Flowering time and seed dormancy control use external coincidence to generate life history strategy

eLife

Volumn 2015, Issue 4, 2015, Pages

  Springthorpe, Vicki ^a   Penfield, Steven ^b  

^a UNIVERSITY OF YORK   (United Kingdom)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; ARTICLE; CLIMATE CHANGE; ENVIRONMENTAL TEMPERATURE; FLOWERING; GERMINATION; LIFE CYCLE; NONHUMAN; SEED DORMANCY; SEEDLING; WINTER DORMANCY; ARABIDOPSIS; CLIMATE; DORMANCY; ENVIRONMENT; EUROPE; FLOWER; GENETICS; GENOTYPE; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; MUTATION; PLANT SEED; SEASON; TEMPERATURE; TIME FACTOR;

ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CLIMATE; CLIMATE CHANGE; ENVIRONMENT; EUROPE; FLOWERS; GENOTYPE; GEOGRAPHY; GERMINATION; LIFE CYCLE STAGES; MUTATION; PLANT DORMANCY; SEASONS; SEEDS; TEMPERATURE; TIME FACTORS;

EID: 84926322312     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.05557     Document Type: Article

References (40)

1. Andrés F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13:627–639. doi: 10.1038/nrg3291.
2. Atwell S, Huang YS, Vilhjá lmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JD, Michael T, Nemri A, Roux F, Salt DE, Tang C, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M. 2010.Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631. doi: 10.1038/nature08800.
3. Batlla D, Grundy A, Dent KC, Clay HA, Finch-Savage WE. 2009. A quantitative analysis of temperature dependent dormancy changes in Polygonum aviculare seeds. Weed Research 49:428–438. doi: 10.1111/j.1365-3180.2009.00706.x.
4. Bentsink L, Jowett J, Hanhart CJ, Koornneef M. 2006. Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proceedings of the National Academy of Sciences of USA 103:17042–17047. doi: 10.1073/pnas.0607877103.
5. Borthwick HA, Parker MW, Heinze PH. 1943. Effect of photoperiod and temperature on development of barley. Botanical Gazette 103:326–341. doi: 10.1086/335045.
6. Bradford KJ. 2005. Threshold models applied to seed germination ecology. The New Phytologist 165:338–341. doi: 10.1111/j.1469-8137.2004.01302.x.
7. Burghardt LT, Metcalf CJE, Wilczek AM, Schmitt J, Donohue K. 2015. Modeling the influence of genetic and environmental variation on the expression of plant life history cycles across landscapes. The American Naturalist 185:212–227. doi: 10.1086/679439.
8. Chiang GC, Bartsch M, Barua D, Nakabayashi K, Debieu M, Kronholm I, Koornneef M, Soppe WJ, Donohue K, De Meaux J. 2011. DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana. Molecular Ecology 20:3336–3349. doi: 10.1111/j.1365-294X.2011.05181.x.
9. Chiang GC, Barua D, Dittmar E, Kramer EM, de Casas RR, Donohue K. 2013. Pleiotropy in the wild: the dormancy gene DOG1 exerts cascading control on life cycles. Evolution 67:883–893. doi: 10.1111/j.1558-5646.2012.01828.x.
10. Chiang GC, 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 USA 106:11661–11666. doi: 10.1073/pnas.0901367106.
11. Childs DZ, Metcalf CJE, Rees M. 2010.Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants. Proceedings Biological sciences/The Royal Society 277:1149–1151. doi: 10.1098/rspb.2010.0707.
12. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD. 2007. Shifting plant phenology in response to global change. Trends in Ecology & Evolution 22:357–365. doi: 10.1016/j.tree.2007.04.003.
13. Cotton PA. 2003. Avian migration phenology and global climate change. Proceedings of the National Academy of Sciences of USA 100:12219–12222. doi: 10.1073/pnas.1930548100.
14. Donohue K, Burghardt LT, Runcie D, Bradford KJ, Schmitt J. 2014. Applying developmental threshold models to evolutionary ecology. Trends in Ecology & Evolution 30:66–77. doi: 10.1016/j.tree.2014.11.008.
15. Fenner M. 1991. The effects of parental environment on seed germinability. Seed Science Research 1:75–81.
16. Fitter AH, Fitter RS. 2002. Rapid changes in flowering time in British plants. Science 296:1689–1691. doi: 10.1126/science.1071617.
17. Footitt S, Douterelo-Soler I, Clay H, Finch-Savage WE. 2011. Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proceedings of the National Academy of Sciences of USA 108:20236–20241. doi: 10.1073/pnas.111632510832.
18. Footitt S, Huang Z, Clay HA, Mead A, Finch-Savage WE. 2013. Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling, resulting in winter and summer annual phenotypes. The Plant Journal 74: 1003–1015. doi: 10.1111/tpj.12186.
19. Grime JP. 1988. The C-S-R model of plant primary strategies- origins, implications and tests. In: Gottlieb LD, Jain SK, editors. Plant evolutionary biology. p. 371–393.
20. Grime JP, Mason G, Curtis AV, Rodman J, Band SR, Mowforth MA, Neal AM, Shaw SC. 1981. A comparative study of germination characteristcs in local flora. The Journal of Ecology 69:1017–1059. doi: 10.2307/2259651.
21. Gualano NA, Benech-Arnold RL. 2009. Predicting pre-harvest sprouting susceptibility in barley: Looking for ‘sensitivity windows’ to temperature throughout grain filling in various commercial cultivars. Field Crops Research 114:35–44. doi: 10.1016/j.fcr.2009.06.016.
22. Kendall SL, Hellwege A, Marriot P, Whalley C, Graham IA, Penfield S. 2011. Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. The Plant Cell 23:2568–2580. doi: 10.1105/tpc.111.087643.
23. Li P, Filiault D, Box MS, Kerdaffrec E, van Oosterhout C, Wilczek AM, Schmitt J, McMullan M, Bergelson J, Nordborg M, Dean C. 2014. Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana. Genes & Development 28:1635–1640. doi: 10.1101/gad.245993.114.
24. Lundemo S, Falahati-Anbaran M, Stenoien HK. 2009. Seed banks cause elevated generation times and effective population sizes of Arabidopsis thalisana in northern Europe. Molecular Ecology 18:2798–2811. doi: 10.1111/j.1365-294X.2009.04236.
25. MacGregor DR, Kendall SL, Fedi F, Florance H, Paszkievicz K, Smirnoff N, Penfield S. 2015. Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism. The New Phytologist 205:642–652. doi: 10.1111/nph.13090.
26. Menzel A, Fabian P. 1999. Growing season extended in Europe. Nature 397:659. doi: 10.1038/17709.
27. 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. doi: 10.1371/journal.pone.0007213.
28. Montesinos-Navarro A, Picó FX, Tonsor SJ. 2012. Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana. Evolution 66:3417–3431. doi: 10.1111/j.1558-5646.2012.01689.x.
29. Parmesan C, Yohe G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. doi: 10.1038/nature01286.
30. Robbelen G. 1965. The laibach standard collection of natural races. Arabidopsis Information Service 02S.
31. 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. doi: 10.1093/aob/mcl012.
32. Shindo C, Lister C, Crevillen P, Nordborg M, Dean C. 2006. Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes & Development 20:3079–3083. doi: 10.1101/gad.405306.
33. Sung S, Amasino RM. 2004. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164. doi: 10.1038/nature02195.
34. Thomas JF, Raper CD. 1976. Photoperiodic control of seed filling for soybeans. Crop Science 16:667–672. doi: 10.2135/cropsci1976.0011183X001600050017x.
35. Thompson L. 1994. The spatiotemporal effects of nitrogen and litter on the population dynamics of Arabidopsis thaliana. The Journal of Ecology 82:63–68. doi: 10.2307/2261386.
36. Toomajian C, Hu TT, Aranzana MJ, Lister C, Tang C, Zheng H, Zhao K, Calabrese P, Dean C, Nordborg M. 2006. A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLOS Biology 4:e137. doi: 10.1371/journal.pbio.0040137.
37. Toorop PE, Cuerva RC, Begg GS, Locardi B, Squire GR, Iannetta PP. 2012. Co-adaptation of seed dormancy and flowering time in the arable weed Capsella bursa-pastoris (shepherd’s purse). Annals of Botany 109:481–489. doi: 10.1093/aob/mcr301.
38. Totterdell S, Roberts EH. 1979. Effects of low temperatures on the loss of innate dormancy and the development of induced dormancy in seeds of Rumex obtusifolius L. and Rumex crispus L. Plant, Cell & Environment 2: 131–137. doi: 10.1111/j.1365-3040.1979.tb00783.x.
39. Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J, Egan JF, Moyers BT, Petipas R, Giakountis A, Charbit E, Coupland G, Welch SM, Schmitt J. 2009. Effects of genetic perturbation on seasonal life history plasticity. Science 323:930–934. doi: 10.1126/science.1165826.
40. Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC. 2008. Phylogenetic patterns of species loss in Thoreau’s woods are driven by climate change. Proceedings of the National Academy of Sciences of USA 105: 17029–17033. doi: 10.1073/pnas.0806446105.