An augmented Arabidopsis phenology model reveals seasonal temperature control of flowering time

New Phytologist

Volumn 194, Issue 3, 2012, Pages 654-665

  Chew, Yin Hoon ^a,b   Wilczek, Amity M ^c   Williams, Mathew ^d   Welch, Stephen M ^e   Schmitt, Johanna ^f   Halliday, Karen J ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b King's Buildings   (United Kingdom)

^c Deep Springs College   (United States)

^d Institute of Geography School of GeoSciences   (United Kingdom)

^e KANSAS STATE UNIVERSITY   (United States)

^f BROWN UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; Crop science; Flowering; Mathematical models; Photoperiodism; Seasonal breeding

Indexed keywords

DICOTYLEDON; FLOWERING; LIGHT EFFECT; MOLECULAR ANALYSIS; NUMERICAL MODEL; PHENOLOGY; PHOTOPERIOD; PLANT BREEDING; SEASONALITY; TEMPERATURE EFFECT;

ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; BREEDING; ENVIRONMENT; FLOWER; GENETICS; LIGHT; MUTATION; PHENOTYPE; PHOTOPERIODICITY; PHYSIOLOGY; RADIATION EXPOSURE; SEASON; TEMPERATURE; TIME;

ARABIDOPSIS; BREEDING; ENVIRONMENT; FLOWERS; LIGHT; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; PHOTOPERIOD; SEASONS; TEMPERATURE; TIME FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84863393543     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04069.x     Document Type: Article

References (92)

1. Amasino R. 2010. Seasonal and developmental timing of flowering. Plant Journal 61: 1001-1013.
2. Arana MV, Marin-de la Rosa N, Maloof JN, Blazquez MA, Alabadi D. 2011. Circadian oscillation of gibberellin signaling in Arabidopsis. Proceedings of the National Academy of Sciences, USA 108: 9292-9297.
3. Bagnall DJ, King RW, Whitelam GC, Boylan MT, Wagner D, Quail PH. 1995. Flowering responses to altered expression of phytochrome in mutants and transgenic lines of Arabidopsis thaliana (L) Heynh. Plant Physiology 108: 1495-1503.
4. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D. 2006. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. Plos Genetics 2: 980-989.
5. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C. 2004. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427: 164-167.
6. Blazquez MA, Ahn JH, Weigel D. 2003. A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nature Genetics 33: 168-171.
7. Cerdan PD, Chory J. 2003. Regulation of flowering time by light quality. Nature 423: 881-885.
8. Chuine I. 2000. A unified model for budburst of trees. Journal of Theoretical Biology 207: 337-347.
9. Corbesier L, Vincent C, Jang SH, Fornara F, Fan QZ, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033.
10. David KM, Armbruster U, Tama N, Putterill J. 2006. Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark. FEBS Letters 580: 1193-1197.
11. 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. European Journal of Agronomy 28: 74-89.
12. Dingkuhn M, Sow A, Samb A, Diack S, Asch F. 1995. Climatic determinants of irrigated rice performance in the Sahel. 1. Photothermal and mcro-climatic responses of flowering. Agricultural Systems 48: 385-410.
13. Dorca-Fornell C, Gregis V, Grandi V, Coupland G, Colombo L, Kater MM. 2011. The Arabidopsis SOC1-like genes AGL42, AGL71 and AGL72 promote flowering in the shoot apical and axillary meristems. The Plant Journal 67: 1006-1017.
14. Easterling DR, Horton B, Jones PD, Peterson TC, Karl TR, Parker DE, Salinger MJ, Razuvayev V, Plummer N, Jamason P et al. 1997. Maximum and minimum temperature trends for the globe. Science 277: 364-367.
15. Edwards KD, Akman OE, Knox K, Lumsden PJ, Thomson AW, Brown PE, Pokhilko A, Kozma-Bognar L, Nagy F, Rand DA et al. 2010. Quantitative analysis of regulatory flexibility under changing environmental conditions. Molecular Systems Biology 6: 424.
16. Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA. 2010. Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS ONE 5: e14101.
17. Estrella N, Sparks TH, Menzel A. 2007. Trends and temperature response in the phenology of crops in Germany. Global Change Biology 13: 1737-1747.
18. Fornara F, Panigrahi KCS, Gissot L, Sauerbrunn N, Ruhl M, Jarillo JA, Coupland G. 2009. Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Developmental Cell 17: 75-86.
19. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Coupland G, Putterill J. 1999. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. Embo Journal 18: 4679-4688.
20. Fowler SG, Cook D, Thomashow ME. 2005. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiology 137: 961-968.
21. Franklin KA, Quail PH. 2010. Phytochrome functions in Arabidopsis development. Journal of Experimental Botany 61: 11-24.
22. Gendall AR, Levy YY, Wilson A, Dean C. 2001. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107: 525-535.
23. Giakountis A, Cremer F, Sim S, Reymond M, Schmitt J, Coupland G. 2010. Distinct patterns of genetic variation alter flowering responses of Arabidopsis accessions to different daylengths. Plant Physiology 152: 177-191.
24. 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. Annals of Botany 89: 595-604.
25. Greb T, Mylne JS, Crevillen P, Geraldo N, An HL, Gendall AR, Dean C. 2007. The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Current Biology 17: 73-78.
26. Halliday KJ, Salter MG, Thingnaes E, Whitelam GC. 2003. Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant Journal 33: 875-885.
27. Halliday KJ, Whitelam GC. 2003. Changes in photoperiod or temperature alter the functional relationships between phytochromes and reveal roles for phyD and phyE. Plant Physiology 131: 1913-1920.
28. Hanano S, Goto K. 2011. Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell 23: 3172-3184.
29. Harrington CA, Gould PJ, St Clair JB. 2010. Modeling the effects of winter environment on dormancy release of Douglas-fir. Forest Ecology and Management 259: 798-808.
30. Heo JB, Sung S. 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76-79.
31. Hepworth SR, Valverde F, Ravenscroft D, Mouradov A, Coupland G. 2002. Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. Embo Journal 21: 4327-4337.
32. Imaizumi T, Kay SA. 2006. Photoperiodic control of flowering: not only by coincidence. Trends in Plant Science 11: 550-558.
33. Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA. 2005. FKF1F-BOX protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309: 293-297.
34. Ishikawa M, Kiba T, Chua NH. 2006. The Arabidopsis SPA1 gene is required for circadian clock function and photoperiodic flowering. Plant Journal 46: 736-746.
35. Jack T. 2004. Molecular and genetic mechanisms of floral control. Plant Cell 16: S1-S17.
36. Kim W, Ahn HJ, Chiou TJ, Ahn JH. 2011. The role of the miR399-PHO2 module in the regulation of flowering time in response to different ambient temperatures in Arabidopsis thaliana. Molecules and Cells 32: 83-88.
37. Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, Kim MD, Lee MH, Moon J, Lee I, Kim J. 2004. A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nature Genetics 36: 167-171.
38. King RW, Hisamatsu T, Goldschmidt EE, Blundell C. 2008. The nature of floral signals in Arabidopsis. I. Photosynthesis and a far-red photoresponse independently regulate flowering by increasing expression of FLOWERING LOCUS T (FT). Journal of Experimental Botany 59: 3811-3820.
39. Kobayashi Y, Weigel D. 2007. Move on up, it's time for change - mobile signals controlling photoperiod-dependent flowering. Genes & Development 21: 2371-2384.
40. Koornneef M, Hanhart CJ, Vanderveen JH. 1991. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Molecular & General Genetics 229: 57-66.
41. Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH. 2010. Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Research 38: 3081-3093.
42. Lee I, Amasino RM. 1995. Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA Gene. Plant Physiology 108: 157-162.
43. Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH. 2007. Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes & Development 21: 397-402.
44. Luterbacher J, Liniger MA, Menzel A, Estrella N, Della-Marta PM, Pfister C, Rutishauser T, Xoplaki E. 2007. Exceptional European warmth of autumn 2006 and winter 2007: historical context, the underlying dynamics, and its phenological impacts. Geophysical Research Letters 34: L12704.
45. Mai YX, Wang L, Yang HQ. 2011. A gain-of-function mutation in IAA7/AXR2 confers late flowering under short-day light in Arabidopsis. Journal of Integrative Plant Biology 53: 480-492.
46. Mazzella MA, Bertero D, Casal JJ. 2000. Temperature-dependent internode elongation in vegetative plants of Arabidopsis thaliana lacking phytochrome B and cryptochrome 1. Planta 210: 497-501.
47. Messina CD, Jones JW, Boote KJ, Vallejos CE. 2006. A gene-based model to simulate soybean development and yield responses to environment. Crop Science 46: 456-466.
48. Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956.
49. Mockler TC, Guo HW, Yang HY, Duong H, Lin CT. 1999. Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development 126: 2073-2082.
50. Moe R. 1990. Effect of day and night temperature slternations and of plant-growth regulators on stem elongation and flowering of the long-day plant Campanula isophylla Moretti. Scientia Horticulturae 43: 291-305.
51. Mohammed AR, Tarpley L. 2009. Impact of high nighttime temperature on respiration, membrane stability, antioxidant capacity, and yield of rice plants. Crop Science 49: 313-322.
52. Monteith JL. 1981. Climatic variation and the growth of crops. Quarterly Journal of the Royal Meteorological Society 107: 749-774.
53. Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I. 2003. The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant Journal 35: 613-623.
54. Morgan PW, Guy LW, Pao CI. 1987. Genetic-regulation of development in Sorghum bicolor. 3. Asynchrony of thermoperiods with photoperiods promotes floral initiation. Plant Physiology 83: 448-450.
55. Mutasa-Gottgens E, Hedden P. 2009. Gibberellin as a factor in floral regulatory networks. Journal of Experimental Botany 60: 1979-1989.
56. Napp-Zinn K. 1957. Untersuchungen iiber das Vernalisationsverhalten einer winterannuellen Rasse von Arabidopsis thaliana. Planta 50: 177-210.
57. Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG. 1999. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285: 1579-1582.
58. Peng SB, Huang JL, Sheehy JE, Laza RC, Visperas RM, Zhong XH, Centeno GS, Khush GS, Cassman KG. 2004. Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences, USA 101: 9971-9975.
59. Pouteau S, Albertini C. 2009. The significance of bolting and floral transitions as indicators of reproductive phase change in Arabidopsis. Journal of Experimental Botany 60: 3367-3377.
60. Pouteau S, Carre I, Gaudin V, Ferret V, Lefebvre D, Wilson M. 2008. Diversification of photoperiodic response patterns in a collection of early-flowering mutants of Arabidopsis. Plant Physiology 148: 1465-1473.
61. Pouteau S, Ferret V, Lefebvre D. 2006. Comparison of environmental and mutational variation in flowering time in Arabidopsis. Journal of Experimental Botany 57: 4099-4109.
62. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J. 1993. Mutations in the gene for the Red Far-Red light receptor phytochrome-B alter cell elongation and physiological-responses throughout Arabidopsis development. Plant Cell 5: 147-157.
63. Rikin A, Dillwith JW, Bergman DK. 1993. Correlation between the circadian-rhythm of resistance to extreme temperatures and changes in fatty-acid composition in cotton seedlings. Plant Physiology 101: 31-36.
64. Robertson GW. 1968. A biometeorological time scale for a cereal crop involving day and night temperatures and photoperiod. International Journal of Biometeorology 12: 191-223.
65. Sablowski R. 2007. Flowering and determinacy in Arabidopsis. Journal of Experimental Botany 58: 899-907.
66. Salazar JD, Saithong T, Brown PE, Foreman J, Locke JCW, Halliday KJ, Carre IA, Rand DA, Millar AJ. 2009. Prediction of photoperiodic regulators from quantitative gene circuit models. Cell 139: 1170-1179.
67. Seo E, Lee H, Jeon J, Park H, Kim J, Noh YS, Lee I. 2009. Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell 21: 3185-3197.
68. Stavang JA, Gallego-Bartolome J, Gomez MD, Yoshida S, Asami T, Olsen JE, Garcia-Martinez JL, Alabadi D, Blazquez MA. 2009. Hormonal regulation of temperature-induced growth in Arabidopsis. Plant Journal 60: 589-601.
69. Stavang JA, Junttila O, Moe R, Olsen JE. 2007. Differential temperature regulation of GA metabolism in light and darkness in pea. Journal of Experimental Botany 58: 3061-3069.
70. Strasser B, Alvarez MJ, Califano A, Cerdan PD. 2009. A complementary role for ELF3 and TFL1 in the regulation of flowering time by ambient temperature. Plant Journal 58: 629-640.
71. Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. 2001. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116-1120.
72. Sung SB, Amasino RM. 2004. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: 159-164.
73. Swiezewski S, Liu FQ, Magusin A, Dean C. 2009. Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature 462: 799-802.
74. Tao FL, Yokozawa M, Xu YL, Hayashi Y, Zhang Z. 2006. Climate changes and trends in phenology and yields of field crops in China, 1981-2000. Agricultural and Forest Meteorology 138: 82-92.
75. Thingnaes E, Torre S, Ernstsen A, Moe R. 2003. Day and night temperature responses in Arabidopsis: effects on gibberellin and auxin content, cell size, morphology and flowering time. Annals of Botany 92: 601-612.
76. Tiwari SB, Shen Y, Chang HC, Hou YL, Harris A, Ma SF, McPartland M, Hymus GJ, Adam L, Marion C et al. 2010. The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytologist 187: 57-66.
77. Turck F, Fornara F, Coupland G. 2008. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annual Review of Plant Biology 59: 573-594.
78. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G. 2004. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303: 1003-1006.
79. Wang EL, Engel T. 1998. Simulation of phenological development of wheat crops. Agricultural Systems 58: 1-24.
80. Weir AH, Bragg PL, Porter JR, Rayner JH. 1984. A wnter-wheat crop simulation-model without water or nutrient limitations. Journal of Agricultural Science 102: 371-382.
81. Wenden B, Dun EA, Hanan J, Andrieu B, Weller JL, Beveridge CA, Rameau C. 2009. Computational analysis of flowering in pea (Pisum sativum). New Phytologist 184: 153-167.
82. White JW, Hoogenboom G. 1996. Simulating effects of genes for physiological traits in a process-oriented crop model. Agronomy Journal 88: 416-422.
83. Wilczek AM, Burghardt LT, Cobb AR, Cooper MD, Welch SM, Schmitt J. 2010. Genetic and physiological bases for phenological responses to current and predicted climates. Philosophical Transactions of the Royal Society B-Biological Sciences 365: 3129-3147.
84. Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J et al. 2009. Effects of genetic perturbation on seasonal life history plasticity. Science 323: 930-934.
85. Williams GD. 1974. Deriving a biophotothermal time scale for barley. International Journal of Biometeorology 18: 57-69.
86. Wilson RN, Heckman JW, Somerville CR. 1992. Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiology 100: 403-408.
87. Xia J, Han Y, Zhang Z, Wan S. 2009. Effects of diurnal warming on soil respiration are not equal to the summed effects of day and night warming in a temperate steppe. Biogeosciences 6: 1361-1370.
88. Yang HQ, Mai YX, Wang L. 2011. A gain-of-function mutation in IAA7/AXR2 confers late flowering under short-day light in Arabidopsis. Journal of Integrative Plant Biology 53: 480-492.
89. Yanovsky MJ, Kay SA. 2002. Molecular basis of seasonal time measurement in Arabidopsis. Nature 419: 308-312.
90. Yin XY, Kropff MJ, Goudriaan J. 1996. Differential effects of day and night temperature on development to flowering in rice. Annals of Botany 77: 203-213.
91. Yin XY, Kropff MJ, Horie T, Nakagawa H, Centeno HGS, Zhu DF, Goudriaan J. 1997. A model for photothermal responses of flowering in rice. 1. Model description and parameterization. Field Crops Research 51: 189-200.
92. Yu JW, Rubio V, Lee NY, Bai SL, Lee SY, Kim SS, Liu LJ, Zhang YY, Irigoyen ML, Sullivan JA et al. 2008. COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Molecular Cell 32: 617-630.