TsMIP6 enhances the tolerance of transgenic rice to salt stress and interacts with target proteins

Journal of Plant Biology - Tập 58 - Trang 285-292 - 2015
Linlin Sun1,2, Guohong Yu2, Xiaori Han1, Shichao Xin2,3, Xiaojing Qiang2, Linlin Jiang2, Shuhui Zhang1,2, Xianguo Cheng2
1College of Land and Environment, Shenyang Agricultural University, Shenyang, Liaoning, PR China
2Key Lab of Plant Nutrition and Fertilizers, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Zhongguancun, Beijing, PR China
3Key Laboratory of Rubber Biology, Ministry of Agriculture, Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou, Hainan, PR China

Tóm tắt

Aquaporins (AQPs), a large family of channel proteins in plants, play an important role in regulating the balance of osmotic potential in cells. We isolated an AQP gene, TsMIP6, from the halophyte Thellungiella salsuginea and functionally characterized it in transgenic rice (Oryza sativa). This gene belongs to a subfamily of tonoplast intrinsic proteins and is localized at the plasma membrane. Real-time PCR showed that expression of TsMIP6 in shoots or roots of T. salsuginea was markedly induced by salinity, whereas its ectopic expression in ‘Kitaake’ lines of rice significantly increased plant tolerance to salt stress. Physiological data suggested that TsMIP6 is involved in regulating ion homeostasis and water channel activity in salt-stressed transgenic rice. Heterologous expression analysis indicated that TsMIP6 specifically interacts with a member of the glycoside hydrolase family 64 protein #617 in yeast cells. This suggests that the relationship between TsMIP6 and #617 has a crucial role in mediating osmotic balance in plant cells. Moreover, TsMIP6 might help to modulate the transport of some neutral molecules and may function through a pathway regulating solute equilibrium to maintain osmotic potential.

Tài liệu tham khảo

Alexandersson E, Fraysse L, Sjövall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484 Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201 Bae EK, Lee H, Lee JS, Noh EW (2011) Drought, salt and wounding stress induce the expression of the plasma membrane intrinsic protein 1 gene in poplar (Populus alba × P. tremula var. glandulosa). Gene 483:43–48 Berggard T, Linse S, James P (2007) Methods for the detection and analysis of protein-protein interactions. Proteomics 7:2833–2842 Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:252–258 Biela A, Grote K, Otto B, Hoth S, Hedrich R, Kaldenhoff R (1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J 18:565–570 Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol 6:26 Bienert GP, Bienert MD, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66:306–317 Dong J, Kharb P, Teng WM, Hall TC (2011) Characterization of rice transformed via an Agrobacterium-mediated inflorescence approach. Mol Breed 7:187–194 Gao ZX, He XL, Zhao BC, Zhou CJ, Liang YZ, Ge RC, Shen YZ, Huang ZJ (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant Cell Physiol 51:767–775 Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16:277–286 Haffani S, Mezni M, Slama I, Ksontini M, Chaïbi W (2014) Plant growth, water relations and proline content of three vetch species under water-limited conditions. Grass Forage Sci 69:323–333 Hagège D, Feutry S, Krsnik-Rasol M, Poder D, Menez JF (1995) Estimation of free and bound MDA in plant extracts: comparison between spectrophotometric and HPLC methods. In: Plant Lipid Metabolism, Kluwer Academic Publishers. pp 259–261 Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369 Kaneko K, Tabuchi M, Sueyoshi N, Ishida A, Utsumi T, Kameshita I (2014) Cellular localization of CoPK12, a Ca2+/calmodulindependent protein kinase in mushroom Coprinopsis cinerea, is regulated by N-myristoylation. Biochem mvu018; 156(1):51–61 Leyva A, Quintana A, Sanchez M, Rodriguez EN, Cremata J, Sanchez JC (2008) Rapid and sensitive anthrone-sulfuric acid assay in microplate format to quantify carbohydrate in biopharmaceutical products: method development and validation. Biologicals 36:134–141 Liu JJ, Sturrock R, Ekramoddoullah AK (2010) The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Rep 29:419–436 Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408 Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Plant Biol 59:595–624 Möckli N, Deplazes A, Hassa P, Zhang Z, Peter M, Hottiger M, Stagljar I, Auerbach D (2007) Yeast split-ubiquitin-based cytosolic screening system to detect interactions between transcriptionally active proteins. Biotechniques 42:725–730 Ogura Y, Ihara N, Komatsu A, Tokioka Y, Nishioka M, Takase T, Kiyosue T (2008) Gene expression, localization, and protein–protein interaction of Arabidopsis SKP1-like (ASK) 20A and 20B. Plant Sci 174:485–495 Peng Y, Lin W, Cai W, Arora R (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226:729–740 Rao VS, Srinivas K, Sujini GN, Kumar GN (2014) Protein-protein interaction detection: methods and analysis. Proteomics:1–12 Ribas AF, Dechamp E, Champion A, Bertrand B, Combes M-C, Verdeil J-L, Lapeyre F, Lashermes P, Etienne H (2011) Agrobacterium-mediated genetic transformation of Coffea arabica (L.) is greatly enhanced by using established embryogenic callus cultures. BMC Plant Biol 11:92 Saadia M, Jamil A, Akram NA, Ashraf M (2012) A study of proline metabolism in canola (Brassica napus L.) seedlings under salt stress. Molecules 17:5803–5815 Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108 Stackpole E, Akins MR, Fallon JR (2014) N-myristoylation regulates the axonal distribution of the Fragile X-related protein FXR2P. Mol Cell Neurosci 62:42–50 Stynen B, Tournu H, Tavernier J, van Dijck P (2012) Diversity in genetic in vivo methods for protein-protein interaction studies: from the yeast two-hybrid system to the mammalian split- Lucifer system. Microbiol Mol Biol Rev 76:331–382 Wang LL, Chen AP, Zhong NQ, Liu N, Wu XM, Wang F, Yang CL, Remero MF, Xia CX (2014) The Thellungiella salsuginea tonoplast aquaporin TsTIP1;2 functions in multiple abiotic stress protection. Plant Cell Physiol 55:148–161 Wu H, Zhang ZH, Wang JY, Oh DH, Dassanayake M, Liu BH, Huang QF, Sun HX, Xia R, Wu YR, Wang YN, Yang Z, Liu Y, Zhang WK, Zhang HW, Chu JF, Yan CY, Fang S, Zhang JS, Wang YQ, Zhang FX, Wang GD, Lee SY, Cheeseman JM, Yang BC, Li B, Min J, Yang L, Wang J, Chu C, Chen S, Bohnert H, Zhu J, Wang X, Xie Q (2012) Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc Natl Acad Sci USA 109:12219–12224 Xin S, Yu G, Sun L, Qiang X, Xu N, Cheng X (2014) Expression of tomato SlTIP2;2 enhances the tolerance to salt stress in the transgenic Arabidopsis and interacts with target proteins. J Plant Res 127:695–708 Yang JW, Fu JX, Li J, Cheng XL, Li F, Dong JF, Liu ZL, Zhuang CX (2013) A novel co-immunoprecipitation protocol based on protoplast transient gene expression for studying protein–protein interactions in rice. Plant Mol Biol Rep 32:153–161 Yukoh H, Shozo O, Toshihiko K, Takashi K (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282 Yukoh H, Toshihiko K, Tomoaki K (1997) Transformation of rice mediated by Agrobacterium tumefaciens. Plant Mol Biol 35:205–218 Zhang J, Blackmer A, Blackmer T, Kyveryga P, Ellsworth J (2007) Nitrogen deficiency and recovery in sustainable corn production as revealed by leaf chlorophyll measurements. Agron Sustain Dev 27:313–319 Zhang Y, Su J, Duan S, Ao Y, Dai J, Liu J, Wang P, Li Y, Liu B, Feng D, Wang J, Wang H (2011) A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast related processes. Plant Methods 7:30–43 Zhao CX, Shao HB, Chu LY (2008) Aquaporin structure-function relationships: water flow through plant living cells. Colloids Surf B 62:163–172 Zhao JP, Su XH (2010) Patterns of molecular evolution and predicted function in thaumatin-like proteins of Populus trichocarpa. Planta 232:949–962