biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 64:465-472, 2020 | DOI: 10.32615/bp.2020.021

Transcriptome analysis deciphers the mechanisms of exogenous nitric oxide action on the response of melon leaves to chilling stress

Q. DIAO1, Y. CAO1, H. FAN2,*, Y. ZHANG1,*
1 Horticultural Research Institute and Shanghai Key Laboratory of Protected Horticultural Technology, Shanghai Academy of Agricultural Sciences, Shanghai 201403, P.R. China
2 Shanghai Agriculture Technology Extension and Service Center, Shanghai 201103, P.R. China

Chilling stress is a major abiotic factor that limits the growth and productivity of melon (Cucumis melo L.). The application of nitric oxide (NO) can enhance plant tolerance to chilling stress; however, the underlying molecular mechanisms for this process remain poorly understood. In this study, RNA sequencing was performed on melon seedlings exposed to control conditions, chilling stress, or chilling stress in the presence of NO donor sodium nitroprusside (SNP), to identify NO-mediated transcript changes in response to chilling stress. The results identified 488, 1 012, and 1 589 differentially expressed genes (DEGs) between plants in optimum conditions (CK) and chilling stress (CS) groups, plants in the CS and chilling stress + SNP (CN) groups, and those in CK and CN groups, respectively. Through gene ontology (GO) database and Kyoto encyclopedia of genes and genomes (KEGG) enrichment analyses, the DEGs were classified as predominantly involved in saccharide metabolism, biosynthesis of other secondary metabolites, lipid metabolism, amino-acid metabolism, and signal transduction pathways. In addition, 39 genes related to sugar metabolism including those encoding UDP-glucuronate-4-epimerase, β-glucosidase, glucuronosyltransferase, α-1,4-galacturonosyl transferase, and hexokinase, were upregulated in the CK vs. CS comparison, and genes encoding fructose-bisphosphate aldolase and glucan-endo-1,3-β-glucosidase were upregulated in the CS vs. CN, and CK vs. CN comparisons. A gene encoding an EREBP-like factor was upregulated in the CK vs. CS, CS vs. CN, and CK vs. CN comparisons. The expression profiles of 10 selected genes were analyzed using real-time quantitative PCR, and the candidate gene expression patterns were consistent with the DEG classification from RNA-seq. Overall, the data provide insight into the transcriptional regulation by exogenous NO in the response of melon seedlings to chilling stress. The data from this study are relevant for further research on the molecular mechanisms that underlie chilling resistance in melon plants.

Keywords: Cucumis melo, differentially expressed genes, RNA sequencing, sodium nitropruside, sugar metabolism.

Received: October 25, 2019; Revised: January 31, 2020; Accepted: February 5, 2020; Published online: June 26, 2020  Show citation

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DIAO, Q., CAO, Y., FAN, H., & ZHANG, Y. (2020). Transcriptome analysis deciphers the mechanisms of exogenous nitric oxide action on the response of melon leaves to chilling stress. Biologia plantarum64, Article 465-472. https://doi.org/10.32615/bp.2020.021
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References

  1. An, D., Yang, J., Zhang, P.: Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. - BMC Genomics 13: 64. 2012. Go to original source...
  2. Cantrel, C., Vazquez, T., Puyaubert, J., Rezé, N., Lesch, M., Kaiser, W.M., Baudouin, E.: Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. - New Phytol. 189: 415-427, 2011. Go to original source...
  3. Chen, K., Chen, L., Fan, J., Fu, J.: Alleviation of heat damage to photosystem II by nitric oxide in tall fescue. - Photosynth. Res. 116: 21-31, 2013. Go to original source...
  4. Chen, L.G., Song, Y., Li, S.J., Zhang, L.P., Zou, C.S., Yu, D.Q.: The role of WRKY transcription factors in plant abiotic stresses. - Biochim. biophys. Acta 1819: 120-128, 2012. Go to original source...
  5. Cock, P.J., Fields, C.J., Goto, N., Heuer, M.L., Rice, P.M.: The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants. - Nucl. Acids Res. 38: 1767-1771, 2009. Go to original source...
  6. Conesa, A., Götz, S., García-Gómez, J.M., Terol, J., Talón, M., Robles, M.: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. - Bioinformatics 21: 3674-3676, 2005. Go to original source...
  7. Davies, P.J.: The plant hormones: their nature, occurrence, and functions. - In: Davies, P.J. (ed.): Plant Hormones: Biosynthesis, Signal Transduction, Action. Pp. 1-15. Springer, Dordrecht - Ithaca - New York 2010. Go to original source...
  8. Du, Z., Zhou, X., Ling, Y., Zhang, Z., Su, Z.: agriGO: a GO analysis toolkit for the agricultural community. - Nucl. Acids Res. 38: W64-W70, 2010. Go to original source...
  9. Fan, H.F., Du, C.X., Guo, S.R.: Nitric oxide enhances salt tolerance in cucumber seedlings by regulating free polyamine content. - Environ. exp. Bot. 86: 52-59. 2013. Go to original source...
  10. Filippou, P., Antoniou, C., Fotopoulos, V.: The nitric oxide donor sodium nitro-prusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. - Free Radicals Biol. Med. 56: 172-183, 2013. Go to original source...
  11. Gan, S.: The hormonal regulation of senescence. - In: Davies, P.J. (ed.): Plant Hormones: Biosynthesis, Signal Transduction, Action. Pp. 597-617. Springer, Dordrecht - Ithaca - New York 2010. Go to original source...
  12. Garcia-Mas, J., Benjak, A., Sanseverino, W., Bourgeois, M., Mir, G., González, V. M., Alioto, T.: The genome of melon (Cucumis melo L.). - Proc. nat. Acad. Sci. USA 109: 11872-11877, 2012. Go to original source...
  13. Hagen, G., Guilfoyle, T.J.: Auxin-responsive gene expression: genes, promoters and regulatory factors. - Plant mol. Biol. 49: 373-385, 2002. Go to original source...
  14. Hoagland, D.R., Snyder, W.C.: Nutrition of strawberry plants under controlled conditions: (a) Effects of deficiencies of boron and certain other elements; (b) Susceptibility to injury from sodium salts. - Proc. amer. Soc. hort. Sci. 30: 288-294, 1933.
  15. Hu, X., Yang, J., Li, C.: Transcriptomic response to nitric oxide treatment in Larix olgensis Henry. - Int. J. mol. Sci. 16: 28582-28597, 2015. Go to original source...
  16. Keunen, E., Peshev, D., Vangronsveld, J., Ende,W., Cuypers, A.: Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. - Plant Cell Environ. 36: 1242-1255, 2013. Go to original source...
  17. Jian, W., Zhang, D.W., Zhu, F., Wang, S.X., Pu, X.J., Deng, X.G., Lin, H.H.: Alternative oxidase pathway is involved in the exogenous SNP-elevated tolerance of Medicago truncatula to salt stress. - J. Plant Physiol. 193: 79-87, 2016. Go to original source...
  18. Lindermayr, C., Saalbach, G., Durner, J.: Proteomic identification of S-nitrosylated proteins in Arabidopsis. - Plant Physiol. 137: 921-930, 2005. Go to original source...
  19. Li, S.W., Leng, Y., Shi, R.F.: Transcriptome characterization of gene profiling during early stage of nitric oxide-induced adventitious rooting in mung bean seedlings. - J. Plant Growth Regul. 39: 1-26, 2019. Go to original source...
  20. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔCT method. - Methods 25: 402-408, 2001. Go to original source...
  21. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., DePristo, M.A.: The genome analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. - Genome Res. 20: 1297-1303, 2010. Go to original source...
  22. O'Hara, L., Paul, M., Wingler, A.: How do sugars regulate plant growth and development? New insight in to the role of trehalose-6-phosphate. - Mol. Plants 6: 261-274, 2013. Go to original source...
  23. Rizwan, M., Mostofa, M.G., Ahmad, M.Z., Imtiaz, M., Mehmood, S., Adeel, M., Tu, S.: Nitric oxide induces rice tolerance to excessive nickel by regulating nickel uptake, reactive oxygen species detoxification and defense-related gene expression. - Chemosphere 191: 23-35, 2018. Go to original source...
  24. Rosa, M., Prado, C., Podazza, G., Interdonato, R., Gonzalez, J.A., Hilal, M., Prado, F.E.: Soluble sugars- metabolism, sensing and abiotic stress. - Plant Signal Behav. 4: 388-393, 2009. Go to original source...
  25. Ruan, Y.L.: Sucrose metabolism: gateway to diverse carbon use and sugar signaling. - Annu. Rev. Plant Biol. 65: 33-67, 2014. Go to original source...
  26. Sami, F., Yusuf, M., Faizan, M., Faraz, A., Hayat, S.: Role of sugars under abiotic stress. - Plant Physiol. Biochem. 109: 54-61, 2016. Go to original source...
  27. Seifert, G. J.: Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. - Curr. Opin. Plant Biol. 7: 277-284, 2004. Go to original source...
  28. Shi, H., Ye, T., Zhu, J. K., Chan, Z.: Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. - J. exp. Bot. 65: 4119-4131, 2014. Go to original source...
  29. Shi, H.T., Li, R.J., Cai, W., Liu, W., Fu, Z.W., Lu, Y.T.: In vivo role of nitric oxide in plant response to abiotic and biotic stress. - Plant Signal Behav. 7: 438-440, 2012. Go to original source...
  30. Shin, A.Y., Kim, Y.M., Koo, N., Lee, S.M., Nahm, S., Kwon, S.Y.: Transcriptome analysis of the oriental melon (Cucumis melo L. var. makuwa) during fruit development. - Peer J. 5: e2834, 2017. Go to original source...
  31. Siddiqui, M.H., Al-Whaibi, M.H., Basalah, M.O.: Role of nitric oxide in tolerance of plants to abiotic stress. - Protoplasma 248: 447-455, 2011. Go to original source...
  32. Sitnicka, D., Orzechowski, S.: Cold-induced starch degradation in potato leaves - intercultivar differences in the gene expression and activity of key enzymes. - Biol. Plant. 58: 659-666, 2014. Go to original source...
  33. Song, Y., Chen, Q., Ci, D., Zhang, D.: Transcriptome profiling reveals differential transcript abundance in response to chilling stress in populus simonii. - Plant Cell Rep. 32: 1407-1425, 2013. Go to original source...
  34. Sun, C., Liu, L., Yu, Y., Liu, W., Lu, L., Jin, C.: Nitric oxide alleviates aluminum induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. - J. integr. Plant Biol. 57: 550-561, 2015. Go to original source...
  35. Wang L.M., Zhang, L.D., Chen, J.B., Huang, D.F., Zhang, Y.D.: Physiological analysis and transcriptome comparison of two muskmelon (Cucumis melo L.) cultivars in response to salt stress. - Genet. mol. Res. 15: 1-18, 2016. Go to original source...
  36. Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., Wei, L.: KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. - Nucl. Acids Res. 39: W316-W322, 2011. Go to original source...
  37. Xu, J., Zhang, M., Liu, G., Yang, X., Hou, X.: Comparative transcriptome profiling of chilling stress responsiveness in grafted watermelon seedlings. - Plant Physiol. Biochem. 109: 561-570, 2016. Go to original source...
  38. Yano, R., Nonaka, S., Ezura, H.: Melonet, D.B.: a grand RNA-Seq gene expression atlas in melon (Cucumis melo L.). - Plant Cell Physiol. 59: e4-e4, 2017. Go to original source...
  39. Yue, C., Cao, H.L., Wang, L., Zhou, Y.H., Huang, Y.T., Hao, X.Y., Wang, X.C.: Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. - Plant mol. Biol. 88: 591-608, 2015. Go to original source...
  40. Zago, E., Morsa, S., Dat, J.F., Alard, P., Ferrarini, A., Inzé, D., Van Breusegem, F.: Nitric oxide-and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. - Plant Physiol. 141: 404-411, 2006. Go to original source...
  41. Zeng, F., Sun, F., Li, L., Liu, K., Zhan, Y.: Genome-scale transcriptome analysis in response to nitric oxide in birch cells: implications of the triterpene biosynthetic pathway. - PloS ONE 9: 116-157, 2014. Go to original source...
  42. Zhang, H., Wang, H., Yi, H., Zhai, W., Wang, G., Fu, Q.: Transcriptome profiling of Cucumis melo fruit development and ripening. - Hort. Res. 3: 16014, 2016. Go to original source...
  43. Zhang, T., Zhao, X., Wang, W., Pan, Y., Huang, L., Liu, X., Fu, B.: Comparative transcriptome profiling of chilling stress responsiveness in two contrasting rice genotypes. - PloS ONE 7: e43274, 2012. Go to original source...
  44. Zhao, R., Sheng, J., Shengnan, L.V., Zheng, Y.: Nitric oxide participates in the regulation of LeCBF1 gene expression and improves cold tolerance in harvested tomato fruit. - Postharvest Biol. Technol. 62: 121-126, 2011. Go to original source...
  45. Zhu, J.H., Dong, C.H., Zhu, J.K.: Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. - Curr. Opin. Plant Biol. 10: 290-295, 2007. Go to original source...