Adaptation to seasonality and the winter freeze

Frontiers in Plant Science

Volumn 4, Issue JUN, 2013, Pages

  Preston, Jill C ^a   Sandve, Simen R ^b  

^a UNIVERSITY OF VERMONT   (United States)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Cold acclimation; Endodormancy; Freezing tolerance; Plant adaptation; Seasonality; Vernalization responsiveness

Indexed keywords

EID: 84892462923     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00167     Document Type: Review

References (261)

1. Adhikari, K. N., Buirchell, B. J., and Sweetingham, M. W. (2012). Length of vernalization period affects flowering time in three lupin species. Plant Breed. 131, 631-636. doi: 10.1111/j.1439-0523.2012.01996.x
2. Adrian, J., Torti, S., and Turck, F. (2009). From decision to commitment: the molecular memory of flowering. Mol. Plant 2, 628-642. doi: 10.1093/mp/ssp031
3. Agarwal, P. K., and Jha, B. (2010). Transcription factors in plants and ABA dependent and independent abiotic stress signaling. Biol. Plant. 54, 201-212. doi: 10.1007/s10535-010-0038-7
4. Alessandro, M. S., Galmarini, C. R., Iorizzo, M., and Simon, P. W. (2013). Molecular mapping of vernalization requirement and fertility restoration genes in carrot. Theor. Appl. Genet. 126, 415-423. doi: 10.1007/s00122-012-1989-1
5. Alonso, A., Queiroz, C. S., and Magalhaes, A. C. (1997). Chilling stress leads to increased cell membrane rigidity in roots of coffee (Coffea arabica L.) seedlings. Biochim. Biophys. Acta 1323, 75-84. doi: 10.1016/S0005-2736(96)00177-0
6. Alonso-Peral, M., Oliver, S. N., Casao, M. C., Greenup, A. A., and Trevaskis, B. (2011). The promoter of the cereal VERNALIZATION1 gene is sufficient for transcriptional induction by prolonged cold. PLoS ONE 6:e29456. doi: 10.1371/journal.pone.0029456
7. Amasino, R. (2010). Arabidopsis: a rich harvest 10 years after completion of the genome sequence. Plant J. 61, 1001-1013. doi: 10.1111/j.1365-313X.2010.04148.x
8. Améglio, T., Cochard, H., and Ewers, F. W. (2001). Stem diameter variations and cold hardiness in walnut trees. J. Exp. Bot. 52, 2135-2142. doi: 10.1093/jexbot/52.364.2135
9. Andersen, J. R., Jensen, L. B., Asp, T., and Lubberstedt, T. (2006). Vernalization response in perennial ryegrass (Lolium perenne L.) and wheat (Triticum monococcum) VRN1 and rice (Oryza sativa) Hd1. Plant Mol. Biol. 60, 481-494. doi: 10.1007/s11103-005-4815-1
10. Andreini, L., Viti, R., Bartolini, S., Ruiz, D., Egea, J., and Campoy, J. A. (2012). The relationship between xylem differentiation and dormancy evolution in apricot flower buds (Prunus armeniaca L.): the influence of environmental conditions in two Mediterranean areas. Trees Struct. Funct. 26, 919-928. doi: 10.1007/s00468-011-0668-1
11. Andres, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639. doi: 10.1038/nrg3291
12. Angel, A., Song, J., Dean, C., and Howard, M. (2011). A polycomb-based switch underlying quantitative epigenetic memory. Nature 476, 105-109. doi: 10.1038/nature10241
13. Aro, E. M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., et al. (2005). Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56, 347-356. doi: 10.1093/jxb/eri041
14. Aro, E. M., Virgin, I., and Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage, and turnover. Biochim. Biophys. Acta 1143, 113-134. doi: 10.1016/0005-2728(93)90134-2
15. Asante, D. K. A., Yakovlev, I. A., Fossdal, C. G., Holefors, A., Opseth, L., Olsen, J. E., et al. (2011). Gene expression changes during short day induced terminal bud formation in Norway spruce. Plant Cell Environ. 34, 332-346. doi: 10.1111/j.1365-3040.2010.02247.x
16. Badawi, M., Reddy, Y. V., Agharbaoui, Z., Tominaga, Y., Danyluk, J., Sarhan, F., et al. (2008). Structure and functional analysis of wheat ICE (inducer of CBF expression) Genes. Plant Cell Physiol. 49, 1237-1249. doi: 10.1093/pcp/pcn100
17. Balasubramanian, S., Sureshkumar, S., Agawal, M., Michael, T. P., Wessinger, C., Maloof, J. N., et al. (2006). The PHYTOCHROME C photoreceptor mediates natural variation in flowering and growth responsiveness in Arabidopsis thaliana. Nat. Genet. 38, 71-715. doi: 10.1038/ng1818
18. Ballerini, E. S., and Kramer, E. M. (2011). Environmental and molecular analysis of the floral transition in the lower eudicot Aquilegia formosa. Evodevo 2, 4. doi: 10.1186/2041-9139-2-4
19. Bascuñán-Godoy, L., Sanhueza, C., Cuba, M., Zuniga, G. E., Corcuera, L. J., and Bravo, L. A. (2012). Cold-acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis Kunt Bartl (Caryophyllaceae). BMC Plant Biol. 12:114. doi: 10.1186/1471-2229-12-114
20. Becker, A., and Theissen, G. (2003). The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29, 464-489. doi: 10.1016/S1055-7903(03)00207-0
21. Bhyan, S. B., Minami, A., Kaneko, Y., Suzuki, S., Arakawa, K., Sakata, Y., et al. (2012). Cold acclimation in the moss Physcomitrella patens involves abscisic acid-dependent signaling. J. Plant Physiol. 169, 137-145. doi: 10.1016/j.jplph.2011.08.004
22. Biasi, L. A., de Carvalho, R. I. N., and Zannette, F. (2010). Dormancy dynamics of grape and kiwi tree buds in a region of low chilling occurrence. Rev. Bras. Frutic. 32, 1244-1249. doi: 10.1590/S0100-29452010005000118
23. Bilavcik, A., Zamecnik, J., Grospietsch, M., Faltus, M., and Jadrna, P. (2012). Dormancy development during cold hardening of in vitro cultured Malus domestica Borkh. plants in relation to their frost resistance and cryotolerance. Trees Struct. Funct. 26, 1181-1192. doi: 10.1007/s00468-012-0694-7
24. Bond, D. M., Dennis, E. S., and Finnegan, E. J. (2011). The low temperature response pathways for cold acclimation and vernalization are independent. Plant Cell Environ. 34, 1737-1748. doi: 10.1111/j.1365-3040.2011.02370.x
25. Bouché, N., Scharlat, A., Snedden, W., Bouchez, D., and Fromm, H. (2002). A novel family of calmodulin-binding transcription activators in multicellular organisms. J. Biol. Chem. 277, 21851-21861. doi: 10.1074/jbc.M200268200
26. Bradshaw, A. D. (1972). Some evolutionary consequences of being a plant. Evol. Biol. 5, 25-47. doi: 10.1007/978-1-4757-0256-9_2
27. Briggs, D., and Walters, S. M. (1997). Plant Variation and Evolution. Cambridge: Cambridge University Press.
28. Byard, S., Wisniewski, M., Li, J., and Karlson, D. (2010). Interspecific analysis of xylem freezing responses in Acerand Betula. HortScience 45, 165-168.
29. Caffarra, A., Donnelly, A., Chuine, I., and Jones, M. B. (2011). Modelling the timing of Betula pubescens budburst. I. Temperature and photoperiod: a conceptual model. Clim. Res. 46, 147-157. doi: 10.3354/BR00980
30. Campbell, R. K., and Sugano, A. I. (1979). Genecology of bud-burst phenology in Douglas-fir: response to flushing temperature and chilling. Bot. Gaz. 140, 223-231. doi: 10.1086/337079
31. Campoy, J. A., and Egea, D. R. J. (2011). Dormancy in temperate fruit trees in a global warming context. Sci. Hortic. (Amsterdam) 130, 357-372. doi: 10.1016/j.scienta.2011.07.011
32. Campoy, J. A., Ruiz, D., Cook, N. G., Allderman, L., and Egea, J. (2011). High temperatures and time to budbreak in low chill apricot 'Palsteyn'. Towards a better understanding of chill and heat requirements fulfillment. Sci. Hortic. (Amsterdam) 129, 649-655. doi: 10.1016/j.scienta.2011.05.008
33. Capicciotti, C. J., Leclere, M., Perras, F. A., Bryce, D. L., Paulin, H., Harden, J., et al. (2012). Potent inhibition of ice recrystallization by low molecular weight carbohydrate-based surfactants and hydrogelators. Chem. Sci. 3, 1408-1416. doi: 10.1039/c2sc00885h
34. Carvallo, M. A., Pino, M. T., Jeknic, Z., Zou, C., Doherty, C. J., Shiu, S. H., et al. (2011). A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. J. Exp. Bot. 62, 3807-3819. doi: 10.1093/jxb/err066
35. Catalá, R., Medina, J., and Salina, J. (2011). Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 16475-16480. doi: 10.1073/pnas.1107161108
36. Cave, R. L., Birch, C. J., Hammer, G. L., Erwin, G. E., and Johnston, M. E. (2011). Juvenility and flowering of Brunonia australis (Goodeniaceae) and Calandrinia sp. (Portulacaceae) in relation to vernalization and daylength. Ann. Bot. 108, 215-220. doi: 10.1093/aob/mBR116
37. Cavendar-Bares, J., Cortes, P., Rambal, S., Joffre, R., Miles, B., and Rocheteau, A. (2005). Summer and winter sensitivity of leaves and xylem to minimum freezing temperatures: a comparison of co-occurring Mediterranean oaks that differ in leaf lifespan. New Phytol. 168, 597-612. doi: 10.1111/j.1469-8137.2005.01555.x
38. Charrier, G., Bonhomme, M., Lacointe, A., and Ameglio, T. (2011). Are budburst dates, dormancy and cold acclimation in walnut trees (Juglans regia L.) under mainly genotypic or environmental control? Int. J. Biometeorol. 55, 763-774. doi: 10.1007/s00484-011-0470-1
39. Chen, T. H., and Gusta, L. V. (1983). Abscisic acid-induced freezing resistance in cultured plant cells. Plant Physiol. 73, 71-75. doi: 10.1104/pp.73.1.71
40. Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B. H., Hong, X., Agarwal, M., et al. (2003). ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 17, 1043-1054. doi: 10.1101/gad.1077503
41. Chouard, P. (1960). Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. 11, 191-238. doi: 10.1146/annurev.pp.11.060160.001203
42. Chuine, I., Aitken, S. N., and Ying, C. C. (2001). Temperature thresholds of shoot elongation in provenances of Pinus contorta. Can. J. For. Res. 31, 1444-1455. doi: 10.1139/x01-072
43. Clayton, W. D., and Renvoize, S. A. (1986). Genera Graminum: Grasses of the World. Kew Bulletin Additional Series XIII. Kew: Royal Botanic Gardens.
44. Cook, B. I., Wolkovich, E. M., and Parmesan, C. (2012). Divergent responses to spring and winter warming drive community level flowering trends. Proc. Natl. Acad. Sci. U.S.A. 109, 9000-9005. doi: 10.1073/pnas.1118364109
45. Coustham, V., Li, P., Strange, A., Lister, C., Song, J., and Dean, C. (2012). Quantitative modulation of polycomb silencing underlies natural variation in vernalization. Science 337, 584-587. doi: 10.1126/science.1221881
46. Cuevas, J. C., Lopez-Cobollo, R., Alcazar, R., Zarza, X., Koncz, C., Altabella, T., et al. (2008). Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol. 148, 1094-1105. doi: 10.1104/pp.108.122945
47. Dallaire, S., Houde, M., Gagne, Y., Saini, H. S., Boileau, S., Chevrier, N., et al. (1994). ABA and low temperature induce freezing tolerance via distinct regulatory pathways in wheat. Plant Cell Physiol. 35, 1-9.
48. Dall'Osto, L., Caffarri, S., and Bassi, R. (2005). A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17, 1217-1232. doi: 10.1105/ tpc.104.030601
49. Davis, J. I., and Soreng, R. J. (2008). A phylogenetic analysis of the grasses (Poaceae), with attention to subfamily Pooideae and structural features of the plastid and nuclear genomes, including an intron loss in GBSSI. Aliso 23, 335-348.
50. De la Rosa, R., Rallo, L., and Rapoport, H. F. (2000). Olive floral bud growth and starch content during winter rest and spring budbreak. HortScience 35, 1223-1227.
51. Dhillion, T., Pearce, S. P., Stockinger, E. J., Distelfeld, A., Li, C., Knox, A. K., et al. (2010). Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 connection. Plant Physiol. 153, 1846-1858. doi: 10.1104/pp.110.159079
52. Diaz-Riquelme, J., Grimplet, J., Martinez-Zapater, J. M., and Carmona, M. J. (2012). Transcriptome variation along bud development in grapevine (Vitis vinifera L.). BMC Plant Biol. 12:181. doi: 10.1186/1471-2229-12-181 doi: 10.1186/1471-2229-12-181
53. Distelfeld, A., Li, C., and Dubcovsky, J. (2009). Regulation of flowering in temperate cereals. Curr. Opin. Plant Biol. 12, 178-184. doi: 10.1016/j.pbi.2008.12.010
54. Dogramaci, M., Horvath, D. P., Christoffers, M. J., and Anderson, J. V. (2011). Dehydration and vernalization treatments identify overlapping molecular networks impacting endodormancy maintenance in leafy spurge crown buds. Funct. Integr. Genomics 11, 611-626. doi: 10.1007/s10142-011-0239-y
55. Doherty, C. J., Van Buskirk, H. A., Myers, S. J., and Thomashow, M. F. (2009). Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21, 972-984. doi: 10.1105/ tpc.108.063958
56. Domagalska, M. A., and Leyser, O. (2011). Signal integration in the control of shoot branching. Nat. Rev. Mol. Cell Biol. 12, 211-221. doi: 10.1038/nrm3088
57. Domínguez, T., Hernández, M. L., Pennycooke, J. C., Jiménez, P., Martínez-Rivas, J. M., Sanz, C., et al. (2010). Increasing omega-3 desaturase expression in tomato results in altered aroma profile and enhanced resistance to cold stress. Plant Physiol. 153, 655-665. doi: 10.1104/pp.110.154815
58. Dong, C. H., Hu, X., Tang, W., Zheng, X., Kim, Y. S., Lee, B. H., et al. (2006). A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol. Cell. Biol. 26, 9533-9543. doi: 10.1128/MCB.01063-06
59. Donoghue, M. J. (2008). A phylogenetic perspective on the distribution of plant diversity. Proc. Natl. Acad. Sci. U.S.A. 105, 11549-11555. doi: 10.1073/pnas.0801962105
60. Doucet, C. J., Byass, L., Elias, L., Worrall, D., Smallwood, M., and Bowles, D. J. (2000). Distribution and characterization of recrystallization inhibitor activity in plant and lichen species from the UK and maritime Antarctic. Cryobiology 40, 218-227. doi: 10.1006/cryo.2000.2241
61. Doust, A. N. (2007). Grass architecture: genetic and environmental control of branching. Curr. Opin. Plant Biol. 10, 1-5. doi: 10.1016/j.pbi.2006.11.015
62. Edwards, E. J., and Smith, S. A. (2010). Phylogenetic analyses reveal the shady history of C4 grasses. Proc. Natl. Acad. Sci. U.S.A. 107, 2532-2537. doi: 10.1073/pnas.0909672107
63. El-Din El-Assal, S., Alonso-Blanco, C., Peeters, A. J., Raz, V., and Koorneef, M. (2001). A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat. Genet. 29, 435-440. doi: 10.1038/ng767
64. Erez, A., and Couvillon, G. A. (1987). Characterization of the influence of moderate temperatures on rest completion in peach. J. Am. Soc. Hortic. Sci. 112, 677-680.
65. Fausey, B. A., and Cameron, A. C. (2007). Differing vernalization responses of Veronica spicata 'Red Fox' and Laurentia axillaris. J. Am. Soc. Hortic. Sci. 132, 751-757.
66. Faust, M., Liu, D., Wang, S. Y., and Stutte, G. W. (1995). Involvement of apical dormancy in winter dormancy of apple buds. Acta Hortic. 395, 47-56.
67. Feng, X. M., Zhao, Q., Zhao, L. L., Qiao, Y., Xie, X. B., Li, H. F., et al. (2012). The cold-induced basic helix-loop-helix transcription factor gene MdClbHLH1 encodes and ICE-like protein in apple. BMC Plant Biol. 12:22. doi: 10.1186/1471-2229-12-22
68. Finch-Savage, W. E., and Leubner-Metzger, G. (2006). Seed dormancy and the control of germination. New Phytol. 171, 501-523. doi: 10.1111/j.1469-8137.2006.01787.x
69. Fine, P. V. A., and Ree, R. H. (2006). Evidence for a time-integrated species-area effect on the latitudinal gradient in tree diversity. Am. Nat. 168, 796-804. doi: 10.1086/508635
70. Fornara, F., Panigrahi, K. C., Gissot, L., Sauerbrunn, N., Rühl, M., Jarillo, J. A., et al. (2009). Arabidopsis DOF transcription factors act redundantly with CONSTANS protein in photoperiodic flowering. Science 303, 1003-1006. doi: 10.1016/j.devcel.2009.06.015
71. Fowler, S., and Thomashow, M. F. (2002). Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14, 1675-1690. doi: 10.1105/tpc.003483
72. Fowler, S. G., Cook, D., and Thomashow, M. F. (2005). Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 137, 961-968. doi: 10.1104/pp.104.058354
73. Franks, S. J., Sim, S., and Weis, A. E. (2007). Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc. Natl. Acad. Sci. U.S.A. 104, 1278-1282. doi: 10.1073/pnas.0608379104
74. Friedman, J., and Willis, J. H. (2013). Major QTLs for critical photoperiod and vernalization underlie extensive variation in flowering time in the Mimulus guttatus species complex. New Phytol. doi: 10.1111/nph.12260 [Epub ahead of print].
75. Fu, D., Szucs, P., Yan, L., Helguera, M., Skinner, J. S., von Zitzewitz, J., et al. (2005). Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol. Genet. Genomics 273, 54-65. doi: 10.1007/s00438-004-1095-4
76. Fujikawa, S., Jitsuyama, Y., and Kuroda, K. (1999). Determination of the role of cold acclimation-induced diverse changes in plant cells from the viewpoint of avoidance of freezing injury. J. Plant Res. 112, 237-244. doi: 10.1007/PL00013880
77. Ghelardini, L., Santini, A., Black-Samuelsson, S., Myking, T., and Falusi, M. (2010). Bud dormancy release in elm (Ulmus spp.) clones-a case study of photoperiod and temperature responses. Tree Physiol. 30, 264-274. doi: 10.1093/treephys/tpp110
78. Gilmour, S. J., Hajela, R. K., and Thomashow, M. F. (1988). Cold acclimation in Arabidopsis thaliana. Plant Physiol. 87, 745-750. doi: 10.1104/pp.87.3.745
79. Gould, S. J., and Vrba, E. S. (1982). Exaptation: a missing term in the science of form. Paleobiology 8, 4-15.
80. Gray, G. R., Chauvin, L. P., Sarhan, F., and Huner, N. P. A. (1997). Cold acclimation and freezing tolerance (a complex interaction of light and temperature). Plant Physiol. 114, 467-474.
81. Greenup, A. G., Sasani, S., Oliver, S. N., Talbot, M. J., Dennis, E. S., Hemming, M. N., et al. (2010). ODDSOC2 is a MADS-box floral repressor that is down-regulated by vernalization in temperate cereals. Plant Physiol. 153, 1062-1073. doi: 10.1104/pp.109.152488
82. Greenup, A. G., Sasani, S., Oliver, S. N., Walford, S. A., Millar, A. A., and Trevaskis, B. (2011). Transcriptome analysis of the vernalization response in barley (Hordeum vulgare) seedlings. PLoS ONE 6:e17900. doi: 10.1371/journal.pone.0017900
83. Griffith, M., and Yaish, M. W. F. (2004). Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci. 9, 399-405. doi: 10.1016/j.tplants.2004.06.007
84. Gusta, L., Trischuk, R., and Weiser, C. J. (2005). Plant cold acclimation: the role of abscisic acid. J. Plant Growth Regul. 24, 308-318. doi: 10.1007/s00344-005-0079-x
85. Guzy-Wrobelska, J., Filek, M., Kaliciak, A., Szarejko, I., Machackova, I., Krekule, J., et al. (2013). Vernalization and photoperiod-related changes in the DNA methylation state in winter and spring rapeseed. Acta Physiol. Plant. 35, 817-827. doi: 10.1007/s11738-012-1126-4
86. Gyllenstrand, N., Clapham, D., Kallman, T., and 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
87. Hammel, H. T. (1967). Freezing of xylem sap without cavitation. Plant Physiol. 42, 55-66. doi: 10.1104/pp.42.1.55
88. Hanin, M., Brini, F., Ebel, C., Toda, Y., Takeda, S., and Masmoudi, K. (2011). Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal. Behav. 6, 1503-1509. doi: 10.4161/psb.6.10.17088
89. Hemming, M. N., Fieg, S., Peacock, J., Dennis, E. A., and Trevaskis, B. (2009). Regions associated with repression of the barley (Hordeum vulgare) VERNALIZATION1 gene are not required for cold induction. Mol. Genet. Genomics 282, 107-117. doi: 10.1007/s00438-009-0449-3
90. Hemming, M. N., Peacock, W. J., Dennis, E. S., and Trevaskis, B. (2008). Low-temperature and daylength cue are integrated to regulated FLOWERING LOCUS T in barley. Plant Physiol. 147, 1-12. doi: 10.1104/pp.108.116418
91. Hemming, M. N., and Trevaskis, B. (2011). Make hay when the sun shines: the role of MADS-box genes in temperature-dependant seasonal flowering responses. Plant Sci. 180, 447-453. doi: 10.1016/j.plantsci.2010.12.001
92. Heo, J. B., and Sung, S. (2010). Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79. doi: 10.1126/science.1197349
93. Hetherington, S. E., He, J., and Smillie, R. M. (1989). Photoinhibition at low temperature in chilling-sensitive and-resistant plants. Plant Physiol. 90, 1609-1615. doi: 10.1104/pp.90.4.1609
94. Hisano, H., Kanazawa, A., Kawakami, A., Yoshida, M., Shimamoto, Y., and Yamada, T. (2004). Transgenic perennial ryegrass plants expressing wheat fructosyltransferase genes accumulate increased amounts of fructan and acquire increased tolerance on a cellular level to freezing. Plant Sci. 167, 861-868. doi: 10.1016/j.plantsci.2004.05.037
95. Horvath, D. P., Chao, W. S., Suttle, J. C., Thimmapuram, J., and Anderson, J. V. (2008). Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions in leafy spurge (Euphorbia esula L.). BMC Genomics 9:536. doi: 10.1186/1471-2164-9-536
96. Hoth, S., Morgante, M., Sanchez, J. P., Hanafey, M. K., Tingey, S. V., and Chua, N. H. (2002). Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J. Cell Sci. 115, 4891-4900. doi: 10.1242/jcs.00175
97. Howe, G. T., Aitken, S. N., Neale, D. B., Jermstad, K. D., Wheeler, N. C., and Chen, T. H. H. (2003). From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can. J. Bot. 81, 1247-1266. doi: 10.1139/b03-141
98. Hsu, C.-Y., Adams, J. P., Kim, H., No, K., Ma, C., Strauss, S. H., et al. (2011). FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc. Natl. Acad. Sci. U.S.A. 108, 10756-10771. doi: 10.1073/pnas.1104713108
99. Humphreys, A. M., and Linder, H. P. (2013). Evidence for recent evolution of cold tolerance in grasses suggests current distribution is not limited by (low) temperature. New Phytol. 198, 1261-1273. doi: 10.1111/ nph.12244.
100. Huner, N., Oguist, G., Hurry, V., Krol, M., Falk, S., and Griffith, M. (1993). Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth. Res. 37, 19-39. doi: 10.1007/ BF02185436
101. Ietswaart, R., Wu, Z., and Dean, C. (2012). Flowering time control: another window to the connection between antisense RNA and chromatin. Trends Genet. 28, 445-453. doi: 10.1016/j.tig.2012.06.002
102. Imaizumi, T. (2010). Arabidopsis circadian clock and photoperiodism: time to think about location. Curr. Opin. Plant Biol. 13, 83-89. doi: 10.1016/j.pbi.2009.09.007
103. Ivany, L. C., Patterson, W. P., and Lohmann, K. C. (2000). Cooler winters as a possible cause of mass extinctions at the Eocene/Oligocene boundary. Nature 407, 887-890. doi: 10.1038/35038044
104. Jang, S., Marchal, V., Panigrahi, K. C., Wenkel, S., Soppe, W., Deng, X. W., et al. (2008). Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiod flowering response. EMBO J. 27, 1277-1288. doi: 10.1038/emboj.2008.68
105. Janská, A., Aprile, A., Zámečnik, J., Cattivelli, L., and Ovesná, J. (2011). Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. Funct. Integr. Genomics 11, 307-325. doi: 10.1007/s10142-011-0213-8
106. Jones, H. G., Hillis, R. M., Gordon, S. L., and Brennan, R. M. (2013). An approach to the determination of winter chill requirements for different Ribes cultivars. Plant Biol. 15, 18-27. doi: 10.1111/j.1438-8677.2012.00590.x
107. Joon Seo, P., Jung, J. H., Park, M. J., Lee, K., and Park, C. M. (2013). Controlled turnover of CONSTANS protein by the HOS1 E3 ligase regulates floral transition at low temperatures. Plant Signal. Behav. 8, e23780. doi: 10.4161/psb.23780
108. Kalberer, S. R., Arora, R., Leyva-Estrada, N., and Krebs, S. L. (2007). Cold hardiness of floral buds of deciduous azaleas: dehardening, rehardening, and endodormancy in late winter. J. Am. Soc. Hortic. Sci. 132, 73-79.
109. Kane, N. A., Danyluk, J., Tardif, G., Ouellet, F., Laliberte, J.-F., Limin, A. E., et al. (2005). TaVRT-2, a member of the StMADS-11 clade of flowering repressors, is regulated by vernalization and photoperiod in wheat. Plant Physiol. 138, 2354-2363. doi: 10.1104/pp.105.061762
110. Karlberg, A., Bako, L., and Bhalerao, R. P. (2011). Short day-mediated cessation of growth requires the downregulation of AINTEGUMENTALIKE1 transcription factor in hybrid aspen. PLoS Genet. 7:e1002361. doi: 10.1371/journal.pgen.1002361
111. Karlgren, A., Gyllenstrand, N., Kallman, T., Sundstrom, J. F., Moore, D., Lascoux, M., et al. (2011). Evolution of the PEBP gene family in plants: functional diversification of seed plant evolution. Plant Physiol. 156, 1967-1977. doi: 10.1104/pp.111.176206
112. Karlson, D. T., Xiang, Q. Y., Stirm, V. E., Shirazi, A. M., and Ashworth, E. N. (2004). Phylogenetic analyses in cornus substantiate ancestry of xylem supercooling freezing behavior and reveal lineage of desiccation related proteins. Plant Physiol. 135, 1654-1665. doi: 10.1104/pp.103.037473
113. Kawamata, M., Nishida, E., Ohara, H., Ohkawa, K., and Matsui, H. (2002). Changes in the intensity of bud dormancy and internal compositions of current shoot in fig. J. Jpn. Soc. Hortic. Sci. 71, 177-182. doi: 10.2503/jjshs.71.177
114. Kaymak, H. C., and Guvenc, I. (2010). The influence of vernalization time and day length on flower induction of radish (Raphanus sativus L.) under controlled and field conditions. Turk. J. Agric. For. 34, 401-413. doi: 10.3906/tar-0901-14
115. Khodakovskaya, M., McAvoy, R., Peters, J., Wu, H., and Li, Y. (2006). Enhanced cold tolerance in transgenic tobacco expressing a chloroplast 3 fatty acid desaturase gene under the control of a cold-inducible promoter. Planta 223, 1090-1100. doi: 10.1007/s00425-005-0161-4
116. Kim, D.-H., Doyle, M. R., Sung, S., and Amasino, R. M. (2009). Vernalization: winter and the timing of flowering in plants. Annu. Rev. Cell Dev. Biol. 25, 277-299. doi: 10.1146/annurev.cellbio. 042308.113411
117. King, R. W., and Heide, O. M. (2009). Seasonal flowering and evolution: the heritage from Charles Darwin. Funct. Plant Biol. 36, 1027-1036. doi: 10.1071/FP09170
118. Klintenäs, M., Pin, P. A., Benlloch, R., Ingvarsson, P. K., and Nilsson, O. (2012). Analysis of conifer FLOWERING LOCUS T/TERMINAL-FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytol. 196, 1260-1273. doi: 10.1111/j.1469-8137.2012.04332.x
119. Knight, H., Mugford, S. G., Ulker, B., Gao, D., Thorlby, G., and Knight, M. R. (2009). Identification of SFR6, a key component in cold acclimation acting post-translationally on CBF function. Plant J. 58, 97-108. doi: 10.1111/j.1365-313X. 2008.03763.x
120. Knight, H., Zarka, D. G., Okamoto, H., Thomashow, M. F., and Knight, M. R. (2004). Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol. 135, 1710-1707. doi: 10.1104/pp.104.043562
121. Kobayashi, F., Takumi, S., and Handa, H. (2008). "Characterization of ABA sensitivity in mutants with altered abiotic stress tolerance in common wheat, " in Proceedings of the 11th International Wheat Genetics Symposium, Vol. 3 (Sydney: Sydney University Press), 907-909.
122. Kramer, P. J., and Kozlowski, T. T. (1979). Physiology of Woody Plants. New York: Academic Press.
123. Krause, G. H. (1988). Photoinhibition of photosynthesis. an evaluation of damaging and protective mechanisms. Physiol. Plant. 74, 566-574. doi: 10.1111/j.1399-3054.1988.tb02020.x
124. Krug, H. (1991). Investigations of changes in growth-activity of rhubarb (Rheum-rhaponticum × rhabarbarum) and consequences for production and forcing. Gartenbauwissenschaft 56, 93-98.
125. Kubota, S., Momose, H., Yoneda, K., and Koshioka, M. (2010). Lavandula × intermedia is a vernalization type plant. Jpn. Agric. Res. Q. 44, 67-72. doi: 10.6090/jarq.44.67
126. Lang, G. A., Early, J. D., Martin, G. C., and Darnell, R. L. (1987). Endodormancy, paradormancy, and ecodormancy-physiological terminology and classification for dormancy research. HortScience 22, 371-377.
127. Larcher, W. (2005). Climatic constraints drive the evolution of low temperature resistance in woody plants. J. Agric. Meterol. 61, 189-202. doi: 10.2480/agrmet.61.189
128. Latham, R. E., and Ricklefs, R. E. (1993). Global patterns of tree species richness in moist forests: energy-diversity theory does not account for variation in species richness. Oikos 67, 325-333. doi: 10.2307/3545479
129. Lee, B.-H., Henderson, D. A., and Zhu, J.-K. (2005). The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17, 3155-3175. doi: 10.1105/tpc.105.035568
130. Lee, B.-H., Lee, H., Xiong, L., and Zhu, J.-K. (2002). A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14, 1235-1251. doi: 10.1105/tpc.010433
131. Lee, C. M., and Thomashow, M. F. (2012). Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 109, 15054-15059. doi: 10.1073/pnas.1211295109
132. Lee, J. H., Yoo, S. J., Park, S. H., Hwang, I., Lee, J. S., and Ahn, J. H. (2007). Role of SVP in the control of flowering time by ambient temperatures in Arabidopsis. Genes Dev. 21, 397-402. doi: 10.1101/gad.1518407
133. Lenahan, O. M., Graves, W. R., and Arora, R. (2010). Cold-hardiness and deacclimation of Styrax americanus from three provenances. HortScience 45, 1819-1823.
134. Lewandowska-Sabat, A. M., Winge, P., Fjellheim, S., Dorum, G., Bones, A. M., and Rognli, O. A. (2012). Genome wide transcriptional profiling of acclimation to photoperiod in high-latitude accessions of Arabidopsis thaliana. Plant Sci. 186, 143-155. doi: 10.1016/j.plantsci.2011.10.009
135. Li, W., Li, M., Zhang, W., Welti, R., and Wang, X. (2004). The plasma membrane-bound phospholipase D[delta] enhances freezing tolerance in Arabidopsis thaliana. Nat. Biotechnol. 22, 427-433. doi: 10.1038/nbt949
136. Lin, M., Starman, T. W., Wang, Y. T., Niu, G. H., and Cothren, J. T. (2011). Deferring flowering of nobile dendrobium hybrids by holding plants under low temperature after vernalization. Sci. Hortic. 130, 869-873. doi: 10.1016/j.scienta.2011.08.027
137. Lin, S.-I., Wang, J.-G., Poon, S.-Y., Su, C.-L., Wang, S.-S., and Chiou, T.-J. (2005). Differential regulation of FLOWERING LOCUS C expression by vernalization in cabbage and Arabidopsis. Plant Physiol. 137, 1037-1048. doi: 10.1104/pp. 104.058974
138. Litt, A., and Irish, V. F. (2003). Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for evolution of floral development. Genetics 165, 821-833.
139. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., et al. (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391-1406.
140. Llorente, F., Oliveros, J. C., Martinez-Zapater, J. M., and Salinas, J. (2000). A freezing-sensitive mutant of Arabidopsis, frs1, is a new aba3 allele. Planta 211, 648-655. doi: 10.1007/s004250000340
141. Loik, M. E., Still, C. J., Huxman, T. E., and Harte, J. (2004). In situ photosynthetic freezing tolerance for plants exposed to a global warming manipulation in the Rocky Mountains, Colorado, USA. New Phytol. 162, 331-341. doi: 10.1111/j.1469-8137.2004.01002.x
142. Lopez, R. G., and Runkle, E. S. (2006). Temperature and photoperiod regulate flowering of potted Miltoniopsis orchids. Hortic. Sci. 41, 593-597.
143. Mantyla, E., Lang, V., and Palva, E. T. (1995). Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LT178 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol. 107, 141-148.
144. Maruyama, K., Takeda, M., Kidokoro, S., Yamada, K., Sakuma, Y., Urano, K., et al. (2009). Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol. 150, 1972-1980. doi: 10.1104/pp.109.135327
145. Mas, P., Kim, W. Y., Somers, D. E., and Kay, S. A. (2003). Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567-570. doi: 10.1038/nature02163
146. Meideros, J. A. S., and Pockman, W. T. (2011). Drought increases freezing tolerance of both leaves and xylem of Larrea tridentata. Plant Cell Environ. 34, 43-51. doi: 10.1111/j.1365-3040.2010.02224.x
147. Melis, A. (1999). Photosystem II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci. 4, 130-135. doi: 10.1016/S1360-1385(99)01387-4
148. Méndez-Vigo, B., Picó, F. X., Ramiro, M., Martínez-Zapater, J. M., and Alonso-Blanco, C. (2011). Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis. Plant Physiol. 157, 1942-1955. doi: 10.1104/pp.111.183426
149. Mewes, S., and Pank, F. (2007). Influence of cold temperature and light on the flower induction of thyme (Thymus vulgaris L.). Eur. J. Hortic. Sci. 72, 80-84.
150. Meyer, K., Keil, M., and Naldrett, M. J. (1999). A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Lett. 447, 171-178. doi: 10.1016/S0014-5793(99)00280-X
151. Michaels, S. D., and Amasino, R. M. (1999). FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956. doi: 10.1105/tpc.11.5.949
152. Michaels, S. D., and Amasino, R. (2001). Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous-pathway mutations, but not responsiveness to vernalization. Plant Cell 13, 935-941. doi: 10.1105/tpc.13.4.935
153. Moellering, E. R., Muthan, B., and Benning, C. (2010). Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330, 226-228. doi: 10.1126/science.1191803
154. Mojtahedi, N., Masuda, J., Hiramatstu, M., Nguyen, T. L. H., and Okubo, H. (2013). Role of temperature in dormancy induction and release in one-year-old seedlings of Lilium longiflorum populations. J. Jpn. Soc. Hortic. Sci. 82, 63-68. doi: 10.2503/jjshs1.82.63
155. Mutasa-Gottgens, E. S., Joshi, A., Holmes, H. F., Hedden, P., and Gottgens, B. (2012). A new RNAseq-based reference transcriptome for sugar beet and its application in transcriptome-scale analysis of vernalization and gibberellin responses. BMC Genomics 13:99. doi: 10.1186/1471-2164-13-99
156. Nagao, M., Matsui, K., and Uemura, M. (2008). Klebsormidium flaccidum, a charophycean green alga, exhibits cold acclimation that is closely associated with compatible solute accumulation and ultrastructural changes. Plant Cell Environ. 31, 872-885. doi: 10.1111/j.1365-3040. 2008.01804.x
157. Nakano, Y., Kawashima, H., Kinoshita, T., Yoshikawa, H., and Hisamatsu, T. (2011). Characterization of FLC, SOC1 and FT homologs in Eustoma grandiflorum: effects of vernalization and post-vernalization conditions on flowering and gene expression. Physiol. Plant. 141, 383-393. doi: 10.1111/j.1399-3054.2011.01447.x
158. Naor, A., Flaishman, M., Stern, R., Moshe, A., and Erez, A. (2003). Temperature effects on dormancy completion of vegetative buds in apple. J Am. Soc. Hortic. Sci. 128, 636-641.
159. National Research Council. (2010). Advancing the Science of Climate Change. Washington, DC: The National Academies Press.
160. Nishitani, C., Saito, T., Ubi, B. E., Moriguchi, T., Saito, T., Yamamoto, T., et al. (2012). Transcriptome analysis of Pyrus pyrifolia leaf buds during transition from endodormancy to ecodormancy. Sci. Hortic. 147, 49-55. doi: 10.1016/j.scienta.2012.09.001
161. Novillo, F., Alonso, J. M., Ecker, J. R., and Salinas, J. (2004). CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101, 3985-3990. doi: 10.1073/pnas.0303029101
162. Offord, C. A. (2011). Pushed to the limit: consequences of climate change for the Araucariaceae: a relictual rain forest family. Ann. Bot. 108, 347-357. doi: 10.1093/aob/mBR135
163. Oliver, S. N., Finnegan, E. J., Dennis, E. S., Peacock, W. J., and Trevaskis, B. (2009). Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc. Natl. Acad. Sci. U.S.A. 106, 8336-8391. doi: 10.1073/pnas.0903566106
164. Örvar, B. L., Sangwan, V., Omann, F., and Dhindsa, R. S. (2000). Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J. 23, 785-794. doi: 10.1046/j.1365-313x.2000.00845.x
165. Padhye, S. R., and Cameron, A. C. (2008). Dianthus gratianopolitanus Vill. 'Bath's Pink' has a near-obligate vernalization requirement. HortScience 43, 346-349.
166. Padhye, S. R., and Cameron, A. C. (2009). Vernalization responses of campanula 'Birch Hybrid'. J. Am. Soc. Hortic. Sci. 134, 497-504.
167. Pandey, N., Ranjan, A., Pant, P., Tripathi, R. K., Ateek, F., Pandley, H. P., et al. (2013). CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14, 216. doi: 10.1186/1471-2164-14-216
168. Pennycooke, J., Cheng, H., Roberts, S., Yang, Q., Rhee, S., and Stockinger, E. J. (2008). The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements. Plant Mol. Biol. 67, 483-497. doi: 10.1007/s11103-008-9333-5
169. Pietsch, G. M., Anderson, N. O., and Li, P. H. (2009). Cold tolerance and short day acclimation in perennial Gaura coccinea and G. Drummondii. Sci. Hortic. 120, 418-425. doi: 10.1016/j.scienta.2008.11.030
170. Pin, P. A., Benlloch, R., Bonnet, D., Wremerth-Weich, E., Kraft, T., Gielen, J. J. L., et al. (2010). An antagonistic pair of FT homologs mediates the control of flowering in sugar beet. Science 330, 1397-1400. doi: 10.1126/science.1197004
171. Pin, P. A., Zhang, W., Vogt, S. H., Dally, N., Buttner, B., Schulze-Buxloh, G., et al. (2012). The role of a pseudo-response regulator gene in life cycle adaptation and domestication of beet. Curr. Biol. 22, 1095-1101. doi: 10.1016/j.cub.2012.04.007
172. Prasil, I. T., Prasilova, P., and Pankova, K. (2004). Relationship among vernalization, shoot apex development and frost tolerance in wheat. Ann. Bot. 94, 413-418. doi: 10.1093/aob/mch158
173. Preston, J. C., and Kellogg, E. A. (2006). Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics 174, 421-437. doi: 10.1534/genetics.106.057125
174. Preston, J. C., and Kellogg, E. A. (2008). Discrete developmental roles for temperate cereal grass VERNALIZATION 1/FRUITFUL-like genes in flowering competency and the transition to flowering. Plant Physiol. 146, 265-276. doi: 10.1104/pp.107.109561
175. Rantasen, M., and Palonen, P. (2010). Hot water treatment released endodormancy but reduced number of flowers in potted red raspberry plants. HortScience 45, 894-898.
176. Rapacz, M., Gasior, D., Zwierzyowski, Z., Lesniewska-Bocianowska, A., Humphreys, M. W., and Gay, A. P. (2004). Changes in cold tolerance and the mechanisms of acclimation of photosystem II to cold hardening generated by anther culture of Festuca pratensis × Lolium multiflorum cultivars. New Phytol. 162, 105-114. doi: 10.1111/j.1469-8137.2004.01024.x
177. Rapacz, M., and Markowski, A. (1999). Winter hardiness, frost resistance and vernalization requirement of European winter oilseed rape (Brassica napus var. oleifera) cultivars within the last 20 years. J. Agron. Crop Sci. 183, 243-253. doi: 10.1046/j.1439-037x.1999.00346.x
178. Ratcliffe, O. J., Kumimoto, R. W., Wong, B. J., and Riechmann, J. L. (2003). Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15, 1159-1169. doi: 10.1105/tpc.009506
179. Ricklefs, R. E. (2005). Historical and ecological dimensions of global patterns in plant diversity. Biol. Skr. 55, 583-603.
180. Ricklefs, R. E., and Renner, S. S. (1994). Species richness within families of flowering plants. Evolution 48, 1619-1636. doi: 10.2307/2410252
181. Rinne, P. L. H., Kaikuranta, P. M., and van der Schoot, C. (2001). The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J. 26, 249-264. doi: 10.1046/j.1365-313X.2001.01022.x
182. Rinne, P. L. H., Welling, A., Vahala, J., Ripel, L., Ruonala, R., Kangasjarvi, J., et al. (2011). Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1, 3-beta-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23, 130-146. doi: 10.1105/tpc.110.081307
183. Rohde, A., and Bhalerao, R. P. (2007). Plant dormancy in the perennial context. Trends Plant Sci. 12, 217-223. doi: 10.1016/j.tplants.2007.03.012
184. Rohde, A., Storme, V., Jorge, V., Gaudet, M., Vitacolonna, N., Fabbrini, F., et al. (2011). Bud set in poplar-genetic dissection of a complex trait in natural and hybrid populations. New Phytol. 189, 106-121. doi: 10.1111/j.1469-8137.2010.03469.x
185. Rohwer, C. L., and Heins, R. A. (2007). Daily light integral, prevernalization photoperiod, and vernalization temperature and duration control flowering of easter cactus. HortScience 42, 1596-1604.
186. Rudi, H., Sandve, S. R., Opseth, L., and Rognli, O. A. (2010). Identification of candidate genes important for frost tolerance in Festuca pratensis Huds. by transcriptional profiling. Plant Sci. 180, 78-85. doi: 10.1016/j.plantsci.2010.07.014
187. Salomé, P. A., and McClung, C. R. (2005). PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell 17, 791-803. doi: 10.1105/tpc.104.029504
188. Samach, A., Onouchi, H., Gold, S. E., Ditta, G. S., Schwarz-Sommer, Z., Yanofsky, M. F., et al. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1616. doi: 10.1126/science.288.5471.1613
189. Samis, K. E., Heath, K. D., and 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
190. Sanchez-Perez, R., Dicenta, F., and Martinez-Gomez, P. (2012). Inheritance of chilling and heat requirements for flowering in almond and QTL analysis. Trees Genet. Genom. 8, 379-389. doi: 10.1007/s11295-011-0448-5
191. Sandve, S. R., and Fjellheim, S. (2010). Did gene family expansions during the Eocene-Oligocene boundary climate cooling play a role in Pooideae adaptation to cool climates? Mol. Ecol. 19, 2075-2088. doi: 10.1111/j.1365-294X.2010.04629.x
192. Sandve, S. R., Kosmala, A., Rudi, H., Fjellheim, S., Rapacz, M., Yamada, T., et al. (2011). Molecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates. Plant Sci. 180, 69-77. doi: 10.1016/j.plantsci.2010.07.011
193. Sandve, S. R., Rudi, H., Asp, T., and Rognli, O. A. (2008). Tracking the evolution of a cold stress associated gene family in cold tolerant grasses. BMC Evol. Biol. 8:245. doi: 10.1186/1471-2148-8-245
194. 2+ influx. Plant J. 27, 1-12. doi: 10.1046/j.1365-313x.2001.01052.x
195. Sasaki, R., Yamane, H., Ooka, T., Jotatsu, H., Kitamura, Y., Akagi, T., et al. (2011). Functional and expressional analyses of PmDAM genes associated with endodormancy in Japanese apricot. Plant Physiol. 157, 485-497. doi: 10.1104/pp.111.181982
196. Saure, M. C. (1985). Dormancy release in deciduous fruit trees. Hortic. Rev. 7, 239-300. doi: 10.1002/9781118060735.ch6
197. Sawa, M., Nusinow, D. A., Kay, S. A., and Imaizumi, T. (2007). FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318, 261-265. doi: 10.1126/ science.1146994
198. Schwartz, C. J., Doyle, M. R., Manzandeda, A. J., Rey, P. J., Mitchell-Olds, T., and Amasino, R. M. (2010). Natural variation of flowering time and vernalization responsiveness in Brachypodium distachyon. Bioenergy Res. 3, 38-46. doi: 10.1007/s12155-009-9069-3
199. Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Krober, S., et al. (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
200. Seo, E., Lee, H., Jeon, J., Park, H., Kim, J., Noh, Y.-S., et al. (2009). Crosstalk between cold response and flowering time in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell 21, 3185-3197. doi: 10.1105/tpc.108.063883
201. Shakirova, F., Allagulova, C., Bezrukova, M., Aval'Baev, A., and Gimalov, F. (2009). The role of endogenous ABA in cold-induced expression of the TADHN dehydrin gene in wheat seedlings. Russ. J. Plant Physiol. 56, 720-723. doi: 10.1134/S1021443709050203
202. Shindo, C., Lister, C., Crevillen, P., Nordborg, M., and 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
203. Shinozaki, K., and Yamaguchi-Shinozaki, K. (2000). Molecular responses to dehydration and low temperatures: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3, 217-223.
204. Sidebottom, C., Buckley, S., Pudney, P., Twigg, S., Jarman, C., Holt, C., et al. (2000). Phytochemistry: heat-stable antifreeze protein from grass. Nature 406, 256. doi: 10.1038/35018639
205. Silim, S. N., and Lavender, D. P. (1994). Seasonal patterns of environmental regulation of frost hardiness in shoots of seedlings of Thuja plicata, Chamaecyparis nootkatensis, and Picea glauca. Can. J. Bot. 72, 309-316. doi: 10.1139/b94-040
206. Skinner, J., Zitzewitz, J., Szucs, P., Marquez-Cedillo, L., Filichkin, T., Amundsen, K., et al. (2005). Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol. Biol. 59, 533-551. doi: 10.1007/s11103-005-2498-2
207. Smith, S. A., Beaulieu, J., Stamatakis, A., and Donoghue, M. J. (2011). Understanding angiosperm diversification using large and small phylogenies. Am. J. Bot. 98, 404-414. doi: 10.3732/ajb.1000481
208. Song, Y. H., Smith, R. H., To, B. J., Millar, A. J., and Imaizumi, T. (2012). FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336, 1045-1049. doi: 10.1126/science.1219644
209. Sperry, J. S., Nichols, K. L., Sullivan, J. E., and Eastlack, S. E. (1994). Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75, 1736-1752. doi: 10.2307/1939633
210. Steponkus, P. L., Uemura, M., Joseph, R. A., Gilmour, S. J., and Thomashow, M. F. (1998). Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 95, 14570-14575. doi: 10.1073/pnas.95.24.14570
211. Stevens, P. F. (2001 onward). Angiosperm Phylogeny Website, Version 12, July 2012 [and more or less continuously updated since].
212. Stickley, C. E., St John, K., Koc, N., Jordan, R. W., Passchier, S., Pearce, R. B., et al. (2009). Evidence for middle Eocene Arctic sea ice from diatoms and ice-rafted debris. Nature 460, 376-379. doi: 10.1038/nature08163
213. Stinchcombe, J. R., Weinig, C., Ungerer, M., Olsen, K. M., Mays, C., Halldorsdottir, S. S., et al. (2004). A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc. Natl. Acad. Sci. U.S.A. 101, 4712-4717. doi: 10.1073/pnas.0306401101
214. Stockinger, E. J., Skinner, J. S., Gardner, K. G., Francia, E., and Pecchioni, N. (2007). Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J. 51, 308-321. doi: 10.1111/j.1365-313X.2007.0141.x
215. Strange, A., Li, P., Lister, C., Anderson, J., Warthmann, N., Shindo, C., et al. (2011). Major-effect alleles at relatively few loci underlie distinct vernalization and flowering variation in Arabidopsis accessions. PLoS ONE 6:e19949. doi: 10.1371/journal.pone.0019949
216. Streck, N. A., and Schuh, M. (2005). Simulating the vernalization response of the "snow queen" lily (Lilium longiflorum Thunb.). Sci. Agric. 62, 117-121. doi: 10.1590/S0103-90162005000200004
217. Sutton, F., Chen, D.-G., Ge, X., and Kenefick, D. (2009). Cbf genes of the Fr-A2 alleles are differentially regulated between long-term cold acclimated crown tissue of freeze-resistant and-susceptible, winter wheat mutant lines. BMC Plant Biol. 9:34. doi: 10.1186/1471-2229-9-34
218. Svendsen, E., Wilsen, R., Stevenson, R., Liu, R. S., and Tanino, K. K. (2007). A molecular marker associated with low-temperature induction of dormancy in red osier dogwood (Cornus sericea). Tree Physiol. 27, 385-397. doi: 10.1093/treephys/27.3.385
219. Svensson, J. T., Crosatti, C., Campoli, C., Bassi, R., Stanca, A. M., Close, T. J., et al. (2006). Transcriptome analysis of cold acclimation in barley albina and xantha mutants. Plant Physiol. 141, 257-270. doi: 10.1104/pp.105.072645
220. Swindell, W. R. (2006). The association among gene expression responses to nine abiotic stress treatments in Arabidopsis thaliana. Genetics 174, 1811-1824. doi: 10.1534/genetics.106.061374
221. Szucs, P., Skinner, J. S., Karsai, I., Cuesta-Marcos, A., Haggard, K. G., Corey, A. E., et al. (2007). Validation of the VRN-H2/VRN-H1 epistatic model in barley reveals that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity. Mol. Genet. Genomics 277, 249-261. doi: 10.1007/s00438-006-0195-8
222. Takahashi, S., and Murata, N. (2008). How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 13, 178-182. doi: 10.1016/j.tplants.2008.01.005
223. Tester, M., and Bacic, A. (2005). Abiotic stress tolerance in grasses. From model plants to crop plants. Plant Physiol. 137, 791-793. doi: 10.1104/pp.104.900138
224. Teutonico, R. A., and Osborn, T. C. (1995). Mapping loci controlling vernalization requirement in Brassica rapa. Theor. Appl. Genet. 91, 1279-1283. doi: 10.1007/BF00220941
225. Thomashow, M. F. (1998). Role of cold-responsive genes in plant freezing tolerance. Plant Physiol. 118, 1-8. doi: 10.1104/pp.118.1.1
226. Thomashow, M. F. (1999). Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571-599. doi: 10.1146/annurev.arplant.50.1.571
227. Trevaskis, B., Hemming, M. N., Dennis, E. S., and Peacock, W. J. (2007a). The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci. 12, 352-357. doi: 10.1016/j.tplants.2007.06.010
228. Trevaskis, B., Tadege, M., Hemming, M. N., Peacock, W. J., Dennis, E. S., and Sheldon, C. (2007b). Short vegetative phase-like MADS-box genes inhibit floral meristem identity in barley. Plant Physiol. 143, 225-235. doi: 10.1104/pp.106.090860
229. Trevaskis, B., Hemming, M. N., Peacock, W. J., and Dennis, E. S. (2006). HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol. 140, 1397-1405. doi: 10.1104/pp.105.073486
230. Uemura, M., Joseph, R. A., and Steponkus, P. L. (1995). Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol. 109, 15-30.
231. Urrutia, M. E., Duman, J. G., and Knight, C. A. (1992). Plant thermal hysteresis proteins. Biochim. Biophys. Acta 1121, 199-206. doi: 10.1016/0167-4838(92)90355-H
232. USGCRP. (2009). Global Climate Change Impacts in the United States. New York: Cambridge University Press.
233. Valluru, R., and Van den Ende, W. (2008). Plant fructans in stress environments: emerging concepts and future prospects. J. Exp. Bot. 59, 2905-2916. doi: 10.1093/jxb/ern164
234. Van Buskirk, H. A., and Thomashow, M. F. (2006). Arabidopsis transcription factors regulating cold acclimation. Physiol. Plant. 126, 72-80. doi: 10.1111/j.1399-3054. 2006.00625.x
235. Vegis, A. (1964). Dormancy in higher plants. Annu. Rev. Plant Physiol. 15, 185-224. doi: 10.1146/annurev.pp. 15.060164.001153
236. Vogel, J. T., Zarka, D. G., Buskirk, H. A. V., Fowler, S. G., and Thomashow, M. F. (2005). Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 41, 195-211. doi: 10.1111/j.1365-313X.2004.02288.x
237. Wang, R., Farrona, S., Vincent, C., Joecker, A., Schoof, H., Turck, F., et al. (2009a). PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423-429. doi: 10.1038/nature07988
238. Wang, H., Moore, M. J., Soltis, P. S., Bell, C. D., Brockington, S. F., Alexandre, R., et al. (2009b). Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc. Natl. Acad. Sci. U.S.A. 106, 3853-3858. doi: 10.1073/pnas.0813376106
239. Webb, C. O., and Donoghue, M. J. (2005). Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5, 181-183. doi: 10.1111/j.1471-8286.2004.00829.x
240. Werner, J. D., Borevitz, J. O., Uhlenhaut, N. H., Ecker, J. R., Chory, J., and Weigel, D. (2005). FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170, 1197-1207. doi: 10.1534/genetics.104.036533
241. Whitman, C. M., and Runkle, E. S. (2012). Determining the flowering requirements of two Aquilegia cultivars. HortScience 47, 1261-1264.
242. Wilson, B. C., Sibley, J. L., and Atland, J. E. (2002). Chilling duration affects foliar budbreak of linden cultivars. Horttechnology 12, 660-662.
243. Winfield, M. O., Lu, C., Wilson, I. D., Coghill, J. A., and Edwards, E. J. (2010). Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol. J. 8, 749-771. doi: 10.1111/j.1467-7652.2010.00536.x
244. Wollenberg, A. C., and Amasino, R. M. (2012). Natural variation in the temperature range permissive for vernalization in accessions of Arabidopsis thaliana. Plant Cell Environ. 35, 2181-2191. doi: 10.1111/j.1365-3040.2012.02548.x
245. Worrall, D., Elias, L., Ashford, D., Smallwood, M., Sidebottom, C., Liliford, P., et al. (1998). A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 282, 115-117. doi: 10.1126/science.282.5386.115
246. Xiong, L. M., Ishitani, M., Lee, H., and Zhu, J.-K. (2001). The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress-and osmotic stress-responsive gene expression. Plant Cell 13, 2063-2083.
247. Xiong, Y., and Fei, S.-Z. (2006). Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.). Planta 224, 878-888. doi: 10.1007/s00425-006-0273-5
248. Yamashino, T., Ito, S., Niwa, Y., Kunihiro, A., Nakamichi, N., and Mizuno, T. (2008). Involvement of Arabidopsisclock-associated pseudo-response regulators in diurnal oscillations of gene expression in the presence of environmental time cues. Plant Cell Physiol. 49, 1839-1850. doi: 10.1093/pcp/pcn165
249. Yan, L., Fu, D., Li, C., Blechl, A., Tranquilli, G., Bonafede, M., et al. (2006). The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Acad. Sci. U.S.A. 103, 19581-19586. doi: 10.1073/pnas.0607142103
250. Yan, L., Loukoianov, A., Blechl, A., Tranquilli, G., Ramakrishna, W., SanMiguel, P., et al. (2004). The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303, 1640-1644. doi: 10.1126/science.1094305
251. Yan, L., Loukoianov, A., Tranquilli, G., Helguera, M., Fahima, T., and Dubcovsky, J. (2003). Positional cloning of the wheat vernalization gene VRN1. Proc. Natl. Acad. Sci. U.S.A. 100, 6263-6268.
252. Yanofsky, M. J., and Kay, S. A. (2002). Molecular basis of seasonal time measurement in Arabidopsis. Nature 419, 308-312. doi: 10.1038/nature00996
253. Yang, J.-S., Wang, R., Meng, J.-J., Bi, Y.-P., Xu, P.-L., Guo, F., et al. (2010). Overexpression of Arabidopsis CBF1 gene in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. J. Plant Physiol. 167, 534-539. doi: 10.1016/j.jplph.2009.11.005
254. Yoo, S. Y., Kim, S. Y., Lee, J. S., and Ahn, J. H. (2007). Control of flowering time and cold response by a NAC-domain protein in Arabidopsis. PLoS ONE 2:e642. doi: 10.1371/journal.pone.0000642
255. Zachos, J., Pagani, M., Sloan, L., Thomas, E., and Billups, K. (2001). Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686-693. doi: 10.1126/science.1059412
256. Zhang, C., Fei, C.-Z., Arora, R., and Hannapel, D. (2010). Ice recrystallization inhibition proteins of perennial ryegrass enhance freezing tolerance. Planta 232, 155-164. doi: 10.1007/s00425-010-1163-4
257. Zhang, J. Z., Li, Z. M., Mei, L., Yao, J. L., and Hu, C. G. (2009). PtFLC homolog from trifoliate orange (Poncirus trifoliata) is regulated by alternative splicing and experiences seasonal fluctuations in expression level. Planta 229, 847-859. doi: 10.1007/s00425-008-0885-z
258. Zhou, Z., Wang, M.-J., Zhao, S.-T., Hu, J.-J., and Lu, M.-Z. (2009). Changes in freezing tolerance in hybrid poplar caused by up-and down-regulation of PtFAD2 gene expression. Transgenic Res. 19, 647-654. doi: 10.1007/s11248-009-9349-x
259. Zlesak, D. C., and Anderson, N. O. (2009). Inheritance of non-obligate vernalization requirement for flowering in Lilium formosanum Wallace. Isr. J. Plant Sci. 57, 315-327. doi: 10.1560/IJPS.57.4.315
260. Zuo, Z., Liu, H., Liu, B., and Lin, C. (2011). Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr. Biol. 21, 841-847. doi: 10.1016/ j.cub.2011.03.048
261. Zuther, E., Shulz, E., Childs, L. H., and Hincha, D. K. (2012). Clinal variation in the non-acclimated and cold-acclimated freezing tolerance of Arabidopsis thaliana accessions. Plant Cell Environ. 35, 1860-1878. doi: 10.1111/j.1365-3040.2012.02522.x