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Research paper | Open Access

Early ABA-stimulated maintenance of Cl homeostasis by mepiquat chloride priming confers salt tolerance in cotton seeds

Ning Wang1Xiangru Wang1Hengheng ZhangXiaohong LiuJianbin ShiQiang DongQinghua XuHuiping GuiMeizhen Song( )Gentu Yan( )
State Key Laboratory of Cotton Biology, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, Henan, China

Peer review under responsibility of Crop Science Society of China and Institute of Crop Science, CAAS.

1 These authors contributed equally to this work.

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Abstract

Mepiquat chloride (MC) priming alleviates the effects of salt stress during seed germination in cotton (Gossypium hirsutum L.), but the mechanisms underlying its effects are unknown. We found that MC priming increases salt tolerance, as evidenced by marked increases in seed vigor and germination rates, and alleviated salt toxicity by reducing Cl accumulation in germinating seeds. Consistently, electrophysiological experiments revealed that the seeds with MC priming displayed superior Cl exclusion ability in the root apex. These beneficial effects of MC priming were abolished by the abscisic acid (ABA)-synthesis blocker fluridone under salt stress. MC priming induced an early response to acclimatization and stress, as indicated by rapidly increasing ABA content during initial exposure to salt stress. Transcriptome analyses revealed that MC priming induced an array of differentially expressed genes (DEGs) in germinating seeds. The most noticeable changes in germinating seeds were MC priming-induced increases in the expression of DEGs encoding components of ABA biosynthesis, ABA catabolism, and ABA signaling pathways under salt stress. MC priming also increased the expression of some DEGs encoding Cl ion transporters (e.g. CCC, SLAC1/SLAH1/SLAH3, CLC, and ALMT9) in germinating seeds. These results indicate that MC priming-induced ABA contributes to Cl homeostasis in tissues and acts as a positive regulator of salt tolerance via regulation of Cl transporters (particularly CCC and SLAC1/SLAH1/SLAH3). Taken together, these findings shed light on the molecular mechanism underlying MC-mediated tolerance to salt stress during seed germination.

References

[1]

X.Q. Kong, Z. Luo, Y.J. Zhang, W. Li, H.Z. Dong, Soaking in H2O2 regulates ABA biosynthesis and GAs catabolism in germinating cotton seeds under salt stress, Acta Physiol. Plant. 39 (2017) 2.

[2]

N. Wang, W.Q. Qiao, X.H. Liu, J.B. Shi, Q.H. Xu, H. Zhou, G.T. Yan, Q. Huang, Relative contribution of Na+/K+ homeostasis, photochemical efficiency and antioxidant defense system to differential salt tolerance in cotton (Gossypium hirsutum L.) cultivars, Plant Physiol. Biochem. 119 (2017) 121–131.

[3]

X. Yang, Y.C. Xu, F.F. Yang, R.O. Magwanga, X.Y. Cai, X.X. Wang, Y.H. Wang, Y.Q. Hou, K.B. Wang, F. Liu, Z.L. Zhou, Y.C. Xu, Genome-wide identification of OSCA gene family and their potential function in the regulation of dehydration and salt stress in Gossypium hirsutum, J. Cotton Res. 2 (2019) 11.

[4]

N. Wang, X.R. Wang, J.B. Shi, X.H. Liu, Q.H. Xu, H. Zhou, M.Z. Song, G.T. Yan, Mepiquat chloride-priming induced salt tolerance during seed germination of cotton (Gossypium hirsutum L.) through regulating water transport and K+/Na+ homeostasis, Environ. Exp. Bot. 159 (2019) 168–178.

[5]

L. Guja, R. Wuhrer, K. Moran, K. Dixon, G. Wardell-Johnson, D.J. Merritt, Full spectrum X-ray mapping reveals differential localization of salt in germinating seeds of differing salt tolerance, Bot. J. Linn. Soc. 173 (2013) 129–142.

[6]

Y. Lai, D.Q. Zhang, J.M. Wang, J.C. Wang, P.R. Ren, L.R. Yao, E.J. Si, Y.H. Kong, H.J. Wang, Integrative transcriptomic and proteomic analyses of molecular mechanism responding to salt stress during seed germination in hulless barley, Int. J. Mol. Sci. 21 (2020) 359.

[7]

M.A. Hossain, S. Bhattacharjee, S.M. Armin, P. Qian, W. Xin, H.Y. Li, D.J. Burritt, M. Fujita, L.S. Tran, Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging, Front. Plant Sci. 6 (2015) 420.

[8]

X.K. Zhang, G.Y. Lu, W.H. Long, X.L. Zou, F. Li, T. Nishio, Recent progress in drought and salt tolerance studies in Brassica crops, Breed. Sci. 64 (2014) 60–73.

[9]

H.J. Zhang, N. Zhang, R.C. Yang, L. Wang, Q.Q. Sun, D.B. Li, Y.Y. Cao, S. Weeda, B. Zhao, S.X. Ren, Y.D. Guo, Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GAs interaction in cucumber (Cucumis sativus L.), J. Pineal Res. 57 (2014) 269–279.

[10]

L.S. Duan, X.L. Tian, Principle and Technology of Crop Chemical Regulation, China Agricultural University Press, Beijing, China, 2011 270–275 (in Chinese).

[11]

N. Wang, X.L. Tian, L.S. Duan, G.T. Yan, Q. Huang, Z.H. Li, Metabolism of reactive oxygen species involved in increasing root vigour of cotton seedlings by soaking seeds with mepiquat chloride, Acta Agron. Sin. 40 (2014) 1220–1226 (in Chinese with English abstract).

[12]

R. Munns, M. Tester, Mechanisms of salinity tolerance, Ann. Rev. Plant Biol. 59 (2008) 651–681.

[13]

J. Sun, M.J. Wang, M.Q. Ding, S.R. Deng, M.Q. Liu, C.F. Lu, X.Y. Zhou, X. Shen, X.J. Zheng, Z.K. Zhang, J. Song, Z.M. Hu, Y. Xu, S.L. Chen, H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells, Plant Cell Environ. 33 (2010) 943–958.

[14]

Y.C. Yu, A.M. Wang, X. Li, M. Kou, W.J. Wang, X.Y. Chen, T. Xu, M. Zhu, D. Ma, Z. Li, J. Sun, Melatonin-stimulated triacylglycerol breakdown and energy turnover under salinity stress contributes to the maintenance of plasma membrane H+-ATPase activity and K+/Na+ homeostasis in sweet potato, Front. Plant Sci. 9 (2018) 256.

[15]

C.S. Zou, A.J. Chen, L.H. Xiao, H.M. Muller, P. Ache, G. Haberer, M.L. Zhang, W. Jia, P. Deng, R. Huang, D.N. Lang, F. Li, D.L. Zhan, X.Y. Wu, H. Zhang, J. Bohm, R.Y. Liu, S. Shabala, R. Hedrich, J.K. Zhu, H. Zhang, A high-quality genome assembly of quinoa provides insights into the molecular basis of salt bladder-based salinity tolerance and the exceptional nutritional value, Cell Res. 27 (2017) 1327–1340.

[16]

W.S Dai, M. Wang, X.Q. Gong, J.H. Liu, The transcription factor FcWRKY40 of Fortunella crassifolia functions positively in salt tolerance through modulation of ion homeostasis and proline biosynthesis by directly regulating SOS2 and P5CS1 homologs, New Phytol. 219 (2018) 972–989.

[17]

J. Liu, S. Shabala, J. Zhang, G.H. Ma, D.D. Chen, L. Shabala, F.R. Zeng, Z.H. Chen, M.M. Zhou, G. Venkataraman, Q.Z. Zhao, Melatonin improves rice salinity stress tolerance by NADPH oxidase-dependent control of the plasma membrane K+ transporters and K+ homeostasis, Plant Cell Environ, 2020https://doi.org/10.1111/pce.13759.

[18]

H.H. Wu, X.C. Zhang, J.P. Giraldo, S. Shabala, It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress, Plant Soil 431 (2018) 1–17.

[19]

Y.Q. He, B. Yang, Y. He, C.F. Zhan, Y.C. Cheng, J.H. Zhang, H.S. Zhang, J.P. Cheng, Z.F. Wang, A quantitative trait locus, qSE3, promotes seed germination and seedling establishment under salinity stress in rice, Plant J. 97 (2019) 1089–1104.

[20]

B. Li, M. Tester, M. Gilliham, Chloride on the move, Trends Plant Sci. 22 (2017) 236–248.

[21]

S.W. Henderson, U. Baumann, D.H. Blackmore, A.R. Walker, R.R. Walker, M. Gilliham, Shoot chloride exclusion and salt tolerance in grapevine is associated with differential ion transporter expression in roots, BMC Plant Biol. 14 (2014) 273.

[22]

L. Wang, J.Y. Xu, W. Jia, Z. Chen, Z.C. Xu, Chloride salinity in a chloride-sensitive plant: focusing on photosynthesis, hormone synthesis and transduction in tobacco, Plant Physiol. Biochem. 153 (2020) 119–130.

[23]

J.M. Colmenero-Flores, J.D. Franco-Navarro, P. Cubero-Font, P. Peinado-Torrubia, M.A. Rosales, Chloride as a beneficial macronutrient in higher plants: new roles and regulation, Int. J. Mol. Sci. 20 (2019) 4686.

[24]

C.M. Geilfus, Chloride: from nutrient to toxicant, Plant Cell Physiol. 59 (2018) 877–886.

[25]

P.P. Wei, L.C. Wang, A.L. Liu, B.J. Yu, H.M. Lam, GmCLC1 confers enhanced salt tolerance through regulating chloride accumulation in soybean, Front. Plant Sci. 7 (2016) 1082.

[26]

J. Zhang, H.Y. Yu, Y.S. Zhang, Y.B. Wang, M.Y. Li, J.C. Zhang, L.S. Duan, M.C. Zhang, Z.H. Li, Increased abscisic acid levels in transgenic maize overexpressing AtLOS5 mediated root ion fluxes and leaf water status under salt stress, J. Exp. Bot. 67 (2016) 1339–1355.

[27]

X.Q. Kong, Z. Luo, H.Z. Dong, A.E Eneji, W.J. Li, H2O2 and ABA signaling are responsible for the increased Na+ efflux and water uptake in Gossypium hirsutum L. roots in the non-saline side under non-uniform root zone salinity, J. Exp. Bot. 267 (2016) 2247–2261.

[28]
V.C.D. Fernando, D.F. Schroeder, Role of ABA in Arabidopsissalt, drought, and desiccation tolerance, in: A.K. Shanker, C.Shanker (Eds.), Abiotic and Biotic Stress in Plants-recentAdvances and Future Perspectives, IntechOpen, Rijeka, Croatia 2016, pp. 507–524.
[29]

A. Himmelbach, Y. Yang, E. Grill, Relay and control of abscisic acid signaling, Curr. Opin. Plant Biol. 6 (2003) 470–479.

[30]

X.L. Liu, H. Zhang, Y.Y. Jin, M.M. Wang, H.Y. Yang, H.Y. Ma, C.J. Jiang, Z.W. Liang, Abscisic acid primes seedlings for enhanced tolerance to alkaline stress by upregulating antioxidant defense and stress tolerance-related genes, Plant Soil 438 (2019) 39–55.

[31]

H. Nabizadeh, M. Valizadeh, M. Norouzi, T. Mahmoud, M.B. Vajovi, Effect of different levels of NaCl salinity on antioxidant enzyme's activity in seedling of different wheat cultivars, Biol. Forum–Int. J. 7 (2015) 180–186.

[32]

A.Y. Tsai, S. Gazzarrini, Overlapping and distinct roles of AKIN10 and FUSCA3 in ABA and sugar signaling during seed germination, Plant Signal. Behav. 7 (2015) 1238–1242.

[33]

J.R. Guo, S.S. Suo, B.S. Wang, Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa, Seed Sci. Res. 25 (2015) 335–344.

[34]

D.J. Yin, J. Zhang, R. Jing, Q.Q. Qu, H.Y. Guan, L.L. Zhang, L. Dong, Effect of salinity on ion homeostasis in three halophyte species, Limonium bicolor, Vitex trifolia Linn. var. simplicifolia Cham and Apocynaceae venetum, Acta Physiol. Plant. 40 (2018) 40.

[35]

Q. Li, E. Fritz, X-ray microanalysis of ion content in stem tip meristem and leaves of Populus grown under potassium and phosphors deficiency, J. Plant Physiol. 136 (1990) 61–65.

[36]

J. Sun, S.L. Chen, S.X. Dai, R.G. Wang, N.Y. Li, X. Shen, X.Y. Zhou, C.F. Lu, X.J. Zheng, Z.M. Hu, Z.K. Zhang, J. Song, Y. Xu, NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species, Plant Physiol. 149 (2009) 1141–1153.

[37]

X.Q. Pan, R. Welti, X.M. Wang, Simultaneous quantification of major phytohormones and related compounds in crude plant extracts by liquid chromatography-electrospray tandem mass spectrometry, Phytochemistry 69 (2008) 1773–1781.

[38]

D. Kim, B. Langmead, S.L. Salzberg, HISAT: a fast spliced aligner with low memory requirements, Nat. Methods 12 (2015) 357–360.

[39]

B. Langmead, S. Salzberg, Fast gapped-read alignment with Bowtie2, Nat. Methods 9 (2012) 357–359.

[40]

K. Shu, X.D. Liu, Q. Xie, Z. He, Two faces of one seed: hormonal regulation of dormancy and germination, Mol. Plant 9 (2016) 34–45.

[41]

Q. Wu, M.W. Du, J. Wu, N. Wang, B.M. Wang, F.J. Li, X.L. Tian, Z.H. Li, Mepiquat chloride promotes cotton lateral root formation by modulating plant hormone homeostasis, BMC Plant Biol. 19 (2019) 573.

[42]

D.C. Cao, H.M. Xu, Y.Y. Zhao, X. Deng, Y.X. Liu, W.J. Soppe, J.X. Lin, Transcriptome and degradome sequencing reveals dormancy mechanisms of Cunninghamia lanceolata seeds, Plant Physiol. 172 (2016) 2347–2362.

[43]

S. Li, N. Wang, D.D. Ji, W.X. Zhang, Y. Wang, Y.C. Yu, S.Z. Zhao, M.H. Lu, J.J. You, Y.Y. Zhang, L.L. Wang, X.F. Wang, Z.H. Liu, J.H. Tong, T.L. Xiao, M.Y. Bai, F.N. Xiang, A GmSIN1/GmNCED3s/GmRbohBs feed-forward loop acts as a signal amplifier that regulates root growth in soybean exposed to salt stress, Plant Cell 31 (2019) 2107–2130.

[44]

M. Wei, Y. Zhuang, H. Li, P.H. Li, H.Q. Huo, D. Shu, W.Z. Huang, S.H. Wang, The cloning and characterization of hypersensitive to salt stress mutant, affected in quinolinate synthase, highlights the involvement of NAD in stress-induced accumulation of ABA and proline, Plant J. 102 (2020) 85–98.

[45]

Y. Huang, M.M. Sun, Q. Ye, X.Q. Wu, W.H. Wu, Y.F. Chen, Abscisic acid modulates seed germination via ABA INSENSITIVE5-mediated PHOSPHATE1, Plant Physiol. 175 (2017) 1661–1668.

The Crop Journal
Pages 387-399
Cite this article:
Wang N, Wang X, Zhang H, et al. Early ABA-stimulated maintenance of Cl homeostasis by mepiquat chloride priming confers salt tolerance in cotton seeds. The Crop Journal, 2021, 9(2): 387-399. https://doi.org/10.1016/j.cj.2020.08.004

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Received: 04 April 2020
Revised: 22 July 2020
Accepted: 09 September 2020
Published: 21 September 2020
© 2020 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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