Epigenetic variation creates potential for evolution of plant phenotypic plasticity

New Phytologist

Volumn 197, Issue 1, 2013, Pages 314-322

  Zhang, Yuan Ye ^a   Fischer, Markus ^a   Colot, Vincent ^b   Bossdorf, Oliver ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b CNRS   (France)

Author keywords

Arabidopsis thaliana; DNA methylation; Drought tolerance; Ecological epigenetics; EpiRILs; Heritability

Indexed keywords

PLANT DNA;

DICOTYLEDON; DNA; DROUGHT; DROUGHT RESISTANCE; EVOLUTIONARY BIOLOGY; EXPERIMENTAL STUDY; GENETIC STRUCTURE; GENETIC VARIATION; HERITABILITY; LIFE HISTORY TRAIT; METHYLATION; NATURAL SELECTION; PHENOTYPIC PLASTICITY; TOLERANCE;

ARABIDOPSIS; ARTICLE; CROSS BREEDING; DNA METHYLATION; DROUGHT; EVOLUTION; FLOWER; GENETIC EPIGENESIS; GENETIC SELECTION; GENETICS; MUTATION; PHENOTYPE; PHYSIOLOGY; PLANT; PLANT ROOT; QUANTITATIVE TRAIT;

ARABIDOPSIS; BIOLOGICAL EVOLUTION; CROSSES, GENETIC; DNA METHYLATION; DNA, PLANT; DROUGHTS; EPIGENESIS, GENETIC; FLOWERS; MUTATION; PHENOTYPE; PLANT ROOTS; PLANT SHOOTS; QUANTITATIVE TRAIT, HERITABLE; SELECTION, GENETIC;

ARABIDOPSIS THALIANA;

EID: 84870231986     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12010     Document Type: Article

References (68)

1. Agrawal AA, Conner JK, Johnson MTJ, Wallsgrove R. 2002. Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56: 2206-2213.
2. Berger SL. 2007. The complex language of chromatin regulation during transcription. Nature 447: 407-412.
3. Bird A. 2007. Perceptions of epigenetics. Nature 447: 396-398.
4. Bossdorf O, Arcuri D, Richards CL, Pigliucci M. 2010. Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evolutionary Ecology 24: 541-553.
5. Bossdorf O, Pigliucci M. 2009. Plasticity to wind is modular and genetically variable in Arabidopsis thaliana. Evolutionary Ecology 23: 669-685.
6. Callahan HS, Pigliucci M. 2005. Indirect consequences of artificial selection on plasticity to light quality in Arabidopsis thaliana. Journal of Evolutionary Biology 18: 1403-1415.
7. Cervera MT, Ruiz-Garcia L, Martinez-Zapater JM. 2002. Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Molecular Genetics and Genomics 268: 543-552.
8. Conner JK, Hartl DL. 2004. A primer of ecological genetics. Sunderland, MA, USA: Sinauer Associates.
9. Cubas P, Vincent C, Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157-161.
10. Dhanda SS, Sethi GS, Behl RK. 2004. Indices of drought tolerance in wheat genotypes at early stages of plant growth. Journal of Agronomy and Crop Science 190: 6-12.
11. Dorn LA, Pyle EH, Schmitt J. 2000. Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution 54: 1982-1994.
12. Endler JA. 1986. Natural selection in the wild. Princeton, NJ, USA: Princeton University Press.
13. Falconer DS, MacKay TFC. 1996. Introduction to quantitative genetics, 4th edn. New York, NY, USA: Longman.
14. Fisher RA. 1930. The genetical theory of natural selection. Oxford, UK: Oxford University Press.
15. Gao LX, Geng YP, Li B, Chen JK, Yang J. 2010. Genome-wide DNA methylation alterations of Alternanthera philoxeroides in natural and manipulated habitats: implications for epigenetic regulation of rapid responses to environmental fluctuation and phenotypic variation. Plant, Cell and Environment 33: 1820-1827.
16. Grant-Downton RT, Dickinson HG. 2005. Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Annals of Botany 96: 1143-1164.
17. Heschel MS, Sultan SE, Glover S, Sloan D. 2004. Population differentiation and plastic responses to drought stress in the generalist annual Polygonum persicaria. International Journal of Plant Sciences 165: 817-824.
18. Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162: 9-24.
19. Hoffmann AA, Sgro CM. 2011. Climate change and evolutionary adaptation. Nature 470: 479-485.
20. Johannes F, Colot V, Jansen RC. 2008. OPINION Epigenome dynamics: a quantitative genetics perspective. Nature Reviews Genetics 9: 883-890.
21. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P et al. 2009. Assessing the impact of transgenerational epigenetic variation on complex traits. Plos Genetics 5: e1000530.
22. Juenger TE, Sen S, Stowe KA, Simms EL. 2005. Epistasis and genotype-environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana. Genetica 123: 87-105.
23. Kamoshita A, Zhang JX, Siopongco J, Sarkarung S, Nguyen HT, Wade LJ. 2002. Effects of phenotyping environment on identification of quantitative trait loci for rice root morphology under anaerobic conditions. Crop Science 42: 255-265.
24. Keyte AL, Percifield R, Liu B, Wendel JF. 2006. Intraspecific DNA methylation polymorphism in cotton (Gossypium hirsutum L.). Journal of Heredity 97: 444-450.
25. van Kleunen M, Fischer M. 2001. Adaptive evolution of plastic foraging responses in a clonal plant. Ecology 82: 3309-3319.
26. van Kleunen M, Fischer M. 2003. Effects of four generations of density-dependent selection on life history traits and their plasticity in a clonally propagated plant. Journal of Evolutionary Biology 16: 474-484.
27. van Kleunen M, Fischer M. 2005. Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytologist 166: 49-60.
28. Koornneef M, Alonso-Blanco C, Vreugdenhil D. 2004. Naturally occurring genetic variation in Arabidopsis thaliana. Annual Review of Plant Biology 55: 141-172.
29. Kozlowski TT, Pallardy SG. 2002. Acclimation and adaptive responses of woody plants to environmental stresses. Botanical Review 68: 270-334.
30. Lacaze X, Hayes PM, Korol A. 2009. Genetics of phenotypic plasticity: QTL analysis in barley, Hordeum vulgare. Heredity 102: 163-173.
31. Lynch M, Walsh JB. 1998. Genetics and analysis of quantitative traits. Sunderland, MA, USA: Sinauer Associates.
32. Manickavelu A, Nadarajan N, Ganesh SK, Gnanamalar RP, Babu RC. 2006. Drought tolerance in rice: morphological and molecular genetic consideration. Plant Growth Regulation 50: 121-138.
33. Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB. 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature Genetics 38: 948-952.
34. Mauricio R. 1998. Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. American Naturalist 151: 20-28.
35. McKay JK, Richards JH, Mitchell-Olds T. 2003. Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Molecular Ecology 12: 1137-1151.
36. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T. 2001. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411: 212-214.
37. Morgan HD, Sutherland HGE, Martin DIK, Whitelaw E. 1999. Epigenetic inheritance at the agouti locus in the mouse. Nature Genetics 23: 314-318.
38. Pigliucci M. 2002. Ecology and evolutionary biology of Arabidopsis. The Arabidopsis Book 1: e0003.
39. Pigliucci M. 2005. Evolution of phenotypic plasticity: where are we going now? Trends in Ecology & Evolution 20: 481-486.
40. Pigliucci M, Kolodynska A. 2002. Phenotypic plasticity to light intensity in Arabidopsis thaliana: invariance of reaction norms and phenotypic integration. Evolutionary Ecology 16: 27-47.
41. Raj S, Braeutigam K, Hamanishi ET, Wilkins O, Thomas BR, Schroeder W, Mansfield SD, Plant AL, Campbell MM. 2011. Clone history shapes Populus drought responses. Proceedings of the National Academy of Sciences, USA 108: 12521-12526.
42. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KVK, Whitelaw E. 2003. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proceedings of the National Academy of Sciences, USA 100: 2538-2543.
43. Rapp RA, Wendel JF. 2005. Epigenetics and plant evolution. New Phytologist 168: 81-91.
44. Reboud X, Bell G. 1997. Experimental evolution in Chlamydomonas.3. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78: 507-514.
45. Reinders J, Wulff BBH, Mirouze M, Mari-Ordonez A, Dapp M, Rozhon W, Bucher E, Theiler G, Paszkowski J. 2009. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes & Development 23: 939-950.
46. Reynolds M, Dreccer F, Trethowan R. 2007. Drought-adaptive traits derived from wheat wild relatives and landraces. Journal of Experimental Botany 58: 177-186.
47. Richards CL, Bossdorf O, Pigliucci M. 2010. What role does heritable epigenetic variation play in phenotypic evolution? BioScience 60: 232-237.
48. Richards EJ. 2006. Opinion - inherited epigenetic variation - revisiting soft inheritance. Nature Reviews Genetics 7: 395-401.
49. Richards EJ. 2009. Quantitative epigenetics: DNA sequence variation need not apply. Genes & Development 23: 1601-1605.
50. Richards EJ. 2011. Natural epigenetic variation in plant species: a view from the field. Current Opinion in Plant Biology 14: 204-209.
51. Roux F, Colome-Tatche M, Edelist C, Wardenaar R, Guerche P, Hospital F, Colot V, Jansen RC. 2011. Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188: 1015-1017.
52. Salmon A, Ainouche ML, Wendel JF. 2005. Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Molecular Ecology 14: 1163-1175.
53. Salmon A, Clotault J, Jenczewski E, Chable V, Manzanares-Dauleux MJ. 2008. Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Science 174: 61-70.
54. Scheiner SM. 1993. Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24: 35-68.
55. Scheiner SM, Berrigan D. 1998. The genetics of phenotypic plasticity. VIII. The cost of plasticity in Daphnia pulex. Evolution 52: 368-378.
56. Scheiner SM, Callahan HS. 1999. Measuring natural selection on phenotypic plasticity. Evolution 53: 1704-1713.
57. Scheiner SM, Mitchell RJ, Callahan HS. 2000. Using path analysis to measure natural selection. Journal of Evolutionary Biology 13: 423-433.
58. Singer T, Yordan C, Martienssen RA. 2001. Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes & Development 15: 591-602.
59. Stinchcombe JR, Agrawal AF, Hohenlohe PA, Arnold SJ, Blows MW. 2008. Estimating nonlinear selection gradients using quadratic regression coefficients: double or nothing? Evolution 62: 2435-2440.
60. Stinchcombe JR, Dorn LA, Schmitt J. 2004. Flowering time plasticity in Arabidopsis thaliana: a reanalysis of Westerman & Lawrence (1970). Journal of Evolutionary Biology 17: 197-207.
61. Strauss SY, Agrawal AA. 1999. The ecology and evolution of plant tolerance to herbivory. Trends in Ecology & Evolution 14: 179-185.
62. Ungerer MC, Halldorsdottir SS, Modliszewski JL, Mackay TFC, Purugganan MA. 2002. Quantitative trait loci for inflorescence development in Arabidopsis thaliana. Genetics 160: 1133-1151.
63. Ungerer MC, Halldorsdottir SS, Purugganan MA, Mackay TFC. 2003. Genotype-environment interactions at quantitative trait loci affecting inflorescence development in Arabidopsis thaliana. Genetics 165: 353-365.
64. Vaughn MW, Tanurdzic M, Lippman Z, Jiang H, Carrasquillo R, Rabinowicz PD, Dedhia N, McCombie WR, Agier N, Bulski A et al. 2007. Epigenetic natural variation in Arabidopsis thaliana. PLoS Biology 5: 1617-1629.
65. Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A. 2010. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytologist 185: 1108-1118.
66. Visser ME. 2008. Keeping up with a warming world: assessing the rate of adaptation to climate change. Proceedings of the Royal Society B-Biological Sciences 275: 649-659.
67. Weinig C, Stinchcombe JR, Schmitt J. 2003. Evolutionary genetics of resistance and tolerance to natural herbivory in Arabidopsis thaliana. Evolution 57: 1270-1280.
68. Westerman JM, Lawrence MJ. 1970. Genotype-environment interaction and developmental regulation in Arabidopsis thaliana. L. Inbred lines - description. Heredity 25: 609-627.