Major quantitative trait loci control divergence in critical photoperiod for flowering between selfing and outcrossing species of monkeyflower (Mimulus)

New Phytologist

Volumn 201, Issue 4, 2014, Pages 1498-1507

  Fishman, Lila ^a   Sweigart, Andrea L ^b   Kenney, Amanda M ^b   Campbell, Samantha ^a  

^a UNIVERSITY OF MONTANA   (United States)

^b University of Georgia   (United States)

Author keywords

Adaptation; Flowering time; Mating system; Phenology; Photoperiod; Quantitative trait locus (QTL) mapping; Speciation

Indexed keywords

ADAPTATION; ARTICLE; CHROMOSOME MAP; CHROMOSOME SEGREGATION; CROSS BREEDING; FLOWER; FLOWERING TIME; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENETICS; HYBRIDIZATION; MATING SYSTEM; PHENOLOGY; PHENOTYPE; PHOTOPERIODICITY; PHYSIOLOGY; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS (QTL) MAPPING; SPECIES DIFFERENTIATION; SYMPATRY;

ADAPTATION; FLOWERING TIME; MATING SYSTEM; PHENOLOGY; PHOTOPERIOD; QUANTITATIVE TRAIT LOCUS (QTL) MAPPING; SPECIATION;

CHROMOSOME SEGREGATION; CROSSES, GENETIC; FLOWERS; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; HYBRIDIZATION, GENETIC; PHENOTYPE; PHOTOPERIOD; PHYSICAL CHROMOSOME MAPPING; QUANTITATIVE TRAIT LOCI; SYMPATRY;

EID: 84894093006     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12618     Document Type: Article

References (57)

1. Alonso-Blanco C, Aarts MGM, Bentsink L, Keurentjes JJB, Reymond M, Vreugdenhil D, Koornneef M. 2009. What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21: 1877-1896.
2. Amasino R. 2010. Seasonal and developmental timing of flowering. Plant Journal 61: 1001-1013.
3. Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T. 2012a. Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proceedings of the Royal Society B: Biological Sciences 279: 3843-3852.
4. Anderson JT, Lee C-R, Rushworth CA, Colautti RI, Mitchell-Olds T. 2012b. Genetic trade-offs and conditional neutrality contribute to local adaptation. Molecular Ecology 22: 699-708.
5. Andrés F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13: 627-639.
6. Ballerini ES, Kramer EM. 2011. In the light of evolution: a reevaluation of conservation in the CO-FT regulon and its role in photoperiodic regulation of flowering time. Frontiers in Plant Science 2: 81.
7. Barr CM, Fishman L. 2010. The nuclear component of a cytonuclear hybrid incompatibility in Mimulus maps to a cluster of pentatricopeptide repeat genes. Genetics 184: 455-465.
8. Basten C, Weir BS, Zeng Z-B. 2002. QTL Cartographer: a reference manual and tutorial for QTL mapping. Raleigh, NC, USA: Statistical Genetics, North Carolina State University.
9. Blackman BK, Rasmussen DA, Strasburg JL, Raduski AR, Burke JM, Knapp SJ, Michaels SD, Rieseberg LH. 2011. Contributions of flowering time genes to sunflower domestication and improvement. Genetics 187: 271-287.
10. Blackman BK, Strasburg JL, Raduski AR, Michaels SD, Rieseberg LH. 2010. The role of recently derived FT paralogs in sunflower domestication. Current Biology 20: 629-635.
11. Bodbyl Roels SA, Kelly JK. 2011. Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65: 2541-2552.
12. Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC et al. 2009. The genetic architecture of maize flowering time. Science 325: 714-718.
13. Case AL, Willis JH. 2008. Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangement. Evolution 62: 1026-1039.
14. Chiang GCK, Barua D, Dittmar E, Kramer EM, de Casas RR, Donohue K. 2012. Pleiotropy in the wild: the dormancy gene DOG1 exerts cascading control on life cycles. Evolution 67: 883-893.
15. Chiang GCK, Barua D, Kramer EM, Amasino RM, Donohue K. 2009. Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 106: 11661-11666.
16. El-Assal S, Alonso-Blanco C, Peeters A. 2001. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nature Genetics 29: 435-440.
17. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G. 2007. Time after time: flowering phenology and biotic interactions. Trends in Ecology & Evolution 22: 432-439.
18. Fishman L, Aagaard J, Tuthill JC. 2008. Toward the evolutionary genomics of gametophytic divergence: patterns of transmission ratio distortion in monkeyflower (Mimulus) hybrids reveal a complex genetic basis for conspecific pollen precedence. Evolution 62: 2958-2970.
19. Fishman L, Kelly AJ, Morgan E, Willis JH. 2001. A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159: 1701-1716.
20. Fishman L, Kelly AJ, Willis JH. 2002. Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution 56: 2138-2155.
21. Fishman L, Willis JH. 2005. A novel meiotic drive locus almost completely distorts segregation in Mimulus (monkeyflower) hybrids. Genetics 169: 347-353.
22. Fishman L, Willis JH, Wu CA, Lee Y-W. 2013. Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae). Heredity, in press.
23. Friedman J, Willis JH. 2013. Major QTLs for critical photoperiod and vernalization underlie extensive variation in flowering in the Mimulus guttatus species complex. New Phytologist 199: 571-583.
24. Gavrilets S, Vose A. 2007. Case studies and mathematical models of ecological speciation. 2. Palms on an oceanic island. Molecular Ecology 16: 2910-2921.
25. Grillo MA, Li C, Hammond M, Wang L, Schemske DW. 2013. Genetic architecture of flowering time differentiation between locally adapted populations of Arabidopsis thaliana. New Phytologist 197: 1321-1331.
26. Hall M, Lowry D, Willis J. 2010. Is local adaptation in Mimulus guttatus caused by trade-offs at individual loci? Molecular Ecology 19: 2739-2753.
27. Hall MC, Basten CJ, Willis JH. 2006. Pleiotropic quantitative trait loci contribute to population divergence in traits associated with life-history variation in Mimulus guttatus. Genetics 172: 1829-1844.
28. Hall MC, Willis JH. 2006. Divergent selection on flowering time contributes to local adaptation in Mimulus guttatus populations. Evolution 60: 2466-2477.
29. Hayama R, Coupland G. 2004. The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiology 135: 677-684.
30. Ivey CT, Carr DE. 2012. Tests for the joint evolution of mating system and drought escape in Mimulus. Annals of Botany 109: 583-598.
31. Kiang YT, Hamrick JL. 1978. Reproductive isolation in the Mimulus guttatus-M. nasutus complex. American Midland Naturalist 100: 269-276.
32. Koskela EA, Mouhu K, Albani MC, Kurokura T, Rantanen M, Sargent DJ, Battey NH, Coupland G, Elomaa P, Hytonen T. 2012. Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiology 159: 1043-1054.
33. Leinonen PH, Remington DL, Leppälä J, Savolainen O. 2012. Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata. Molecular Ecology 22: 709-723.
34. Lekberg Y, Roskilly B, Hendrick MF, Zabinski CA, Barr CM, Fishman L. 2012. Phenotypic and genetic differentiation among yellow monkeyflower populations from thermal and non-thermal soils in Yellowstone National Park. Oecologia 170: 111-122.
35. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
36. Li J, Wang S, Zeng Z-B. 2006. Multiple-interval mapping for ordinal traits. Genetics 173: 1649-1663.
37. Lowry DB, Willis JH. 2010. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biology 8: e1000500.
38. Martin NH, Willis JH. 2007. Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61: 68-82.
39. Méndez-Vigo B, Martínez-Zapater JM, Alonso-Blanco C. 2013. The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the ggenetic background. PLoS Genetics 9: e1003289.
40. Méndez-Vigo B, Picó FX, Ramiro M, Martínez-Zapater JM, Alonso-Blanco C. 2011. Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis. Plant Physiology 157: 1942-1955.
41. Modliszewski JL, Willis JH. 2012. Allotetraploid Mimulus sookensis are highly interfertile despite independent origins. Molecular Ecology 21: 5280-5298.
42. Nakazato T, Rieseberg LH, Wood TE. 2013. The genetic basis of speciation in the Giliopsis lineage of Ipomopsis (Polemoniaceae). Heredity 111: 227-237.
43. Nitcher R, Distelfeld A, Tan C, Yan L, Dubcovsky J. 2013. Increased copy number at the HvFT1 locus is associated with accelerated flowering time in barley. Molecular Genetics and Genomics 288: 261-275.
44. Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJL, Nilsson O. 2010. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330: 1397-1400.
45. Pin PA, Nilsson O. 2012. The multifaceted roles of FLOWERING LOCUS T in plant development. Plant, Cell & Environment 35: 1742-1755.
46. Rieseberg LH, Blackman BK. 2010. Speciation genes in plants. Annals of Botany 106: 439-455.
47. Rieseberg LH, Willis JH. 2007. Plant speciation. Science 317: 910-914.
48. Salome PA, Bomblies K, Laitinen RAE, Yant L, Mott R, Weigel D. 2011. Genetic architecture of flowering-time variation in Arabidopsis thaliana. Genetics 188: 421-433.
49. Sobel JM, Chen GF, Watt LR, Schemske DW. 2010. The biology of speciation. Evolution 64: 295-315.
50. Sweigart AL, Fishman L, Willis JH. 2006. A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics 172: 2465-2479.
51. Sweigart AL, Willis JH. 2003. Patterns of nucleotide diversity are affected by mating system and asymmetric introgression in two species of Mimulus. Evolution 57: 2490-2506.
52. Weller JL, Liew LC, Hecht VFG, Rajandran V, Laurie RE, Ridge S, Wenden B, Vander Schoor JK, Jaminon O, Blassiau C et al. 2012. A conserved molecular basis for photoperiod adaptation in two temperate legumes. Proceedings of the National Academy of Sciences, USA 109: 21158-21163.
53. Wilczek AM, Burghardt LT, Cobb AR, Cooper MD, Welch SM, Schmitt J. 2010. Genetic and physiological bases for phenological responses to current and predicted climates. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 3129-3147.
54. Wilson RN, Heckman JW, Somerville CR. 1992. Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiology 100: 403-408.
55. Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW, Willis JH. 2008. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100: 220-230.
56. Wu CA, Lowry DB, Nutter LI, Willis JH. 2010. Natural variation for drought-response traits in the Mimulus guttatus species complex. Oecologia 162: 23-33.
57. Yano M, Katayose Y, Ashikari M. 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12: 2473-2483.