Hostname: page-component-7d8f8d645b-xmxxh Total loading time: 0 Render date: 2023-05-28T13:32:51.030Z Has data issue: false Feature Flags: { "useRatesEcommerce": true } hasContentIssue false

Mechanism of salt-inhibited early seed germination analysed by transcriptomic sequencing

Published online by Cambridge University Press:  04 March 2019

Kaiwen Xia
Affiliation:
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University, Wuhan, 430079, China
Aili Liu
Affiliation:
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University, Wuhan, 430079, China
Yizhong Wang
Affiliation:
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University, Wuhan, 430079, China
Wannian Yang
Affiliation:
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University, Wuhan, 430079, China
Ye Jin*
Affiliation:
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University, Wuhan, 430079, China
*
Author for correspondence: Ye Jin, Email: jinye@mail.ccnu.edu.cn

Abstract

Seed germination, the first and critical step of the plant's life cycle, is affected by salt stress. However, the underlying mechanism of salt tolerance during early seed germination remains elusive. Here, a comparative RNA-seq analysis was performed using early germinating seeds either under normal conditions or in 100 and 150 mM sodium chloride. A total of 575 genes were up-regulated and 913 genes were down-regulated in the presence of 100 mM NaCl. Under the 150 mM NaCl treatment 1921 genes were up-regulated and 3501 genes were down-regulated. A total of 379 or 863 genes were up-regulated or down-regulated in both 100 and 150mM NaCl. These co-regulated genes were further analysed by GO enrichment. Genes in the categories abscisic acid signaling and synthesis and nutrient reservoir activity were significantly enriched in the up-regulated genes. Transcription factors responsive to gibberellin and auxin were significantly down-regulated by salinity stress. Genes related to anti-oxidant activity were significantly enriched in the down-regulated gene clusters by NaCl treatment. Our results suggest that salt stress inhibits seed germination by activating ABA synthesis and signalling, and depressing GA and auxin signalling, while preserving nutrition and down-regulated anti-oxidant activity. Our study provides more insight into the molecular mechanism of salt tolerance during early seed germination.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Apel, K and Hirt, H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373399.CrossRefGoogle ScholarPubMed
Attia, H, Alamer, KH, Selmi, I, Djebali, W, Chaïbi, W and Nasri, MB (2018) Physiological and structural modifications in snail medic (Medicago scutellata L.) plants exposed to salinity. Acta Biologia Hungaria 69, 336349.CrossRefGoogle ScholarPubMed
Bi, C, Ma, Y, Wu, Z, Yu, YT, Liang, S, Lu, K and Wang, XF (2017) Arabidopsis ABI5 plays a role in regulating ROS homeostasis by activating CATALASE 1 transcription in seed germination. Plant Molecular Biology 94, 197213.CrossRefGoogle Scholar
Chen, H, Zhang, J, Neff, MM, Hong, SW, Zhang, H, Deng, XW and Xiong, L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proceedings of the National Academy of Sciences of the USA 105, 44955000.CrossRefGoogle ScholarPubMed
Cheng, MC, Ko, K, Chang, WL, Kuo, WC, Chen, GH and Lin, TP (2015) Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant Journal 83, 926939.CrossRefGoogle ScholarPubMed
Cheng, Y, Zhang, X, Sun, T, Tian, Q and Zhang, WH (2018) Glutamate receptor homolog3.4 is involved in regulation of seed germination under salt stress in Arabidopsis. Plant and Cell Physiology 59, 978988.CrossRefGoogle ScholarPubMed
Darwin, C (1856) On the action of sea-water on the germination of seeds. Journal of the Proceedings of the Linnean Society London (Botany) 1, 130140.Google Scholar
Das, P, Nutan, KK, Singla-Pareek, SL and Pareek, A (2015) Understanding salinity responses and adopting ‘omics-based’ approaches to generate salinity tolerant cultivars of rice. Frontiers in Environmental Science 6, 712.Google ScholarPubMed
Daszkowska-Golec, A (2011) Arabidopsis seed germination under abiotic stress as a concert of action of phytohormones. OMICS 15, 763764.CrossRefGoogle ScholarPubMed
de Lucas, M, Davière, JM, Rodríguez-Falcón, M, Pontin, M, Iglesias-Pedraz, JM, Lorrain, S, Fankhauser, C, Blázquez, MA, Titarenko, E and Prat, S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480484.CrossRefGoogle ScholarPubMed
Deinlein, U, Stephan, AB, Horie, T, Luo, W, Xu, G and Schroeder, JI (2014) Plant salt-tolerance mechanisms. Trends in Plant Science 19, 371379.CrossRefGoogle ScholarPubMed
FAO (2011). The state of the world's land and water resources for food and agriculture (SOLAW) – managing systems at risk. Food and Agriculture, Organization of the United Nations, Rome and Earthscan, London.Google Scholar
Finkelstein, R, Reeves, W, Ariizumi, T and Steber, C (2008) Molecular aspects of seed dormancy. Annual Review of Plant Biology 59, 387415.CrossRefGoogle ScholarPubMed
Finkelstein, RR and Somerville, CR (1990) Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses. Plant Physiology 94, 11721179.CrossRefGoogle ScholarPubMed
Fujii, H, Verslues, PE and Zhu, JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19, 485494.CrossRefGoogle ScholarPubMed
Furihata, T, Maruyama, K, Fujita, Y, Umezawa, T, Yoshida, R, Shinozaki, K and Yamaguchi-Shinozaki, K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proceedings of the National Academy of Sciences of the USA 103, 198–193.CrossRefGoogle ScholarPubMed
Han, C and Yang, PF (2015) Studies on the molecular mechanisms of seed germination. Proteomics 15, 16711679.CrossRefGoogle ScholarPubMed
Ishibashi, Y, Aoki, N, Kasa, S, Sakamoto, M, Kai, K, Tomokiyo, R, Watabe, G, Yuasa, T and Iwaya-Inoue, M (2017) The interrelationship between abscisic acid and reactive oxygen species plays a key role in barley seed dormancy and germination. Frontiers in Plant Science 8, 275.CrossRefGoogle Scholar
Jin, H, Cominelli, E, Bailey, P, Parr, A, Mehrtens, F, Jones, J, Tonelli, C, Weisshaar, B and Martin, C (2000) Transcriptional repression by AtMYB4 controls production of UV- protecting sunscreens in Arabidopsis. EMBO Journal 19, 61506161.CrossRefGoogle ScholarPubMed
Khajeh-Hosseini, M, Powell, AA and Bingham, IJ (2003) The interaction between salinity stress and seed vigour during germination of soybean seeds. Seed Science and Technology 31, 715725.CrossRefGoogle Scholar
Lariguet, P, Ranocha, P, De Meyer, M, Barbier, O, Penel, C and Dunand, C (2013) Identification of a hydrogen peroxide signalling pathway in the control of light-dependent germination in Arabidopsis. Planta 238, 381395.CrossRefGoogle ScholarPubMed
Li, Z, Xu, J, Gao, Y, Wang, C, Guo, G, Luo, Y, Huang, Y, Hu, W, Sheteiwy, MS, Guan, Y and Hu, J (2017) The synergistic priming effect of exogenous salicylic acid and H2O2 on chilling tolerance enhancement during maize (Zea mays L.) seed germination. Frontiers in Plant Science 8, 1153.CrossRefGoogle ScholarPubMed
Liu, C, Wang, B, Li, Z, Peng, Z and Zhang, J (2018) TsNAC1 is a key transcription factor in abiotic stress resistance and growth. Plant Physiology 176, 742756.CrossRefGoogle Scholar
Lopez-Molina, L, Mongrand, S and Chua, NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 98, 47824787.CrossRefGoogle ScholarPubMed
Ma, QB, Dai, XY, Xu, YY, Guo, J, Liu, YJ, Chen, N, Xiao, J, Zhang, D, Xu, Z, Zhang, X and Chong, K (2009a) Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiology 150, 244256.CrossRefGoogle Scholar
Ma, Y, Szostkiewicz, I, Korte, A, Moes, D, Yang, Y, Christmann, A and Gril, E (2009b) Regulators of PP2C phosphatase activity function as Abscisic acid sensors. Science 324, 10641068.Google Scholar
Macovei, A, Pagano, A, Leonetti, P, Carbonera, D, Balestrazzi, A and Araújo, SS (2017) Systems biology and genome-wide approaches to unveil the molecular players involved in the pre-germinative metabolism: implications on seed technology traits. Plant Cell Reports 36, 669688.CrossRefGoogle ScholarPubMed
Nakashima, K, Fujita, Y, Kanamori, N, Katagiri, T, Umezawa, T, Kidokoro, S, Maruyama, K, Yoshida, T, Ishiyama, K, Kobayashi, M, Shinozaki, K and Yamaguchi-Shinozaki, K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant and Cell Physiology 50, 13451363.CrossRefGoogle ScholarPubMed
Née, G, Kramer, K, Nakabayashi, K, Yuan, B, Xiang, Y, Miatton, E, Finkemeier, I and Soppe, WJJ (2017). DELAY OF GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nature Communications 8, 72.CrossRefGoogle ScholarPubMed
North, H, Baud, S, Debeaujon, I, Dubos, C, Dubreucq, B, Grappin, P, Jullien, M, Lepiniec, L, Marion-Poll, A, Miquel, M, Rajjou, L, Routaboul, JM and Caboche, M (2010) Arabidopsis seed secrets unravelled after a decade of genetic and omics-driven research. Plant Journal 61, 971981.CrossRefGoogle ScholarPubMed
Oracz, K, El-Maarouf-Bouteau, H, Kranner, I, Bogatek, R, Corbineau, F, Bailly, C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signaling during germination. Plant Physiology 150, 494505.CrossRefGoogle ScholarPubMed
Park, SY, Fung, P, Nishimura, N, Jensen, DR, Fujii, H, Zhao, Y, Lumba, S, Santiago, J, Rodrigues, A, Chow, TF, Alfred, SE, Bonetta, D, Finkelstein, R, Provart, NJ, Desveaux, D, Rodriguez, PL, McCourt, P, Zhu, JK, Schroeder, JI, Volkman, BF and Cutler, SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 10681071.Google ScholarPubMed
Preston, J, Tatematsu, K, Kanno, Y, Hobo, T, Kimura, M, Jikumaru, Y, Yano, R, Kamiya, Y and Nambara, E (2009) Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: a comparative study on dormant and non-dormant accessions. Plant and Cell Physiology 50, 17861800.CrossRefGoogle ScholarPubMed
Radhakrishnan, R and Baek, KH (2017) Physiological and biochemical perspectives of non-salt tolerant plants during bacterial interaction against soil salinity. Plant Physiology and Biochemistry 116, 116126.CrossRefGoogle ScholarPubMed
Rajjou, L, Duval, M, Gallardo, K, Catusse, J, Bally, J, Job, C and Job, D (2012) Seed germination and vigor. Annual Review of Plant Biology 63, 507533.CrossRefGoogle ScholarPubMed
Rieu, I, Eriksson, S, Powers, SJ, Gong, F, Griffiths, J, Woolley, L, Benlloch, R, Nilsson, O, Thomas, SG, Hedden, P and Phillips, AL (2008) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20, 24202436.CrossRefGoogle ScholarPubMed
Roy, S (2016). Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant Signaling and Behavior 11, e1117723.CrossRefGoogle ScholarPubMed
Seo, PJ and Park, CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytologist 186, 471483.CrossRefGoogle ScholarPubMed
Shen, X, Wang, Z, Song, X, Xu, J, Jiang, C, Zhao, Y, Ma, C and Zhang, H (2014) Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis. Plant Molecular Biology 86, 303317.CrossRefGoogle ScholarPubMed
Shi, H, Wang, X, Mo, X, Tang, C, Zhong, S and Deng, XW (2015) Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination. Proceedings of the National Academy of Sciences of the USA 112, 38173822.Google ScholarPubMed
Shu, K, Zhang, H, Wang, S, Chen, M, Wu, Y, Tang, S, Liu, C, Feng, Y, Cao, X and Xie, Q (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genetics 9, e1003577.CrossRefGoogle ScholarPubMed
Vannini, C, Locatelli, F, Bracale, M, Magnani, E, Marsoni, M, Osnato, M, Mattana, M, Baldoni, E and Coraggio, I (2004) Overexpression of the rice OsMYB4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. Plant Journal 37, 115127.CrossRefGoogle ScholarPubMed
Vishwakarma, K, Upadhyay, N, Kumar, N, Yadav, G, Singh, J, Mishra, RK, Kumar, V, Verma, R, Upadhyay, RG, Pandey, M and Sharma, S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Frontiers in Plant Science 8, 161.CrossRefGoogle ScholarPubMed
Wan, L, Ross, AR, Yang, J, Hegedus, DD and Kermode, AR (2007) Phosphorylation of the 12 S globulin cruciferin in wild-type and abi1-1 mutant Arabidopsis thaliana (thale cress) seeds. Biochemical Journal 404, 247256.CrossRefGoogle ScholarPubMed
Wang, Y, Hu, Q, Wu, Z, Wang, H, Han, S, Jin, Y, Zhou, J, Zhang, Z, Jiang, J, Shen, Y, Shi, H and Yang, W (2017) HISTONE DEACETYLASE 6 represses pathogen defence responses in Arabidopsis thaliana. Plant, Cell and Environment 40, 29722986.CrossRefGoogle ScholarPubMed
Wang, Y, Yang, L, Zheng, Z, Grumet, R, Loescher, W, Zhu, JK, Yang, P, Hu, Y and Chan, Z (2013). Transcriptomic and physiological variations of three Arabidopsis ecotypes in response to salt stress. PLoS ONE 8, e69036.CrossRefGoogle ScholarPubMed
Weitbrecht, K, Müller, K and Leubner-Metzger, G (2011) First off the mark: early seed germination. Journal of Experimental Botany 62, 32893309.CrossRefGoogle ScholarPubMed
Wilson, RL, Kim, H, Bakshi, A and Binder, BM (2014) The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiology 165, 13531366.CrossRefGoogle ScholarPubMed
Xu, E, Chen, M, He, H, Zhan, C, Cheng, Y, Zhang, H and Wang, Z (2017a) Proteomic analysis reveals proteins involved in seed imbibition under salt stress in rice. Frontiers in Plant Science 7, 2006.CrossRefGoogle Scholar
Xu, XX, Hu, Q, Yang, WN and Jin, Y (2017b) The roles of cell wall invertase inhibitor in regulating chilling tolerance in tomato. BMC Plant Biology 17, 195.CrossRefGoogle Scholar
Yamauchi, Y, Ogawa, M, Kuwahara, A, Hanada, A, Kamiya, Y and Yamaguchi, S (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16, 367378.CrossRefGoogle ScholarPubMed
Yang, A, Xiaoyan, DX and Zhang, WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. Journal of Experimental Botany 63, 25412556.CrossRefGoogle Scholar
Ye, N, Zhu, G, Liu, Y, Zhang, A, Li, Y, Liu, R, Shi, L, Jia, L and Zhang, J (2012) Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. Journal of Experimental Botany 63, 18091822.CrossRefGoogle ScholarPubMed
Zehra, A, Gul, B, Ansari, R and Khan, MA (2012) Role of calcium in alleviating effect of salinity on germination of Phragmites karka seeds. South African Journal of Botany 78, 122128.CrossRefGoogle Scholar
Zhang, HJ, Zhang, N, Yang, RC, Wang, L, Sun, QQ, Li, DB, Cao, YY, Weeda, S, Zhao, B, Ren, S and Guo, YD (2014) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). Journal of Pineal Research 57, 269279.CrossRefGoogle Scholar
Zhao, P, Wang, L, Zhao, X, Chen, G and Ma, XF (2017) A comparative transcriptomic analysis reveals the core genetic components of salt and osmotic stress responses in Braya humilis. PLoS One 12, e0183778.CrossRefGoogle ScholarPubMed
Zhu, JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247273.CrossRefGoogle ScholarPubMed
Zhu, JK (2016). Abiotic stress signaling and responses in plants. Cell 167, 313324.CrossRefGoogle ScholarPubMed
Supplementary material: File

Xia et al. supplementary material

Xia et al. supplementary material 1

Download Xia et al. supplementary material(File)
File 1 MB