Putrescine, spermidine, and spermine play distinct roles in rice salt tolerance

doi:10.1016/S2095-3119(19)62705-X

Journal of Integrative Agriculture ›› 2020, Vol. 19 ›› Issue (3): 643-655.DOI: 10.1016/S2095-3119(19)62705-X

所属专题：水稻耕作栽培合辑Rice Physiology · Biochemistry · Cultivation · Tillage

收稿日期:2018-11-14 出版日期:2020-03-01 发布日期:2020-03-04

Putrescine, spermidine, and spermine play distinct roles in rice salt tolerance

Md Azizul ISlam^{1, 2, 3}, PANG Jin-huan¹, MENG Fan-wei^{1, 2}, LI Ya-wen^{1, 2}, XU Ning¹, YANG Chao^{1, 2}, LIU Jun^{1, 2}

¹ State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences (CAS), Beijing 100101, P.R.China
² CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, P.R.China
³ Department of Biotechnology and Genetic Engineering, Faculty of Applied Science and Technology, Islamic University, Kushtia 7003, Bangladesh

Received:2018-11-14 Online:2020-03-01 Published:2020-03-04
Contact: Correspondence LIU Jun, E-mail: junliu@im.ac.cn; YANG Chao, Tel/Fax: +86-10-64806158, E-mail: chaoyang@im.ac.cn
About author:
Supported by:
The study was supported by the National Key R&D Program (2017YFD0200900) and the Natural Science Foundation of China (31570252 and 31601629). Thanks to the Chinese Academy of Sciences (CAS) and the World Academy of Sciences (TWAS) Presidents Fellowship for supporting Md Azizul Islam as a doctoral student (2015CTF068).

摘要/Abstract

Abstract:

Polyamines (PAs) play diverse roles in plant growth and development, as well as responses to environmental stimuli. In this study, the effects of PAs on rice salt tolerance were investigated. Salt stress resulted in the alteration of endogenous PAs levels in rice roots and leaves, where spermidine (Spd) and spermine (Spm) contents were increased, and putrescine (Put) content was decreased. RT-qPCR analysis revealed that PAs biosynthesis-related genes ADC1, ODC, and Arginase were significantly downregulated by salt treatment; however, SAMDC transcription was significantly upregulated. Exogenous Spm enhanced rice salt tolerance remarkably; however, exogenous Put and Spd undermined rice salt tolerance. Transgenic rice plants overexpressing SAMDC display a higher ratio of Spm/(Put+Spd) and enhanced salt tolerance. Salt stress also increased polyamine oxidase activities in rice, resulting in elevated reactive oxygen species (ROS) production. Our findings revealed that accumulation of Put and Spd substantially reduced salt tolerance in rice, likely by facilitating ROS production; whereas, conversion of Put and Spd to Spm contributes to rice salt tolerance.

. [J]. Journal of Integrative Agriculture, 2020, 19(3): 643-655.

Md Azizul ISlam, PANG Jin-huan, MENG Fan-wei, LI Ya-wen, XU Ning, YANG Chao, LIU Jun. Putrescine, spermidine, and spermine play distinct roles in rice salt tolerance[J]. Journal of Integrative Agriculture, 2020, 19(3): 643-655.

参考文献

Applewhite P B, Kaur-Sawhney R, Galston A W. 2003. A role for spermidine in the bolting and flowering of Arabidopsis. Physiologia Plantarum, 108, 314–320.
Bagni N, Tassoni A. 2001. Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids, 20, 301–317.
Baniasadi F, Saffari V R, Moud A A M. 2018. Physiological and growth responses of Calendula officinalis L. plants to the interaction effects of polyamines and salt stress. Scientia Hortic-Amsterdam, 234, 312–317.
Chattopadhayay M K, Tiwari B S, Chattopadhyay G, Bose A, Sengupta D N, Ghosh B. 2002. Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiologia Plantarum, 116, 192–199.
Chen B X, Li W Y, Gao Y T, Chen Z J, Zhang W N, Liu Q J, Chen Z, Liu J. 2016. Involvement of polyamine oxidase-produced hydrogen peroxide during coleorhiza-limited germination of rice seeds. Frontiers in Plant Science, 7, 1219.
Chen D, Shao Q, Yin L, Younis A, Zheng B. 2018. Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses. Frontiers in Plant Science, 9, 1945.
Cona A, Rea G, Angelini R, Federico R, Tavladoraki P. 2006. Functions of amine oxidases in plant development and defence. Trends in Plant Science, 11, 80–88.
Dionisio-Sese M L, Tobita S. 2000. Effects of salinity on sodium content and photosynthetic responses of rice seedlings differing in salt tolerance. Journal of Plant Physiology, 157, 54–58.
Ghosh N, Adak M K, Ghosh P D, Gupta S, Sen G, Mandal C. 2011. Differential responses of two rice varieties to salt stress. Plant Biotechnology Reports, 5, 89–103.
Ghosh N, Das S P, Mandal C, Gupta S, Das K, Dey N, Adak M K. 2012. Variations of antioxidative responses in two rice cultivars with polyamine treatment under salinity stress. Physiology and Molecular Biology in Plants, 18, 301–313.
Groppa M D, Benavides M P. 2008. Polyamines and abiotic stresses: Recent advances. Amino Acids, 34, 35–45.
Grossi M, Phanstiel O, Rippe C, Sward K, Alajbegovic A, Albinsson S, Forte A, Persson L, Hellstrand P, Nilsson B O. 2016. Inhibition of polyamine uptake potentiates the anti-proliferative cells. Journal of Cellular Physiology, 231, 1334–1342.
Gupta K, Dey A, Gupta B. 2013. Plant polyamines in abiotic stress responses. Acta Physiologiae Plantarum, 35, 2015–2036.
Gupta S, Chattopadhyay M K, Chatterjee P, Ghosh B, Sengupta D N. 1998. Expression of abscisic acid responsive element binding protein in salt tolerant indica rice (Oryza sativa L. cv. Pokkali). Plant Molecular Biology, 37, 629–637.
Hanfrey C, Sommer S, Mayer M J, Burtin D, Michael A J. 2001. Arabidopsis polyamine biosynthesis: Absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. The Plant Journal, 27, 551–560.
Hussain S S, Ali M, Ahmad M, Siddique K H. 2011. Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants. Biotechnology Advances, 29, 300–311.
Jang S J, Wi S J, Choi Y J, An G, Park K Y. 2012. Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: T-DNA mutational analysis of Oryza sativa lysine decarboxylase-like protein 1. Molecules and Cells, 34, 251–262.
Lichtenthaler H K. 2007. Biosynthesis, accumulation and emission of carotenoids, α-tocophenol, plastoquinone and isoprene in leaves under high photosynthetic irradiance. Photosynthesis Research, 92, 163–179.
Miller-Fleming L, Olin-Sandoval V, Campbell K, Ralser M. 2015. Remaining mysteries of molecular biology: The role of polyamines in the cell. Journal of Molecular Biology, 427, 3389–3406.
Moradi F, Ismail A M. 2007. Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Annals of Botany, 99, 1161–1173.
de Oliveira L F, Elbl P, Navarro B V, Macedo A F, Dos Santos A L, Floh E I, Cooke J. 2017. Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. Tree Physiology, 37, 116–130.
Quinet M, Ndayiragije A, Lefèvre I, Lambillotte B, Dupont-Gillain C C, Lutts S. 2010. Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. Journal of Experimental Botany, 61, 2719–2733.
Sajid H, Zhang J, Zhong C, Zhu L, Cao X, Yu S, Allen B J, Hu J, Jin Q. 2017. Effects of salt stress on rice growth, development characteristics, and the regulating ways: A review. Journal of Integrative Agriculture, 16, 2357–2374.
Shao C G, Wang H, Bi Y F. 2015. Relationship between endogenous polyamines and tolerance in Medicago sativa L. under heat stress. Acta Agrestia Sinica, 6, 1214–1219. (in Chinese)
Tian J, Guo S R, Sun J, Wang L P, Yang Y J, Li B. 2011. Effects of exogenous spermidine on lipid peroxidation and membrane proton pump activity of cucumber seedling leaves under high temperature stress. Chinese Journal of Applied Ecology, 12, 3252–3258. (in Chinese)
Xiong Q, Ma B, Lu X, Huang Y H, He S J, Yang C, Yin C C, Zhao H, Zhou Y, Zhang W K, Wang W S, Li Z K, Chen S Y, Zhang J S. 2017. Ethylene-inhibited jasmonic acid biosynthesis promotes mesocotyl/coleoptile elongation of etiolated rice seedlings. The Plant Cell, 29, 1053–1072.
Yamamoto A, Shim I S, Fujihara S. 2017. Inhibition of putrescine biosynthesis enhanced salt stress sensitivity and decreased spermidine content in rice seedlings. Biologia Plantarum, 61, 385–388.
Yang J, Zhang J, Liu K, Wang Z, Liu L. 2007. Involvement of polyamines in the drought resistance of rice. Journal of Experimental Botany, 58, 1545–1555.
Zapata P J, Serrano M, Pretel M T, Amorós A, Botella M A. 2003. Changes in ethylene evolution and polyamine profiles of seedlings of nine cultivars of Lactuca sativa L. in response to salt stress during germination. Plant Science, 164, 557–563.

Putrescine, spermidine, and spermine play distinct roles in rice salt tolerance

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