TaSAUR78 enhances multiple plant abiotic stress responses by regulating the interacting gene TaVDAC1

doi:10.1016/S2095-3119(19)62651-1

Journal of Integrative Agriculture ›› 2019, Vol. 18 ›› Issue (12): 2682-2690.DOI: 10.1016/S2095-3119(19)62651-1

收稿日期:2018-08-24 出版日期:2019-12-01 发布日期:2019-12-23

TaSAUR78 enhances multiple plant abiotic stress responses by regulating the interacting gene TaVDAC1

GUO Yuan^1*, XU Chang-bing^2*, SUN Xian-jun¹, HU Zheng¹, FAN Shou-jin², JIANG Qi-yan¹, ZHANG Hui¹

¹ Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
² College of Life Sciences, Shandong Normal University, Jinan 250014, P.R.China

Received:2018-08-24 Online:2019-12-01 Published:2019-12-23
Contact: Correspondence JIANG Qi-yan, Tel: +86-10-62189045, E-mail: jiangqiyan@caas.cn; ZHANG Hui, Tel: +86-10-62186649, E-mail: zhanghui06@caas.cn
About author: * These authors contributed equally to this study.
Supported by:
This study was supported by the National Natural Science Foundation of China (31601302), the National Key R&D Program of China (2016YFD0100304), the National Transgenic Key Project from the Ministry of Agriculture of China (2016ZX08010-005), and the Agricultural Science and Technology Program for Innovation Team on the Identification and Excavation of Elite Crop Germplasm, Chinese Academy of Agricultural Sciences.

摘要/Abstract

Abstract:

SMALL AUXIN-UP RNAs (SAURs) regulated by abiotic stress play multiple functions in plants. However, the functions of SAURs in abiotic stress are largely unknown. In this study, we cloned a novel SAUR gene, TaSAUR78, from wheat, and we found that TaSAUR78 interacted with TaVDAC1 (voltage-dependent anion channel). Salt stress decreased expression of TaSAUR78 and increased expression of TaVDAC1. Overexpression of TaSAUR78 enhanced tolerance to salt, drought, and freezing stresses in transgenic Arabidopsis and reduced the accumulation of reactive oxygen species (ROS) under salt stress. Overexpression of TaVDAC1 enhanced tolerance to salt stress, while decreased tolerance to drought and low temperature stresses in transgenic Arabidopsis. TaVDAC1 overexpression increased the accumulation of ROS in plants. These results suggested that TaSAUR78 improved plant tolerance to abiotic stresses by regulating TaVDAC1. This study generated valuable information on the functions of TaSAUR78 and TaVDAC1 in multiple abiotic stresses, which may facilitate the deployment of these genes to enhance crop tolerance to abiotic stresses in the future.

Key words: TaSAUR78 , TaVDAC1 , wheat , abiotic stress

. [J]. Journal of Integrative Agriculture, 2019, 18(12): 2682-2690.

GUO Yuan, XU Chang-bing, SUN Xian-jun, HU Zheng, FAN Shou-jin, JIANG Qi-yan, ZHANG Hui. TaSAUR78 enhances multiple plant abiotic stress responses by regulating the interacting gene TaVDAC1[J]. Journal of Integrative Agriculture, 2019, 18(12): 2682-2690.

参考文献

Abu-Hamad S, Sivan S, Shoshan-Barmatz V. 2006. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proceedings of the National Academy of Sciences of the Unitied States of America, 103, 5787–5792.
Bahamonde M I, Fernández-Fernández J M, Guix F X, Vázquez E, Valverde M A. 2003. Plasma membrane voltage-dependent anion channel mediates antiestrogen-activated maxi Cl-currents in C1300 neuroblastoma cells. The Journal of Biological Chemistry, 278, 33284–33289.
Bitar F A, Roosens N, Boxtel J V, Dewaele E, Jacobs M, Homblé F. 2002. Expression of the rice vdac isoform2: Histochemical localization and expression level. Biochimica et Biophysica Acta, 1579, 133–141.
Bitar F A, Roosens N, Smeyers M, Vauterin M, Van Boxtel J, Jacobs M, Homblé F. 2003. Sequence analysis, transcriptional and posttranscriptional regulation of the rice vdac family. Biochimica et Biophysica Acta, 1625, 43–51.
Blachly-Dyson E, Zambronicz E B, Yu W H, Adams V, McCabe E R, Adelman J, Colombini M, Forte M. 1993. Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel. The Journal of Biological Chemistry, 268, 1835–1841.
Chae K, Isaacs C G, Reeves P H, Maloney G S, Muday G K, Nagpal P, Reed J W. 2012. Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. The Plant Journal, 71, 684–697.
Chang L F, Li H H, Wu X Y, Lu Y Q, Zhang J P, Yang X M, Li X Q, Lui W H, Li L H. 2017. Genetic characteristics of a wheat founder parent and a widely planted cultivar derived from the same cross. Journal of Integrative Agriculture, 17, 775–785.
Chen D, Wu X Y, Wu K, Zhang J P, Liu W H, Yang X M, Li X Q, Lu Y Q, Li L H. 2017. Novel and favorable genomic regions for spike related traits in a wheat germplasm Pubing 3504 with high grain number per spike under varying environments. Journal of Integrative Agriculture, 16, 2386–2401.
Chen H X, Han H M, Li Q F, Zhang J P, Lu Y Q, Yang X M, Li X Q, Liu W H, Li L H. 2018. Identification and genetic analysis of multiple P chromosomes of Agropyron cristatum in the background of common wheat. Journal of Integrative Agriculture, 17, 1697–1705.
Desai M K, Mishra R N, Verma D, Nair S, Sopory S K, Reddy M K. 2006. Structural and functional analysis of a salt stress inducible gene encoding voltage dependent anion channel (VDAC) from pearl millet (Pennisetum glaucum). Plant Physiology and Biochemistry, 44, 483–493.
Elkeles A, Devos K M, Graur D, Zizi M, Breiman A. 1995. Multiple cDNAs of wheat voltage-dependent anion channels (VDAC): Isolation, differential expression, mapping and evolution. Plant Molecular Biology, 29, 109–124.
Guo Y, Jiang Q Y, Hu Z, Sun X J, Fan S J, Zhang H. 2018. Function of the auxin-responsive gene TaSAUR75 under salt and drought stress. The Crop Journal, 6, 181–190.
Hou K, Wu W, Gan S S. 2013. SAUR36, a small auxin up RNA gene, is involved in the promotion of leaf senescence in Arabidopsis. Plant Physiology, 161, 1002–1009.
Hückelhoven R. 2004. BAX Inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis, 9, 299–307.
Jiang Q Y, Li X J, Niu F J, Sun X J, Hu Z, Zhang H. 2017. iTRAQ-based quantitative proteomic analysis of wheat root in response to salt stress. Proteomics, 17, 1600265.
Kong Y, Zhu Y, Gao C, She W, Lin W, Chen Y, Han N, Bian H, Zhu M, Wang J. 2013. Tissue-specific expression of SMALL AUXIN UP RNA41 differentially regulates cell expansion and root meristem patterning in Arabidopsis. Plant Cell Physiology, 54, 609–621.
Lawen A, Ly J D, Lane D J, Zarschler K, Messina A, De Pinto V. 2005. Voltage-dependent anion-selective channel 1 (VDAC1) - A mitochondrial protein, rediscovered as a novel enzyme in the plasma membrane. The International Journal of Biochemistry & Cell Biology, 37, 277–282.
Markakis M N, Boron A K, Van L B, Saini K, Cirera S, Verbelen J P, Vissenberg K. 2013. Characterization of a small auxin-up RNA (SAUR)-like gene involved in Arabidopsis thaliana development. PLoS ONE, 8, e82596.
Ni Z Y, Hu Z, Jiang Q Y, Zhang H. 2013. GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Molecular Biology, 82, 113–129.
Osman A. 2004. Yeast two-hybrid assay for studying protein-protein interactions. In: Melville S E, ed., Parasite Genomics Protocols. Methods in Molecular Biology™. vol. 270. Humana Press Inc., Totowa, NJ.
De Pinto V, Messina A, Lane D J, Lawen A. 2010. Voltage-dependent anion-selective channel (VDAC) in the plasma membrane. FEBS Letters, 584, 1793–1799.
Qiu T, Chen Y, Li M, Kong Y, Zhu Y, Han N, Bian H, Zhu M, Wang J. 2013. The tissue-specific and developmentally regulated expression patterns of the SAUR41 subfamily of SMALL AUXIN UP RNA genes. Plant Signaling & Behavior, 8, e25283.
Robert N, d’Erfurth I, Marmagne A, Erhardt M, Allot M, Boivin K, Gissot L, Monachello D, Michaud M, Duchêne A M, Barbier-Brygoo H, Maréchal-Drouard L, Ephritikhine G, Filleur S. 2012. Voltage-dependent-anion-channels (VDACs) in Arabidopsis have a dual localization in the cell but show a distinct role in mitochondria. Plant Molecular Biology, 78, 431–446.
Shi G Q, Fu J Y, Rong L J, Zhang P Y, Guo C J, Xiao K. 2018. TaMIR1119, a miRNA family member of wheat (Triticum aestivum), is essential in the regulation of plant drought tolerance. Journal of Integrative Agriculture, 17, 2369–2378.
Spartz A K, Lee S H, Wenger J P, Gonzalez N, Itoh H, Inzé D, Peer W A, Murphy A S, Overvoorde P J, Gray W M. 2012. The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. The Plant Journal, 70, 978–990.
Spartz A K, Lor V S, Ren H, Olszewski N E, Miller N D, Wu G, Spalding E P, Gray W M. 2017. Constitutive expression of Arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in tomato confers auxin-independent hypocotyl elongation. Plant Physiology, 173, 1453-1462.
Spartz A K, Ren H, Park M Y, Grandt K N, Lee S H, Murphy A S, Sussman M R, Overvoorde P J, Gray W M. 2014. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. The Plant Cell, 26, 2129–2142.
Stamm P, Kumar P P. 2013. Auxin and gibberellin responsive Arabidopsis SMALL AUXIN UP RNA36 regulates hypocotyl elongation in the light. Plant Cell Report, 32, 759–769.
Subbaiah C C, Huber S C, Sachs M M, Rhoads D. 2007. Sucrose synthase: Expanding protein function. Plant Signaling & Behavior, 2, 28–29.
Tateda C, Kusano T, Takahashi Y. 2012. The Arabidopsis voltage-dependent anion channel 2 is required for plant growth. Plant Signaling & Behavior, 7, 31–33.
Tateda C, Watanabe K, Kusano T, Takahashi Y. 2011. Molecular and genetic characterization of the gene family encoding the voltage-dependent anion channel in Arabidopsis. Journal of Experimental Botany, 62, 4773–4785.
Thinnes F P. 2007. Modulator of plasmalemma standing VDAC revealed!? Molecular Genetics and Metabolism, 91, 116–118.
Waadt R, Schmidt L K, Lohse M, Hashimoto K, Bock R, Kudla J. 2008. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. The Plant Journal, 56, 505–516.
Wang Y X, Xu Q F, Chang X P, Hao C Y, Li R Z, Jing R L. 2018. A dCAPS marker developed from a stress associated protein gene TaSAP7-B governing grain size and plant height in wheat. Journal of Integrative Agriculture, 17, 276–284.
Wen G Q, Cai L, Liu Z, Li D K, Luo Q, Li X F, Wan J M, Yang Y. 2011. Arabidopsis thaliana VDAC2 involvement in salt stress response pathway. African Journal of Biotechnology, 10, 11588–11593.
Weng C, Li Y, Xu D, Shi Y, Tang H. 2005. Specific cleavage of Mcl-1 by caspase-3 in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in Jurkat leukemia T cells. The Journal of Biological Chemistry, 280, 10491–10500.
Xu Q F, Mao X G, Wang Y X, Wang J Y, Xi Y J, Jing R L. 2018. A wheat gene TaSAP17-D encoding an AN1/AN1 zinc finger protein improves salt stress tolerance in transgenic Arabidopsis. Journal of Integrative Agriculture, 17, 507–516.
Yang X Y, Chen Z W, Xu T, Qu Z, Pan X D, Qin X H, Ren D T, Liu G Q. 2011. Arabidopsis kinesin KP1 specifically interacts with VDAC3, a mitochondrial protein, and regulates respiration during seed germination at low temperature. The Plant Cell, 23, 1093–1106.
Zhang M, Takano T, Liu S, Zhang X. 2015. Arabidopsis mitochondrial voltage-dependent anion channel 3 (AtVDAC3) protein interacts with thioredoxin m2. FEBS Letters, 589, 1207–1213.

TaSAUR78 enhances multiple plant abiotic stress responses by regulating the interacting gene TaVDAC1

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics