Abstract
Accumulation of the stress hormone abscisic acid (ABA) induces many cellular mechanisms associated with drought resistance. Recent years have seen a rapid advance in our knowledge of how increased ABA levels are perceived by ABA receptors, particularly the PYL/RCAR receptors, but there has been relatively less new information about how ABA accumulation is controlled and matched to stress severity. ABA synthesis and catabolism, conjugation and deconjugation to glucose, and ABA transport all are involved in controlling ABA levels. This highly buffered system of ABA metabolism represents both a challenge and opportunity in developing a mechanistic understanding of how plants detect and respond to drought. Recent data have also shown that direct manipulation of cytokinin levels in transgenic plants has dramatic effect on drought phenotypes and prompted new interest in the role of cytokinins and cytokinin signaling in drought. Both ABA and cytokinins will continue to be major foci of drought research but likely with different trajectories both in terms of basic research and in translational research aimed at increasing plant performance during drought.
Similar content being viewed by others
References
Alvarez S, Choudhury SR, Hicks LM, Pandey S (2013) Quantitative proteomics-based analysis supports a significant role of GTG proteins in regulation of ABA response in Arabidopsis roots. J Proteome Res 12:1487–1501. doi:10.1021/pr301159u
Bauer H et al (2013) The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Curr Biol 23:53–57. doi:10.1016/j.cub.2012.11.022
Bhaskara GB, Thao Thi N, Verslues PE (2012) Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiol 160:379–395. doi:10.1104/pp.112.202408
Boursiac Y, Leran S, Corratge-Faillie C, Gojon A, Krouk G, Lacombe B (2013) ABA transport and transporters. Trends Plant Sci 18:325–333. doi:10.1016/j.tplants.2013.01.007
Brandt B et al (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109:10593–10598. doi:10.1073/pnas.1116590109
Brenner WG, Ramireddy E, Heyl A, Schmülling T (2012) Gene regulation by cytokinin. Front Plant Sci. doi:10.3389/fpls.2012.00008
Cao MJ et al (2013) An ABA-mimicking ligand that reduces water loss and promotes drought resistance in plants. Cell Res 23:1043–1054. doi:10.1038/cr.2013.95
Christmann A, Hoffmann T, Teplova I, Grill E, Muller A (2005) Generation of active pools of abscisic acid revealed by in vivo Imaging of water-stressed Arabidopsis. Plant Physiol 137:209–219. doi:10.1104/pp.104.053082
Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant J 52:167–174. doi:10.1111/j.1365-313X.2007.03234.x
Claeys H, Inze D (2013) The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol 162:1768–1779. doi:10.1104/pp.113.220921
Creelman RA, Zeevaart JAD (1985) Abscisic acid accumulation in spinach leaf slices in the presence of penetrating and nonpenetrating solutes. Plant Physiol 77:25–28. doi:10.1104/pp.77.1.25
Cutler AJ, Krochko JE (1999) Formation and breakdown of ABA. Trends Plant Sci 4:472–478. doi:10.1016/s1360-1385(99)01497-1
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Ann Rev Plant Biol 61:651–679. doi:10.1146/annurev-arplant-042809-112122
Davies WJ, Kudoyarova G, Hartung W (2005) Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought. J Plant Growth Regul 24:285–295. doi:10.1007/s00344-005-0103-1
Dong T, Xu ZY, Park Y, Kim DH, Lee Y, Hwang I (2014) Abscisic acid uridine diphosphate glucosyltransferases play a crucial role in abscisic acid homeostasis in Arabidopsis. Plant Physiol 165:277–289. doi:10.1104/pp.114.239210
Du S-Y et al (2012) Roles of the different components of magnesium chelatase in abscisic acid signal transduction. Plant Mol Biol 80:519–537. doi:10.1007/s11103-012-9965-3
Dupeux F et al (2011) A thermodynamic switch modulates abscisic acid receptor sensitivity. EMBO J 30:4171–4184. doi:10.1038/emboj.2011.294
Endo A et al (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147:1984–1993. doi:10.1104/pp.108.116632
Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452. doi:10.1093/jxb/err004
Fujii H et al (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–664. doi:10.1038/nature08599
Gan SS, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988. doi:10.1126/science.270.5244.1986
Gao YJ, Zeng QN, Guo JJ, Cheng J, Ellis BE, Chen JG (2007) Genetic characterization reveals no role for the reported ABA receptor, GCR2, in ABA control of seed germination and early seedling development in Arabidopsis. Plant J 52:1001–1013. doi:10.1111/j.1365-313X.2007.03291.x
Ghanem ME et al (2011) Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 62:125–140. doi:10.1093/jxb/erq266
Gonzalez-Guzman M et al (2012) Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 24:2483–2496. doi:10.1105/tpc.112.098574
Guo JJ, Zeng QN, Emami M, Ellis BE, Chen JG (2008) The GCR2 gene family is not required for aba control of seed germination and early seedling development in Arabidopsis. PLoS One. doi:10.1371/journal.pone.0002982
Hao Q et al (2011) The molecular basis of ABA-independent inhibition of PP2Cs by a subclass of PYL proteins. Mol Cell 42:662–672. doi:10.1016/j.molcel.2011.05.011
Hartung W, Sauter A, Hose E (2002) Abscisic acid in the xylem: where does it come from, where does it go to? J Exp Bot 53:27–32. doi:10.1093/jexbot/53.366.27
Haswell ES, Verslues PE (2015) The ongoing search for the molecular basis of plant osmosensing. J Gen Physiol 145:389–394. doi:10.1085/jgp.201411295
Hauser F, Waadtl R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:R346–R355. doi:10.1016/j.cub.2011.03.015
Havlova M et al (2008) The role of cytokinins in responses to water deficit in tobacco plants over-expressing trans-zeatin O-glucosyltransferase gene under 35S or SAG12 promoters. Plant Cell Environ 31:341–353. doi:10.1111/j.1365-3040.2007.01766.x
Holbrook NM, Shashidhar VR, James RA, Munns R (2002) Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. J Exp Bot 53:1503–1514. doi:10.1093/jexbot/53.373.1503
Hou BK, Lim EK, Higgins GS, Bowles DJ (2004) N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. J Biol Chem 279:47822–47832. doi:10.1074/jbc.M409569200
Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708. doi:10.1101/gad.1953910
Hwang I, Sheen J, Mueller B (2012) Cytokinin signaling networks. Ann Rev Plant Biol 63:353–380
Ishitani M, Xiong LM, Stevenson B, Zhu JK (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: Interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9:1935–1949. doi:10.1105/tpc.9.11.1935
Iuchi S et al (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333. doi:10.1046/j.1365-313x.2001.01096.x
Jeon J et al (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23369–23384. doi:10.1074/jbc.M109.096644
Jin SH, Ma XM, Kojima M, Sakakibara H, Wang YW, Hou BK (2013) Overexpression of glucosyltransferase UGT85A1 influences trans-zeatin homeostasis and trans-zeatin responses likely through O-glucosylation. Planta 237:991–999. doi:10.1007/s00425-012-1818-4
Johnston CA et al (2007) Comment on “A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid”. Science. doi:10.1126/science.1143230
Jones AM (2015) A new look at stress: abscisic acid patterns and dynamics at high-resolution. New Phytol. doi:10.1111/nph.13552
Jones AM, Danielson JA, ManojKumar SN, Lanquar V, Grossmann G, Frommer WB (2014) Abscisic acid dynamics in roots detected with genetically encoded FRET sensors. Elife. doi:10.7554/eLife.01741
Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci USA 107:2355–2360. doi:10.1073/pnas.0909222107
Kang NY, Cho C, Kim NY, Kim J (2012) Cytokinin receptor-dependent and receptor-independent pathways in the dehydration response of Arabidopsis thaliana. J Plant Physiol 169:1382–1391. doi:10.1016/j.jplph.2012.05.007
Kanno Y et al (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc Natl Acad Sci USA 109:9653–9658. doi:10.1073/pnas.1203567109
Kant S, Burch D, Badenhorst P, Palanisamy R, Mason J, Spangenberg G (2015) Regulated expression of a cytokinin biosynthesis gene ipt delays leaf senescence and improves yield under rainfed and irrigated conditions in canola (Brassica napus L.). PLoS One. doi:10.1371/journal.pone.0116349
Kiba T, Takei K, Kojima M, Sakakibara H (2013) Side-chain modification of cytokinins controls shoot growth in Arabidopsis. Dev Cell 27:452–461. doi:10.1016/j.devcel.2013.10.004
Kieber JJ, Schaller GE (2010) The perception of cytokinin: a story 50 years in the making. Plant Physiol 154:487–492. doi:10.1104/pp.110.161596
Ko D et al (2014) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc Natl Acad Sci USA 111:7150–7155. doi:10.1073/pnas.1321519111
Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic, San Diego
Krochko JE, Abrams GD, Loewen MK, Abrams SR, Cutler AJ (1998) (+)-Abscisic acid 8′-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiol 118:849–860. doi:10.1104/pp.118.3.849
Kumar MN, Verslues PE (2015) Stress physiology functions of the Arabidopsis histidine kinase cytokinin receptors. Physiol Plant 154:369–380. doi:10.1111/ppl.12290
Kumar MN, Jane W-N, Verslues PE (2013) Role of the putative osmosensor Arabidopsis histidine kinase1 in dehydration avoidance and low-water-potential response. Plant Physiol 161:942–953. doi:10.1104/pp.112.209791
Kuppu S et al (2013) Water-deficit inducible expression of a cytokinin biosynthetic gene IPT Improves drought tolerance in cotton. PLoS One. doi:10.1371/journal.pone.0064190
Kuromori T et al (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci USA 107:2361–2366. doi:10.1073/pnas.0912516107
Kuromori T, Sugimoto E, Shinozaki K (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 67:885–894. doi:10.1111/j.1365-313X.2011.04641.x
Kushiro T et al (2004) The Arabidopsis cytochrome P450CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656. doi:10.1038/sj.emboj.7600121
Lee KH et al (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120. doi:10.1016/j.cell.2006.07.034
Lin PC, Hwang SG, Endo A, Okamoto M, Koshiba T, Cheng WH (2007) Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis promotes seed dormancy and stress tolerance. Plant Physiol 143:745–758. doi:10.1104/pp.106.084103
Liu XG, Yue YL, Li B, Nie YL, Li W, Wu WH, Ma LG (2007) A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315:1712–1716. doi:10.1126/science.1135882
Liu Z et al (2015) UDP-glucosyltransferase71c5, a major glucosyltransferase, mediates abscisic acid homeostasis in Arabidopsis. Plant Physiol 167:1659–1670. doi:10.1104/pp.15.00053
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068. doi:10.1126/science.1172408
Mackova H et al (2013) Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot 64:2805–2815. doi:10.1093/jxb/ert131
Marchadier E, Hetherington AM (2014) Involvement of two-component signalling systems in the regulation of stomatal aperture by light in Arabidopsis thaliana. New Phytol 203:462–468. doi:10.1111/nph.12813
Marshall A et al (2012) Tackling drought stress: receptor-like kinases present new approaches. Plant Cell 24:2262–2278. doi:10.1105/tpc.112.096677
Martin RC, Mok MC, Mok DWS (1999) Isolation of a cytokinin gene, ZOG1, encoding zeatin O-glucosyltransferase from Phaseolus lunatus. Proc Natl Acad Sci USA 96:284–289. doi:10.1073/pnas.96.1.284
Melcher K et al (2009) A gate–latch–lock mechanism for hormone signalling by abscisic acid receptors. Nature 462:602–608. doi:10.1038/nature08613
Merewitz EB, Du H, Yu W, Liu Y, Gianfagna T, Huang B (2012) Elevated cytokinin content in IPT transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation. J Exp Bot 63:1315–1328. doi:10.1093/jxb/err372
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Ann Rev Plant Biol 56:165–185. doi:10.1146/annurev.arplant.56.032604.144046
Nishimura N et al (2009) Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326:1373–1379. doi:10.1126/science.1181829
Nishimura N et al (2010) PYR/PYL/RCAR family members are major in vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61:290–299. doi:10.1111/j.1365-313X.2009.04054.x
Nishiyama R et al (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183. doi:10.1105/tpc.111.087395
Nishiyama R et al (2013) Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc Natl Acad Sci USA 110:4840–4845. doi:10.1073/pnas.1302265110
Okamoto M et al (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107. doi:10.1104/pp.106.079475
Okamoto M, Kushiro T, Jikumaru Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2011) ABA 9′-hydroxylation is catalyzed by CYP707A in Arabidopsis. Phytochemistry 72:717–722. doi:10.1016/j.phytochem.2011.02.004
Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136:136–148. doi:10.1016/j.cell.2008.12.026
Park SY et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071. doi:10.1126/science.1173041
Park SY, Peterson FC, Mosquna A, Yao J, Volkman BF, Cutler SR (2015) Agrochemical control of plant water use using engineered abscisic acid receptors. Nature 520:545–548
Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol J 9:747–758. doi:10.1111/j.1467-7652.2010.00584.x
Peterson FC et al (2010) Structural basis for selective activation of ABA receptors. Nat Struct Mol Biol 17:1109–1113. doi:10.1038/nsmb.1898
Pierce M, Raschke K (1980) Correlation between loss of turgor and accumulation of abscisic acid in detached leaves. Planta 148:174–182. doi:10.1007/bf00386419
Pierce M, Raschke K (1981) Synthesis and metabolism of abscisic acid in detached leaves of Phaseolus vulgaris L. after loss and recovery of turgor. Planta 153:156–165. doi:10.1007/bf00384097
Priest DM et al (2006) Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J 46:492–502. doi:10.1111/j.1365-313X.2006.02701.x
Qin XQ, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96:15354–15361. doi:10.1073/pnas.96.26.15354
Qin XQ, Zeevaart JAD (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128:544–551. doi:10.1104/pp.010663
Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401. doi:10.1016/j.tplants.2010.04.006
Ren H et al (2007) Dynamic analysis of ABA accumulation in relation to the rate of ABA catabolism in maize tissues under water deficit. J Exp Bot 58:211–219. doi:10.1093/jxb/erl117
Risk JM, Day CL, Macknight RC (2009) Reevaluation of abscisic acid-binding assays shows that G-protein-coupled receptor2 does not bind abscisic acid. Plant Physiol 150:6–11. doi:10.1104/pp.109.135749
Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636. doi:10.1073/pnas.0709453104
Rivero RM, Shulaev V, Blumwald E (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol 150:1530–1540. doi:10.1104/pp.109.139378
Rivero RM, Gimeno J, Van Deynze A, Walia H, Blumwald E (2010) Enhanced cytokinin synthesis in tobacco plants expressing P-SARK:IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol 51:1929–1941. doi:10.1093/pcp/pcq143
Saab IN, Sharp RE (1989) Non-hydraulic signals from maize roots in drying soil—inhibition of leaf elongation but not stomatal conductance. Planta 179:466–474. doi:10.1007/bf00397586
Sauter A, Dietz KJ, Hartung W (2002) A possible stress physiological role of abscisic acid conjugates in root-to-shoot signalling. Plant Cell Env 25:223–228. doi:10.1046/j.1365-3040.2002.00747.x
Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874. doi:10.1126/science.276.5320.1872
Schwartz SH, Qin XQ, Zeevaart JAD (2003) Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol 131:1591–1601. doi:10.1104/pp.102.017921
Shang Y et al (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935. doi:10.1105/tpc.110.073874
Sharma S, Verslues PE (2010) Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant Cell Environ 33:1838–1851. doi:10.1111/j.1365-3040.2010.02188.x
Sharp RE (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25:211–222. doi:10.1046/j.1365-3040.2002.00798.x
Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53:33–37. doi:10.1093/jexbot/53.366.33
Shen YY et al (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826. doi:10.1038/nature05176
Soon FF et al (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335:85–88. doi:10.1126/science.1215106
Szostkiewicz I et al (2010) Closely related receptor complexes differ in their ABA selectivity and sensitivity. Plant J 61:25–35. doi:10.1111/j.1365-313X.2009.04025.x
Takeuchi J et al (2014) Designed abscisic acid analogs as antagonists of PYL-PP2C receptor interactions. Nat Chem Biol 10:477–482. doi:10.1038/nchembio.1524
Tan BC, Cline K, McCarty DR (2001) Localization and targeting of the VP14 epoxy-carotenoid dioxygenase to chloroplast membranes. Plant J 27:373–382. doi:10.1046/j.1365-313X.2001.01102.x
Tan BC, Joseph LM, Deng WT, Liu LJ, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56. doi:10.1046/j.1365-313X.2003.01786.x
Tran LSP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623
Tsuzuki T et al (2011) Mg-chelatase H subunit affects ABA signaling in stomatal guard cells, but is not an ABA receptor in Arabidopsis thaliana. J Plant Res 124:527–538. doi:10.1007/s10265-011-0426-x
Umezawa T et al (2006) CYP707A3, a major ABA 8′-hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. Plant J 46:171–182. doi:10.1111/j.1365-313X.2006.02683.X
Umezawa T, Sugiyama N, Takahashi F, Anderson JC, Ishihama Y, Peck SC, Shinozaki K (2013) Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci Signal. doi:10.1126/scisignal.2003509
Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743
Verslues PE, Bray EA (2004) LWR1 and LWR2 are required for osmoregulation and osmotic adjustment in Arabidopsis. Plant Physiol 136:2831–2842. doi:10.1104/pp.104.045856
Verslues PE, Bray EA (2006) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J Exp Bot 57:201–212. doi:10.1093/jxb/erj026
Verslues PE, Zhu JK (2005) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans 33:375–379
Verslues PE, Zhu JK (2007) New developments in abscisic acid perception and metabolism. Curr Opin Plant Biol 10:447–452. doi:10.1016/j.pbi.2007.08.004
Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu JH, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539. doi:10.1111/j.1365-313X.2005.02593.x
Verslues PE, Bhaskara GB, Kesari R, Kumar MN (2013) Drought tolerance mechanisms and their molecular basis. In: Jenks MA, Hasegawa PM (eds) Plant abiotic stress, 2nd edn. Wiley, Ames, pp 15–46
Waadt R, Hitomi K, Nishimura N, Hitomi C, Adams SR, Getzoff ED, Schroeder JI (2014) FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis. Elife. doi:10.7554/eLife.01739
Wang J, Ma XM, Kojima M, Sakakibara H, Hou BK (2011a) N-glucosyltransferase UGT76C2 is involved in cytokinin homeostasis and cytokinin response in Arabidopsis thaliana. Plant Cell Physiol 52:2200–2213. doi:10.1093/pcp/pcr152
Wang ZY, Xiong LM, Li WB, Zhu JK, Zhu JH (2011b) The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis. Plant Cell 23:1971–1984. doi:10.1105/tpc.110.081943
Wang PC et al (2013) Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc Natl Acad Sci USA 110:11205–11210. doi:10.1073/pnas.1308974110
Wang ZY, Gehring C, Zhu JH, Li FM, Zhu JK, Xiong LM (2015) The Arabidopsis vacuolar sorting receptor1 is required for osmotic stress-induced abscisic acid biosynthesis. Plant Physiol 167:137–152. doi:10.1104/pp.114.249268
Werner T, Nehnevajova E, Kollmer I, Novak O, Strnad M, Kramer U, Schmulling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920. doi:10.1105/tpc.109.072694
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210. doi:10.1046/j.0016-8025.2001.00824.x
Wilson ME, Basu MR, Bhaskara GB, Verslues PE, Haswell ES (2014) Plastid osmotic stress activates cellular stress responses in Arabidopsis. Plant Physiol 165:119–128. doi:10.1104/pp.114.236620
Wu FQ et al (2009) The magnesium-chelatase H subunit binds abscisic acid and functions in abscisic acid signaling: new evidence in Arabidopsis. Plant Physiol 150:1940–1954. doi:10.1104/pp.109.140731
Xiong L, Lee H, Ishitani M, Zhu J-K (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277:8588–8596. doi:10.1074/jbc.M109275200
Xu Z-J, Nakajima M, Suzuki Y, Yamaguchi I (2002) Cloning and characterization of the abscisic acid-specific glucosyltransferase gene from adzuki bean seedlings. Plant Physiol 129:1285–1295. doi:10.1104/pp.001784
Xu ZY et al (2012) A vacuolar beta-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:2184–2199. doi:10.1105/tpc.112.095935
Yuan F et al (2014) OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514:367–371. doi:10.1038/nature13593
Zhang K et al (2014) Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat Commun. doi:10.1038/ncomms4274
Zhou R et al (2004) A new abscisic acid catabolic pathway. Plant Physiol 134:361–369. doi:10.1104/pp.103.030734
Zwack PJ, Rashotte AM (2015) Interactions between cytokinin signalling and abiotic stress responses. J Exp Bot. doi:10.1093/jxb/erv172
Acknowledgments
Work in the Verslues laboratory is supported by funding from Academia Sinica and the Taiwan Ministry of Science and Technology.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Verslues, P.E. ABA and cytokinins: challenge and opportunity for plant stress research. Plant Mol Biol 91, 629–640 (2016). https://doi.org/10.1007/s11103-016-0458-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-016-0458-7