Variation in circadian rhythms is maintained among and within populations in Boechera stricta

Plant Cell and Environment

Volumn 39, Issue 6, 2016, Pages 1293-1303

  Salmela, Matti J ^a   Greenham, Kathleen ^b   Lou, Ping ^b   Mcclung, C Robertson ^b   Ewers, Brent E ^a   Weinig, Cynthia ^a  

^a UNIVERSITY OF WYOMING   (United States)

^b Lamont Doherty Earth Observatory   (United States)

Author keywords

Adaptation; Circadian clock; Environmental heterogeneity; Genetic differentiation; Genotype environment interaction; Maintenance of genetic variation

Indexed keywords

ADAPTATION; CIRCADIAN RHYTHM; EXPERIMENTAL STUDY; FITNESS; GENETIC VARIATION; GENOTYPE-ENVIRONMENT INTERACTION; HERB; HETEROGENEITY; LIFE HISTORY TRAIT; POPULATION GENETICS; ROOT-SHOOT RATIO;

UNITED STATES; WYOMING;

ARABIDOPSIS; BOECHERA STRICTA;

BRASSICACEAE; CIRCADIAN RHYTHM; GENETIC VARIATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; POPULATION; SEASON;

BRASSICACEAE; CIRCADIAN RHYTHM; GENETIC VARIATION; POPULATION; SEASONS;

EID: 84966705320     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12670     Document Type: Article

References (45)

1. Barton N.H. & Keightley P.D. (2002) Understanding quantitative genetic variation. Nature Reviews Genetics 3, 11-21.
2. Bell-Pedersen D., Cassone V.M., Earnest D.J., Golden S.S., Hardin P.E., Thomas T.L. & Zoran M.J. (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nature Reviews Genetics 6, 544-556.
3. Brown S.A., Kunz D., Dumas A., Westermark P.O., Vanselow K., Tilmann-Wahnschaffe A., Herzel H. & Kramer A. (2008) Molecular insights into human daily behavior. Proceedings of the National Academy of Sciences of the United States of America 105, 1602-1607.
4. Chapin F.S. III & Chapin M.C. (1981) Ecotypic differentiation of growth processes in Carex aquatilis along latitudinal and local gradients. Ecology 62, 1000-1009.
5. Cockerham C.C. (1963) Estimation of genetic variances. In Statistical Genetics and Plant Breeding (eds Hanson W.D. & Robertson H.F.), pp. 53-94. National Academy of Sciences, Washington, D.C., USA.
6. de Montaigu A., Giakountis A., Rubin M., Tóth R., Cremer F., Sokolova V., ... Coupland G. (2015) Natural diversity in daily rhythms of gene expression contributes to phenotypic variation. Proceedings of the National Academy of Sciences of the United States of America 112, 905-910.
7. Dodd A.N., Salathia N., Hall A., Kévei E., Tóth R., Nagy F., ... Webb A.A.R. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633.
8. Edwards K.D., Lynn J.R., Gyula P., Nagy F. & Millar A.J. (2005) Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170, 387-400.
9. Ellner S. & Hairston N.G. Jr. (1994) Role of overlapping generations in maintaining genetic variation in a fluctuating environment. American Naturalist 143, 403-417.
10. Falconer D.S. & Mackay T.F.C. (1996) Introduction to Quantitative Genetics. 4th edn. Pearson Education Limited, Harlow, England.
11. Fleury F., Allemand R., Vavre F., Fouillet P. & Boulétreau M. (2000) Adaptive significance of a circadian clock: temporal segregation of activities reduces intrinsic competitive inferiority in Drosophila parasitoids. Proceedings of the Royal Society B 267, 1005-1010.
12. Gillespie J.H. & Turelli M. (1989) Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121, 129-138.
13. Graf A., Schlereth A., Stitt M. & Smith A.M. (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proceedings of the National Academy of Sciences of the United States of America 107, 9458-9463.
14. Green R.M., Tingay S., Wang Z.-Y. & Tobin E.M. (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiology 129, 576-584.
15. Greenham K., Lou P., Farid H., Remsen S.E. & McClung C.R. (2015) TRiP: Tracking Rhythms in Plants, an automated leaf movement analysis program for circadian period estimation. Plant Methods 11, 33.
16. Helm B. & Visser M.E. (2010) Heritable circadian period length in a wild bird population. Proceedings of the Royal Society B 277, 3335-3342.
17. Hereford J. (2009) A quantitative survey of local adaptation and fitness trade-offs. American Naturalist 173, 579-588.
18. Hoffmann A.A. & Sgrò C.M. (2011) Climate change and evolutionary adaptation. Nature 470, 479-485.
19. Hut R.A., Paolucci S., Dor R., Kyriacou C.P. & Daan S. (2013) Latitudinal clines: an evolutionary view on biological rhythms. Proceedings of the Royal Society B 280, 20130433.
20. Kawecki T.J. & Ebert D. (2004) Conceptual issues in local adaptation. Ecology Letters 7, 1225-1241.
21. Kruuk L.E.B., Charmantier A. & Garant D. (2014) The study of quantitative genetics in wild populations. In Quantitative Genetics in the Wild (eds Charmantier A., Garant D. & Kruuk L.E.B.), pp. 1-15. Oxford University Press, Oxford, England.
22. Kusakina J., Gould P.D. & Hall A. (2014) A fast circadian clock at high temperatures is a conserved feature across Arabidopsis accessions and likely to be important for vegetative yield. Plant, Cell and Environment 37, 327-340.
23. Lankinen P. (1993) North-south differences in circadian eclosion rhythm in European populations of Drosophila subobscura. Heredity 71, 210-218.
24. Larsen H.S., South D.B. & Boyer J.M. (1986) Root growth potential, seedling morphology and bud dormancy correlate with survival of loblolly pine seedlings planted in December in Alabama. Tree Physiology 1, 253-263.
25. Leimu R. & Fischer M. (2008) A meta-analysis of local adaptation in plants. PLoS One 3, e4010.
26. Linhart Y.B. & Grant M.C. (1996) Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics 27, 237-277.
27. Lloret F., Casanovas C. & Peñuelas J. (1999) Seedling survival of Mediterranean shrubland species in relation to root:shoot ratio, seed size and water and nitrogen use. Functional Ecology 13, 210-216.
28. McClung C.R. & Davis S.J. (2010) Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Current Biology 20, R1086-R1092.
29. Méndez-Vigo B., Gomaa N.H., Alonso-Blanco C. & Picó F.X. (2013) Among- and within-population variation in flowering time of Iberian Arabidopsis thaliana estimated in field and glasshouse conditions. New Phytologist 197, 1332-1343.
30. Michael T.P., Salomé P.A., Yu H.J., Spencer T.R., Sharp E.L., McPeek M.A., ... McClung C.R. (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302, 1049-1053.
31. Millar A.J., Carré I.A., Strayer C.A., Chua N.H. & Kay S.A. (1995) Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267, 1161-1163.
32. Mitchell-Olds T. (1992) Does environmental variation maintain genetic variation? A question of scale. Trends in Ecology and Evolution 7, 397-398.
33. Ouyang Y., Andersson C.R., Kondo T., Golden S.S. & Johnson C.H. (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America 95, 8660-8664.
34. Pittendrigh C.S. (1981) Circadian systems: general perspective. In Handbook of Behavioral Neurobiology Volume 4: Biological Rhythms (ed Aschoff J.), pp. 57-80. Plenum Press, New York, NY.
35. Poorter H., Niklas K.J., Reich P.B., Oleksyn J., Poot P. & Mommer L. (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193, 30-50.
36. Rushworth C.A., Song B.-H., Lee C.-R. & Mitchell-Olds T. (2011) Boechera, a model system for ecological genomics. Molecular Ecology 20, 4843-4857.
37. Salmela M.J. (2014) Rethinking local adaptation: mind the environment!. Forest Ecology and Management 312, 271-281.
38. Salomé P.A., Michael T.P., Kearns E.V., Fett-Neto A.G., Sharrock R.A. & McClung C.R. (2002) The out of phase 1 mutant defines a role for PHYB in circadian phase control in Arabidopsis. Plant Physiology 129, 1674-1685.
39. Savolainen O., Pyhäjärvi T. & Knürr T. (2007) Gene flow and local adaptation in trees. Annual Review of Ecology, Evolution, and Systematics 38, 595-619.
40. Song B.-H., Clauss M.J., Pepper A. & Mitchell-Olds T. (2006) Geographic patterns of microsatellite variation in Boechera stricta, a close relative of Arabidopsis. Molecular Ecology 15, 357-369.
41. Tindall A.J., Waller J., Greenwood M., Gould P.D., Hartwell J. & Hall A. (2015) A comparison of high-throughput techniques for assaying circadian rhythms in plants. Plant Methods 11, 32.
42. West A.C. & Bechtold D.A. (2015) The cost of circadian desynchrony: evidence, insights and open questions. BioEssays 37, 777-788.
43. Woelfle M.A., Ouyang Y., Phanvijhitsiri K. & Johnson C.H. (2004) The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Current Biology 14, 1481-1486.
44. Yerushalmi S. & Green R.M. (2009) Evidence for the adaptive significance of circadian rhythms. Ecology Letters 12, 970-981.
45. Zhang C., Xie Q., Anderson R.G., Ng G., Seitz N.C., Peterson T., ... Lu H. (2013) Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathogens 9, e1003370.