these loci can be attributed directly to the process of divergence. In Southern California, two ecotypes of Mimulus aurantiacus are parapatric and differ primarily in flower color, with an anthocyanic, red-flowered morph in the west and an anthocyanin-lacking, yellow-flowered morph in the east. Evidence suggests that the genetic changes responsible for this shift in flower color have been essential for divergence and have become fixed in natural populations of each ecotype due to almost complete differences in pollinator preference. In this study, we demonstrate that a cis-regulatory mutation in an R2R3-MYB transcription factor results in differential regulation of enzymes in the anthocyanin biosynthetic pathway and is the major contributor to differences in floral pigmentation. In addition, molecular population genetic data show that, despite gene flow at neutral loci, divergent selection has driven the fixation of alternate alleles at this gene between ecotypes. Therefore, by identifying the genetic basis underlying ecologically based divergent selection in flower color between these ecotypes, we have revealed the ecological and functional mechanisms involved in the evolution of pre-mating isolation at the early stages of incipient speciation.

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  • In Mimulus, MaMyb2, an R2R3-MYB transcription factor identified as a candidate gene for differences in floral pigmentation, has been shown to locate in a sharp peak of genomic differentiation.

    “In Mimulus, an R2R3-MYB transcription factor, MaMyb2, which was identified as a candidate gene for differences in floral pigmentation (Streisfeld et al., 2013), has been shown to locate in a sharp peak of genomic differentiation (Stankowski et al., 2019).”

    From Genomics of plant speciation (2023) · cites this paper as Streisfeld et al., 2013

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  1. [1]Coyne JA, Orr HA (1998) The evolutionary genetics of speciation. Phil Trans Royal Soc London B 353: 287– 305. PMC1692208 9533126
  2. [3]Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16: 372– 380. 11403870
  3. [4]Orr HA (2005) The genetic basis of reproductive isolation: Insights from Drosophila. Proc Natl Acad Sci USA 102: 6522– 6526. 15851676 PMC1131866
  4. [5]Sobel JM, Chen GF, Watt LR, Schemske DW (2010) The biology of speciation. Evolution 64: 295– 315. 19891628
  5. [7]Rundle HD, Nosil P (2005) Ecological speciation. Ecology Letters 8: 336– 352.
  6. [8]Schluter D (2009) Evidence for ecological speciation and its alternative. Science 323: 737– 741. 19197053
  7. [9]Noor MAF (2003) Evolutionary biology - Genes to make new species. Nature 423: 699– 700. 12802320
  8. [10]Wu CI, Ting CT (2004) Genes and speciation. Nat Rev Genet 5: 114– 122. 14735122
  9. [11]Barbash DA, Siino DF, Tarone AM, Roote J (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA 100: 5302– 5307. 12695567 PMC154340
  10. [12]Nosil P, Schluter D (2011) The genes underlying the process of speciation. Trends Ecol Evol 26: 160– 167. 21310503
  11. [13]Via S (2009) Natural selection in action during speciation. Proc Natl Acad Sci USA 106: 9939– 9946. 19528641 PMC2702801
  12. [15]Noor MAF, Feder JL (2006) Speciation genetics: evolving approaches. Nat Rev Genet 7: 851– 861. 17033626
  13. [16]Rice WR, Hostert EE (1993) Laboratory experiments on speciation: What have we learned in 40 years? Evolution 47: 1637– 1653. 28568007
  14. [17]Hewitt GM (1988) Hybrid zones - natural laboratories for evolutionary studies. Trends Ecol Evol 3: 158– 167. 21227192
  15. [18]Harrison RG (1990) Hybrid zones: windows on evolutionary process. Oxford Surveys in Evolutionary Biology 7: 69– 128.
  16. [20]Endler JA (1977) Geographic Variation, Speciation, and Clines. Princeton: Princeton University Press. 409931
  17. [22]Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil Trans Royal Soc B 363: 3009– 3021. PMC2607309 18579478
  18. [23]Grant V (1949) Pollination systems as isolating mechanisms in Angiosperms. Evolution 3: 82– 97. 18115119
  19. [24]Grant V (1981) Plant Speciation. New York: Columbia University Press.
  20. [25]Grant V (1993) Origin of floral isolation between ornithophilous and sphingophilous plant-species. Proc Natl Acad Sci USA 90: 7729– 7733. 11607421 PMC47216
  21. [26]Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426: 176– 178. 14614505
  22. [27]Hopkins R, Rausher MD (2012) Pollinator-mediated selection on flower color allele drives reinforcement. Science 335: 1090– 1092. 22300852
  23. [28]Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, 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. 10449578 PMC144295
  24. [29]Hoballah ME, Gubitz T, Stuurman J, Broger L, Barone M, et al (2007) Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19: 779– 790. 17337627 PMC1867374
  25. [30]Whibley AC, Langlade NB, Andalo C, Hanna AI, Bangham A, et al (2006) Evolutionary paths underlying flower color variation in Antirrhinum. Science 313: 963– 966. 16917061
  26. [31]Cooley AM, Modliszewski JL, Rommel ML, Willis JH (2011) Gene duplication in Mimulus underlies parallel floral evolution via independent trans-regulatory changes. Current Biology 21: 700– 704. 21474312
  27. [32]Streisfeld M, Kohn J (2007) Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J Evol Biol 20: 122– 132. 17210005
  28. [33]Streisfeld M, Kohn J (2005) Contrasting patterns of floral and molecular variation across a cline in Mimulus aurantiacus. Evolution 59: 2548– 2559. 16526503
  29. [35]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. Mol Biol Evol 26: 433– 444. 19029190
  30. [36]Rausher MD (2006) The evolution of flavonoids and their genes. In: Grotewold E, editor. The Science of Flavonoids. New York: Springer. pp. 175–212.
  31. [37]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.
  32. [38]Streisfeld MA, Rausher MD (2011) Population genetics, pleiotropy, and the preferential fixation of mutations during adaptive evolution. Evolution 65: 629– 642. 21054357
  33. [39]Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Op Plant Biol 4: 447– 456. 11597504
  34. [40]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. 16531495 PMC1425845
  35. [41]Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, et al (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15: 573– 581. 20674465
  36. [42]Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14: 671– 688. 15723660
  37. [43]Liu YL, Schiff M, Marathe R, Dinesh-Kumar SP (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J 30: 415– 429. 12028572
  38. [44]Wittkopp PJ, Haerum BK, Clark AG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85– 88. 15229602
  39. [45]Munz PA, Keck DD (1973) A California Floral and Supplement. Berkeley, CA: University of California Press.
  40. [46]Beardsley PM, Schoenig SE, Whittall JB, Olmstead RG (2004) Patterns of evolution in Western North American Mimulus (Phrymaceae). Am J Bot 91: 474– 489. 21653403
  41. [47]Szymura JM, Barton NH (1986) Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and Bombina variegata, near Cracow in Southern Poland. Evolution 40: 1141– 1159. 28563502
  42. [48]Porter AH, Wenger R, Geiger H, Scholl A, Shapiro AM (1997) The Pontia daplidice-edusa hybrid zone in northwestern Italy. Evolution 51: 1561– 1573. 28568618
  43. [49]Payseur BA (2010) Using differential introgression in hybrid zones to identify genomic regions involved in speciation. Mol Ecol Res 10: 806– 820. 21565092
  44. [50]Barton NH, Hewitt GM (1989) Adaptation, speciation and hybrid zones. Nature 341: 497– 503. 2677747
  45. [51]Barton NH, Gale KS (1993) Genetic analysis of hybrid zones. In: Harrison RG, editor. Hybrid Zones and the Evolutionary Process. New York: Oxford University Press. pp. 13–45.
  46. [52]Nosil P, Egan SR, Funk DJ (2008) Heterogeneous genomic differentiation between walking-stick ecotypes: “Isolation by adaptation” and multiple roles for divergent selection. Evolution 62: 316– 336. 17999721
  47. [53]Payseur BA, Krenz JG, Nachman MW (2004) Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58: 2064– 2078. 15521462
  48. [54]Lowry DB, Hall MC, Salt DE, Willis JH (2009) Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytologist 183: 776– 788. 19549130

Cited by

Sorted by citations

  • Genomics of plant speciation

    Bock, D. G., Cai, Z., Elphinstone, C., González-Segovia, E., Hirabayashi, K., Huang, K., Keais, G. L., Kim, A., Owens, G. L., & Rieseberg, L. H. (2023) · Plant Communications · doi:10.1016/j.xplc.2023.100599 · Cited by 84 · see citing works

    “In Mimulus, an R2R3-MYB transcription factor, MaMyb2, which was identified as a candidate gene for differences in floral pigmentation (Streisfeld et al., 2013), has been shown to locate in a sharp peak of genomic differentiation (Stankowski et al.”

Authors
Streisfeld, M. A., Young, W. N., & Sobel, J. M.
Affiliations
University of Oregon (US)
Corresponding author
Streisfeld, Matthew A.
ORCID
Venue
PLoS Genetics
Publisher
Public Library of Science (PLoS)
Published
2013-03-21
Volume
9
Issue
3
Pages
e1003385
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1003385
PMC
PMC3605050
OpenAlex
W2055407907
Cited by
91
References
2
Citations by year
2026: 2 · 2025: 5 · 2024: 6 · 2023: 6 · 2022: 6 · 2021: 8 · 2020: 4 · 2019: 2 · 2018: 6 · 2017: 6 · 2016: 10 · 2015: 11 · 2014: 16 · 2013: 3
FWCI
5.98
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
University of Oregon
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Gene Expression Analysis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
divergent selection, R2R3-MYB transcription factor, incipient speciation, premating isolation, flower pigmentation, flower color, anthocyanin biosynthesis, cis-regulatory mutations, gene flow, genetic differentiation, pollinator preference, speciation genes
MeSH terms
California, Biological Evolution, Genetics, Population, Mutation, Pigmentation, Plant Proteins, Transcription Factors, Ecosystem, Arabidopsis Proteins, Mimulus, Flowers, Biodiversity, Genetic Speciation

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