The role of gibberellin signalling in plant responses to abiotic stress

Journal of Experimental Biology - Tập 217 Số 1 - Trang 67-75 - 2014
Ellen Colebrook1, Stephen G. Thomas1, Andrew L. Phillips1, Peter Hedden1
1Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ (UK)

Tóm tắt

Plant hormones are small molecules that regulate plant growth and development, as well as responses to changing environmental conditions. By modifying the production, distribution or signal transduction of these hormones, plants are able to regulate and coordinate both growth and/or stress tolerance to promote survival or escape from environmental stress. A central role for the gibberellin (GA) class of growth hormones in the response to abiotic stress is becoming increasingly evident. Reduction of GA levels and signalling has been shown to contribute to plant growth restriction on exposure to several stresses, including cold, salt and osmotic stress. Conversely, increased GA biosynthesis and signalling promote growth in plant escape responses to shading and submergence. In several cases, GA signalling has also been linked to stress tolerance. The transcriptional regulation of GA metabolism appears to be a major point of regulation of the GA pathway, while emerging evidence for interaction of the GA-signalling molecule DELLA with components of the signalling pathway for the stress hormone jasmonic acid suggests additional mechanisms by which GA signalling may integrate multiple hormone signalling pathways in the response to stress. Here, we review the evidence for the role of GA in these processes, and the regulation of the GA signalling pathway on exposure to abiotic stress. The potential mechanisms by which GA signalling modulates stress tolerance are also discussed.

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Tài liệu tham khảo

Achard, 2006, Integration of plant responses to environmentally activated phytohormonal signals, Science, 311, 91, 10.1126/science.1118642

Achard, 2008, The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism, Plant Cell, 20, 2117, 10.1105/tpc.108.058941

Achard, 2008, Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species, Curr. Biol., 18, 656, 10.1016/j.cub.2008.04.034

Achard, 2009, Gibberellin signaling controls cell proliferation rate in Arabidopsis, Curr. Biol., 19, 1188, 10.1016/j.cub.2009.05.059

Atwell, 1990, The effect of soil compaction on wheat during early tillering, New Phytol., 115, 29, 10.1111/j.1469-8137.1990.tb00918.x

Bai, 2012, Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis, Nat. Cell Biol., 14, 810, 10.1038/ncb2546

Bailey-Serres, 2010, Life in the balance: a signaling network controlling survival of flooding, Curr. Opin. Plant Biol., 13, 489, 10.1016/j.pbi.2010.08.002

Beemster, 1996, Effects of soil resistance to root penetration on leaf expansion in wheat (Triticum aestivum L.): composition, number and size of epidermal cells in mature blades, J. Exp. Bot., 47, 1651, 10.1093/jxb/47.11.1651

Bengough, 2011, Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits, J. Exp. Bot., 62, 59, 10.1093/jxb/erq350

Benschop, 2006, Long-term submergence-induced elongation in Rumex palustris requires abscisic acid-dependent biosynthesis of gibberellin1, Plant Physiol., 141, 1644, 10.1104/pp.106.082636

Boter, 2004, Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis, Genes Dev., 18, 1577, 10.1101/gad.297704

Chan, 2012, Comparison of salt stress resistance genes in transgenic Arabidopsis thaliana indicates that extent of transcriptomic change may not predict secondary phenotypic or fitness effects, Plant Biotech. J., 10, 284, 10.1111/j.1467-7652.2011.00661.x

Chapman, 2011, Water supply and not nitrate concentration determines primary root growth in Arabidopsis, Plant Cell Environ., 34, 1630, 10.1111/j.1365-3040.2011.02358.x

Christmann, 2007, A hydraulic signal in root-to-shoot signalling of water shortage, Plant J., 52, 167, 10.1111/j.1365-313X.2007.03234.x

Claeys, 2012, DELLA signaling mediates stress-induced cell differentiation in Arabidopsis leaves through modulation of anaphase-promoting complex/cyclosome activity, Plant Physiol., 159, 739, 10.1104/pp.112.195032

Coelho Filho, 2013, The involvement of gibberellin signalling in the effect of soil resistance to root penetration on leaf elongation and tiller number in wheat, Plant Soil, 371, 81, 10.1007/s11104-013-1662-8

Cox, 2006, The stimulating effects of ethylene and auxin on petiole elongation and on hyponastic curvature are independent processes in submerged Rumex palustris, Plant Cell Environ., 29, 282, 10.1111/j.1365-3040.2005.01420.x

Dai, 2011, Drought under global warming: a review, Wiley Interdiscip. Rev. Clim. Change, 2, 45, 10.1002/wcc.81

Davière, 2008, Transcriptional factor interaction: a central step in DELLA function, Curr. Opin. Genet. Dev., 18, 295, 10.1016/j.gde.2008.05.004

Davies, 2010, The plant hormones: their nature, occurrence, and function, Plant Hormones: Biosynthesis, Signal Transduction, Action!, 1, 10.1007/978-1-4020-2686-7_1

de Lucas, 2008, A molecular framework for light and gibberellin control of cell elongation, Nature, 451, 480, 10.1038/nature06520

Djakovic-Petrovic, 2007, DELLA protein function in growth responses to canopy signals, Plant J., 51, 117, 10.1111/j.1365-313X.2007.03122.x

Dubois, 2013, The ETHYLENE RESPONSE FACTOR 6 acts as central regulator of leaf growth under water limiting conditions in Arabidopsis thaliana, Plant Physiol., 162, 319, 10.1104/pp.113.216341

Feng, 2008, Coordinated regulation of Arabidopsis thaliana development by light and gibberellins, Nature, 451, 475, 10.1038/nature06448

Franklin, 2008, Shade avoidance, New Phytol., 179, 930, 10.1111/j.1469-8137.2008.02507.x

Frigerio, 2006, Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis, Plant Physiol., 142, 553, 10.1104/pp.106.084871

Fukao, 2008, Ethylene – a key regulator of submergence responses in rice, Plant Sci., 175, 43, 10.1016/j.plantsci.2007.12.002

Fukao, 2008, Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice, Proc. Natl. Acad. Sci. USA, 105, 16814, 10.1073/pnas.0807821105

Fukao, 2006, A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice, Plant Cell, 18, 2021, 10.1105/tpc.106.043000

Fukao, 2011, The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice, Plant Cell, 23, 412, 10.1105/tpc.110.080325

Gallego-Bartolomé, 2012, Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis, Proc. Natl. Acad. Sci. USA, 109, 13446, 10.1073/pnas.1119992109

Gao, 2012, Predicting penetrometer resistance from the compression characteristic of soil, Soil Sci. Soc. Am. J., 76, 361, 10.2136/sssaj2011.0217

Gilley, 1998, Gibberellin antagonizes paclobutrazol-induced stress protection in wheat seedlings, J. Plant Physiol., 153, 200, 10.1016/S0176-1617(98)80066-7

Griffiths, 2006, Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis, Plant Cell, 18, 3399, 10.1105/tpc.106.047415

Halevy, 1963, Increased tolerance of bean plants to soil drought by means of growth-retarding substances, Nature, 197, 310, 10.1038/197310a0

Hattori, 2009, The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water, Nature, 460, 1026, 10.1038/nature08258

Hedden, 2012, Gibberellin biosynthesis and its regulation, Biochem. J., 444, 11, 10.1042/BJ20120245

Hirano, 2012, The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity, Plant J., 71, 443, 10.1111/j.1365-313X.2012.05000.x

Hisamatsu, 2005, The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of Arabidopsis, Plant Physiol., 138, 1106, 10.1104/pp.104.059055

Hou, 2010, DELLAs modulate jasmonate signaling via competitive binding to JAZs, Dev. Cell, 19, 884, 10.1016/j.devcel.2010.10.024

Hruz, 2008, Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes, Adv. Bioinformatics, 2008, 420747, 10.1155/2008/420747

Hussain, 1999, Novel approaches for examining the effects of differential soil compaction on xylem sap abscisic acid concentration, stomatal conductance and growth in barley (Hordeum vulgare L.), Plant Cell Environ., 22, 1377, 10.1046/j.1365-3040.1999.00504.x

Hussain, 1999, Soil compaction. A role for ethylene in regulating leaf expansion and shoot growth in tomato?, Plant Physiol., 121, 1227, 10.1104/pp.121.4.1227

Jackson, 1997, Hormones from roots as signals for the shoots of stressed plants, Trends Plant Sci., 2, 22, 10.1016/S1360-1385(96)10050-9

Jackson, 2008, Ethylene-promoted elongation: an adaptation to submergence stress, Ann. Bot., 101, 229, 10.1093/aob/mcm237

Ju, 2012, CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis, Proc. Natl. Acad. Sci. USA, 109, 19486, 10.1073/pnas.1214848109

Jung, 2010, The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors, Plant Physiol., 152, 1674, 10.1104/pp.109.152157

Kaneko, 2003, Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants?, Plant J., 35, 104, 10.1046/j.1365-313X.2003.01780.x

Kasahara, 2002, Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis, J. Biol. Chem., 277, 45188, 10.1074/jbc.M208659200

Kavanová, 2008, Nitrogen deficiency inhibits leaf blade growth in Lolium perenne by increasing cell cycle duration and decreasing mitotic and post-mitotic growth rates, Plant Cell Environ., 31, 727, 10.1111/j.1365-3040.2008.01787.x

Keller, 2011, Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades, Plant J., 67, 195, 10.1111/j.1365-313X.2011.04598.x

Keuskamp, 2010, Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition, Proc. Natl. Acad. Sci. USA, 107, 22740, 10.1073/pnas.1013457108

Keuskamp, 2010, Physiological regulation and functional significance of shade avoidance responses to neighbors, Plant Signal. Behav., 5, 655, 10.4161/psb.5.6.11401

Kieber, 1993, CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases, Cell, 72, 427, 10.1016/0092-8674(93)90119-B

Kilian, 2007, The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses, Plant J., 50, 347, 10.1111/j.1365-313X.2007.03052.x

Kinoshita, 2012, IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress, Plant Cell, 24, 3590, 10.1105/tpc.112.097006

Ko, 2006, Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis, Plant J., 47, 343, 10.1111/j.1365-313X.2006.02782.x

Koornneef, 1980, Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh, Theor. Appl. Genet., 58, 257, 10.1007/BF00265176

Krugman, 2011, Alteration in expression of hormone-related genes in wild emmer wheat roots associated with drought adaptation mechanisms, Funct. Int. Genom., 11, 565, 10.1007/s10142-011-0231-6

Lawlor, 2013, Genetic engineering to improve plant performance under drought: physiological evaluation of achievements, limitations, and possibilities, J. Exp. Bot., 64, 83, 10.1093/jxb/ers326

Leach, 2011, Primary root elongation rate and abscisic acid levels of maize in response to water stress, Crop Sci., 51, 157, 10.2135/cropsci2009.12.0708

Lee, 2011, Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia, New Phytol., 190, 457, 10.1111/j.1469-8137.2010.03590.x

Leung, 1997, The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction, Plant Cell, 9, 759

Liu, 2003, Hydraulic and chemical signals in the control of leaf expansion and stomatal conductance in soybean exposed to drought stress, Funct. Plant Biol., 30, 65, 10.1071/FP02170

Lobell, 2012, The influence of climate change on global crop productivity, Plant Physiol., 160, 1686, 10.1104/pp.112.208298

Magome, 2004, dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor, Plant J., 37, 720, 10.1111/j.1365-313X.2003.01998.x

Magome, 2008, The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis, Plant J., 56, 613, 10.1111/j.1365-313X.2008.03627.x

Mittler, 2006, Abiotic stress, the field environment and stress combination, Trends Plant Sci., 11, 15, 10.1016/j.tplants.2005.11.002

Mizoguchi, 2010, Two closely related subclass II SNRK2 protein kinases cooperatively regulate drought-inducible gene expression, Plant Cell Physiol., 51, 842, 10.1093/pcp/pcq041

Mizoi, 2012, AP2/ERF family transcription factors in plant abiotic stress responses, Biochim. Biophys. Acta, 1819, 86, 10.1016/j.bbagrm.2011.08.004

Navarro, 2008, DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling, Curr. Biol., 18, 650, 10.1016/j.cub.2008.03.060

O'Neill, 2010, Regulation of the gibberellin pathway by auxin and DELLA proteins, Planta, 232, 1141, 10.1007/s00425-010-1248-0

Passioura, 1991, Soil structure and plant growth, Aust. J. Soil Res., 29, 717, 10.1071/SR9910717

Pierik, 2009, Auxin and ethylene regulate elongation responses to neighbor proximity signals independent of gibberellin and DELLA proteins in Arabidopsis, Plant Physiol., 149, 1701, 10.1104/pp.108.133496

Pierik, 2011, Growth-mediated stress escape: convergence of signal transduction pathways activated upon exposure to two different environmental stresses, New Phytol., 189, 122, 10.1111/j.1469-8137.2010.03458.x

Polko, 2011, Petiole hyponasty: an ethylene-driven, adaptive response to changes in the environment, AoB Plants, plr031

Rademacher, 2000, Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways, Annu. Rev. Plant Physiol. Plant Mol. Biol., 51, 501, 10.1146/annurev.arplant.51.1.501

Rockwell, 2006, Phytochrome structure and signaling mechanisms, Annu. Rev. Plant Biol., 57, 837, 10.1146/annurev.arplant.56.032604.144208

Saucedo, 2012, An altered hydrotropic response (ahr1) mutant of Arabidopsis recovers root hydrotropism with cytokinin, J. Exp. Bot., 63, 3587, 10.1093/jxb/ers025

Schwechheimer, 2011, Gibberellin signaling in plants – the extended version, Front. Plant Sci., 2, 107

Shi, 2012, Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis, Plant Cell, 24, 2578, 10.1105/tpc.112.098640

Shyu, 2012, JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis, Plant Cell, 24, 536, 10.1105/tpc.111.093005

Skirycz, 2010, More from less: plant growth under limited water, Curr. Opin. Biotechnol., 21, 197, 10.1016/j.copbio.2010.03.002

Skirycz, 2010, Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress, Plant Physiol., 152, 226, 10.1104/pp.109.148965

Skirycz, 2011, Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest, Plant Cell, 23, 1876, 10.1105/tpc.111.084160

Smith, 1982, Light quality, photoperception, and plant strategy, Annu. Rev. Plant Physiol., 33, 481, 10.1146/annurev.pp.33.060182.002405

Sponsel, 2004, Gibberellin, biosynthesis and inactivation, Plant Hormones Biosynthesis, Signal Transduction, Action!, 63

Stamm, 2010, The phytohormone signal network regulating elongation growth during shade avoidance, J. Exp. Bot., 61, 2889, 10.1093/jxb/erq147

Sun, 2011, The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants, Curr. Biol., 21, R338, 10.1016/j.cub.2011.02.036

Tao, 2008, Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants, Cell, 133, 164, 10.1016/j.cell.2008.01.049

Thomas, 1999, Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation, Proc. Natl. Acad. Sci. USA, 96, 4698, 10.1073/pnas.96.8.4698

Ubeda-Tomás, 2009, Gibberellin signaling in the endodermis controls Arabidopsis root meristem size, Curr. Biol., 19, 1194, 10.1016/j.cub.2009.06.023

Ueguchi-Tanaka, 2010, The perception of gibberellins: clues from receptor structure, Curr. Opin. Plant Biol., 13, 503, 10.1016/j.pbi.2010.08.004

Ueguchi-Tanaka, 2005, GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin, Nature, 437, 693, 10.1038/nature04028

Verelst, 2010, Abscisic acid, ethylene and gibberellic acid act at different developmental stages to instruct the adaptation of young leaves to stress, Plant Signal. Behav., 5, 473, 10.4161/psb.5.4.11421

Vettakkorumakankav, 1999, A crucial role for gibberellins in stress protection of plants, Plant Cell Physiol., 40, 542, 10.1093/oxfordjournals.pcp.a029575

Wang, 2008, Influence of water stress on endogenous hormone contents and cell damage of maize seedlings, J. Integr. Plant Biol., 50, 427, 10.1111/j.1774-7909.2008.00638.x

Weston, 2008, The Pea DELLA proteins LA and CRY are important regulators of gibberellin synthesis and root growth, Plant Physiol., 147, 199, 10.1104/pp.108.115808

Whalley, 2006, Does soil strength play a role in wheat yield losses caused by soil drying?, Plant Soil, 280, 279, 10.1007/s11104-005-3485-8

Whalley, 2008, The effect of soil strength on the yield of wheat, Plant Soil, 306, 237, 10.1007/s11104-008-9577-5

Wild, 2012, The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses, Plant Cell, 24, 3307, 10.1105/tpc.112.101428

Wilkinson, 2002, ABA-based chemical signalling: the co-ordination of responses to stress in plants, Plant Cell Environ., 25, 195, 10.1046/j.0016-8025.2001.00824.x

Xu, 2006, Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice, Nature, 442, 705, 10.1038/nature04920

Yamaguchi, 2008, Gibberellin metabolism and its regulation, Annu. Rev. Plant Biol., 59, 225, 10.1146/annurev.arplant.59.032607.092804

Yang, 2012, Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade, Proc. Natl. Acad. Sci. USA, 109, E1192, 10.1073/pnas.1201616109

Young, 1997, Mechanical impedance of root growth directly reduces leaf elongation rates of cereals, New Phytol., 135, 613, 10.1046/j.1469-8137.1997.00693.x

Zentella, 2007, Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis, Plant Cell, 19, 3037, 10.1105/tpc.107.054999

Zhu, 2011, Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis, Proc. Natl. Acad. Sci. USA, 108, 12539, 10.1073/pnas.1103959108