Barley Brassinosteroid Mutants Provide an Insight into Phytohormonal Homeostasis in Plant Reaction to Drought Stress

. 2016 ; 7 () : 1824. [epub] 20161202

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid27994612

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.

Zobrazit více v PubMed

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace