Biologia plantarum 63:610-617, 2019 | DOI: 10.32615/bp.2019.066
Identification of differentially expressed genes of Haloxylon ammodendronin response to salinity stress
- Biotechnology Research Centre, Inner Mongolia Academy of Agriculture & Animal Husbandry Sciences,
- 1 Hohhot, 010030, P.R. China
- Reproductive Centre, Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010050, P.R. China2
- 3 Lethbridge Research Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta T1J4B1, Canada
Haloxylon ammodendron (C.A. Mey.), an endangered desert tree with excellent drought and salinity tolerance, provides a unique genotype to characterize and understand the tolerance mechanisms. In this study, four RNA-Seq libraries were constructed and sequenced from H. ammodendron under salinity stress. Total 12 027 differentially expressed genes (DEGs) were identified, in which 4 023, 3 517, 4 487 genes were differentially expressed under light salinity stress (200 mM NaCl), moderate salinity stress (400 mM NaCl), and severe salinity stress (800 mM NaCl), respectively. The up-regulated DEGs included several transcription factors (e.g., MYB and bHLH), hormone-related genes (e.g., cytochrome P450), protein kinases (e.g., Atpk2-Atpk19 like), and genes involved in carbon metabolism (e.g., UDP glycosyltransferase), osmotic regulation (e.g., proline transporter), and ubiquitin proteasome system (e.g., ubiquitin-conjugating enzymes). Heat shock proteins were identified as positive regulators of salinity tolerance in H. ammodendron. The expression patterns of 13 DEGs verified by real-time quantitative PCR were identically consistent with the variations in transcript abundance identified by RNA-Seq. Our results provide new insights into molecular mechanism of H. ammodendron in response to salinity stress.
Keywords: carbon metabolism, drought and salinity tolerance, heat shock proteins, hormone-related genes, NaCl, RNA-Seq, transcription factors.
Received: May 24, 2018; Revised: March 25, 2019; Accepted: April 8, 2019; Published online: September 16, 2019 Show citation
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References
- Andjelkovic, V., Thompson, R.: Changes in gene expression in maize kernel in response to water and salt stress. - Plant Cell Rep. 25: 71-79, 2006.
Go to original source... - Audic, S., Claverie, J.M.: The significance of digital gene expression profiles. - Genome Res. 7: 986-995, 1997.
Go to original source... - Bak, S., Beisson, F., Bishop, G., Hamberger, B., Höfer, R., Paquette, S., Werck-Reichhart, D. (ed.): The Arabidopsis Book - Cytochromes P450. - The American Society of Plant Biologists, Washington 2011.
Go to original source... - Barragán, V., Leidi, E.O., Andrés, Z., Rubio, L., De Luca, A., Fernández, J.A., Cubero, B., Pardo, J.M.: Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. - Plant Cell 24: 1127-1142, 2012.
Go to original source... - Chang, B., Yang, L., Cong, W., Zu, Y., Tang, Z.: The improved resistance to high salinity induced by trehalose is associated with ionic regulation and osmotic adjustment in Catharanthus roseus. - Plant Physiol. Biochem. 77: 140-148, 2014.
Go to original source... - Cockburn, W., Whitelam, G.C., Broad, A., Smith, J.: The participation of phytochrome in the signal transduction pathway of salt stress responses in Mesembryanthemum crystallinum L. - J. exp. Bot. 47: 647-53, 1996.
Go to original source... - De Hoon, M.J.L., Imoto, S., Satoru, M.: Open source clustering software. - Bioinformatics 20: 250-251, 2002.
- Fang, Y.J., You, J., Xie, K., Xie, W.B., Xiong, L.Z.: Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. - Mol. gen. Genomics 280: 547-563, 2008.
Go to original source... - Flowers, T. J: Improving crop salinity tolerance. - J. exp. Bot. 55: 307-319, 2004.
Go to original source... - Gao, S., Su, P., Yan, Q., Ding, S.: Canopy and leaf gas exchange of Haloxylon ammodendron under different soil moisture regimes. - Sci. China Life Sci. 6: 718-728, 2010.
Go to original source... - Ge, Y., Li, Y., Zhu, Y.M., Bai, X., Lv, D.K., Guo, D., Ji, W., Cai, H.: Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. - BMC Plant Biol. 6: 718-728, 2010.
Go to original source... - Hao, Y.J., Wei, W., Song, Q.X., Chen, H.W., Zhang, Y.Q., Wang, F., Zou, H.F., Lei, G., Tian, A.G., Zhang, W.K., Ma, B., Zhang, J.S., Chen, S.Y.: Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. - Plant J. 68: 302-313, 2011.
Go to original source... - Harris, M.A., Clark, J., Ireland, A., Lomax, J., Ashburner, M., Foulger, R.: The Gene ontology (GO) data-base and informatics resource. - Nucl. Acids Res. 32: 258-261, 2004.
Go to original source... - He, J.F., Goyal, R.K., Laroche, A., Zhao, M.G., Lu, Z.X.: Effects of salinity stress on starch morphology, composition and physicochemical properties during grain development in triticale. - Can. J. Plant Sci. 93: 765-777, 2013.
Go to original source... - He, X.J., Mu, R.L., Cao, W.H., Zhang, Z.G., Zhang, J.S., Chen, S. Y.: AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. - Plant J. 44: 903-916, 2005.
Go to original source... - Hu, H., Dai, M., Yao, J., Xiao, B., Li, X., Zhang, Q., Xiong, L.: Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. - Proc. nat. Acad. Sci. USA 103: 12987-12992, 2006.
Go to original source... - Huang, P., Ju, H.W., Min, J.H., Zhang, X., Kim, S.H., Yang, K.Y.: Overexpression of L-type lectin-like protein kinase 1 confers pathogen resistance and regulates salinity response in Arabidopsis thaliana. - Plant Sci. 203: 98-106, 2013.
Go to original source... - Jakoby, M., Weisshaar, B., Dröge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., Parcy, F.: bZIP transcription factors in Arabidopsis. -Trends Plant Sci. 3: 106-111, 2002.
Go to original source... - Jeong, J.S., Kim, Y.S., Baek, K.H., Jung, H., Ha, S.H., Choi, Y.D., Kim, J.K.: Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. - Plant Physiol. 153: 185-197, 2010.
Go to original source... - Jia, B.W., Sun, M.Z., Duanmu, H.Z., Ding, X.D., Zhu. Y.M., Sun, X.L.: GsCHX19.3, a member of cation/H+ exchanger superfamily from wild soybean contributes to high salinity and carbonate alkaline tolerance. - Sci. Rep. 7: 9423, 2017.
Go to original source... - Jia, Q., Zheng, C., Sun, S., Amjad, H., Liang, K., Lin, W.: The role of plant cation/proton antiporter gene family in salt tolerance. - Biol. Plant. 62: 617-629, 2018.
Go to original source... - Jiang, J.J., Ma, S.H., Ye, N.H., Jiang, M., Cao, J.S., Zhang, J.H.: WRKY transcription factors in plant responses to stresses. - J. integr. Plant Biol. 59: 86-101, 2017.
Go to original source... - Kakumanu, A., Ambavaram, M.M.R., Klumas, C., Krishnan, A., Batlang, U., Myers, E.: Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. - Plant Physiol. 160: 846-867, 2012.
Go to original source... - Kanehisa, M., Goto, S., Hattori, M., Aoki-Kinoshita, K.F., Itoh, M., Kawashima, S.: From genomics to chemical genomics: new developments in KEGG. - Nucl. Acids Res. 34: 354-357, 2006.
Go to original source... - Kawasaki, S., Borchert, C., Deyholos, M., Wang, H., Brazille, S., Kawai, K., Galbraith, D., Bohnert, H.J.: Gene expression profiles during the initial phase of salt stress in rice. - Plant Cell 13: 889-905, 2001.
Go to original source... - Li, S.F., Fan, L.C.M., Li,Y., Zhang, J.H., Sun, J.H., Chen, Y.H., Tian, C.Y., Su, X.H., Lu, M.Z., Liang, C.Z., Hu, Z.M.: Effects of drought and salt-stresses on gene expression in Caragana korshinskii seedlings revealed by RNA-Seq. - BMC Genomics 17: 200-209, 2016.
Go to original source... - Long, Y., Zhang J.W., Tian, X.J., Wu, S.S., Zhang. Q., Zhang, J.P., Dang, Z.H., Pei, X.W.: De novo assembly of the desert tree Haloxylon ammodendron (C.A. Mey) based on RNA-Seq data provides insight into drought response, gene discovery and marker identification. - BMC Genomics 15: 1471-2164, 2014.
Go to original source... - Mao, G., Seebeck, T., Schrenker, D., Yu, O.: CYP709B3, a cytochrome P450 monooxygenase gene involved in salt tolerance in Arabidopsis thaliana. - BMC Plant Biol. 13: 169-181, 2013.
Go to original source... - Nam, K.H., Nam, K.J., An, J.H., Jeong, S.C., Park, K.W.: Comparative analysis of key nutrient composition between drought-tolerant transgenic rice and its non-transgenic counterpart. - Food Sci. Biotechnol. 22: 1-7, 2013.
Go to original source... - Naya, L., Ladrera, R., Ramos, J., González, E.M., Arrese-Igor, C., Minchin, F.R.: The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. - Plant Physiol. 144: 1104-1114, 2007.
Go to original source... - Niu, C.F., Wei, W., Zhou, Q.Y., Tian, A.G., Hao, Y.J., Zhang, W.K.: Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. - Plant Cell Environ. 35: 56-70, 2012.
Go to original source... - Powell, S. R., Herrmann, J., Lerman, A., Patterson, C., Wang, X. J.: The ubiquitin- proteasome system and cardiovascular diseases. - Prog. Mol. Biol. Transl. Sci. 109: 295-346, 2012.
Go to original source... - Rentsch, D., Hirner, B., Schmelzer, E., Frommer, W.B.: Salt stress-induced proline transporter and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease targeting mutant. - Plant Cell. 8: 1437-1446, 1996.
Go to original source... - Roy, S.J., Negrão, S., Tester, M.: Salt resistant crop plants. - Curr. Opin. Biotechnol. 26: 115-124, 2014.
Go to original source... - Saldanha, A.J.: Java Tree View - extensible visualization of microarray data. - Bioinformatics 20: 3246-3248, 2004.
Go to original source... - Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y.: Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full-length cDNA microarray. - Plant J. 31: 279-292, 2002.
Go to original source... - Sun, X.L., Yua, Q.Y., Tang, L.L., Ji, W., Bai, X., Cai, H.: GsSRK, a G-type lectin S-receptor-like serine/threonine protein kinase, is a positive regulator of plant tolerance to salt stress. - J. Plant Physiol. 170: 505-515, 2013.
Go to original source... - Takasaki, H., Maruyama, K., Kidokoro, S., Ito, Y., Fujita, Y., Shinozaki, K.: The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. - Mol. gen. Genomics 284: 173-183. 2010.
Go to original source... - Tran, L.S., Nakashima, K., Sakuma, Y., Simpson, S.D., Fujita, Y., Maruyama, K., Fujita, M., Seki, M., Shinozaki, K., Yamaguchi-Shinozaki, K.: Isolation and functional analysis of Arabidopsis stress inducible NAC transcription factors that bind to a drought responsive cis-element in the early responsive to dehydration stress 1 promoter. - Plant Cell 16: 2481-2498, 2004.
Go to original source... - Umezawa, T., Yoshida, R., Maruyama, K., Yamaguchi-Shinozaki, K., Shinozaki, K.: SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. - Proc. natl. Acad. Sci. USA 101: 17306-17311, 2004.
Go to original source... - Wang. P., Ma, L., Y.L., Wang, S.: Transcriptome analysis reveals sunflower cytochrome P450 CYP93A1 responses to high salinity treatment at the seedling stage. - Genes Genomics 6: 581-591, 2017.
Go to original source... - Wu, H., Shabala, L., Liu, X., Azzarello, E., Zhou, M., Pandolfi, C., Bose, J., Chen, Z.H., Mancuso, S., Shabala S.: Linking salinity stress tolerance with tissue-specific Na+ sequestration in wheat roots. - Front. Plant Sci. 6: 71, 2015.
Go to original source... - Xie, T.T., Zhang, X.M., Liang, S.M., Shan, L.S., Yang, X.L., Hua, Y.H.: Effects of different irrigations on the water physiological characteristics of Haloxylon ammodendron in Taklimakan desert hinterland. - Ying Yong Sheng Tai Xue Bao 19: 711-716, 2008. [In Chin.]
- Yang, Y.F, Zhou, H.F, Xu, L.G.: Dynamic variations of soil moisture in Haloxylon ammodendron root zone in Gurbantunggut desert. - Ying Yong Sheng Tai Xue Bao 22: 1711-1716, 2011. [In Chin.]
- Ye, J., Fang, L., Zheng, H.K., Zhang, Y., Chen, J., Zhang, Z.J.: WEGO: a web tool for plotting GO annotations. - Nucl. Acids Res. 34: 293-297, 2006.
Go to original source... - You, Q., Zhang, L., Yi, X., Zhang, K., Yao, D., Zhang, X., Wang, Q., Zhao, X., Ling, Y., Xu, W., Li, F., Su, Z.: Co-expression network analyses identify functional modules associated with development and stress response in Gossypium arboretum. - Sci. Rep. 6: 1-15, 2016.
Go to original source... - Zhang, J., Feng, J.J., Lu, J., Yang, Y.Z., Zhang, X., Wan, D.S., Liu, J.Q.: Transcriptome differences between two sister desert poplar species under salt stress. - BMC Genomics 15: 337-350, 2014.
Go to original source...



