Genetic and physiological bases for phenological responses to current and predicted climates

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1555, 2010, Pages 3129-3147

  Wilczek, A M ^a   Burghardt, L T ^a   Cobb, A R ^b   Cooper, M D ^a   Welch, S M ^c   Schmitt, J ^a  

^a BROWN UNIVERSITY   (United States)

^b SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

Genetic architecture; Life history evolution; Local adaptation; Phenology; Seasonal timing

Indexed keywords

CLIMATE VARIATION; ECOLOGICAL MODELING; ENVIRONMENTAL CUE; FLOWERING; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC VARIATION; GEOGRAPHICAL REGION; GROWING SEASON; HERB; LIFE HISTORY TRAIT; LOCAL ADAPTATION; PHENOLOGY; PHYSIOLOGICAL RESPONSE; QUANTITATIVE ANALYSIS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77958063390     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0128     Document Type: Article

References (168)

1. Aitken, S. N., Yeaman, S., Holliday, J. A., Wang, T. L. & Curtis-Mclane, S. 2008 Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol. Appl. 1, 95-111. (doi:10.1111/j.1752-4571. 2007.00013.x)
2. Akin, W. E. 1990 Global patterns: climate, vegetation and soils. Norman, OK: University of Oklahoma Press.
3. Alexandre, C. M. & Hennig, L. 2008 FLC or not FLC: the other side of vernalization. J. Exp. Bot. 59, 1127-1135. (doi:10.1093/jxb/ern070)
4. Alonso-Blanco, C., Bentsink, L., Hanhart, C. J., Blankestijnde Vries, H. & Koornneef, M. 2003 Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164, 711-729.
5. Alonso-Blanco, C., Mendez-Vigo, B. & Koornneef, M. 2005 From phenotypic to molecular polymorphisms involved in naturally occurring variation of plant development. Int. J. Dev. Biol. 49, 717-732. (doi:10.1387/ijdb. 051994ca)
6. Alonso-Blanco, C., Aarts, M. G. M., Bentsink, L., Keurentjes, J. J. B., Reymond, M., Vreugdenhil, D. & Koornneef, M. 2009 what has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21, 1877-1896. (doi:10.1105/tpc.109.068114)
7. Balasubramanian, S. et al. 2006a The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nat. Genet. 38, 711-715. (doi:10.1038/ng1818)
8. Balasubramanian, S., Sureshkumar, S., Lempe, J. & Weigel, D. 2006b Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2, 980-989.
9. Baurle, I. & Dean, C. 2006 The timing of developmental transitions in plants. Cell 125, 655-664. (doi:10.1016/j. cell.2006.05.005)
10. Beck, J. B., Schmuths, H. & Schaal, B. A. 2008 Native range genetic variation in Arabidopsis thaliana is strongly geographically structured and reflects Pleistocene glacial dynamics. Mol. Ecol. 17, 902-915.
11. Bertin, R. I. 2008 Plant phenology and distribution in relation to recent climate change. J. Torrey Bot. Soc. 135, 126-146.
12. Betancourt, J. L. & Schwartz, M. 2005 Implementing a U. S. national phenology network. EOS Trans. AGU 86, 539-541.
13. Blackman, B., Strasburg, J. L., Raduski, A., Michaels, S. & Rieseberg, L. 2010 The role of recently derived FT paralogs in sunflower domestication. Curr. Biol. 20, 629-635. (doi:10.1016/j.cub.2010.01.059)
14. Blazquez, M. A., Ahn, J. H. & Weigel, D. 2003 A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat. Genet. 33, 168-171. (doi:10.1038/ng1085)
15. Bohlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A. M., Jansson, S., Strauss, S. H. & Nilsson, O. 2006 CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312, 1040-1043. (doi:10.1126/science.1126038)
16. Borchert, R., Robertson, K., Schwartz, M. D. & Williams-Linera, G. 2005 Phenology of temperate trees in tropical climates. Int. J. Biometeorol. 50, 57-65. (doi:10. 1007/s00484-005-0261-7)
17. Boss, P. K., Bastow, R. M., Mylne, J. S. & Dean, C. 2004 Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16, S18-S31. (doi:10.1105/tpc.015958)
18. Bradshaw, W. E. & Holzapfel, C. M. 2001 Genetic shift in photoperiodic response correlated with global warming. Proc. Natl Acad. Sci. USA 98, 14 509-14 511. (doi:10. 1073/pnas.241391498)
19. Bradshaw, W. E. & Holzapfel, C. M. 2008 Genetic response to rapid climate change: it's seasonal timing that matters. Mol. Ecol. 17, 157-166. (doi:10.1111/j.1365-294X.2007. 03509.x)
20. Cesaraccio, C., Spano, D., Duce, P. & Snyder, R. L. 2001 An improved model for determining degree-day values from daily temperature data. Int. J. Biometeorol. 45, 161-169.
21. Charles-Edwards, D. A., Doley, D. & Rimmington, G. M. 1986 Modelling plant growth and development. North Ryde, Australia: Academic Press.
22. Chiang, G. C. K., Barua, D., Kramer, E. M., Amasino, R. M. & Donohue, K. 2009 Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 106, 11 661-11 666. (doi:10.1073/pnas.0901367106)
23. Chuine, I. 2010 Why does phenology drive species distribution? Phil. Trans. R. Soc. B 365, 3149-3160. (doi:10. 1098/rstb.2010.0142)
24. Chuine, I. & Beaubien, E. G. 2001 Phenology is a major determinant of tree species range. Ecol. Lett. 4, 500-510. (doi:10.1046/j.1461-0248.2001. 00261.x)
25. Cockram, J., Chiapparino, E., Taylor, S. A., Stamati, K., Donini, P., Laurie, D. A. & O'Sullivan, D. M. 2007a Haplotype analysis of vernalization loci in European barley germplasm reveals novel VRN-H1 alleles and a predominant winter VRN-H1/VRN-H2 multi-locus haplotype. Theor. Appl. Genet. 115, 993-1001. (doi:10.1007/s00122-007-0626-x)
26. Cockram, J., Jones, H., Leigh, F. J., O'Sullivan, D., Powell, W., Laurie, D. A. & Greenland, A. J. 2007b Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. J. Exp. Bot. 58, 1231-1244. (doi:10.1093/jxb/erm042)
27. Cockram, J., Norris, C. & O'Sullivan, D. M. 2009 PCR-based markers diagnostic for spring and winter seasonal growth habit in barley. Crop Sci. 49, 403-410. (doi:10. 2135/cropsci2008.07.0398)
28. Colasanti, J. & Coneva, V. 2009 Mechanisms of floral induction in grasses: something borrowed, something new. Plant Physiol. 149, 56-62. (doi:10.1104/pp. 108. 130500)
29. Cooper, M. & Hammer, G. (eds) 1996 Plant adaptation and crop improvement. Wallingford, CT: CAB International.
30. Cooper, M., Podlich, D. W. & Smith, O. S. 2005. Gene-tophenotype models and complex trait genetics. Aust. J. Agric. Res. 56, 895-918. (doi:10.1071/AR05154)
31. Corbesier, L. et al. 2007 FT protein movement contributes to long-distance signaling in floral induction in Arabidopsis. Science 316, 1030-1033. (doi:10.1126/science. 1141752)
32. Damascos, M. A., Prado, C. & Ronquim, C. C. 2005 Bud composition, branching patterns and leaf phenology in Cerrado woody species. Ann. Bot. 96, 1075-1084. (doi:10.1093/aob/mci258)
33. Davis, M. B., Shaw, R. G. & Etterson, J. R. 2005 Evolutionary responses to changing climate. Ecology 86, 1704-1714. (doi:10.1890/03-0788)
34. Davis, C. C., Willis, C. G., Primack, R. B. & Miller-Rushing, A. J. 2010 The importance of phylogeny to the study of phenological response to global climate change. Phil. Trans. R. Soc. B 365, 3201-3213. (doi:10.1098/rstb. 2010.0130)
35. Delworth, T. L. et al. 2006 GFDL's CM2 global coupled climate models. Part I: formulation and simulation characteristics. J. Climate 19, 643-674. (doi:10.1175/JCLI3629.1)
36. Dingkuhn, M., Kouressy, M., Vaksmann, M., Clerget, B. & Chantereau, J. 2008 A model of sorghum photoperiodism using the concept of threshold-lowering during prolonged appetence. Eur. J. Agron. 28, 74-89. (doi:10.1016/j.eja. 2007.05.005)
37. Dong, Z. S. 2003 Incorporation of genomic information into the simulation of flowering time in Arabidopsis thaliana. Manhattan, KS: Kansas State University.
38. Donohue, K. 2009 Completing the cycle: maternal effects as the missing link in plant life histories. Phil. Trans. R. Soc. B 364, 1059-1074. (doi:10.1098/rstb.2008.0291)
39. Donohue, K., Dorn, L., Griffith, C., Kim, E., Aguilera, A., Polisetty, C. R. & Schmitt, J. 2005 The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution 59, 758-770.
40. Durant, J. M., Hjermann, D. O., Anker-Nilssen, T., Beaugrand, G., Mysterud, A., Pettorelli, N. & Stenseth, N. C. 2005 Timing and abundance as key mechanisms affecting trophic interactions in variable environments. Ecol. Lett. 8, 952-958. (doi:10.1111/j.1461-0248.2005. 00798.x)
41. Engelmann, K. & Purugganan, M. 2006 The molecular evolutionary ecology of plant development: flowering time in Arabidopsis thaliana. Adv. Bot. Res. 44, 507-526. (doi:10.1016/S0065-2296 (06) 44013-1)
42. Finnegan, E. J. & Dennis, E. S. 2007 Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr. Biol. 17, 1978-1983. (doi:10.1016/j.cub.2007.10.026)
43. Fisher, J. I., Richardson, A. D. & Mustard, J. F. 2007 Phenology model from surface meteorology does not capture satellite-based greenup estimations. Global Change Biol. 13, 707-721. (doi:10.1111/j.1365-2486.2006. 01311.x)
44. Fitter, A. H. & Fitter, R. S. R. 2002 Rapid changes in flowering time in British plants. Science 296, 1689-1691. (doi:10.1126/science.1071617)
45. Franks, S. J., Sim, S. & Weis, A. E. 2007 Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc. Natl Acad. Sci. USA 104, 1278-1282. (doi:10.1073/pnas.0608379104)
46. Galiba, G., Vagujfalvi, A., Li, C. X., Soltesz, A. & Dubcovsky, J. 2009 Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci. 176, 12-19. (doi:10.1016/j.plantsci.2008.09.016)
47. GBIF Data Portal, data.gbif.org. Accessed 2009-07-01.
48. Geraldo, N., Baurle, I., Kidou, S., Hu, X. Y. & Dean, C. 2009 FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol. 150, 1611-1618. (doi:10.1104/pp. 109.137448)
49. Granier, C., Massonnet, C., Turc, O., Muller, B., Chenu, K. & Tardieu, F. 2002 Individual leaf development in Arabidopsis thaliana: a stable thermal-time-based programme. Ann. Bot. 89, 595-604. (doi:10.1093/aob/mcf085)
50. Greenup, A., Peacock, W. J., Dennis, E. S. & Trevaskis, B. 2009 The molecular biology of seasonal floweringresponses in Arabidopsis and the cereals. Ann. Bot. 103, 1165-1172. (doi:10.1093/aob/mcp063)
51. Griffith, T. M. & Watson, M. A. 2006 Is evolution necessary for range expansion? Manipulating reproductive timing of a weedy annual transplanted beyond its range. Am. Nat. 167, 153-164.
52. Gyllenstrand, N., Clapham, D., Kallman, T. & Lagercrantz, U. 2007 A Norway spruce FLOWERING LOCUS T homolog is implicated in control of growth rhythm in conifers. Plant Physiol. 144, 248-257. (doi:10.1104/pp. 107.095802)
53. Hall, D., Luquez, V., Garcia, V. M., St Onge, K. R., Jansson, S. & Ingvarsson, P. K. 2007 Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits. Evolution 61, 2849-2860. (doi:10.1111/j.1558-5646. 2007.00230.x)
54. Ham, J. M. 2004 Useful equations in micrometeorology. In Micrometeorology of agricultural systems (eds J. L. Hatfield & J. M. Baker). Madison, WI: ASA-CSSA-SSSA.
55. Hammer, G. L., Cooper, M., Tardieu, F., Welch, S. M., Walsh, B., van Eeuwijk, F., Chapman, S. & Podlich, D. 2006 Models for navigating biological complexity in breeding improved crop plants. Trends Plant Sci. 11, 587-593. (doi:10.1016/j.tplants.2006.10.006)
56. Harrington, C. A., Gould, P. J. & St. Clair, J. B. 2010 Modeling the effects of winter environment on dormancy release of Douglas-fir. For. Ecol. Manage. 259, 798-808. (doi:10.1016/j.foreco.2009.06.018)
57. Hayama, R. & Coupland, G. 2004 The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol. 135, 677-684. (doi:10. 1104/pp. 104.042614)
58. Hayama, R., Yokoi, S., Tamaki, S., Yano, M. & Shimamoto, K. 2003 Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422, 719-722. (doi:10.1038/nature01549)
59. Hedman, H., Kallman, T. & Lagercrantz, U. 2009 Early evolution of the MFT-like gene family in plants. Plant Mol. Biol. 70, 359-369. (doi:10.1007/s11103-009-9478-x)
60. Henderson, I. R., Shindo, C. & Dean, C. 2003 The need for winter in the switch to flowering. Annu. Rev. Genet. 37, 371-392. (doi:10.1146/annurev. genet.37.110801.142640)
61. Heschel, M. S., Butler, C. M., Barua, D., Chiang, G. C. K., Wheeler, A., Sharrock, R. A., Whitelam, G. C. & Donohue, K. 2008 New roles of phytochromes during seed germination. Int. J. Plant Sci. 169, 531-540. (doi:10.1086/528753)
62. Hoffmann, M. H. 2002 Biogeography of Arabidopsis thaliana (L.) Heynh. (Brassicaceae). J. Biogeog. 29, 125-134. (doi:10.1046/j.1365-2699.2002.00647.x)
63. Hoffmann, M. H., 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 Oecol. Int. J. Ecol. 28, 181-187. (doi:10. 1016/j.actao.2005.03. 010)
64. Holdsworth, M. J., Bentsink, L. & Soppe, W. J. J. 2008 Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol. 179, 33-54. (doi:10.1111/j.1469-8137.2008.02437.x)
65. Howe, G. T., Aitken, S. N., Neale, D. B., Jermstad, K. D., Wheeler, N. C. & Chen, T. H. H. 2003 From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can. J. Bot. Rev. 81, 1247-1266. (doi:10.1139/b03-141)
66. Huang, X., Schmitt, J., Dorn, L., Griffith, C., Effgen, S., Takao, S., Koornneef, M. & Donohue, K. 2010 The earliest stages of adaptation in an experimental plant population: strong selection on QTLS for seed dormancy. Mol. Ecol. 19, 1335-1351. (doi:10.1111/j.1365-294x. 2010.04557.x)
67. Ibáñez, I., Primack, R. B., Miller-Rushing, A. J., Ellwood, E., Higuchi, H., Lee, S. D., Kobori, H. & Silander, J. A. 2010 Forecasting phenology under global warming. Phil. Trans. R. Soc. B 365, 3247-3260. (doi:10.1098/rstb.2010.0120)
68. Ingvarsson, P. K., Garcia, M. V., Hall, D., Luquez, V. & Jansson, S. 2006 Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 172, 1845-1853. (doi:10.1534/genetics.105.047522)
69. Ingvarsson, P. K., Garcia, M. V., Luquez, V., Hall, D. & Jansson, S. 2008 Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics 178, 2217-2226. (doi:10.1534/genetics.107.082354)
70. Jenkins, J. L., Powell, J. A., Logan, J. A. & Bentz, B. J. 2001 Low seasonal temperatures promote life cycle synchronization. Bull. Math. Biol. 63, 573-595. (doi:10.1006/bulm.2001.0237)
71. Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R. & Dean, C. 2000 Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344-347. (doi:10.1126/science.290. 5490.344)
72. Jones, H. et al. 2008 Population-based resequencing reveals that the flowering time adaptation of cultivated barley originated east of the fertile crescent. Mol. Biol. Evol. 25, 2211-2219. (doi:10.1093/molbev/msn167)
73. Joost, S., Bonin, A., Bruford, M., Després, L., Conord, C., Erhardt, G. & Taberlet, P. 2007 A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Mol. Ecol. 16, 3955-3969. (doi:10.1111/j.1365-294X. 2007.03442.x)
74. Kikuchi, R., Kawahigashi, H., Ando, T., Tonooka, T. & Handa, H. 2009 Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering. Plant Physiol. 149, 1341-1353. (doi:10.1104/pp. 108.132134)
75. Kim, S. Y., He, Y. H., Jacob, Y., Noh, Y. S., Michaels, S. & Amasino, R. 2005 Establishment of the vernalizationresponsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17, 3301-3310. (doi:10.1105/tpc.105.034645)
76. Kim, S. Y. et al. 2007 Delayed flowering time in Arabidopsis and Brassica rapa by the overexpression of FLOWERING LOCUS C (FLC) homologs isolated from Chinese cabbage (Brassica rapa L. ssp pekinensis). Plant Cell Rep. 26, 327-336. (doi:10.1007/s00299-006-0243-1)
77. Kobayashi, Y. & Weigel, D. 2007 Move on up, it's time for change-mobile signals controlling photoperioddependent flowering. Gen. Dev 21, 2371-2384.
78. Koornneef, M., Hanhart, C. J. & Vanderveen, J. H. 1991 A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol. Gen. Genet. 229, 57-66.
79. Koornneef, M., Alonso-Blanco, C. & Vreugdenhil, D. 2004 Naturally occurring genetic variation in Arabidopsis thaliana. Annu. Rev. Plant Biol. 55, 141-172. (doi:10.1146/annurev. arplant.55.031903.141605)
80. Korves, T. M., Schmid, K. J., Caicedo, A. L., Mays, C., Stinchcombe, J. R., Purugganan, M. D. & Schmitt, J. 2007 Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. Am. Nat. 169, E141-E157.
81. Landsberg, H. 1941 Physical climatology. State College, PA: Gray Printing Company.
82. Laurie, D. A., Griffiths, S., Dunford, R. P., Christodoulou, V., Taylor, S. A., Cockram, J., Beales, J. & Turner, A. 2004 Comparative genetic approaches to the identification of flowering time genes in temperate cereals. Field Crops Res. 90, 87-99. (doi:10.1016/j.fcr.2004.07.007)
83. Lee, I. & Amasino, R. M. 1995 Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the Frigida gene. Plant Physiol. 108, 157-162.
84. Lehikoinen, E., Sparks, T. H. & Zalakevicius, M. 2004 Arrival and departure dates. In The effects of climate change on birds (eds A. P. Moller, W. Fielder & P. Berthold), pp. 1-31. New York, NY: Academic Press Ltd.
85. Lempe, J., Balasubramanian, S., Sureshkumar, S., Singh, A., Schmid, M. & Weigel, D. 2005 Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet. 1, 109-118.
86. Li, Y., Roycewicz, P., Smith, E. & Borevitz, J. O. 2006 Genetics of local adaptation in the laboratory: flowering time quantitative trait loci under geographic and seasonal conditions in Arabidopsis. PLoS ONE 1, e105. (doi:10. 1371/journal.pone.0000105)
87. Li, Z. G., Reighard, G. L., Abbott, A. G. & Bielenberg, D. G. 2009 Dormancy-associated MADS genes from the EVG locus of peach Prunus persica (L.) Batsch have distinct seasonal and photoperiodic expression patterns. J. Exp. Bot. 60, 3521-3530. (doi:10.1093/jxb/erp195)
88. Lifschitz, E., Eviatar, T., Rozman, A., Shalit, A., Goldshmidt, A., Amsellem, Z., Alvarez, J. P. & Eshed, Y. 2006 The tomato FTortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl Acad. Sci. USA 103, 6398-6403. (doi:10.1073/pnas.0601620103)
89. Linacre, E. 1992 Climate, data and resources: a reference and guide. New York, NY: Routledge.
90. Lister, D. L. et al. 2009 Latitudinal variation in a photoperiod response gene in European barley: insight into the dynamics of agricultural spread from 'historic' specimens. J. Archaeol. Sci. 36, 1092-1098. (doi:10.1016/j. jas.2008.12.012)
91. Locke, J. C. W., Southern, M. M., Kozma-Bognar, L., Hibberd, V., Brown, P. E., Turner, M. S. & Millar, A. J. 2005 Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol. Syst. Biol. 1. (doi:10.1038/msb4100018)
92. Locke, J. C. W., Kozma-Bognar, L., Gould, P. D., Feher, B., Kevei, E., Nagy, F., Turner, M. S., Hall, A. & Millar, A. J. 2006 Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol. Syst. Biol. 2, 6.
93. Luquez, V., Hall, D., Albrectsen, B. R., Karlsson, J., Ingvarsson, P. & Jansson, S. 2008 Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genet. Genomes 4, 279-292. (doi:10.1007/s11295-007-0108-y)
94. Malmberg, R. L., Held, S., Waits, A. & Mauricio, R. 2005 Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field and in the greenhouse. Genetics 171, 2013-2027. (doi:10.1534/genetics. 105.046078)
95. Maloof, J. N. et al. 2001 Natural variation in light sensitivity of Arabidopsis. Nat. Genet. 29, 441-446. (doi:10.1038/ng777)
96. Menzel, A. et al. 2006a European phenological response to climate change matches the warming pattern. Global Change Biol. 12, 1969-1976. (doi:10.1111/j.1365-2486. 2006.01193.x)
97. Menzel, A., Von Vopelius, J., Estrella, N., Schleip, C. & Dose, V. 2006b Farmers' annual activities are not tracking the speed of climate change. Climate Res. 32, 201-207.
98. Michael, T. P., Salome, P. A. & McClung, C. R. 2003 Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc. Natl Acad. Sci. USA 100, 6878-6883. (doi:10. 1073/pnas.1131995100)
99. Michaels, S. D., He, Y. H., Scortecci, K. C. & Amasino, R. M. 2003 Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summerannual flowering behavior in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 10 102-10 107. (doi:10.1073/pnas. 1531467100)
100. Michaels, S. D., Bezerra, I. C. & Amasino, R. M. 2004 FRIGIDA-related genes are required for the winterannual habit in Arabidopsis. Proc. Natl Acad. Sci. USA 101, 3281-3285. (doi:10.1073/pnas.0306778101)
101. Miller-Rushing, A. J. & Primack, R. B. 2008 Global warming and flowering times in Thoreau's concord: a community perspective. Ecology 89, 332-341. (doi:10. 1890/07-0068.1)
102. Miller-Rushing, A. J., Primack, R. B., Primack, D. & Mukunda, S. 2006 Photographs and herbarium specimens as tools to document phenological changes in response to global warming. Am. J. Bot. 93, 1667-1674. (doi:10.3732/ajb.93. 11.1667)
103. Mizoguchi, T. et al. 2005 Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17, 2255-2270. (doi:10.1105/tpc. 105.033464)
104. Moller, A. P., Rubolini, D. & Lehikoinen, E. 2008 Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc. Natl Acad. Sci. USA 105, 16 195-16 200. (doi:10. 1073/pnas.0803825105)
105. Montesinos, A., Tonsor, S. J., Alonso-Blanco, C. & Xavier Pico, F. 2009 Demographic and genetic patterns of variation among populations of Arabidopsis thaliana from contrasting native environments. PLoS ONE 4, no. e7213. (doi:10.1371/journal.pone.0007213)
106. Moon, J., Lee, H., Kim, M. & Lee, I. 2005 Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol. 46, 292-299. (doi:10.1093/pcp/pci024)
107. Morin, X., Augspurger, C. & Chuine, I. 2007 Process-based modeling of species' distributions: what limits temperate tree species' range boundaries? Ecology 88, 2280-2291. (doi:10.1890/06-1591.1)
108. Nemoto, Y., Kisaka, M., Fuse, T., Yano, M. & Ogihara, Y. 2003 Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice. Plant J. 36, 82-93. (doi:10. 1046/j.1365-313X.2003.01859.x)
109. NOAA GFDL (US Department of Commerce/NOAA/Geophysical Fluid Dynamics Laboratory) 2004 IPCC Fourth Assessment and US CCSP Projects. Princeton, NJ, USA. See http://data1.gfdl.noaa.gov/CM2. X/references/ (Accessed).
110. Parmesan, C. 2006 Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637-669. (doi:10.1146/annurev. ecolsys.37.091305. 110100)
111. Parmesan, C. & Yohe, G. 2003 A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37-42. (doi:10.1038/nature01286)
112. Petipas, R. H., Wilczek, A. M., Schmitt, J. & Savolainen, O. In preparation. Demography of Arabidopsis thaliana at its northern range limit in Finland.
113. Post, E. & Forchhammer, M. C. 2008 Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Phil. Trans. R. Soc. B 363, 2369-2375. (doi:10.1098/rstb.2007.2207)
114. Post, E. et al. 2009 Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355-1358. (doi:10.1126/science. 1173113)
115. Powell, J. A. & Logan, J. A. 2005 Insect seasonality: circle map analysis of temperature-driven life cycles. Theor. Popul. Biol. 67, 161-179. (doi:10.1016/j.tpb.2004.10.001)
116. Primack, D., Imbres, C., Primack, R. B., Miller-Rushing, A. J. & Del Tredici, P. 2004 Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. Am. J. Bot. 91, 1260-1264. (doi:10.3732/ajb.91.8. 1260)
117. Primack, R. B., Ibanez, I., Higuchi, H., Lee, S. D., Miller-Rushing, A. J., Wilson, A. M. & Silander, J. A. 2009 Spatial and interspecific variability in phenological responses to warming temperatures. Biol. Conserv. 142, 2569-2577. (doi:10.1016/j.biocon. 2009.06.003)
118. Ray, P. M. & Alexander, W. E. 1966 Photoperiodic adaptation to latitude in Xanthium strumarium. Am. J. Bot. 53, 806-816. (doi:10.2307/2440183)
119. Reeves, P. A., He, Y. H., Schmitz, R. J., Amasino, R. M., Panella, L. W. & Richards, C. M. 2007 Evolutionary conservation of the FLOWERING LOCUS C-mediated vernalization response: evidence from the sugar beet (Beta vulgaris). Genetics 176, 295-307. (doi:10.1534/genetics.106.069336)
120. Roetzer, T., Wittenzeller, M., Haeckel, H. & Nekovar, J. 2000 Phenology in central Europe-differences and trends of spring phenophases in urban and rural areas. Int. J. Biometeorol. 44, 60-66. (doi:10.1007/ s004840000062)
121. Rosenzweig, C. et al. 2008 Attributing physical and biological impacts to anthropogenic climate change. Nature 453, 353-357. (doi:10.1038/nature06937)
122. Salazar, J. D., Saithong, T., Brown, P. E., Foreman, J., Locke, J. C. W., Halliday, K. J., Carre, I. A., Rand
123. D. A. & Millar, A. J. 2009 Prediction of photoperiodic regulators from quantitative gene circuit models. Cell 139, 1170-1179. (doi:10.1016/j.cell. 2009.11.029)
124. Samis, K. E., Heath, K. D. & Stinchcombe, J. R. 2008 Discordant longitudinal clines in flowering time and phytochrome c in Arabidopsis thaliana. Evolution 62, 2971-2983. (doi:10.1111/j.1558-5646.2008.00484.x)
125. Savolainen, O., Pyhajarvi, T. & Knurr, T. 2007 Gene flow and local adaptation in trees. Annu. Rev. Ecol. Evol. Syst. 38, 595-619. (doi:10.1146/annurev. ecolsys.38. 091206.095646)
126. Scarcelli, N. & Kover, P. X. 2009 Standing genetic variation in FRIGIDA mediates experimental evolution of flowering time in Arabidopsis. Mol. Ecol. 18, 2039-2049. (doi:10.1111/j.1365-294X.2009.04145.x)
127. Scarcelli, N., Cheverud, J. M., Schaal, B. A. & Kover, P. X. 2007 Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. Proc. Natl Acad. Sci. USA 104, 16 986-16 991. (doi:10.1073/pnas. 0708209104)
128. Schaber, J. & Badeck, F. W. 2002 Evaluation of methods for the combination of phenological time series and outlier detection. Tree Physiol. 22, 973-982.
129. Schlappi, M. R. 2006 FRIGIDA LIKE 2 is a functional allele in Landsberg erecta and compensates for a nonsense allele of FRIGIDA LIKE 1. Plant Physiol. 142, 1728-1738. (doi:10.1104/pp. 106.085571)
130. Schmid, K., Torjek, O., Meyer, R., Schmuths, H., Hoffmann, M. H. & Altmann, T. 2006 Evidence for a large-scale population structure of Arabidopsis thaliana from genome-wide single nucleotide polymorphism markers. Theor. Appl. Genet. 112, 1104-1114. (doi:10.1007/s00122-006-0212-7)
131. Schmitz, R. J., Sung, S. & Amasino, R. M. 2008 Histone arginine methylation is required for vernalization-induced epigenetic silencing of FLC in winter-annual Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 105, 411-416. (doi:10.1073/pnas.0710423104)
132. Schmuths, H., Bachmann, K., Weber, W. E., Horres, R. & Hoffmann, M. H. 2006 Effects of preconditioning and temperature during germination of 73 natural accessions of Arabidopsis thaliana. Ann. Bot. 97, 623-634. (doi:10. 1093/aob/mcl012)
133. Searle, I., He, Y. H., Turck, F., Vincent, C., Fornara, F., Krober, S., Amasino, R. A. & Coupland, G. 2006 The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20, 898-912. (doi:10.1101/gad. 373506)
134. Sellers, W. D. 1965 Physical climatology. Chicago, IL: University of Chicago Press.
135. Serrano, G., Herrera-Palau, R., Romero, J. M., Serrano, A., Coupland, G. & Valverde, F. 2009 Chlamydomonas CONSTANS and the evolution of plant photoperiodic signaling. Curr. Biol. 19, 359-368. (doi:10.1016/j.cub. 2009.01.044)
136. Sheldon, C. C., Hills, M. J., Lister, C., Dean, C., Dennis, E. S. & Peacock, W. J. 2008 Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc. Natl Acad. Sci. USA 105, 2214-2219. (doi:10.1073/pnas.0711453105)
137. Shindo, C., Aranzana, M. J., Lister, C., Baxter, C., Nicholls, C., Nordborg, M. & Dean, C. 2005 Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol. 138, 1163-1173. (doi:10.1104/pp. 105.061309)
138. 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 Dev. 20, 3079-3083. (doi:10.1101/gad. 405306)
139. Singer, M. C. & Parmesan, C. 2010 Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Phil. Trans. R. Soc. B 365, 3161-3176. (doi:10.1098/rstb. 2010.0144)
140. Springer, C. J., Orozco, R. A., Kelly, J. K. & Ward, J. K. 2008 Elevated CO2 influences the expression of floralinitiation genes in Arabidopsis thaliana. New Phytol. 178, 63-67. (doi:10.1111/j.1469-8137.2008.02387.x)
141. Stenoien, H. K., Fenster, C. B., Kuittinen, H. & Savolainen, O. 2002 Quantifying latitudinal clines to light responses in natural populations of Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 89, 1604-1608. (doi:10.3732/ajb.89.10.1604)
142. Stinchcombe, J. R., Caicedo, A. L., Hopkins, R., Mays, C., Boyd, E. W., Purugganan, M. D. & Schmitt, J. 2005 Vernalization sensitivity in Arabidopsis thaliana (Brassicaceae): the effects of latitude and FLC variation. Am. J. Bot. 92, 1701-1707. (doi:10.3732/ajb.92.10.1701)
143. Sung, S. B. & Amasino, R. M. 2004 Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159-164. (doi:10.1038/nature02195)
144. Tamaki, S., Matsuo, S., Wong, H. L., Yokoi, S. & Shimamoto, K. 2007 Hd3a protein is a mobile flowering signal in rice. Science 316, 1033-1036. (doi:10.1126/science.1141753)
145. Thompson, L. 1994 The spatiotemporal effects of nitrogen and litter on the population-dynamics of Arabidopsis thaliana. J. Ecol. 82, 63-68.
146. Trevaskis, B., Hemming, M. N., Dennis, E. S. & Peacock, W. J. 2007 The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci. 12, 352-357. (doi:10.1016/j.tplants.2007.06.010)
147. Turck, F., Fornara, F. & Coupland, G. 2008 Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573-594. (doi:10.1146/annurev. arplant.59.032607.092755)
148. Turner, A., Beales, J., Faure, S., Dunford, R. P. & Laurie, D. A. 2005 The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310, 1031-1034. (doi:10.1126/science.1117619)
149. UK National Weather Service 2009 See http://www.metoffice.gov. uk/climate/uk/. (Accessed 10 January 2009)
150. van Buskirk, J., Mulvihill, R. S. & Leberman, R. C. 2009 Variable shifts in spring and autumn migration phenology in North American songbirds associated with climate change. Global Change Biol. 15, 760-771. (doi:10.1111/j.1365-2486.2008.01751.x)
151. van der Jeugd, H. P., Eichhorn, G., Litvin, K. E., Stahl, J., Larsson, K., van der Graaf, A. J. & Drent, R. H. 2009 Keeping up with early springs: rapid range expansion in an avian herbivore incurs a mismatch between reproductive timing and food supply. Global Change Biol. 15, 1057-1071. (doi:10.1111/j.1365-2486.2008.01804.x)
152. Walther, G. R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J. C., Fromentin, J. M., Hoegh-Guldberg, O. & Bairlein, F. 2002 Ecological responses to recent climate change. Nature 416, 389-395. (doi:10.1038/416389a)
153. Wang, R. H., Farrona, S., Vincent, C., Joecker, A., Schoof, H., Turck, F., Alonso-Blanco, C., Coupland, G. & Albani, M. C. 2009 PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423-427. (doi:10.1038/ nature07988)
154. Weinig, C., Ungerer, M. C., Dorn, L. A., Kane, N. C., Toyonaga, Y., Halldorsdottir, S. S., Mackay, T. F. C., Purugganan, M. D. & Schmitt, J. 2002 Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162, 1875-1884.
155. Welch, S. M., Roe, J. L. & Dong, Z. S. 2003 A genetic neural network model of flowering time control in Arabidopsis thaliana. Agron. J. 95, 71-81.
156. Welch, S. M., Dong, Z. S., Roe, J. L. & Das, S. 2005 Flowering time control: gene network modelling and the link to quantitative genetics. Aust. J. Agric. Res. 56, 919-936. (doi:10.1071/AR05155)
157. Wilczek, A. M. et al. 2009 Effects of genetic perturbation on seasonal life-history plasticity. Science 323, 930-934. (doi:10.1126/science.1165826)
158. Wilkie, J. D., Sedgley, M. & Olesen, T. 2008 Regulation of floral initiation in horticultural trees. J. Exp. Bot. 59, 3215-3228. (doi:10.1093/jxb/ern188)
159. Williams, J. W. & Jackson, S. T. 2007 Novel climates, no-analog communities, and ecological surprises. Front. Ecol. Environ. 5, 475-482. (doi:10.1890/070037)
160. Williams, J. W., Jackson, S. T. & Kutzbacht, J. E. 2007 Projected distributions of novel and disappearing climates by 2100 AD. Proc. Natl Acad. Sci. USA 104, 5738-5742. (doi:10.1073/pnas.0606292104)
161. Willis, C. G., Ruhfel, B., Primack, R. B., Miller-Rushing, A. J. & Davis, C. C. 2008 Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proc. Natl Acad. Sci. USA 105, 17 029-17 033. (doi:10. 1073/pnas.0806446105)
162. Worland, A. J., Borner, A., Korzun, V., Li, W. M., Petrovic, S. & Sayers, E. J. 1998 The influence of photoperiod genes on the adaptability of European winter wheats (Reprinted from Wheat: Prospects for global improvement, 1998). Euphytica 100, 385-394. (doi:10.1023/A:1018327700985)
163. Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M. & Araki, T. 2005 TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol. 46, 1175-1189. (doi:10.1093/pcp/pci151)
164. Zeilinger, M. N., Farre, E. M., Taylor, S. R., Kay, S. A. & Doyle, F. J. 2006 A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Mol. Syst. Biol. 2, 13.
165. Zhang, X. Y., Friedl, M. A. & Schaaf, C. B. 2006 Global vegetation phenology from moderate resolution imaging spectroradiometer (MODIS): evaluation of global patterns and comparison with in situ measurements. J. Geophys. Res. Biogeosci. 111, G04017.
166. Zhang, Q. Z. et al. 2008 Association of the circadian rhythmic expression of GmCRY1a with a latitudinal cline in photoperiodic flowering of soybean. Proc. Natl Acad. Sci. USA 105, 21 028-21 033. (doi:10.1073/pnas. 0810585105)
167. Zhang, J. Z., Li, Z. M., Mei, L., Yao, J. L. & Hu, C. G. 2009 PtFLC homolog from trifoliate orange (Poncirus trifoliata) is regulated by alternative splicing and experiences seasonal fluctuation in expression level. Planta 229, 847-859. (doi:10.1007/s00425-008-0885-z)
168. Zobell, O., Coupland, G. & Reiss, B. 2005 The family of CONSTANS-like genes in Physcomitrella patens. Plant Biol. 7, 266-275. (doi:10.1055/s-2005- 865621)