Physiological impacts of ABA–JA interactions under water-limitation

Plant Molecular Biology - Tập 91 Số 6 - Trang 641-650 - 2016
de Ollas, Carlos1, Dodd, Ian C.1
1Lancaster Environment Centre, Lancaster University, Lancaster, UK

Tóm tắt

Plant responses to drought stress depend on highly regulated signal transduction pathways with multiple interactions. This complex crosstalk can lead to a physiological outcome of drought avoidance or tolerance/resistance. ABA is the principal mediator of these responses due to the regulation of stomatal closure that determines plant growth and survival, but also other strategies of drought resistance such as osmotic adjustment. However, other hormones such as JA seem responsible for regulating a subset of plant responses to drought by regulating ABA biosynthesis and accumulation and ABA-dependent signalling, but also by ABA independent pathways. Here, we review recent reports of ABA–JA hormonal and molecular interactions within a physiological framework of drought tolerance. Understanding the physiological significance of this complex regulation offers opportunities to find strategies of drought tolerance that avoid unwanted side effects that limit growth and yield, and may allow biotechnological crop improvement.

Tài liệu tham khảo

citation_journal_title=Plant Cell; citation_title=Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression; citation_author=H Abe, K Yamaguchi-Shinozaki, T Urao, T Iwasaki, D Hosokawa, K Shinozaki; citation_volume=9; citation_publication_date=1997; citation_pages=1859-1868; citation_id=CR1 citation_journal_title=Plant Cell; citation_title=Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling; citation_author=H Abe, T Urao, T Ito, M Seki, K Shinozaki, K Yamaguchi-Shinozaki; citation_volume=15; citation_publication_date=2003; citation_pages=63-78; citation_doi=10.1105/tpc.006130; citation_id=CR2 citation_journal_title=J Plant Physiol; citation_title=Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress; citation_author=V Arbona, R Argamasilla, A Gómez-Cadenas; citation_volume=167; citation_publication_date=2010; citation_pages=1342-1350; citation_doi=10.1016/j.jplph.2010.05.012; citation_id=CR3 citation_journal_title=J Exp Bot; citation_title=Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery; citation_author=R Aroca, P Vernieri, JM Ruiz-Lozano; citation_volume=59; citation_publication_date=2008; citation_pages=2029-2041; citation_doi=10.1093/jxb/ern057; citation_id=CR4 citation_journal_title=Acta Physiol Plant; citation_title=The effect of jasmonic acid on the accumulation of ABA, proline and spermidine and its influence on membrane injury under water deficit in two barley genotypes; citation_author=H Bandurska, A Stroiński, J Kubiś; citation_volume=25; citation_publication_date=2003; citation_pages=279-285; citation_doi=10.1007/s11738-003-0009-0; citation_id=CR5 citation_journal_title=Funct Plant Biol; citation_title=Towards a conceptual ABA ideotype in plant breeding for water limited environments; citation_author=A Blum; citation_volume=42; citation_publication_date=2015; citation_pages=502-513; citation_doi=10.1071/FP14334; citation_id=CR6 citation_journal_title=J Plant Growth Regul; citation_title=Interplay between abscisic acid and jasmonic acid and its role in water-oxidative stress in wild-type, ABA-deficient, JA-deficient, and ascorbate-deficient arabidopsis plants; citation_author=R Brossa, M Lopez-Carbonell, T Jubany-Mari, L Alegre; citation_volume=30; citation_publication_date=2011; citation_pages=322-333; citation_doi=10.1007/s00344-011-9194-z; citation_id=CR7 citation_journal_title=Plant Physiol; citation_title=The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals; citation_author=M-C Cheng, P-M Liao, W-W Kuo, T-P Lin; citation_volume=162; citation_publication_date=2013; citation_pages=1566-1582; citation_doi=10.1104/pp.113.221911; citation_id=CR8 citation_journal_title=Front Plant Sci; citation_title=Open or close the gate—stomata action under the control of phytohormones in drought stress conditions; citation_author=A Daszkowska-Golec, I Szarejko; citation_publication_date=2013; citation_id=CR9 citation_journal_title=Plant Cell; citation_title=12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis; citation_author=A Dave, ML Hernández, Z He, VME Andriotis, FE Vaistij, TR Larson, IA Graham; citation_volume=23; citation_publication_date=2011; citation_pages=583-599; citation_doi=10.1105/tpc.110.081489; citation_id=CR10 citation_journal_title=Physiol Plant; citation_title=Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions; citation_author=C Ollas, B Hernando, V Arbona, A Gómez-Cadenas; citation_volume=147; citation_publication_date=2013; citation_pages=296-306; citation_doi=10.1111/j.1399-3054.2012.01659.x; citation_id=CR11 citation_journal_title=Plant Cell Environ; citation_title=Jasmonoyl isoleucine accumulation is needed for abscisic acid build-up in roots of Arabidopsis under water stress conditions; citation_author=C Ollas, V Arbona, A Gómez-Cadenas; citation_publication_date=2015; citation_id=CR12 citation_journal_title=New Phytol; citation_title=Abscisic acid and stomatal closure: a hydraulic conductance conundrum?; citation_author=IC Dodd; citation_volume=197; citation_publication_date=2013; citation_pages=6-8; citation_doi=10.1111/nph.12052; citation_id=CR13 citation_journal_title=J Exp Bot; citation_title=Model-assisted integration of physiological and environmental constraints affecting the dynamic and spatial patterns of root water uptake from soils; citation_author=X Draye, Y Kim, G Lobet, M Javaux; citation_volume=61; citation_publication_date=2010; citation_pages=2145-2155; citation_doi=10.1093/jxb/erq077; citation_id=CR14 citation_journal_title=Plant Physiol; citation_title=Ethylene Response Factor6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis; citation_author=M Dubois, A Skirycz, H Claeys, K Maleux, S Dhondt, S Bodt, R Vanden Bossche, L Milde, T Yoshizumi, M Matsui, D Inzé; citation_volume=162; citation_publication_date=2013; citation_pages=319-332; citation_doi=10.1104/pp.113.216341; citation_id=CR15 citation_journal_title=J Plant Res; citation_title=ABA-mediated transcriptional regulation in response to osmotic stress in plants; citation_author=Y Fujita, M Fujita, K Shinozaki, K Yamaguchi-Shinozaki; citation_volume=124; citation_publication_date=2011; citation_pages=509-525; citation_doi=10.1007/s10265-011-0412-3; citation_id=CR16 citation_journal_title=J Exp Bot; citation_title=Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants; citation_author=ME Ghanem, A Albacete, AC Smigocki, I Frébort, H Pospíilová, C Martínez-Andújar, M Acosta, J Sánchez-Bravo, S Lutts, IC Dodd, F Pérez-Alfocea; citation_volume=62; citation_publication_date=2011; citation_pages=125-140; citation_doi=10.1093/jxb/erq266; citation_id=CR17 citation_journal_title=Plant Physiol; citation_title=Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth; citation_author=A Harb, A Krishnan, MMR Ambavaram, A Pereira; citation_volume=154; citation_publication_date=2010; citation_pages=1254-1271; citation_doi=10.1104/pp.110.161752; citation_id=CR18 citation_journal_title=Plant J; citation_title=Research on plant abiotic stress responses in the post-genome era: past, present and future; citation_author=T Hirayama, K Shinozaki; citation_volume=61; citation_publication_date=2010; citation_pages=1041-1052; citation_doi=10.1111/j.1365-313X.2010.04124.x; citation_id=CR19 citation_journal_title=Plant Physiol; citation_title=Involvement of endogenous abscisic acid in methyl jasmonate-induced stomatal closure in Arabidopsis; citation_author=MA Hossain, S Munemasa, M Uraji, Y Nakamura, IC Mori, Y Murata; citation_volume=156; citation_publication_date=2011; citation_pages=430-438; citation_doi=10.1104/pp.111.172254; citation_id=CR20 citation_journal_title=Proc Natl Acad Sci USA; citation_title=Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice; citation_author=H Hu, M Dai, J Yao, B Xiao, X Li, Q Zhang, L Xiong; citation_volume=103; citation_publication_date=2006; citation_pages=12987-12992; citation_doi=10.1073/pnas.0604882103; citation_id=CR21 citation_journal_title=Plant Physiol; citation_title=Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions; citation_author=JS Jeong, YS Kim, KH Baek, H Jung, S-H Ha, Y Do Choi, M Kim, C Reuzeau, J-K Kim; citation_volume=153; citation_publication_date=2010; citation_pages=185-197; citation_doi=10.1104/pp.110.154773; citation_id=CR22 citation_journal_title=J Exp Bot; citation_title=Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal; citation_author=F Jiang, W Hartung; citation_volume=59; citation_publication_date=2008; citation_pages=37-43; citation_doi=10.1093/jxb/erm127; citation_id=CR23 citation_journal_title=Plant Signal Behav; citation_title=The RHA2a-interacting proteins anac019 and anac055 may play a dual role in regulating aba response and jasmonate response; citation_author=H Jiang, H Li, Q Bu, C Li; citation_volume=4; citation_publication_date=2009; citation_pages=464-466; citation_doi=10.4161/psb.4.5.8543; citation_id=CR24 citation_journal_title=Trends Plant Sci; citation_title=Diverse roles of jasmonates and ethylene in abiotic stress tolerance; citation_author=K Kazan; citation_volume=20; citation_publication_date=2015; citation_pages=219-229; citation_doi=10.1016/j.tplants.2015.02.001; citation_id=CR25 citation_journal_title=Mol Plant; citation_title=MYC2: the master in action; citation_author=K Kazan, JM Manners; citation_volume=6; citation_publication_date=2013; citation_pages=686-703; citation_doi=10.1093/mp/sss128; citation_id=CR26 citation_journal_title=Plant Physiol; citation_title=Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice 1[W][OA]; citation_author=EH Kim, YS Kim, S-H Park, YJ Koo, YD Choi, Y-Y Chung, I-J Lee, J-K Kim; citation_volume=149; citation_publication_date=2009; citation_pages=1751-1760; citation_doi=10.1104/pp.108.134684; citation_id=CR27 citation_journal_title=Irrig Sci; citation_title=Measurement of plant water status: historical perspectives and current concerns; citation_author=PJ Kramer; citation_volume=9; citation_publication_date=1988; citation_pages=275-287; citation_doi=10.1007/BF00296703; citation_id=CR28 citation_journal_title=Planta; citation_title=Involvement of root ABA and hydraulic conductivity in the control of water relations in wheat plants exposed to increased evaporative demand; citation_author=G Kudoyarova, S Veselova, W Hartung, R Farhutdinov, D Veselov, G Sharipova; citation_volume=233; citation_publication_date=2011; citation_pages=87-94; citation_doi=10.1007/s00425-010-1286-7; citation_id=CR29 citation_journal_title=Chin Sci Bull; citation_title=Regulatory role of DREB transcription factors in plant drought, salt and cold tolerance; citation_author=Q Liu, N Zhao, K Yamaguch-Shinozaki, K Shinozaki; citation_volume=45; citation_publication_date=2000; citation_pages=970-975; citation_doi=10.1007/BF02884972; citation_id=CR30 citation_journal_title=J Exp Bot; citation_title=Ethylene independent induction of lycopene biosynthesis in tomato fruits by jasmonates; citation_author=L Liu, J Wei, M Zhang, L Zhang, C Li, Q Wang; citation_volume=63; citation_publication_date=2012; citation_pages=5751-5762; citation_doi=10.1093/jxb/ers224; citation_id=CR31 citation_journal_title=Plant Cell; citation_title=ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense; citation_author=O Lorenzo, R Piqueras, JJ Sánchez-Serrano, R Solano; citation_volume=15; citation_publication_date=2003; citation_pages=165-178; citation_doi=10.1105/tpc.007468; citation_id=CR32 citation_journal_title=Plant Cell; citation_title=JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in arabidopsis; citation_author=O Lorenzo, JM Chico, JJ Sánchez-Serrano, R Solano; citation_volume=16; citation_publication_date=2004; citation_pages=1938-1950; citation_doi=10.1105/tpc.022319; citation_id=CR33 citation_journal_title=PLoS One; citation_title=ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis; citation_author=CS Moffat, RA Ingle, DL Wathugala, NJ Saunders, H Knight, MR Knight; citation_volume=7; citation_publication_date=2012; citation_pages=e35995; citation_doi=10.1371/journal.pone.0035995; citation_id=CR34 citation_journal_title=PLoS Biol; citation_title=An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in arabidopsis; citation_author=J-L Montillet, N Leonhardt, S Mondy, S Tranchimand, D Rumeau, M Boudsocq, AV Garcia, T Douki, J Bigeard, C Laurière, A Chevalier, C Castresana, H Hirt; citation_publication_date=2013; citation_id=CR35 citation_journal_title=Plant Physiol; citation_title=The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production; citation_author=S Munemasa, K Oda, M Watanabe-Sugimoto, Y Nakamura, Y Shimoishi, Y Murat; citation_volume=143; citation_publication_date=2007; citation_pages=1398-1407; citation_doi=10.1104/pp.106.091298; citation_id=CR100 citation_journal_title=Plant Signal Behav; citation_title=Methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid in guard cells; citation_author=S Munemasa, IC Mori, Y Murata; citation_volume=6; citation_publication_date=2011; citation_pages=939-941; citation_doi=10.4161/psb.6.7.15439; citation_id=CR36 citation_journal_title=Curr Opin Plant Biol; citation_title=Mechanisms of abscisic acid-mediated control of stomatal aperture; citation_author=S Munemasa, F Hauser, J Park, R Waadt, B Brandt, JI Schroeder; citation_volume=28; citation_publication_date=2015; citation_pages=154-162; citation_doi=10.1016/j.pbi.2015.10.010; citation_id=CR37 citation_journal_title=Plant J; citation_title=Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice; citation_author=K Nakashima, L-SP Tran, D Nguyen, M Fujita, K Maruyama, D Todaka, Y Ito, N Hayashi, K Shinozaki, K Yamaguchi-Shinozaki; citation_volume=51; citation_publication_date=2007; citation_pages=617-630; citation_doi=10.1111/j.1365-313X.2007.03168.x; citation_id=CR38 citation_journal_title=Biochim Biophys Acta; citation_title=NAC transcription factors in plant abiotic stress responses; citation_author=K Nakashima, H Takasaki, J Mizoi, K Shinozaki, K Yamaguchi-Shinozaki; citation_volume=1819; citation_publication_date=2012; citation_pages=97-103; citation_doi=10.1016/j.bbagrm.2011.10.005; citation_id=CR39 citation_journal_title=Annu Rev Plant Biol; citation_title=Abscisic acid biosynthesis and catabolism; citation_author=E Nambara, A Marion-Poll; citation_volume=56; citation_publication_date=2005; citation_pages=165-185; citation_doi=10.1146/annurev.arplant.56.032604.144046; citation_id=CR40 citation_journal_title=Genes Genet Syst; citation_title=OsNAC6, a member of the NAC gene family, is induced by various stresses in rice; citation_author=T Ohnishi, S Sugahara, T Yamada, K Kikuchi, Y Yoshiba, H-Y Hirano, N Tsutsumi; citation_volume=80; citation_publication_date=2005; citation_pages=135-139; citation_doi=10.1266/ggs.80.135; citation_id=CR41 citation_journal_title=New Phytol; citation_title=The dual effect of abscisic acid on stomata; citation_author=F Pantin, F Monnet, D Jannaud, JM Costa, J Renaud, B Muller, T Simonneau, B Genty; citation_volume=197; citation_publication_date=2013; citation_pages=65-72; citation_doi=10.1111/nph.12013; citation_id=CR42 citation_journal_title=Plant Growth Regul; citation_title=Drought and drought tolerance; citation_author=JB Passioura; citation_volume=20; citation_publication_date=1996; citation_pages=79-83; citation_doi=10.1007/BF00024003; citation_id=CR43 citation_journal_title=Plant Cell Environ; citation_title=Long-distance abscisic acid signalling under different vertical soil moisture gradients depends on bulk root water potential and average soil water content in the root zone; citation_author=J Puértolas, R Alcobendas, JJ Alarcón, IC Dodd; citation_volume=36; citation_publication_date=2013; citation_pages=1465-1475; citation_doi=10.1111/pce.12076; citation_id=CR44 citation_journal_title=Trends Plant Sci; citation_title=NAC proteins: regulation and role in stress tolerance; citation_author=S Puranik, PP Sahu, PS Srivastava, M Prasad; citation_volume=17; citation_publication_date=2012; citation_pages=369-381; citation_doi=10.1016/j.tplants.2012.02.004; citation_id=CR45 citation_journal_title=BMC Genom; citation_title=Tobacco drought stress responses reveal new targets for Solanaceae crop improvement; citation_author=RC Rabara, P Tripathi, RN Reese, DL Rushton, D Alexander, MP Timko, QJ Shen, PJ Rushton; citation_volume=16; citation_publication_date=2015; citation_pages=484; citation_doi=10.1186/s12864-015-1575-4; citation_id=CR46 citation_journal_title=Plant Cell Rep; citation_title=Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress; citation_author=A Roychoudhury, S Paul, S Basu; citation_volume=32; citation_publication_date=2013; citation_pages=985-1006; citation_doi=10.1007/s00299-013-1414-5; citation_id=CR47 citation_journal_title=Plant Cell Environ; citation_title=Enhancement of root hydraulic conductivity by methyl jasmonate and the role of calcium and abscisic acid in this process; citation_author=B Sánchez-Romera, JM Ruiz-Lozano, G Li, D-T Luu, MDC Martínez-Ballesta, M Carvajal, AM Zamarreño, JM García-Mina, C Maurel, R Aroca; citation_volume=37; citation_publication_date=2014; citation_pages=995-1008; citation_doi=10.1111/pce.12214; citation_id=CR48 citation_journal_title=Plant Physiol; citation_title=Functional convergence of oxylipin and abscisic acid pathways controls stomatal closure in response to drought; citation_author=T Savchenko, VA Kolla, C-Q Wang, Z Nasafi, DR Hicks, B Phadungchob, WE Chehab, F Brandizzi, J Froehlich, K Dehesh; citation_volume=164; citation_publication_date=2014; citation_pages=1151-1160; citation_doi=10.1104/pp.113.234310; citation_id=CR49 citation_journal_title=Plant J; citation_title=OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice; citation_author=J-S Seo, J Joo, M-J Kim, Y-K Kim, BH Nahm, SI Song, J-J Cheong, JS Lee, J-K Kim, YD Choi; citation_volume=65; citation_publication_date=2011; citation_pages=907-921; citation_doi=10.1111/j.1365-313X.2010.04477.x; citation_id=CR50 citation_journal_title=PLoS One; citation_title=Ethylene response factor 6 is a regulator of reactive oxygen species signaling in Arabidopsis; citation_author=N Sewelam, K Kazan, SR Thomas-Hall, BN Kidd, JM Manners, PM Schenk; citation_volume=8; citation_publication_date=2013; citation_pages=e70289; citation_doi=10.1371/journal.pone.0070289; citation_id=CR51 citation_journal_title=Plant J; citation_title=Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA?; citation_author=A Shatil-Cohen, Z Attia, M Moshelion; citation_volume=67; citation_publication_date=2011; citation_pages=72-80; citation_doi=10.1111/j.1365-313X.2011.04576.x; citation_id=CR52 citation_journal_title=Plant Physiol; citation_title=Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure; citation_author=D Suhita, AS Raghavendra, JM Kwak, A Vavasseur; citation_volume=134; citation_publication_date=2004; citation_pages=1536-1545; citation_doi=10.1104/pp.103.032250; citation_id=CR53 Tardieu F (2012) Plant tolerance to drought, the solutions exist in nature [Tolérance des plantes à la sécheresse, des solutions existent dans la nature]. Biofutur 42–44 + 46 citation_journal_title=Plant J; citation_title=Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid; citation_author=AJ Thompson, AC Jackson, RC Symonds, BJ Mulholland, AR Dadswell, PS Blake, A Burbidge, IB Taylor; citation_volume=23; citation_publication_date=2000; citation_pages=363-374; citation_doi=10.1046/j.1365-313x.2000.00789.x; citation_id=CR55 citation_journal_title=Plant Cell Environ; citation_title=Regulation and manipulation of ABA biosynthesis in roots; citation_author=AJ Thompson, BJ Mulholland, AC Jackson, JMT McKee, HW Hilton, RC Symonds, T Sonneveld, A Burbidge, P Stevenson, IB Taylor; citation_volume=30; citation_publication_date=2007; citation_pages=67-78; citation_doi=10.1111/j.1365-3040.2006.01606.x; citation_id=CR56 citation_journal_title=Plant Cell Physiol; citation_title=Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport; citation_author=T Umezawa, K Nakashima, T Miyakawa, T Kuromori, M Tanokura, K Shinozaki, K Yamaguchi-Shinozaki; citation_volume=51; citation_publication_date=2010; citation_pages=1821-1839; citation_doi=10.1093/pcp/pcq156; citation_id=CR57 citation_journal_title=Field Crop Res; citation_title=Root hydraulics: the forgotten side of roots in drought adaptation; citation_author=V Vadez; citation_volume=165; citation_publication_date=2014; citation_pages=15-24; citation_doi=10.1016/j.fcr.2014.03.017; citation_id=CR58 citation_journal_title=Biotechnol Adv; citation_title=Action of jasmonates in plant stress responses and development—applied aspects; citation_author=C Wasternack; citation_volume=32; citation_publication_date=2014; citation_pages=31-39; citation_doi=10.1016/j.biotechadv.2013.09.009; citation_id=CR59 citation_journal_title=Plant J; citation_title=In planta ORFeome analysis by large-scale over-expression of GATEWAY®-compatible cDNA clones: screening of ERF transcription factors involved in abiotic stress defense; citation_author=C Weiste, T Iven, U Fischer, L Oñate-Sánchez, W Dröge-Laser; citation_volume=52; citation_publication_date=2007; citation_pages=382-390; citation_doi=10.1111/j.1365-313X.2007.03229.x; citation_id=CR60 citation_journal_title=Photosynthetica; citation_title=Effects of osmotic- and high-light stresses on PSII efficiency of attached and detached leaves of three tree species adapted to different water regimes; citation_author=J-H Weng, C-T Chien, C-W Chen, X-M Lai; citation_volume=49; citation_publication_date=2011; citation_pages=555-563; citation_doi=10.1007/s11099-011-0072-5; citation_id=CR61 citation_journal_title=Plant Cell Environ; citation_title=ABA-based chemical signalling: the co-ordination of responses to stress in plants; citation_author=S Wilkinson, WJ Davies; citation_volume=25; citation_publication_date=2002; citation_pages=195-210; citation_doi=10.1046/j.0016-8025.2001.00824.x; citation_id=CR62 citation_journal_title=Annu Rev Plant Biol; citation_title=Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses; citation_author=K Yamaguchi-Shinozaki, K Shinozaki; citation_volume=57; citation_publication_date=2006; citation_pages=781-803; citation_doi=10.1146/annurev.arplant.57.032905.105444; citation_id=CR63 citation_journal_title=Plant Cell Rep; citation_title=Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis; citation_author=X Yang, X Wang, L Ji, Z Yi, C Fu, J Ran, R Hu, G Zhou; citation_volume=34; citation_publication_date=2015; citation_pages=943-958; citation_doi=10.1007/s00299-015-1756-2; citation_id=CR64 citation_journal_title=Curr Opin Plant Biol; citation_title=ABA-dependent and ABA-independent signaling in response to osmotic stress in plants; citation_author=T Yoshida, J Mogami, K Yamaguchi-Shinozaki; citation_volume=21; citation_publication_date=2014; citation_pages=133-139; citation_doi=10.1016/j.pbi.2014.07.009; citation_id=CR65 citation_journal_title=Bioinformatics; citation_title=Cis-regulatory element based targeted gene finding: genome-wide identification of abscisic acid- and abiotic stress-responsive genes in Arabidopsis thaliana; citation_author=W Zhang, J Ruan, T-HD Ho, Y You, T Yu, RS Quatrano; citation_volume=21; citation_publication_date=2005; citation_pages=3074-3081; citation_doi=10.1093/bioinformatics/bti490; citation_id=CR66 citation_journal_title=Int J Mol Sci; citation_title=Modulation role of abscisic acid (ABA) on growth, water relations and glycinebetaine metabolism in two maize (zea mays L.) cultivars under drought stress; citation_author=L Zhang, M Gao, J Hu, X Zhang, K Wang, M Ashraf; citation_volume=13; citation_publication_date=2012; citation_pages=3189-3202; citation_doi=10.3390/ijms13033189; citation_id=CR67