Co-Variation between Seed Dormancy, Growth Rate and Flowering Time Changes with Latitude in Arabidopsis thaliana

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Debieu, Marilyne ^a,b   Tang, Chunlao ^c   Stich, Benjamin ^b   Sikosek, Tobias ^d   Effgen, Sigi ^b   Josephs, Emily ^e   Schmitt, Johanna ^f   Nordborg, Magnus ^g   Koornneef, Maarten ^b,h   de Meaux, Juliette ^b,d  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e BROWN UNIVERSITY   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

^h WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; ARTICLE; EVOLUTIONARY ADAPTATION; FLOWERING; GENETIC TRAIT; GENETIC VARIABILITY; GROWTH RATE; LATITUDE; LIFE HISTORY TRAIT; NONHUMAN; PLANT LIFE CYCLE STAGE; POPULATION GENETIC STRUCTURE; SEED DORMANCY; VEGETATIVE GROWTH;

ARABIDOPSIS; BIOLOGICAL EVOLUTION; EUROPE; FLOWERS; GENOTYPE; GERMINATION; PHENOTYPE; PHYLOGEOGRAPHY; PLANT DORMANCY; POLYMORPHISM, SINGLE NUCLEOTIDE; SEASONS; SEEDS;

EID: 84878154928     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061075     Document Type: Article

References (80)

1. Montesinos-Navarro A, Picó FX, Tonsor SJ, (2012) Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana. Evolution 66: 3417-3431.
2. Biere A, (1991) Parental effects in Lychnis-Flos-Cuculi. 1. seed size, germination and seedling performance in a controlled environment. Journal of Evolutionary Biology 4(3): 447-465.
3. Gross KL, Smith AD, (1991) Seed mass and emergence time effects on performance of Panicum dichotomiflorum Michx across environments. Oecologia 87: 270-278.
4. Kalisz S, (1989) Fitness consequences of mating system, seed weight, and emergence date in a winter annual, Collinsia verna. Evolution 43: 1263-1272.
5. Masuda M, Washitani I, (1992) Differentiation of spring emerging and autumn emerging ecotypes in Galium spurium L. var. echinospermon. Oecologia 89: 42-46.
6. Donohue K, Dorn L, Griffith C, Kim E, Aguilera A, et al. (2005) The evolutionary ecology of seed germination of Arabidopsis thaliana: Variable natural selection on germination timing. Evolution 59: 758-770.
7. Miller MR, White A, Boots M, (2007) Host life span and the evolution of resistance characteristics. Evolution 61: 2-14.
8. Hilhorst HWM, (1995) A critical update on seed dormancy. 1. Primary dormancy. Seed Science Research 5: 61-73.
9. Bewley JD, (1997) Seed germination and dormancy. Plant Cell 9: 1055-1066.
10. Baskin JM, Baskin CC, (2004) A classification system for seed dormancy. Seed Science Research 14: 1-16.
11. Finch-Savage WE, Leubner-Metzger G, (2006) Seed dormancy and the control of germination. New Phytologist 171: 501-523.
12. Vleeshouwers LM, Bouwmeester HJ, Karssen CM, (1995) Redefining seed dormancy: An attempt to integrate physiology and ecology. Journal of Ecology 83: 1031-1037.
13. Baskin CC, Baskin JM (1998) Ecology, biogeography, and evolution of dormancy and germination - introduction. Seeds: 1-3.
14. Cadman CSC, Toorop PE, Hilhorst HWM, Finch-Savage WE, (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant Journal 46: 805-822.
15. Mitchell-Olds T, (1996) Genetic constraints on life-history evolution: Quantitative-trait loci influencing growth and flowering in Arabidopsis thaliana. Evolution 50: 140-145.
16. Geber MA, (1990) The cost of meristem limitation in Polygonum-arenastrum - negative genetic correlations between fecundity and growth. Evolution 44: 799-819.
17. Stratton DA, (1998) Reaction norm functions and QTL-environment interactions for flowering time in Arabidopsis thaliana. Heredity 81: 144-155.
18. Simpson GG, Dean C, (2002) Arabidopsis, the rosetta stone of flowering time? Science 296: 285-289.
19. Munguia-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA, (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters 14(5): 511-521.
20. Andres F, Coupland G, (2012) The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13(9): 627-639.
21. Michaels SD, (2009) Flowering time regulation produces much fruit. Current Opinion in Plant Biology 12(1): 75-80.
22. de Casas RR, Kovach K, Dittmar E, Barua D, Barco B, et al. (2012) Seed after-ripening and dormancy determine adult life history independently of germination timing. New Phytologist 194(3): 868-879.
23. King D, Roughgarden J, (1982) Graded allocation between vegetative and reproductive growth for annual plants in growing seasons of random length. Theoretical Population Biology 22: 1-16.
24. McGraw JB, Garbutt K, (1990) The analysis of plant growth in ecological and evolutionary studies. Trends in Ecology & Evolution 5: 251-254.
25. Stearns SC, Stearns SC (1992) The evolution of life histories. The evolution of life histories.: i-xii, 1-249.
26. Roff DA, Fairbairn DJ, (2007) The evolution of trade-offs: Where are we? Journal of Evolutionary Biology 20: 433-447.
27. Metcalf CJE, Mitchell-Olds T, (2009) Life history in a model system: Opening the black box with Arabidopsis thaliana. Ecology Letters 12: 593-600.
28. Hoffmann MH, (2005) Evolution of the realized climatic niche in the genus Arabidopsis (Brassicaceae). Evolution 59: 1425-1436.
29. Schmuths H, Bachmann K, Weber WE, Horres R, Hoffmann MH, (2006) Effects of preconditioning and temperature during germination of 73 natural accessions of Arabidopsis thaliana. Annals of Botany 97: 623-634.
30. Alonso-Blanco C, Aarts MGM, Bentsink L, Keurentjes JJB, Reymond M, et al. (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21: 1877-1896.
31. Aarssen LW, Clauss MJ, (1992) Genotypic variation in fecundity allocation in Arabidopsis-thaliana. Journal of Ecology 80: 109-114.
32. Li B, Suzuki JI, Hara T, (1998) Latitudinal variation in plant size and relative growth rate in Arabidopsis thaliana. Oecologia 115: 293-301.
33. Perez-Perez JM, Serrano-Cartagena J, Micol JL, (2002) Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves. Genetics 162: 893-915.
34. Koornneef M, Alonso-Blanco C, Vreugdenhil D, (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annual Review of Plant Biology 55: 141-172.
35. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, et al. (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiology 138: 1163-1173.
36. Caicedo AL, Stinchcombe JR, Olsen KM, 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 of the United States of America 101: 15670-15675.
37. Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, et al. (2009) Effects of genetic perturbation on seasonal life history plasticity. Science 323: 930-934.
38. Griffith C, Kim E, Donohue K, (2004) Life-history variation and adaptation in the historically mobile plant Arabidopsis thaliana (Brassicaceae) in north america. American Journal of Botany 91: 837-849.
39. Donohue K, Dorn D, Griffith C, Kim E, Aguilera A, et al. (2005) Niche construction through germination cueing: Life-history responses to timing of germination in Arabidopsis thaliana. Evolution 59: 771-785.
40. Korves TM, Schmid KJ, Caicedo AL, Mays C, Stinchcombe JR, et al. (2007) Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. American Naturalist 169: E141-E157.
41. Kronholm I, Pico FX, Alonso-Blanco C, Goudet J, de Meaux J, (2012) Genetic basis of adaptation in Arabidopsis thaliana: local adaptation at the seed dormancy QTL DOG1. Evolution 66(7): 2287-2302.
42. Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, et al. (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proceedings of the National Academy of Sciences of the United States of America 101(13): 4712-4717.
43. Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. Plos Genetics 1: 109-118.
44. Mendez-Vigo B, Pico FX, Ramiro M, Martinez-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(4): 1942-1955.
45. Samis KE, Murren CJ, Bossdorf O, Donohue K, Fenster CB, et al. (2012) Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana. Ecology and Evolution 2: 1162-1180.
46. Mayr E, (1956) Geographical character gradients and climatic adaption. Evolution 10(1): 105-108.
47. Endler JA (1977) Geographic variation, speciation, and clines. Monogr Popul Biol 10: 1-246.
48. Montesinos-Navarro A, Wig J, Pico FX, Tonsor SJ, (2011) Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. New Phytologist 189: 282-294.
49. Kivela SM, Valimaki P, Oksanen J, Kaitala A, Kaitala V, (2009) Seasonal clines of evolutionarily stable reproductive effort in insects. American Naturalist 174(4): 526-536.
50. Burke S, Pullin AS, Wilson RJ, Thomas CD, (2005) Selection for discontinuous life-history traits along a continuous thermal gradient in the butterfly Aricia agestis. Ecological Entomology 30(6): 613-619.
51. Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627-631.
52. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, (2005) The pattern of polymorphism in Arabidopsis thaliana. Plos Biology 3: 1289-1299.
53. Leister D, Varotto C, Pesaresi P, Niwergall A, Salamini F, (1999) Large-scale evaluation of plant growth in Arabidopsis thaliana by non-invasive image analysis. Plant Physiology and Biochemistry 37: 671-678.
54. El-Lithy ME, Clerkx EJM, Ruys GJ, Koornneef M, Vreugdenhil D, (2004) Quantitative trait locus analysis of growth-related traits in a new Arabidopsis recombinant line population. Plant Physiology 135: 444-458.
55. Alonso-Blanco C, Bentsink L, Hanhart CJ, Vries HBE, Koornneef M, (2003) Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164: 711-729.
56. Warthmann N, Fitz J, Weigel D, (2007) MSQT for choosing SNP assays from multiple DNA alignments. Bioinformatics 23: 2784-2787.
57. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
58. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software structure: A simulation study. Molecular Ecology 14: 2611-2620.
59. 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 of the United States of America 106: 11661-11666.
60. Wagmann K, Hautekèete NC, Piquot Y, Meunier C, Schmitt SE, et al. (2012) Seed dormancy distribution: explanatory ecological factors. Annuals of Botany 1-15.
61. Johanson U, West J, Lister C, Michaels S, Amasino R, et al. (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347.
62. Donohue K, (2002) Germination timing influences natural selection on life-history characters in Arabidopsis thaliana. Ecology 83: 1006-1016.
63. Rees M, Childs DZ, Metcalf JC, Rose KE, Sheppard AW, et al. (2006) Seed dormancy and delayed flowering in monocarpic plants: Selective interactions in a stochastic environment. American Naturalist 168: E53-E71.
64. Huang X, Schmitt J, Dorn L, Griffith C, Effgen S, et al. (2010) The earliest stages of adaptation in an experimental plant population: Strong selection on QTLs for seed dormancy. Molecular Ecology 19: 1335-1351.
65. Baskin JM, Baskin CC, (1983) Seasonal-changes in the germination responses of buried seeds of Arabidopsis-thaliana and ecological interpretation. Botanical Gazette 144: 540-543.
66. Meng PH, Macquet A, Loudet O, Marion-Poll A, North HM, (2008) Analysis of natural allelic variation controlling Arabidopsis thaliana seed germinability in response to cold and dark: Identification of three major quantitative trait loci. Molecular Plant 1: 145-154.
67. Montesinos A, Tonsor SJ, Alonso-Blanco C, Pico FX, (2009) Demographic and genetic patterns of variation among populations of Arabidopsis thaliana from contrasting native environments. PLoS One 4: e7213.
68. Hopkins R, Schmitt J, Stinchcombe JR, (2008) A latitudinal cline and response to vernalization in leaf angle and morphology in Arabidopsis thaliana (Brassicaceae). New Phytologist 179: 155-164.
69. Salomé PA, Bomblies K, Laitinen RAE, Yant L, Mott R, et al. (2011) Genetic architecture of flowering time variation in Arabidopsis thaliana. Genetics 188: 421-U313.
70. Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, et al. (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. Plos Genetics 6.
71. Weinig C, Ungerer MC, Dorn LA, Kane NC, Toyonaga Y, et al. (2002) Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162: 1875-1884.
72. Stillwell RC, Morse GE, Fox CW, (2007) Geographic variation in body size and sexual size dimorphism of a seed-feeding beetle. American Naturalist 170: 358-369.
73. Sharbel TF, Haubold B, Mitchell-Olds T, (2000) Genetic isolation by distance in Arabidopsis thaliana: Biogeography and postglacial colonization of Europe. Molecular Ecology 9: 2109-2118.
74. Beck JB, Schmuths H, Schaal BA, (2008) Native range genetic variation in Arabidopsis thaliana is strongly geographically structured and reflects pleistocene glacial dynamics. Molecular Ecology 17: 902-915.
75. Francois O, Blum MGB, Jakobsson M, Rosenberg NA (2008) Demographic history of european populations of Arabidopsis thaliana. Plos Genetics 4.
76. Fournier-Level A, Korte A, Cooper MD, Nordborg M, Schmitt J, et al. (2011) A Map of Local Adaptation in Arabidopsis thaliana. Science 333: 86-89.
77. Hancock AM, Brachi B, Faure N, Horton MW, Jarymowycz LB, et al. (2011) Adaptation to Climate Across the Arabidopsis thaliana Genome. Science 333: 83-86.
78. Agren J, Schemske DW, (2012) Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytologist 194: 1112-1122.
79. Rutter MT, Fenster CB, (2007) Testing for adaptation to climate in Arabidopsis thaliana: A calibrated common garden approach. Annals of Botany 99: 529-536.
80. Korte A, Vilhjalmsson BJ, Segura V, Platt A, Long Q, et al. (2012) A mixed-model approach for genome-wide association studies of correlated traits in structured populations. Nature Genetics 44(9): 1066-+.