Major QTLs for critical photoperiod and vernalization underlie extensive variation in flowering in the Mimulus guttatus species complex

New Phytologist

Volumn 199, Issue 2, 2013, Pages 571-583

  Friedman, Jannice ^a,b   Willis, John H ^a  

^a DUKE UNIVERSITY   (United States)

^b SYRACUSE UNIVERSITY   (United States)

Author keywords

Climate; Flowering time; Life history; Local adaptation; Mimulus guttatus; Photoperiod; Quantitative trait loci; Vernalization

Indexed keywords

DICOTYLEDON; FLOWERING; LIFE HISTORY TRAIT; LOCAL ADAPTATION; PERENNIAL PLANT; PHOTOPERIOD; SEMELPARITY; SOIL MOISTURE; SPECIES COMPLEX; TEMPERATURE EFFECT; VERNALIZATION;

ARTICLE; COLD; FLOWER; GENETIC MARKER; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; MIMULUS; NORTH AMERICA; PHOTOPERIODICITY; PHYSIOLOGY; QUANTITATIVE TRAIT LOCUS; SPECIES DIFFERENCE; STATISTICAL MODEL;

COLD TEMPERATURE; FLOWERS; GENETIC MARKERS; GENOTYPE; LINEAR MODELS; MIMULUS; NORTH AMERICA; PHOTOPERIOD; QUANTITATIVE TRAIT LOCI; SPECIES SPECIFICITY;

MIMULUS GUTTATUS;

EID: 84879695598     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12260     Document Type: Article

References (65)

1. Albani MC, Coupland G. 2010. Comparative analysis of flowering in annual and perennial plants. Plant Development 91: 323-348.
2. Amasino RM. 2010. Seasonal and developmental timing of flowering. Plant Journal 61: 1001-1013.
3. Anderson JT, Lee C-R, Mitchell-Olds T. 2011. Life-history QTLS and natural selection on flowering time in Boechera stricta, a perennial relative of Arabidopsis. Evolution 65: 771-787.
4. Andrés F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13: 627-639.
5. Beardsley P, Schoenig S, Whittall JB, Olmstead R. 2004. Patterns of evolution in Western North American Mimulus (Phrymaceae). American Journal of Botany 91: 474-489.
6. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O. 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040-1043.
7. Brock MT, Stinchcombe JR, Weinig C. 2009. Indirect effects of FRIGIDA: floral trait (co)variances are altered by seasonally variable abiotic factors associated with flowering time. Journal of Evolutionary Biology 22: 1826-1838.
8. Caicedo AL, Stinchcombe JR, Olsen K, Schmitt J, Purugganan MD. 2004. Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proceedings of the National Academy of Sciences, USA 101: 15 670-15 675.
9. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033.
10. Dennis ES, Peacock WJ. 2009. Vernalization in cereals. Journal of Biology 8: 57.
11. Etterson JR. 2004. Evolutionary potential of Chamaecrista fasciculata in relation to climate change. I. Clinal patterns of selection along an environmental gradient in the great plains. Evolution 58: 1446-1458.
12. Fenster CB, Diggle PK, Barrett SCH, Ritland K. 1995. The genetics of floral development differentiating two species of Mimulus (Scrophulariaceae). Heredity 74: 258-266.
13. 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.
14. Hall MC, Basten C, 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.
15. Hall MC, Willis JH. 2006. Divergent selection on flowering time contributes to local adaptation in Mimulus guttatus populations. Evolution 60: 2466-2477.
16. Hall MC, Lowry DB, Willis JH. 2010. Is local adaptation in Mimulus guttatus caused by trade-offs at individual loci? Molecular Ecology 19: 2739-2753.
17. Hayama R, Coupland G. 2004. The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiology 135: 677-684.
18. Hoffmann M, Tomiuk E, Schmuths H, Koch C, Bachmann K. 2005. Phenological and morphological responses to different temperature treatments differ among a world-wide sample of accessions of Arabidopsis thaliana. Acta Oecologica 28: 181-187.
19. Izawa T. 2007. Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. Journal of Experimental Biology 58: 3091-3097.
20. Jaeger KE, Wigge PA. 2007. FT protein acts as a long-range signal in Arabidopsis. Current Biology 17: 1050-1054.
21. Johanson U, West J, Lister C, Michaels SD, Amasino RM, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347.
22. Kelly AJ, Willis JH. 1998. Polymorphic microsatellite loci in Mimulus guttatus and related species. Molecular Ecology Notes 7: 769-774.
23. Kian YT, Hamrick JL. 1978. Reproductive isolation in Mimulus guttatus-M. nasutus complex. American Midland Naturalist 100: 269-276.
24. Kim D-H, Doyle MR, Sung S, Amasino RM. 2009. Vernalization: winter and the timing of flowering in plants. Annual Review of Cell and Developmental Biology 25: 277-299.
25. Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W. 1998. Genetic control of flowering time in Arabidopsis. Annual Review of Plant Physiology and Plant Molecular Biology 49: 345-370.
26. Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH. 2007. Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes & Development 21: 397-402.
27. Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D. 2005. Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genetics 1: e6.
28. Levy YY, Dean C. 1998. The transition to flowering. Plant Cell 10: 1973-1990.
29. Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C. 2002. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297: 243-246.
30. Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595.
31. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
32. Li Y, Roycewicz P, Smith E, Borevitz JO. 2006. Genetics of local adaptation in the laboratory: flowering time quantitative trait loci under geographic and seasonal conditions in Arabidopsis. PLoS ONE 1: e105.
33. Liljegren SJ, Gustafson-Brown C, Pinyopich A, Ditta GS, Yanofsky MF. 1999. Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11: 1007-1018.
34. Lowry DB, Rockwood RC, Willis JH. 2008. Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution 62: 2196-2214.
35. 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.
36. Magwene PM, Willis JH, Kelly JK. 2011. The statistics of bulk segregant analysis using next generation sequencing. PLoS Computational Biology 7: e1002255.
37. Maloof JN, Borevitz JO, Dabi T, Lutes J, Nehring RB, Redfern JL, Trainer GT, Wilson JM, Asami T, Berry CC et al. 2001. Natural variation in light sensitivity of Arabidopsis. Nature Genetics 29: 441-446.
38. Martin N, 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, 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.
40. Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956.
41. Michaels SD, Amasino RM. 2000. Memories of winter: vernalization and the competence to flower. Plant, Cell and Environment 23: 1145-1153.
42. Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM. 2005. Integration of flowering signals in winter-annual Arabidopsis. Plant Physiology 137: 149-156.
43. Pennell FW. 1947. Some hitherto undescribed Scrophulariaceae of the Pacific states. Proceedings of the Academy of Natural Sciences of Philadelphia 99: 151-171.
44. Rathcke B, Lacey EP. 1985. Phenological patterns of terrestrial plants. Annual Review of Ecology and Systematics 16: 179-214.
45. Sandring S, Ågren JA. 2009. Pollinator-mediated selection on floral display and flowering time in the perennial herb Arabidopsis lyrata. Evolution 63: 1292-1300.
46. Scarcelli N, Cheverud JM, Schaal BA, Kover PX. 2007. Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. Proceedings of the National Academy of Sciences, USA 104: 16 986-16 991.
47. Scarcelli N, Kover PX. 2009. Standing genetic variation in FRIGIDA mediates experimental evolution of flowering time in Arabidopsis. Molecular Ecology 18: 2039-2049.
48. Simpson GG, Dean C. 2002. Arabidopsis, the Rosetta stone of flowering time? Science 296: 285-289.
49. Stearns S. 1976. Life-history tactics: a review of the ideas. Quarterly Review of Biology 51: 3-47.
50. Stinchcombe JR, Weinig C, Ungerer MC, Olsen K, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J. 2004. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proceedings of the National Academy of Sciences, USA 101: 4712-4717.
51. Stokes ME, Davis CS, Koch GG. 2000 Categorical data analysis using the SAS system, 2nd edn. Cary, NC: SAS Institute Inc.
52. Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. 2001. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116-1120.
53. Tooke F, Ordidge M, Chiurugwi T, Battey N. 2005. Mechanisms and function of flower and inflorescence reversion. Journal of Experimental Biology 56: 2587-2599.
54. USGCRP. 2009. In: Karl TR, Melillo JM, Peterson TC, eds. Global climate change impacts in the United States. Cambridge, UK: Cambridge University Press.
55. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G. 2004. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303: 1003-1006.
56. Verhoeven KJF, Poorter H, Nevo E, Biere A. 2008. Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations. Molecular Ecology 17: 3416-3424.
57. Vickery R Jr. 1978. Case studies in the evolution of species complexes in Mimulus. Evolutionary Biology 11: 405-507.
58. Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC. 2009. PEP1 regulates perennial flowering in Arabis alpina. Nature 459: 423-U138.
59. Weinig C, Ungerer MC, Dorn LA, Kane NC, Toyonaga Y, Halldorsdottir SS, Mackay TFC, Purugganan MD, Schmitt J. 2002. Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162: 1875-1884.
60. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D. 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059.
61. Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J et al. 2009. Effects of genetic perturbation on seasonal life history plasticity. Science 323: 930-934.
62. Wilson RN, Heckman JW, Somerville CR. 1992. Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiology 100: 403-408.
63. Wu CA, Lowry DB, Cooley AM, Wright KM, Lee Y-W, Willis JH. 2008. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100: 220-230.
64. 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.
65. Yang CH, Chou ML. 1999. FLD interacts with CO to affect both flowering time and floral initiation in Arabidopsis thaliana. Plant Cell Physiology 40: 647-650.