Barley Brassinosteroid Mutants Provide an Insight into Phytohormonal Homeostasis in Plant Reaction to Drought Stress
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
27994612
PubMed Central
PMC5133261
DOI
10.3389/fpls.2016.01824
Knihovny.cz E-zdroje
- Klíčová slova
- barley, brassinosteroids, drought, homeostasis, mutants, phytohormones,
- Publikační typ
- časopisecké články MeSH
Brassinosteroids (BRs) are a class of steroid phytohormones, which regulate various processes of morphogenesis and physiology-from seed development to regulation of flowering and senescence. An accumulating body of evidence indicates that BRs take part in regulation of physiological reactions to various stress conditions, including drought. Many of the physiological functions of BRs are regulated by a complicated, and not fully elucidated network of interactions with metabolic pathways of other phytohormones. Therefore, the aim of this study was to characterize phytohormonal homeostasis in barley (Hordeum vulgare) in reaction to drought and validate role of BRs in regulation of this process. Material of this study included the barley cultivar "Bowman" and five Near-Isogenic Lines (NILs) representing characterized semi-dwarf mutants of several genes encoding enzymes participating in BR biosynthesis and signaling. Analysis of endogenous BRs concentrations in these NILs confirmed that their phenotypes result from abnormalities in BR metabolism. In general, concentrations of 18 compounds, representing various classes of phytohormones, including brassinosteroids, auxins, cytokinins, gibberellins, abscisic acid, salicylic acid and jasmonic acid were analyzed under control and drought conditions in the "Bowman" cultivar and the BR-deficient NILs. Drought induced a significant increase in accumulation of the biologically active form of BRs-castasterone in all analyzed genotypes. Another biologically active form of BRs-24-epi-brassinolide-was identified in one, BR-insensitive NIL under normal condition, but its accumulation was drought-induced in all analyzed genotypes. Analysis of concentration profiles of several compounds representing gibberellins allowed an insight into the BR-dependent regulation of gibberellin biosynthesis. The concentration of the gibberellic acid GA7 was significantly lower in all NILs when compared with the "Bowman" cultivar, indicating that GA7 biosynthesis represents an enzymatic step at which the stimulating effect of BRs on gibberellin biosynthesis occurs. Moreover, the accumulation of GA7 is significantly induced by drought in all the genotypes. Biosynthesis of jasmonic acid is also a BR-dependent process, as all the NILs accumulated much lower concentrations of this hormone when compared with the "Bowman" cultivar under normal condition, however the accumulation of jasmonic acid, abscisic acid and salicylic acid were significantly stimulated by drought.
Department of Plant Physiology University of Agriculture in Krakow Krakow Poland
Franciszek Gorski Institute of Plant Physiology Polish Academy of Sciences Krakow Poland
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Abe H., Takatsuto S., Nakayama M., Yokota T. (1995). 28-Homotyphasterol, a new natural brassinosteroid from rice (Oryza sativa L.) bran. Biosci. Biotech. Biochem. 59, 176–178. 10.1271/bbb.59.176 DOI
Ahmadi S. H., Andersen M. N., Plauborg F., Poulsen R. T., Jensen C. R., Sepaskhah A. R., et al. (2010). Effects of irrigation strategies and soil on field grown potatoes: yield and water productivity. Agric. Water Manag. 97, 1923–1930. 10.1016/j.agwat.2010.07.007 DOI
Bai M. Y., Shang J. X., Oh E., Fan M., Bai Y., Zentella R., et al. . (2012). Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat. Cell Biol. 14, 810–817. 10.1038/ncb2546 PubMed DOI PMC
Bajguz A., Hayat S. (2009). Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol. Biochem. 47, 1–8. 10.1016/j.plaphy.2008.10.002 PubMed DOI
Bajguz A., Tretyn A. (2003). The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62, 1027–1046. 10.1016/S0031-9422(02)00656-8 PubMed DOI
Bari R., Jones J. D. (2009). Role of plant hormones in plant defence responses. Plant Mol. Biol. 69, 473–488. 10.1007/s11103-008-9435-0 PubMed DOI
Chen Z., Zheng Z., Huang J., Lai Z., Fan B. (2009). Biosynthesis of salicylic acid in plants. Plant Signal. Behav. 4, 493–496. 10.4161/psb.4.6.8392 PubMed DOI PMC
Choe S., Schmitz R. J., Fujioka S., Takatsuto S., Lee M. O., Yoshida S., et al. . (2002). Arabidopsis brassinosteroid-insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3-like kinase. Plant Physiol. 130, 1506–1515. 10.1104/pp.010496 PubMed DOI PMC
Chong J., Pierrel M. A., Atanassova R., Werck-Reichhart D., Fritig B., Saindrenan P. (2001). Free and conjugated benzoic acid in tobacco plants and cell cultures. Induced accumulation upon elicitation of defense responses and role as salicylic acid precursors. Plant Physiol. 125, 318–328. 10.1104/pp.125.1.318 PubMed DOI PMC
Chono M., Honda I., Zeniya H., Yoneyama K., Saisho D., Takeda K., et al. . (2003). A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol. 133, 1209–1219. 10.1104/pp.103.026195 PubMed DOI PMC
Choudhary S. P., Yu J. Q., Yamaguchi-Shinozaki K., Shinozaki K., Tran L. S. (2012). Benefits of brassinosteroid crosstalk. Trends Plant Sci. 17, 594–605. 10.1016/j.tplants.2012.05.012 PubMed DOI
Chung Y., Choe V., Fujioka S., Takatsuto S., Han M., Jeon J. S., et al. . (2012). Constitutive activation of brassinosteroid signaling in the Arabidopsis elongated-D/bak1 mutant. Plant Mol. Biol. 80, 489–501. 10.1007/s11103-012-9963-5 PubMed DOI
Chung Y., Kwon S. I., Choe S. (2014). Antagonistic regulation of Arabidopsis growth by brassinosteroids and abiotic stresses. Mol. Cells 37, 795–803. 10.14348/molcells.2014.0127 PubMed DOI PMC
Chung Y., Maharjan P. M., Lee O., Fujioka S., Jang S., Kim B., et al. . (2011). Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabisopsis. Plant J. 66, 564–578. 10.1111/j.1365-313X.2011.04513.x PubMed DOI
Deb A., Grewal R. K., Kundu S. (2016). Regulatory cross-talks and cascades in rice hormone biosynthesis pathways contribute to stress signaling. Front. Plant Sci. 7:1303. 10.3389/fpls.2016.01303 PubMed DOI PMC
Divi U. K., Rahman T., Krishna P. (2010). Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol. 10:151. 10.1186/1471-2229-10-151 PubMed DOI PMC
Dockter C., Gruszka D., Braumann I., Druka A., Druka I., Franckowiak J., et al. . (2014). Induced variations in brassinosteroid genes define barley height and sturdiness, and expand the green revolution genetic toolkit. Plant Physiol. 166, 1912–1927. 10.1104/pp.114.250738 PubMed DOI PMC
Domagalska M. A., Sarnowska E., Nagy F., Davis S. J. (2010). Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PLoS ONE 5:e14012. 10.1371/journal.pone.0014012 PubMed DOI PMC
Druka A., Franckowiak J., Lundqvist U., Bonar N., Alexander J., Houston K., et al. . (2011). Genetic dissection of barley morphology and development. Plant Physiol. 155, 617–627. 10.1104/pp.110.166249 PubMed DOI PMC
Dziurka M., Janeczko A., Juhász C., Gullner G., Oklestková J., Novák O., et al. . (2016). Local and systemic hormonal responses in pepper leaves during compatible and incompatible pepper-tobamovirus interactions. Plant Physiol. Biochem. 109, 355–364. 10.1016/j.plaphy.2016.10.013 PubMed DOI
Ferrero-Serrano A., Assmann S. M. (2016). The α-subunit of the rice heterotrimeric G protein, RGA1, regulates drought tolerance during the vegetative phase in the dwarf rice mutant d1. J. Exp. Bot. 67, 3433–3443. 10.1093/jxb/erw183 PubMed DOI PMC
Gallego-Bartolomé J., Minguet E. G., Grau-Enguix F., Abbas M., Locascio A., Thomas S. G., et al. . (2012). Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 13446–13451. 10.1073/pnas.1119992109 PubMed DOI PMC
Gan L., Wu H., Wu D., Zhang Z., Guo Z., Yang N., et al. . (2015). Methyl jasmonate inhibits lamina joint inclination by repressing brassinosteroid biosynthesis and signaling in rice. Plant Sci. 241, 238–245. 10.1016/j.plantsci.2015.10.012 PubMed DOI
Gruszka D. (2013). Brassinosteroid signaling pathway - new key players and interconnections with other signaling networks crucial for plant development and stress tolerance. Int. J. Mol. Sci. 14, 8740–8774. 10.3390/ijms14058740 PubMed DOI PMC
Gruszka D., Gorniak M., Glodowska E., Wierus E., Oklestkova J., Janeczko A., et al. . (2016). A Reverse-genetics mutational analysis of the barley HvDWARF gene results in identification of a series of alleles and mutants with short stature of various degree and disturbance in BR biosynthesis allowing a new insight into the process. Int. J. Mol. Sci. 17:600. 10.3390/ijms17040600 PubMed DOI PMC
Gruszka D., Szarejko I., Maluszynski M. (2011a). New allele of HvBRI1 gene encoding brassinosteroid receptor in barley. J. Appl. Genet. 52, 257–268. 10.1007/s13353-011-0031-7 PubMed DOI PMC
Gruszka D., Szarejko I., Maluszynski M. (2011b). Identification of barley DWARF gene involved in brassinosteroid synthesis. Plant Growth Regul. 65, 343–358. 10.1007/s10725-011-9607-9 DOI
Hansen M., Chae H. S., Kieber J. J. (2009). Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J. 57, 606–614. 10.1111/j.1365-313X.2008.03711.x PubMed DOI PMC
Hardtke C. S., Dorcey E., Osmont K. S., Sibout R. (2007). Phytohormone collaboration: zooming in on auxin-brassinosteroid interactions. Trends Cell Biol. 17, 485–492. 10.1016/j.tcb.2007.08.003 PubMed DOI
Hayat Q., Hayat S., Irfan M., Ahmad A. (2010). Effect of exogenous salicylic acid under changing environment: a review. Environ. Exp. Bot. 68, 14–25. 10.1016/j.envexpbot.2009.08.005 DOI
Hedden P., Thomas S. G. (2012). Gibberellin biosynthesis and its regulation. Biochem. J. 444, 11–25. 10.1042/BJ20120245 PubMed DOI
Huang D., Wu W., Abrams S. R., Cutler A. J. (2008). The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J. Exp. Bot. 11, 2991–3007. 10.1093/jxb/ern155 PubMed DOI PMC
Jager C. E., Symons G. M., Ross J. J., Reid J. B. (2008). Do brassinosteroids mediate the water stress response? Physiol. Plant. 133, 417–425. 10.1111/j.1399-3054.2008.01057.x PubMed DOI
Jager C. E., Symons G. M., Ross J. J., Smith J. J., Reid J. B. (2005). The brassinosteroid growth response in pea is not mediated by changes in gibberellin content. Planta 221, 141–148. 10.1007/s00425-004-1454-8 PubMed DOI
Janeczko A., Gruszka D., Pociecha E., Dziurka M., Filek M., Jurczyk B., et al. . (2016). Physiological and biochemical characterisation of watered and drought-stressed barley mutants in the HvDWARF gene encoding C6-oxidase involved in brassinosteroid biosynthesis. Plant Physiol. Biochem. 99, 126–141. 10.1016/j.plaphy.2015.12.003 PubMed DOI
Janeczko A., Swaczynova J. (2010). Endogenous brassinosteroids in wheat treated with 24-epibrassinolide. Biol. Plant. 54, 477–482. 10.1007/s10535-010-0084-1 DOI
Joo S. H., Jang M. S., Kim M. K., Lee J. E., Kim S. K. (2015). Biosynthetic relationship between C28-brassinosteroids and C29-brassinosteroids in rice (Oryza sativa) seedlings. Phytochemistry 111, 84–90. 10.1016/j.phytochem.2014.11.006 PubMed DOI
Jung J. H., Lee M., Park C. M. (2010). A transcriptional feedback loop modulating signaling crosstalks between auxin and brassinosteroid in Arabidopsis. Mol. Cells 29, 449–456. 10.1007/s10059-010-0055-6 PubMed DOI
Kagale S., Divi U. K., Krochko J. E., Keller W. A., Krishna P. (2007). Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225, 353–364. 10.1007/s00425-006-0361-6 PubMed DOI
Kim B., Fujioka S., Kwon M., Jeon J., Choe S. (2013). Arabidopsis brassinosteroid-overproducing gulliver3-D/dwarf4-D mutants exhibit altered responses to jasmonic acid and pathogen. Plant Cell Rep. 32, 1139–1149. 10.1007/s00299-012-1381-2 PubMed DOI
Kim B. K., Fujioka S., Takatsuto S., Tsujimoto M., Choe S. (2008). Castasterone is a likely end product of brassinosteroid biosynthetic pathway in rice. Biochem. Biophys. Res. Commun. 374, 614–619. 10.1016/j.bbrc.2008.07.073 PubMed DOI
Kim E. H., Kim Y. S., Park S. H., Koo Y. J., Choi Y. D., Chung Y. Y., et al. . (2009). Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol. 149, 1751–1760. 10.1104/pp.108.134684 PubMed DOI PMC
Kim S. Y., Kim B. H., Lim C. J., Lim C. O., Nam K. H. (2010). Constitutive activation of stress-inducible genes in a brassinosteroid-insensitive 1 (bri1) mutant results in higher tolerance to cold. Physiol. Plant. 138, 191–204. 10.1111/j.1399-3054.2009.01304.x PubMed DOI
Kitanaga Y., Jian C., Hasegawa M., Yazaki J., Kishimoto N., Kikuchi S., et al. . (2006). Sequential regulation of gibberellin, brassinosteroid, and jasmonic acid biosynthesis occurs in rice coleoptiles to control the transcript levels of anti-microbial thionin genes. Biosci. Biotechnol. Biochem. 70, 2410–2419. 10.1271/bbb.60145 PubMed DOI
Krasensky J., Jonak C. (2012). Drought, salt and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593–1608. 10.1093/jxb/err460 PubMed DOI PMC
Kurepin L. V., Qaderi M. M., Back T. G., Reid D. M., Pharis R. P. (2008). A rapid effect of applied brassinolide on abscisic acid concentrations in Brassica napus leaf tissue subjected to short-term heat stress. Plant Growth Regul. 55, 165–167. 10.1007/s10725-008-9276-5 DOI
Li Z. Y., Xu Z. S., He G. Y., Yang G. X., Chen M., Li L. C., et al. . (2012). A mutation in Arabidopsis BSK5 encoding a brassinosteroid-signaling kinase protein affects responses to salinity and abscisic acid. Biochem. Biophys. Res. Commun. 426, 522–527. 10.1016/j.bbrc.2012.08.118 PubMed DOI
Liu Y., Zhao Z., Si J., Di C., Han J., An L. (2009). Brassinosteroids alleviate chilling induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. Plant Growth Regul. 59, 207–214. 10.1007/s10725-009-9405-9 DOI
Llanes A., Andrade A., Alemano S., Luna V. (2016). Alterations of endogenous hormonal levels in plants uncer drought and salinity. Am. J. Plant Sci. 7, 1357–1371. 10.4236/ajps.2016.79129 DOI
Mahajan S., Tuteja N. (2005). Cold, salinity and stresses: an overview. Arch. Biochem. Biophys. 444, 139–158. 10.1016/j.abb.2005.10.018 PubMed DOI
Müssig C., Biesgen C., Lisso J., Uwer U., Weiler E. W., Altmann T. (2000). A novel stress-inducible 12-oxophytodienoate reductase from Arabidopsis thaliana provides a potential link between brassinosteroid-action and jasmonic-acid synthesis. J. Plant Physiol. 157, 143–152. 10.1016/S0176-1617(00)80184-4 DOI
Nakashita H., Yasuda M., Nitta T., Asami T., Fujioka S., Arai Y., et al. . (2003). Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 33, 887–898. 10.1046/j.1365-313X.2003.01675.x PubMed DOI
Nemhauser J. L., Hong F., Chory J. (2006). Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126, 467–475. 10.1016/j.cell.2006.05.050 PubMed DOI
Northey J. G., Liang S., Jamshed M., Deb S., Foo E., Reid J. B., et al. . (2016). Farnesylation mediates brassinosteroid biosynthesis to regulate abscisic acid responses. Nat. Plants 2:16114. 10.1038/nplants.2016.114 PubMed DOI
Outlaw W. H. (2003). Integration of cellular and physiological functions of guard cells. Crit. Rev. Plant Sci. 22, 503–529. 10.1080/713608316 DOI
Ren C., Han C., Peng W., Huang Y., Peng Z., Xiong X., et al. . (2009). A leaky mutation in DWARF4 reveals an antagonistic role of brassinosteroid in the inhibition of root growth by jasmonate in Arabidopsis. Plant Physiol. 151, 1412–1420. 10.1104/pp.109.140202 PubMed DOI PMC
Rodrigues A., Santiago J., Rubio S., Saez A., Osmont K. S., Gadea J., et al. . (2009). The short-rooted phenotype of the brevis radix mutant partly reflects root abscisic acid hypersensitivity. Plant Physiol. 149, 1917–1928. 10.1104/pp.108.133819 PubMed DOI PMC
Ryu H., Cho H., Bae W., Hwang I. (2014). Control of early seedling development by BES1/TPL/HDA19-mediated epigenetic regulation of ABI3. Nat. Commun. 5, 4138. 10.1038/ncomms5138 PubMed DOI
Saini S., Sharma I., Pati K. P. (2015). Versatile roles of brassinosteroid in plants in the context of its homeostasis, signaling and crosstalks. Front. Plant Sci. 6:950. 10.3389/fpls.2015.00950 PubMed DOI PMC
Saisho D., Tanno K., Chono M., Honda I., Kitano H., Takeda K. (2004). Spontaneous brassinolide-insensitive barley mutants “uzu” adapted to East Asia. Breed. Sci. 54, 409–416. 10.1270/jsbbs.54.409 DOI
Salvi S., Druka A., Milner S., Gruszka D. (2014). Induced genetic variation, TILLING and NGS-based cloning, in Biotechnological Approaches to Barley Improvement. Biotechnology in Agriculture and Forestry 69, eds Kumlehn J., Stein N. (Berlin: Heidelberg: Springer-Verlag; ), 287–310.
Schmidt J., Spengler B., Yokota T., Nakayama M., Takatsuto S., Voigt B., et al. (1995). Secasterone, the first naturally occurring 2,3-epoxybrassinosteroid from Secale cereale. Phytochemistry 38, 1095–1097. 10.1016/0031-9422(94)00797-W DOI
Shimada A., Ueguchi-Tanaka M., Sakamoto T., Fujioka S., Takatsuto S., Yoshida S., et al. . (2006). The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid biosynthesis. Plant J. 48, 390–402. 10.1111/j.1365-313X.2006.02875.x PubMed DOI
Steber C. M., McCourt P. (2001). A role for brassinosteroids in germination in Arabidopsis. Plant Physiol. 125, 763–769. 10.1104/pp.125.2.763 PubMed DOI PMC
Symons G. M., Ross J. J., Jager C. E., Reid J. B. (2008). Brassinosteroid transport. J. Exp. Bot. 59, 17–24. 10.1093/jxb/erm098 PubMed DOI
Tarkowská D., Novák O., Oklestkova J., Strnad M. (2016). The determination of 22 natural brassinosteroids in a minute sample of plant tissue by UHPLC–ESI–MS/MS. Anal. Bioanal. Chem. 408, 6799–6812. 10.1007/s00216-016-9807-2 PubMed DOI
Tong H., Xiao Y., Liu D., Gao S., Liu L., Yin Y., et al. . (2014). Brassinosteroid regulates cell elongation by modulating gibbrellin metabolism in rice. Plant Cell 26, 4376–4393. 10.1105/tpc.114.132092 PubMed DOI PMC
Unterholzner S. J., Rozhon W., Papacek M., Ciomas J., Lange T., Kugler K. G., et al. . (2015). Brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell 27, 2261–2272. 10.1105/tpc.15.00433 PubMed DOI PMC
Vriet C., Russinova E., Reuzeau C. (2012). Boosting crop yields with plant steroids. Plant Cell 24, 842–857. 10.1105/tpc.111.094912 PubMed DOI PMC
Wang W., Vinocur B., Altman A. (2003). Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1–14. 10.1007/s00425-003-1105-5 PubMed DOI
Xia X. J., Wang Y. J., Zhou Y. H., Tao Y., Mao W. H., Shi K., et al. . (2009). Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol. 150, 801–814. 10.1104/pp.109.138230 PubMed DOI PMC
Yamaguchi S. (2008). Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 59, 225–251. 10.1146/annurev.arplant.59.032607.092804 PubMed DOI
Yi H. C., Joo S., Nam K. H., Lee J. S., Kang B. G., Kim W. T. (1999). Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.). Plant Mol. Biol. 41, 443–454. 10.1023/A:1006372612574 PubMed DOI
Yuan G. F., Jia C. G., Li Z., Sun B., Zhang L. P., Liu N., et al. (2010). Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. Sci. Hortic. 126, 103–108. 10.1016/j.scienta.2010.06.014 DOI
Zhang A., Zhang J., Zhang J., Ye N., Zhang H., Tan M., et al. . (2011). Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol. 52, 181–192. 10.1093/pcp/pcq187 PubMed DOI
Zhang S., Cai Z., Wang X. (2009). The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 4543–4548. 10.1073/pnas.0900349106 PubMed DOI PMC
Zhou J., Wang J., Li X., Xia X. J., Zhou Y. H., Shi K., et al. . (2014). H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J. Exp. Bot. 65, 4371–4383. 10.1093/jxb/eru217 PubMed DOI PMC
Zhu J. K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247–273. 10.1146/annurev.arplant.53.091401.143329 PubMed DOI PMC