Cell wall/vacuolar inhibitor of fructosidase 1 regulates ABA response and salt tolerance in Arabidopsis

References

• Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 2003;218:1–9. doi:10.1007/s00425-003-1105-5.
   PubMed Web of Science ®Google Scholar
• Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Bio. 2006;9:436–442. doi:10.1016/j.pbi.2006.05.014.
   PubMed Web of Science ®Google Scholar
• Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol. 2010;51:1821–1839. doi:10.1093/pcp/pcq156.
   PubMed Web of Science ®Google Scholar
• Yoshida T, Mogami J, Yamaguchi-Shinozaki K. ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol. 2014;21:133–139. doi:10.1016/j.pbi.2014.07.009.
   PubMed Web of Science ®Google Scholar
• Song L, Huang SC, Wise A, Castanon R, Nery JR, Chen H, Watanabe M, Thomas J, Bar-Joseph Z, Ecker JR. A transcription factor hierarchy defines an environmental stress response network. Science. 2016;354:aag1550. doi:10.1126/science.aag1550.
   PubMed Web of Science ®Google Scholar
• Tian H, Chen S, Yang W, Wang T, Zheng K, Wang Y, Cheng Y, Zhang N, Liu S, Li D, et al. A novel family of transcription factors conserved in angiosperms is required for ABA signalling. Plant Cell Environ. 2017;40:2958–2971.
   PubMed Web of Science ®Google Scholar
• Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science. 2009;324:1064–1068. doi:10.1126/science.1172408.
   PubMed Web of Science ®Google Scholar
• Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science. 2009;324:1068–1071. doi:10.1126/science.1173041.
   PubMed Web of Science ®Google Scholar
• Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Marquez JA, Cutler SR, Rodriguez PL. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 2009;60:575–588. doi:10.1111/j.1365-313X.2009.03981.x.
   PubMed Web of Science ®Google Scholar
• Rodriguez PL, Leube MP, Grill E. Molecular cloning in Arabidopsis thaliana of a new protein phosphatase 2C (PP2C) with homology to ABI1 and ABI2. Plant Mol Biol. 1998;38:879–883. doi:10.1023/A:1006012218704.
   PubMed Web of Science ®Google Scholar
• Gosti F, Beaudoin N, Serizet C, Webb AA, Vartanian N, Giraudat J. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell. 1999;11:1897–1910. doi:10.1105/tpc.11.10.1897.
   PubMed Web of Science ®Google Scholar
• Fujii H, Verslues PE, Zhu JK. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell. 2007;19:485–494. doi:10.1105/tpc.106.048538.
   PubMed Web of Science ®Google Scholar
• Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J. KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell. 2006;18:3415–3428. doi:10.1105/tpc.106.046532.
   PubMed Web of Science ®Google Scholar
• Liu H, Stone SL. Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell. 2010;22:2630–2641. doi:10.1105/tpc.110.076075.
   PubMed Web of Science ®Google Scholar
• Chen YT, Liu HX, Stone S, Callis J. ABA and the ubiquitin E3 ligase KEEP ON GOING affect proteolysis of the Arabidopsis thaliana transcription factors ABF1 and ABF3. Plant J. 2013;75:965–976. doi:10.1111/tpj.12259.
   PubMed Web of Science ®Google Scholar
• Park SY, Peterson FC, Mosquna A, Yao J, Volkman BF, Cutler SR. Agrochemical control of plant water use using engineered abscisic acid receptors. Nature. 2015;520:545–548. doi:10.1038/nature14123.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Chan Z, Gao J, Xing L, Cao M, Yu C, Hu Y, You J, Shi H, Zhu Y, et al. ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci USA. 2016;113:1949–1954. doi:10.1073/pnas.1522840113.
   PubMed Web of Science ®Google Scholar
• Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, et al. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 2009;50:2123–2132. doi:10.1093/pcp/pcp147.
   PubMed Web of Science ®Google Scholar
• Yoshida T, Fujita Y, Maruyama K, Mogami J, Todaka D, Shinozaki K, Yamaguchi-Shinozaki K. Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signaling in response to osmotic stress. Plant Cell Environ. 2015;38:35–49. doi:10.1111/pce.12351.
   PubMed Web of Science ®Google Scholar
• Koch K. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol. 2004;7:235–246. doi:10.1016/j.pbi.2004.03.014.
   PubMed Web of Science ®Google Scholar
• Sturm A. Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol. 2002;121:1–8. doi:10.1104/pp.121.1.1.
   Web of Science ®Google Scholar
• Van den Ende W, Lammens W, Van Laere A, Schroeven L, Le Roy K. Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes. FEBS J. 2009;276:5788–5798. doi:10.1111/j.1742-4658.2009.07316.x.
   PubMed Web of Science ®Google Scholar
• Wan H, Wu L, Yang Y, Zhou G, Ruan YL. Evolution of sucrose metabolism: the dichotomy of invertases and beyond. Trends Plant Sci. 2018;23:163–177. doi:10.1016/j.tplants.2017.11.001.
   PubMed Web of Science ®Google Scholar
• Rolland F, Baena-Gonzalez E, Sheen J. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol. 2006;57:675–709. doi:10.1146/annurev.arplant.57.032905.105441.
   PubMed Web of Science ®Google Scholar
• Ruan Y-L. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol. 2014;65:33–67. doi:10.1146/annurev-arplant-050213-040251.
   PubMed Web of Science ®Google Scholar
• Balibrea Lara ME, Gonzalez Garcia M-C, Fatima T, Ehneß R, Lee TK, Proels R, Tanner W, Roitsch T. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell. 2004;16:1276–1287. doi:10.1105/tpc.018929.
   PubMed Web of Science ®Google Scholar
• Albacete A, Cantero-Navarro E, Großkinsky DK, Arias CL, Balibrea ME, Bru R, Fragner L, Ghanem ME, González Mde L, Hernández JA, et al. Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato. J Exp Bot. 2015;66:863–878. doi:10.1093/jxb/eru448.
   PubMed Web of Science ®Google Scholar
• Bhaskar PB, Wu L, Busse JS, Whitty BR, Hamernik AJ, Jansky SH, Buell CR, Bethke PC, Jiang J. Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiol. 2010;154:939–948. doi:10.1104/pp.110.162545.
   PubMed Web of Science ®Google Scholar
• Zhu X, Gong H, He Q, Zeng Z, Busse JS, Jin W, Bethke PC, Jiang J. Silencing of vacuolar invertase and asparagine synthetase genes and its impact on acrylamide formation of fried potato products. Plant Biotechnol J. 2016;14:709–718. doi:10.1111/pbi.12421.
   PubMed Web of Science ®Google Scholar
• Qian W, Xiao B, Wang L, Hao X, Yue C, Cao H, Wang Y, Li N, Yu Y, Zeng J, et al. CsINV5, a tea vacuolar invertase gene enhances cold tolerance in transgenic Arabidopsis. BMC Plant Biol. 2018;18:228. doi:10.1186/s12870-018-1456-5.
   PubMed Web of Science ®Google Scholar
• Rausch T, Greiner S. Plant protein inhibitors of invertases. Biochim Biophys Acta-Proteins Proteomics. 2004;1696:253–261. doi:10.1016/j.bbapap.2003.09.017.
   PubMed Web of Science ®Google Scholar
• Hothorn M, Van den Ende W, Lammens W, Rybin V, Scheffzek K. Structural insights into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein. Proc Natl Acad Sci. 2010;107:17427–17432. doi:10.1073/pnas.1004481107.
   PubMed Web of Science ®Google Scholar
• Su T, Han M, Min J, Zhou H, Zhang Q, Zhao J, Fang Y. Functional characterization of invertase inhibitors PtC/VIF1 and 2 revealed their involvements in the defense response to fungal pathogen in. Populus Trichocarpa Front Plant Sci. 2020;10:1654. doi:10.3389/fpls.2019.01654.
   PubMed Web of Science ®Google Scholar
• Jin Y, Ni D-A, Ruan Y-L. Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell. 2009;21:2072–2089. doi:10.1105/tpc.108.063719.
   PubMed Web of Science ®Google Scholar
• Xu X, Hu Q, Yang W, Jin Y. The roles of cell wall invertase inhibitor in regulating chilling tolerance in tomato. BMC Plant Biol. 2017;17:195. doi:10.1186/s12870-017-1145-9.
   PubMed Web of Science ®Google Scholar
• Su T, Wolf S, Han M, Zhao H, Wei H, Greiner S, Rausch T. Reassessment of an Arabidopsis cell wall invertase inhibitor AtCIF1 reveals its role in seed germination and early seedling growth. Plant Mol Biol. 2016;90:137–155. doi:10.1007/s11103-015-0402-2.
   PubMed Web of Science ®Google Scholar
• Chen SF, Liang K, Yin DM, Ni DA, Zhang ZG, Ruan YL. Ectopic expression of a tobacco vacuolar invertase inhibitor in guard cells confers drought tolerance in Arabidopsis. J Enzyme Inhib Med Chem. 2016;31:1381–1385. doi:10.3109/14756366.2016.1142981.
   PubMed Web of Science ®Google Scholar
• Wang X, Wang X, Hu Q, Dai X, Tian H, Zheng K, Wang X, Mao T, Chen JG, Wang S. Characterization of an activation-tagged mutant uncovers a role of GLABRA2 in anthocyanin biosynthesis in Arabidopsis. Plant J. 2015;83:300–311. doi:10.1111/tpj.12887.
   PubMed Web of Science ®Google Scholar
• Hajdukiewicz P, Svab Z, Maliga P. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol. 1994;25:989–994. doi:10.1007/BF00014672.
   PubMed Web of Science ®Google Scholar
• Cheng Y, Zhang N, Hussain S, Ahmed S, Yang W, Wang S. Integration of a FT expression cassette into CRISPR/Cas9 construct enables fast generation and easy identification of transgene-free mutants in Arabidopsis. PLoS One. 2019;14:e0218583. doi:10.1371/journal.pone.0218583.
   PubMed Web of Science ®Google Scholar
• Wang ZP, Xing HL, Dong L, Zhang HY, Han CY, Wang XC, Chen QJ. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 2015;16:144. doi:10.1186/s13059-015-0715-0.
   PubMed Web of Science ®Google Scholar
• Chen S, Zhang N, Zhang Q, Zhou G, Tian H, Hussain S, Ahmed S, Wang T, Wang S. Genome editing to integrate seed size and abiotic stress tolerance traits in Arabidopsis reveals a role for DPA4 and SOD7 in the regulation of inflorescence architecture. Int J Mol Sci. 2019;20:2695. doi:10.3390/ijms20112695.
   Web of Science ®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
• Guo J, Wang J, Xi L, Huang WD, Liang J, Chen JG. RACK1 is a negative regulator of ABA responses in Arabidopsis. J Exp Bot. 2009;60:3819–3833. doi:10.1093/jxb/erp221.
   PubMed Web of Science ®Google Scholar
• Guo J, Wang S, Valerius O, Hall H, Zeng Q, Li JF, Weston DJ, Ellis BE, Chen JG. Involvement of Arabidopsis RACK1 in protein translation and its regulation by abscisic acid. Plant Physiol. 2011;155:370–383. doi:10.1104/pp.110.160663.
   PubMed Web of Science ®Google Scholar
• Tian H, Guo H, Dai X, Cheng Y, Zheng K, Wang X, Wang S. An ABA down-regulated bHLH transcription repressor gene, bHLH129 regulates root elongation and ABA response when overexpressed in Arabidopsis. Sci Rep. 2015;5:17587. doi:10.1038/srep17587.
   PubMed Web of Science ®Google Scholar
• Greiner S, Rausch T, Sonnewald U, Herbers K. Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers. Nat Biotechnol. 1999;17:708–711. doi:10.1038/10924.
   PubMed Web of Science ®Google Scholar
• Brummell DA, Chen RKY, Harris JC, Zhang H, Hamiaux C, Kralicek AV, McKenzie MJ. Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J Exp Bot. 2011;62:3519–3534. doi:10.1093/jxb/err043.
   PubMed Web of Science ®Google Scholar
• Liu X, Lin Y, Liu J, Song B, Ou Y, Zhang H, Li M, Xie C. StInvInh2 as an inhibitor of StvacINV1 regulates the cold-induced sweetening of potato tubers by specifically capping vacuolar invertase activity. Plant Biotechnol J. 2013;11:640–647. doi:10.1111/pbi.12054.
   PubMed Web of Science ®Google Scholar
• Mckenzie MJ, Chen RKY, Harris JC, Ashworth MJ, Brummell DA. Post-translational regulation of acid invertase activity by vacuolar invertase inhibitor affects resistance to cold-induced sweetening of potato tubers. Plant Cell Environ. 2013;36:176–185. doi:10.1111/j.1365-3040.2012.02565.x.
   PubMed Web of Science ®Google Scholar
• Qin G, Zhu Z, Wang W, Cai J, Chen Y, Li L, Tian S. A tomato vacuolar invertase inhibitor mediates sucrose metabolism and influences fruit ripening. Plant Physiol. 2016;172:1596–1611. doi:10.1104/pp.16.01269.
   PubMed Web of Science ®Google Scholar
• Hothorn M, Wolf S, Aloy P, Greiner S, Scheffzek K. Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins. Plant Cell. 2004;16:3437–3447. doi:10.1105/tpc.104.025684.
   PubMed Web of Science ®Google Scholar
• Tang X, Su T, Han M, Wei L, Wang W, Yu Z, Xue Y, Wei H, Du Y, Greiner S, et al. Suppression of extracellular invertase inhibitor gene expression improves seed weight in soybean (Glycine max). J Exp Bot. 2017;68:469–482. doi:10.1093/jxb/erw425.
   PubMed Web of Science ®Google Scholar
• Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant. 2015;8:1274–1284. doi:10.1016/j.molp.2015.04.007.
   PubMed Web of Science ®Google Scholar
• Li X, Xie Y, Zhu Q, Liu YG. Targeted genome editing in genes and cis-regulatory regions improves qualitative and quantitative traits in crops. Mol Plant. 2017;10:1368–1370. doi:10.1016/j.molp.2017.10.009.
   PubMed Web of Science ®Google Scholar
• He Y, Zhu M, Wang L, Wu J, Wang Q, Wang R, Zhao Y. Programmed self-elimination of the CRISPR/Cas9 construct greatly accelerates the isolation of edited and transgene-free rice plants. Mol Plant. 2018;11:1210–1213. doi:10.1016/j.molp.2018.05.005.
   PubMed Web of Science ®Google Scholar