Molecular and genetic control of plant thermomorphogenesis

Nature Plants

Volumn 2, Issue , 2016, Pages

  Quint, Marcel ^a,b   Delker, Carolin ^a,b   Franklin, Keara A ^c   Wigge, Philip A ^d   Halliday, Karen J ^e   Van Zanten, Martijn ^f  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; PHYTOHORMONE; PIF4 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CIRCADIAN RHYTHM; CLIMATE CHANGE; EPIGENETICS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; RADIATION RESPONSE; SIGNAL TRANSDUCTION; TEMPERATURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CIRCADIAN CLOCKS; CLIMATE CHANGE; EPIGENOMICS; PLANT GROWTH REGULATORS; SIGNAL TRANSDUCTION; TEMPERATURE;

EID: 84954486947     PISSN: None     EISSN: 20550278     Source Type: Journal    
DOI: 10.1038/nplants.2015.190     Document Type: Review

References (100)

1. American Meteorological Society. State of the climate in 2014. Bull. Am. Meteorol. Soc. 96 (special suppl.) (2015).
2. IPCC. Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).
3. Fitter, A. H., Fitter, R. S. R. Rapid changes in flowering time in British plants. Science 296, 1689-1691 (2002).
4. Thuiller, W., Lavorel, S., Araújo, M. B., Sykes, M. T., Prentice, I. C. Climate change threats to plant diversity in Europe. Proc. Natl Acad. Sci. USA 102, 8245-8250 (2005).
5. Willis, C. G., Ruhfel, B., Primack, R. B., Miller-Rushing, A. J., Davis, C. C. Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proc. Natl Acad. Sci. USA 105, 17029-17033 (2008).
6. Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15, 684-692 (2010).
7. Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W., Courchamp, F. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15, 365-377 (2012).
8. Peñuelas, J. et al. Evidence of current impact of climate change on life: a walk from genes to the biosphere. Glob. Change Biol. 19, 2303-2338 (2013).
9. Bita, C., Gerats, T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress tolerant crops. Front. Plant Sci. 4, 273 (2013).
10. Ovaskainen, O. et al. Community-level phenological response to climate change. Proc. Natl Acad. Sci. USA 110, 13434-13439 (2013).
11. CaraDonna, P. J., Iler, A. M., Inouye, D. W. Shifts in flowering phenology reshape a subalpine plant community. Proc. Natl Acad. Sci. USA 111, 4916-4921 (2014).
12. Pauli, H. et al. Recent plant diversity changes on Europe's mountain summits. Science 336, 353-355 (2012).
13. Challinor, A. J. et al. A meta-analysis of crop yield under climate change and adaptation. Nature Clim. Change 4, 287-291 (2014).
14. Battisti, D. S., Naylor, R. L. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323, 240-244 (2009).
15. Lobell, D. B., Gourdji, S. M. The influence of climate change on global crop productivity. Plant Physiol. 160, 1686-1697 (2012).
16. Erwin, J. E., Heins, R. D., Karlsson, M. G. Thermomorphogenesis in Lilium longiflorum. Am. J. Bot. 76, 47-52 (1989).
17. Crawford, A. J., McLachlan, D. H., Hetherington, A. M., Franklin, K. A. High temperature exposure increases plant cooling capacity. Curr. Biol. 22, R396-R397 (2012).
18. Bridge, L. J., Franklin, K. A., Homer, M. E. Impact of plant shoot architecture on leaf cooling: a coupled heat and mass transfer model. J. R. Soc. Interface http://dx.doi.org/10.1098/rsif.2013.0326 (2013).
19. Van Zanten, M., Pons, T. L., Janssen, J. A. M., Voesenek, L. A. C. J., Peeters, A. J. M. On the relevance and control of leaf angle. Crit. Rev. Plant Sci. 29, 300-316 (2010).
20. Van Zanten, M., Bours, R., Pons, T. L., Proveniers, M. C. G. in Temperature and Plant Development (eds Franklin, K. A., Wigge, P. A.) 49-78 (Wiley, 2014).
21. Kotak, S. et al. Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 10, 310-316 (2007).
22. Koini, M. A. et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408-413 (2009).
23. Nomoto, Y. et al. A circadian clock-and PIF4-mediated double coincidence mechanism is implicated in the thermosensitive photoperiodic control of plant architectures in Arabidopsis thaliana. Plant Cell Physiol. 53, 1965-1973 (2012).
24. Yamashino, T. et al. Verification at the protein level of the PIF4-mediated external coincidence model for the temperature-adaptive photoperiodic control of plant growth in Arabidopsis thaliana. Plant Signal. Behav. 8, e23390 (2013).
25. Mizuno, T. et al. Ambient temperature signal feeds into the circadian clock transcriptional circuitry through the EC night-time repressor in Arabidopsis thaliana. Plant Cell Physiol. 55, 958-976 (2014).
26. Box, M. S. et al. ELF3 controls thermoresponsive growth in Arabidopsis. Curr. Biol. 25, 194-199 (2015).
27. Seaton, D. D. et al. Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature. Mol. Syst. Biol. 11, 776 (2015).
28. Raschke, A. et al. Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes. BMC Plant Biol. 15, 197 (2015).
29. Franklin, K. A. et al. PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl Acad. Sci. USA 108, 20231-20235 (2011).
30. Sun, J., Qi, L., Li, Y., Chu, J., Li, C. PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet. 8, e1002594 (2012).
31. Gray, W. M., Östin, A., Sandberg, G., Romano, C. P., Estelle, M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl Acad. Sci. USA 95, 7197-7202 (1998).
32. Stavang, J. A. et al. Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60, 589-601 (2009).
33. Oh, E., Zhu, J.-Y., Wang, Z.-Y. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nature Cell Biol. 14, 802-809 (2012).
34. Oh, E. et al. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. eLife 3, e03031 (2014).
35. Kumar, S. V., Wigge, P. A. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136-147 (2010).
36. Lee, H.-J. et al. FCA mediates thermal adaptation of stem growth by attenuating auxin action in Arabidopsis. Nature Commun. 5, 5473 (2014).
37. Yamori, W., Hikosaka, K., Way, D. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth. Res. 119, 101-117 (2014).
38. Capovilla, G., Schmid, M., Posé, D. Control of flowering by ambient temperature. J. Exp. Bot. 66, 59-69 (2014).
39. Verhage, L., Angenent, G. C., Immink, R. G. H. Research on floral timing by ambient temperature comes into blossom. Trends Plant Sci. 19, 583-591 (2014).
40. Orbovic, V., Poff, K. L. Growth distribution during phototropism of Arabidopsis thaliana seedlings. Plant Physiol. 103, 157-163 (1993).
41. Delker, C. et al. The DET1-COP1-HY5 pathway constitutes a multipurpose signaling module regulating plant photomorphogenesis and thermomorphogenesis. Cell Rep. 9, 1983-1989 (2014).
42. Delker, C. et al. Natural variation of transcriptional auxin response networks in Arabidopsis thaliana. Plant Cell 22, 2184-2200 (2010).
43. Johansson, H. et al. Arabidopsis cell expansion is controlled by a photothermal switch. Nature Commun. 5, 4848 (2014).
44. Bai, M.-Y., Fan, M., Oh, E., Wang, Z.-Y. A triple helix-loop-helix/basic helix-loop-helix cascade controls cell elongation downstream of multiple hormonal and environmental signaling pathways in Arabidopsis. Plant Cell 24, 4917-4929 (2012).
45. Ibañez, C. et al. Developmental plasticity of Arabidopsis thaliana accessions across an ambient temperature range. bioRxiv http://dx.doi.org/10.1101/017285(2015).
46. Miyazaki, Y. ZEITLUPE positively regulates hypocotyl elongation at warm temperature under light in Arabidopsis thaliana. Plant Signal. Behav. 10, e998540 (2015).
47. Maharjan, P., Choe, S. High temperature stimulates DWARF4 (DWF4) expression to increase hypocotyl elongation in Arabidopsis. J. Plant Biol. 54, 425-429 (2011).
48. Hao, Y., Oh, E., Choi, G., Liang, Z., Wang, Z.-Y. Interactions between HLH and bHLH factors modulate light-regulated plant development. Mol. Plant 5, 688-697 (2012).
49. Zhu, W. et al. Natural variation identifies ICARUS1, a universal gene required for cell proliferation and growth at high temperatures in Arabidopsis thaliana. PLoS Genet. 11, e1005085 (2015).
50. Sanchez-Bermejo, E. et al. Genetic architecture of natural variation in thermal responses of Arabidopsis. Plant Physiol. 169, 647-659 (2015).
51. Millenaar, F. F. et al. Ethylene-induced differential growth of petioles in Arabidopsis. analyzing natural variation, response kinetics, and regulation. Plant Physiol. 137, 998-1008 (2005).
52. van Zanten, M., Voesenek, L. A. C. J., Peeters, A. J. M., Millenaar, F. F. Hormone-and light-mediated regulation of heat-induced differential petiole growth in Arabidopsis. Plant Physiol. 151, 1446-1458 (2009).
53. Vile, D. et al. Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects Plant Cell Environ. 35, 702-718 (2012).
54. Vasseur, F., Pantin, F., Vile, D. Changes in light intensity reveal a major role for carbon balance in Arabidopsis responses to high temperature. Plant Cell Environ. 34, 1563-1576 (2011).
55. Franklin, K. A. Shade avoidance. New Phytol. 179, 930-944 (2008).
56. Proveniers, M. C. G., van Zanten, M. High temperature acclimation through PIF4 signaling. Trends Plant Sci. 18, 59-64 (2013).
57. de Wit, M., Lorrain, S., Fankhauser, C. Auxin-mediated plant architectural changes in response to shade and high temperature. Physiol. Plant. 151, 13-24 (2014).
58. Foreman, J. et al. Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J. 65, 441-452 (2011).
59. Nozue, K. et al. Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358-361 (2007).
60. Niwa, Y., Yamashino, T., Mizuno, T. The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant Cell Physiol. 50, 838-854 (2009).
61. Kunihiro, A. et al. PHYTOCHROME-INTERACTING FACTOR 4 and 5 (PIF4 and PIF5) activate the homeobox ATHB2 and auxin-inducible IAA29 genes in the coincidence mechanism underlying photoperiodic control of plant growth of Arabidopsis thaliana. Plant Cell Physiol. 52, 1315-1329 (2011).
62. Nusinow, D. A. et al. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475, 398-402 (2011).
63. Gould, P. D. et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18, 1177-1187 (2006).
64. Covington, M. F. et al. ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell 13, 1305-1316 (2001).
65. Liu, X. L., Covington, M. F., Fankhauser, C., Chory, J., Wagner, D. R. ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13, 1293-1304 (2001).
66. Nieto, C., López-Salmerón, V., Davière, J.-M., Prat, S. ELF3-PIF4 interaction regulates plant growth independently of the evening complex. Curr. Biol. 25, 187-193 (2015).
67. Koornneef, M., Rolff, E., Spruit, C. J. P. Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z. Pflanzenphysiol. 100, 147-160 (1980).
68. Oyama, T., Shimura, Y., Okada, K. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev. 11, 2983-2995 (1997).
69. Toledo-Ortiz, G. et al. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genet. 10, e1004416 (2014).
70. Lee, J. et al. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19, 731-749 (2007).
71. Lorrain, S., Allen, T., Duek, P. D., Whitelam, G. C., Fankhauser, C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 53, 312-323 (2008).
72. Bernardo-Garciá, S. et al. BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth. Genes Dev. 28, 1681-1694 (2014).
73. Dong, J. et al. Arabidopsis DE-ETIOLATED1 represses photomorphogenesis by positively regulating phytochrome-interacting factors in the dark. Plant Cell 26, 3630-3645 (2014).
74. Shi, H. et al. Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination. Proc. Natl Acad. Sci. USA 112, 3817-3822 (2015).
75. de Lucas, M. et al. A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480-484 (2008).
76. Hornitschek, P. et al. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 71, 699-711 (2012).
77. Quint, M., Gray, W. M. Auxin signaling. Curr. Opin. Plant Biol. 9, 448-453 (2006).
78. Delker, C., Raschke, A., Quint, M. Auxin dynamics: the dazzling complexity of a small molecule's message. Planta 227, 929-941 (2008).
79. Chae, K. et al. Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant J. 71, 684-697 (2012).
80. Spartz, A. K. et al. The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J. 70, 978-990 (2012).
81. Spartz, A. K. et al. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+ATPases to promote cell expansion in Arabidopsis. Plant Cell 26, 2129-2142 (2014).
82. Xu, J., Tian, J., Belanger, F. C., Huang, B. Identification and characterization of an expansin gene AsEXP1 associated with heat tolerance in C3 Agrostis grass species. J. Exp. Bot. 58, 3789-3796 (2007).
83. Bai, M.-Y. et al. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nature Cell Biol. 14, 810-817 (2012).
84. Wang, W., Bai, M.-Y., Wang, Z.-Y. The brassinosteroid signaling network-a paradigm of signal integration. Curr. Opin. Plant Biol. 21, 147-153 (2014).
85. Feng, S. et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475-479 (2008).
86. Hersch, M. et al. Light intensity modulates the regulatory network of the shade avoidance response in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 6515-6520 (2014).
87. Rausenberger, J. et al. An integrative model for phytochrome B mediated photomorphogenesis: from protein dynamics to physiology. PLoS One 5, e10721 (2010).
88. Chew, Y. H. et al. Mathematical models light up plant signaling. Plant Cell 26, 5-20 (2014).
89. Arrhenius, S. Quantitative Laws in Biological Chemistry (Bell, 1915).
90. Sidaway-Lee, K., Costa, M., Rand, D., Finkenstadt, B., Penfield, S. Direct measurement of transcription rates reveals multiple mechanisms for configuration of the Arabidopsis ambient temperature response. Genome Biol. 15, R45 (2014).
91. Deal, R. B., Topp, C. N., McKinney, E. C., Meagher, R. B. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A. Z. Plant Cell 19, 74-83 (2007).
92. Stewart, J. L., Maloof, J. N., Nemhauser, J. L. PIF genes mediate the effect of sucrose on seedling growth dynamics. PLoS One 6, e19894 (2011).
93. Liu, Z. et al. Phytochrome interacting factors (PIFs) are essential regulators for sucrose-induced hypocotyl elongation in Arabidopsis. J. Plant Physiol. 168, 1771-1779 (2011).
94. Sairanen, I. et al. Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell 24, 4907-4916 (2012).
95. Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature 490, 254-257 (2012).
96. Parent, B., Tardieu, F. Temperature responses of developmental processes have not been affected by breeding in different ecological areas for 17 crop species. New Phytol. 194, 760-774 (2012).
97. Shen, H. et al. Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato. Nature Biotechnol. 33, 996-1003 (2015).
98. Nakamichi, N. Adaptation to the local environment by modifications of the photoperiod response in crops. Plant Cell Physiol. 56, 594-604 (2014).
99. Boden, S., Kavanova, M., Finnegan, E., Wigge, P. Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A.Z-nucleosomes. Genome Biol. 14, R65 (2013).
100. Hanzawa, T. et al. Cellular auxin homeostasis under high temperature is regulated through a SORTING NEXIN1-dependent endosomal trafficking pathway. Plant Cell 25, 3424-3433 (2013).