The functional analysis of a wheat group 3 late embryogenesis abundant protein in Escherichia coli and Arabidopsis under abiotic stresses

References

• Dure L 3rd, Crouch M, Harada J, Ho TH, Mundy J, Quatrano R, Thomas T, Sung ZR. Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol. 1989;12:1–8. doi:10.1007/BF00036962.
   Web of Science ®Google Scholar
• Houde M, Daniel C, Lachapelle M, Allard F, Laliberte S, Sarhan F. Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J. 1995;8:583–593. doi:10.1046/j.1365-313x.1995.8040583.x.
   PubMed Web of Science ®Google Scholar
• Nylander M, Svensson J, Palva ET, Welin BV. Stress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol Biol. 2001;45:263–279. doi:10.1023/a:1006469128280.
   PubMed Web of Science ®Google Scholar
• Furuki T, Sakurai M. Group 3 LEA protein model peptides protect enzymes against desiccation stress. Biochim Biophys Acta. 2016;1864:1237–1243. doi:10.1016/j.bbapap.2016.04.012.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang L, Jiang S, Pan J, Cai G, Li D. Group 5 LEA protein, ZmLEA5C, enhance tolerance to osmotic and low temperature stresses in transgenic tobacco and yeast. Plant Physiol Biochem. 2014;84:22–31. doi:10.1016/j.plaphy.2014.08.016.
   PubMed Web of Science ®Google Scholar
• Liu Y, Liang J, Sun L, Yang X, Li D. Group 3 LEA Protein, ZmLEA3, Is Involved in Protection from Low Temperature Stress. Front Plant Sci. 2016;7:1011.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang L, Xing X, Sun L, Pan J, Kong X, Zhang M, Li D. ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol. 2013;54:944–959. doi:10.1093/pcp/pct047.
   PubMed Web of Science ®Google Scholar
• Furuki T, Shimizu T, Chakrabortee S, Yamakawa K, Hatanaka R, Takahashi T, Kikawada T, Okuda T, Mihara H, Tunnacliffe A, et al. Effects of Group 3 LEA protein model peptides on desiccation-induced protein aggregation. Biochim Biophys Acta. 2012;1824:891–897. doi:10.1016/j.bbapap.2012.04.013.
   PubMed Web of Science ®Google Scholar
• Dure L 3rd. A repeating 11-mer amino acid motif and plant desiccation. Plant J. 1993;3:363–369. doi:10.1046/j.1365-313x.1993.t01-19-00999.x.
   PubMed Web of Science ®Google Scholar
• Furuki T, Shimizu T, Kikawada T, Okuda T, Sakurai M. Salt Effects on the structural and thermodynamic properties of a group 3 LEA protein model peptide. Biochemistry. 2011;50:7093–7103. doi:10.1021/bi200719s.
   PubMed Web of Science ®Google Scholar
• Hatanaka R, Hagiwara-Komoda Y, Furuki T, Kanamori Y, Fujita M, Cornette R, Sakurai M, Okuda T, Kikawada T. An abundant lea protein in the anhydrobiotic midge, pvlea4, acts as a molecular shield by limiting growth of aggregating protein particles. Insect Biochem Mol Biol. 2013;43:1055–1067.
   PubMed Web of Science ®Google Scholar
• Liu Y, Yang M, Cheng H, Sun N, Liu S, Li S, Wang Y, Zheng Y, Uversky VN. The effect of phosphorylation on the salt-tolerance-related functions of the soybean protein pm18, a member of the group-3 lea protein family. Biochim Biophys Acta Proteins Proteom. 2017;1865:1291–1303.
   PubMed Web of Science ®Google Scholar
• Saucedo AL, Hernandez-Dominguez EE, de Luna-Valdez LA, Guevara-Garcia AA, Escobedo-Moratilla A, Bojorquez-Velazquez E, Del Rio-Portilla F, Fernandez-Velasco DA, Barba De La Rosa AP. Insights on Structure and Function Of a Late Embryogenesis Abundant Protein from Amaranthus Cruentus: an Intrinsically Disordered Protein Involved in Protection against Desiccation, Oxidant Conditions, and Osmotic Stress. Front Plant Sci. 2017;8:497.
   Google Scholar
• Koubaa S, Bremer A, Hincha DK, Brini F. Structural properties and enzyme stabilization function of the intrinsically disordered LEA_4 protein TdLEA3 from wheat. Sci Rep. 2019;9:3720. doi:10.1038/s41598-019-39823-w.
   PubMed Web of Science ®Google Scholar
• Yang J, Zhao S, Zhao B, Li C. Overexpression of TaLEA3 induces rapid stomatal closure under drought stress in Phellodendron amurense Rupr. Plant Sci. 2018;277:100–109. doi:10.1016/j.plantsci.2018.09.022.
   PubMed Web of Science ®Google Scholar
• Liang Y, Kang K, Gan L, Ning S, Xiong J, Song S, Xi L, Lai S, Yin Y, Gu J, et al. Drought-responsive genes, late embryogenesis abundant group3 (LEA3) and vicinal oxygen chelate, function in lipid accumulation in Brassica napus and Arabidopsis mainly via enhancing photosynthetic efficiency and reducing ROS. Plant Biotechnol J. 2019. doi:10.1111/pbi.13127.
   Google Scholar
• Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. doi:10.1046/j.1365-313x.1998.00343.x.
   PubMed Web of Science ®Google Scholar
• Zhang L, Zhao G, Xia C, Jia J, Liu X, Kong X. A wheat R2R3-MYB gene, TaMYB30-B, improves drought stress tolerance in transgenic Arabidopsis. J Exp Bot. 2012;63:5873–5885.
   PubMed Web of Science ®Google Scholar
• Pflugmacher S, Hofmann J, Hubner B. Effects on growth and physiological parameters in wheat (Triticum aestivum L.) grown in soil and irrigated with cyanobacterial toxin contaminated water. Environ Toxicol Chem. 2007;26:2710–2716. doi:10.1897/07-145.1.
   PubMed Web of Science ®Google Scholar
• Furuki T, Sakurai M. Group 3 LEA protein model peptides protect liposomes during desiccation. Biochim Biophys Acta. 2014;1838:2757–2766. doi:10.1016/j.bbamem.2014.07.009.
   PubMed Web of Science ®Google Scholar
• Boswell LC, Hand SC. Intracellular localization of group 3 LEA proteins in embryos of Artemia franciscana. Tissue Cell. 2014;46:514–519. doi:10.1016/j.tice.2014.09.004.
   PubMed Web of Science ®Google Scholar
• Tunnacliffe A, Wise MJ. The continuing conundrum of the LEA proteins. Naturwissenschaften. 2007;94:791–812. doi:10.1007/s00114-007-0254-y.
   PubMed Web of Science ®Google Scholar
• Kovacs D, Agoston B, Tompa P. Disordered plant LEA proteins as molecular chaperones. Plant Signal Behav. 2008;3:710–713. doi:10.4161/psb.3.9.6434.
   PubMedGoogle Scholar
• Xu D, Duan X, Wang B, Hong B, Ho T, Wu R. Expression of a Late Embryogenesis Abundant Protein Gene, HVA1, from Barley Confers Tolerance to Water Deficit and Salt Stress in Transgenic Rice. Plant Physiol. 1996;110:249–257. doi:10.1104/pp.110.1.249.
   PubMed Web of Science ®Google Scholar
• Chen YS, Lo SF, Sun PK, Lu CA, Ho TH, Yu SM. A late embryogenesis abundant protein HVA1 regulated by an inducible promoter enhances root growth and abiotic stress tolerance in rice without yield penalty. Plant Biotechnol J. 2015;13:105–116. doi:10.1111/pbi.12241.
   PubMed Web of Science ®Google Scholar
• Battista JR, Park MJ, McLemore AE. Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology. 2001;43:133–139. doi:10.1006/cryo.2001.2357.
   PubMed Web of Science ®Google Scholar
• Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A. Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem. 2003;278:12977–12984. doi:10.1074/jbc.M212007200.
   PubMed Web of Science ®Google Scholar
• Barros NL, Da Silva DT, Marques DN, de Brito FM, Dos Reis SP, de Souza CR. Heterologous Expression of MeLEA3: A 10 kDa Late Embryogenesis Abundant Protein of Cassava, Confers Tolerance to Abiotic Stress in Escherichia coli with Recombinant Protein Showing In Vitro Chaperone Activity. Protein Pept Lett. 2015;22:689–695.
   PubMed Web of Science ®Google Scholar
• Kim TH, Bohmer M, Hu H, Nishimura N, Schroeder JI. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol. 2010;61:561–591. doi:10.1146/annurev-arplant-042809-112226.
   PubMed Web of Science ®Google Scholar
• Hashimoto M, Negi J, Young J, Israelsson M, Schroeder JI, Iba K. Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nat Cell Biol. 2006;8:391–397. doi:10.1038/ncb1387.
   PubMed Web of Science ®Google Scholar
• Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature. 2008;452:483–486. doi:10.1038/nature06720.
   PubMed Web of Science ®Google Scholar
• Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmaki A, Brosche M, Moldau H, Desikan R, et al. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature. 2008;452:487–U15.
   PubMed Web of Science ®Google Scholar
• Imes D, Mumm P, Böhm J, Al-Rasheid KAS, Marten I, Geiger D, Hedrich R. Open stomata 1 (OST1) kinase controls R–type anion channel QUAC1 in Arabidopsis guard cells. Plant J. 2013;74:372–382. doi:10.1111/tpj.12133.
   PubMed Web of Science ®Google Scholar
• Hua D, Wang C, He J, Liao H, Duan Y, Zhu Z, Guo Y, Chen Z, Gong Z. A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell. 2012;24:2546–2561. doi:10.1105/tpc.112.100107.
   PubMed Web of Science ®Google Scholar
• Geiger D, Maierhofer T, Al-Rasheid KA, Scherzer S, Mumm P, Liese A, Ache P, Wellmann C, Marten I, Grill E, et al. Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal. 2011;4:ra32. doi:10.1126/scisignal.2001346.
   PubMed Web of Science ®Google Scholar
• Zheng X, He K, Kleist T, Chen F, Luan S. Anion channel SLAH3 functions in nitrate-dependent alleviation of ammonium toxicity in Arabidopsis. Plant Cell Environ. 2015;38:474–486.
   PubMed Web of Science ®Google Scholar
• Zhang A, Ren HM, Tan YQ, Qi GN, Yao FY, Wu GL, Yang LW, Hussain J, Sun SJ, Wang YF. S-type Anion Channels SLAC1 and SLAH3 Function as Essential Negative Regulators of Inward K+ Channels and Stomatal Opening in Arabidopsis. Plant Cell. 2016;28:949–955. doi:10.1105/tpc.16.01050.
   PubMed Web of Science ®Google Scholar
• Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, et al. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol. 2006;4:e327. doi:10.1371/journal.pbio.0040327.
   PubMed Web of Science ®Google Scholar
• Latz A, Mehlmer N, Zapf S, Mueller TD, Wurzinger B, Pfister B, Csaszar E, Hedrich R, Teige M, Becker D. Salt stress triggers phosphorylation of the Arabidopsis vacuolar K+ channel TPK1 by calcium-dependent protein kinases (CDPKs). Mol Plant. 2013;6:1274–1289. doi:10.1093/mp/sss158.
   PubMed Web of Science ®Google Scholar
• Lim CW, Lim S, Baek W, Lee SC. The pepper late embryogenesis abundant protein CaLEA1 acts in regulating abscisic acid signaling, drought and salt stress response. Physiol Plant. 2015;154:526–542. doi:10.1111/ppl.12298.
   PubMed Web of Science ®Google Scholar