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Physiological Changes and Transcriptome Analysis of Malus zumi in Response to Salt Stress

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Abstract

Soil salinization has seriously affected plant growth and restricted economic development. Malus zumi is an excellent apple grafting rootstock, and it is also an important tree species to improve saline-alkali land. Under the stress of 200 mM NaCl, the yellowing of Malus zumi leaves became more obvious with time, the activities of antioxidant enzymes increased, and the chlorophyll content increased first and then decreased. Through transcriptome sequencing analysis, 426 new genes were found in a total of 37191 transcriptome sequences, and these new genes were still different from those of apple. After 48 hours of salt stress, compared with the untreated group, 4861 genes were differentially up-regulated and 4413 genes were differentially down-regulated. Through GO function enrichment analysis and pathway function enrichment analysis, it was found that salt stress affected the amino acid synthesis, metabolism, photosynthesis, and other related processes of Malus zumi. Analysis of differential transcription factors revealed that WRKY and ERF families were the important transcription factors involved in salt stress. The gene located at the key positions of metabolic pathway was verified by fluorescence quantitative PCR, and the results were consistent with the results of transcriptome sequencing, which proved the reliability of the data of differentially expressed genes.

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REFERENCES

  1. Chand, K., Sharon, N., and Poonam, S., Potential of plant growth-promoting rhizobacteria-plant interactions in mitigating salt stress for sustainable agriculture: A review, Pedosphere, 2022, vol. 32, p. 223. https://doi.org/10.1016/S1002-0160(21)60070-X

    Article  Google Scholar 

  2. Adhikari, B., Olorunwa, O.J., Wilson, J.C., and Barickman, T.C., Morphological and physiological response of different lettuce genotypes to salt stress, Stresses, 2021, vol. 1, p. 285. https://doi.org/10.3390/stresses1040021

    Article  Google Scholar 

  3. Machado, R.M.A., Serralheiro, R.P., Alvino, A., and Ferreira, A.I., Soil salinity: Effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization, Horticulturae, 2017, vol. 3, p. 30. https://doi.org/10.3390/horticulturae3020030

    Article  Google Scholar 

  4. Razzaq, A., Ali, A., Safdar, L.B., Zafar, M.M., Rui, Y., Shakeel, A., Shaukat, A., Ashraf, M., Gong, W., and Yuan, Y., Salt stress induces physiochemical alterations in rice grain composition and quality, J. Food Sci., 2020, vol. 85, p. 14. https://doi.org/10.1111/1750-3841.14983

    Article  CAS  PubMed  Google Scholar 

  5. Zelm, E., Zhang, Y., and Testerink, C., Salt tolerance mechanisms of plants, Annu. Rev. Plant Biol., 2020, vol. 71, p. 403. https://doi.org/10.1146/annurev-arplant-050718-100005

    Article  CAS  PubMed  Google Scholar 

  6. De Gara, L., Locato, V., Dipierro, S., and Maria, C., Redox homeostasis in plants. The challenge of living with endogenous oxygen production, Resp. Physiol. Neurobiol., 2010, vol. 173, p. S13. https://doi.org/10.1016/j.resp.2010.02.007

    Article  CAS  Google Scholar 

  7. Mahmoud, E.A., Maria, B., Ibrahim, A.A.M., Wang, Z., Ahmed, K., Ahmed, S., Hasan, A., Nauman, K.M., Mohamed, H.H., Ibrahim, M.E., Kuai, J., Zhou, G., and Wang, B., Antioxidative and metabolic contribution to salinity stress responses in two rapeseed cultivars during the early seedling stage, Antioxidants, 2021, vol. 10, p. 1227. https://doi.org/10.3390/ANTIOX10081227

    Article  Google Scholar 

  8. Guo, J.D., Huang, Z., Sun, J.L., Cui, X.M., and Liu, Y., Research progress and future development trends in medicinal plant transcriptomics, Front. Plant Sci., 2021, vol. 12, p. 691838. https://doi.org/10.3389/fpls.2021.691838

    Article  PubMed  PubMed Central  Google Scholar 

  9. Wang, X.J., Li, N., Li, W., Gao, X.L., Cha, M.H., Qin, L.J., and Liu, L.H., Advances in transcriptomics in the response to stress in plants, Glob. Med. Genet., 2020, vol. 7, p. 30. https://doi.org/10.1055/s-0040-1714414

    Article  PubMed  PubMed Central  Google Scholar 

  10. Maehly, A.C. and Chance, B., The assay of catalases and peroxidases, Methods of Biochemical Analysis, Glick, D., Ed., Interscience Publishers, 1954, vol. 1, p. 357. https://doi.org/10.1002/9780470110171.ch14

    Book  Google Scholar 

  11. Constantin, L., Iuliana, M., Feodor, F., Doina, J.C., Teliban, G.C., Simona, G.C., Ioan, P., and Teodor, R., The impact of salinity stress on antioxidant response and bioactive compounds of Nepeta cataria L, Agronomy, 2022, vol. 12, p. 562. https://doi.org/10.3390/AGRONOMY12030562

    Article  Google Scholar 

  12. Djajadi, D., Syaputra, R., and Hidayati, S.N., Effect of salt stress on nutrients content in soil and leaves of three varieties sugarcane, IOP Conf. Ser.: Earth Environ. Sci., 2022, vol. 974. https://doi.org/10.1088/1755-1315/974/1/012048

  13. Lei, M. S., Grafting performance of 7 kinds of apple dwarf rootstocks on Malus zumi, Forest Science and Technology, 2021, vol. 2, p. 53. https://doi.org/10.13456/j.cnki.lykt.2020.06.24.0002

    Article  Google Scholar 

  14. Raja, V., Majeed, U., Kang, H., Andrabi, K.I., and John, R., Abiotic stress: Interplay between ROS, hormones and MAPKs. Environ. Exp. Bot., 2017, vol. 137, p. 142. https://doi.org/10.1016/j.envexpbot.2017.02.010

    Article  CAS  Google Scholar 

  15. Wei, J.Y., Liu, D.B., Liu, Y.W., and Wei, S.X., Physiological analysis and transcriptome sequencing reveal the effects of salt stress on banana (Musa acuminata cv. BD) leaf, Front. Plant Sci., 2022, vol. 13, p. 822838. https://doi.org/10.3389/FPLS.2022.822838

    Article  PubMed  PubMed Central  Google Scholar 

  16. Sami, H., Kathy, S., Mabrouka, E., Lassaad, M., Insaf, B., and Van, L.M.C., Salt stress induced changes in photosynthesis and metabolic profiles of one tolerant (Bonica) and one sensitive (Black Beauty) eggplant cultivars (Solanum melongena L.), Plants, 2022, vol. 11, p. 590. https://doi.org/10.3390/PLANTS11050590

    Article  Google Scholar 

  17. Al-huraby, A.I. and Bafeel, S.O., The effect of salinity stress on the Phaseolus vulgaris L. plant, Afr. J. Bio. Sci, 2022, vol. 4, p. 94. https://doi.org/10.33472/afjbs.4.1.2022.94-107

    Article  CAS  Google Scholar 

  18. Mushtaq, Z., Faizan, S., Gulzar, B., Mushtaq, H., Bushra, S., Hussain, A., and Hakeem, K.R., Changes in growth, photosynthetic pigments, cell viability, lipid peroxidation and antioxidant defense system in two varieties of chickpea (Cicer arietinum L.) subjected to salinity stress, Phyton, 2022, vol. 91, p. 149. https://doi.org/10.32604/phyton.2022.016231

    Article  Google Scholar 

  19. Lee, C., Chung, C.T., Hong, W.J., Lee, Y.S., Lee, J.H., Koh, H.J., and Jung, K.H., Transcriptional changes in the develo** rice seeds under salt stress suggest targets for manipulating seed quality, Front. Plant Sci., 2021, vol. 12, p. 748273. https://doi.org/10.3389/fpls.2021.748273

  20. Zhang, X.X., Liu, P., Qing, C.Y., Yang, C., Shen, Y., and Ma, L.L., Comparative transcriptome analyses of maize seedling root responses to salt stress, PeerJ, 2021, vol. 9, p. e10765. https://doi.org/10.7717/peerj.10765

    Article  PubMed  PubMed Central  Google Scholar 

  21. Chen, L., Sun, H., Kong, J., Xu, H.J., and Yang, X.Y., Integrated transcriptome and proteome analysis reveals complex regulatory mechanism of cotton in response to salt stress, J. Cotton Res., 2021, vol. 4, p. 2. https://doi.org/10.1186/S42397-021-00085-5

    Article  Google Scholar 

  22. Wu, H., Li, H.Y., Zhang, W.H., Tang, H., and Yang, L., Transcriptional regulation and functional analysis of Nicotiana tabacum under salt and ABA stress, Biochem. Biophys. Res. Commun., 2021, vol. 570, p. 110. https://doi.org/10.1016/J.BBRC.2021.07.011

    Article  CAS  PubMed  Google Scholar 

  23. Wang, J.J., An, C., Guo, H.L., Yang, X.Y., Chen, J.B., Zong, J.Q., Li, J.J., and Liu, J.X., Physiological and transcriptomic analyses reveal the mechanisms underlying the salt tolerance of Zoysia japonica Steud, BMC Plant Biology, 2020, vol. 20, p. 114. https://doi.org/10.1186/s12870-020-02330-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wang, R., Wang, X., Liu, K., Zhang, X.J., Zhang, L.Y., and Fan, S.J., Comparative transcriptome analysis of halophyte Zoysia macrostachya in response to salinity stress, Plants, 2020, vol. 9, p. 458. https://doi.org/10.3390/plants9040458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Shu, J.B., Ma, X., Ma, H., Huang, Q.R., Zhang, Y., Guan, M., and Guan, C.Y., Transcriptomic, proteomic, metabolomic, and functional genomic approaches of Brassica napus L. during salt stress, PLoS One, 2022, vol. 17, p. e0262587. https://doi.org/10.1371/journal.pone.0262587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pan, J.W., Li, Z., Dai, S.J., Ding, H.F., Wang, Q.G., Li, X.B., Ding, G.H., Wang, P.F., Guan, Y.N., and Liu, W., Integrative analyses of transcriptomics and metabolomics upon seed germination of foxtail millet in response to salinity, Sci. Rep., 2020, vol. 10, p. 13660. https://doi.org/10.1038/s41598-020-70520-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chang, X.Y., Sun, J.L., Liu, L.L., Wang, H., and Zhao, B.L., Transcriptome analysis of differentially expressed genes in wild jujube seedlings under Salt Stress, J. Am. Soc. Hortic. Sci., 2020, vol. 145, p. 174. https://doi.org/10.21273/jashs04801-19

    Article  CAS  Google Scholar 

  28. Wang, Z.H., Wei, Y.Q., Zhao, Y.R., Wang, Y.J., Zou, F., Huang, S.Q., Yang, X.L., Xu, Z.W., and Hu, H., Physiological and transcriptional evaluation of sweet sorghum seedlings in response to single and combined drought and salinity stress, S. Afr. J. Bot., 2022, vol. 146, p. 459. https://doi.org/10.1016/J.SAJB.2021.11.029

    Article  CAS  Google Scholar 

  29. Feng, G.Y., **ao, P.Q., Wang, X., Huang, L.K., Nie, G., Li, Z., Peng, Y., Li, D.D., and Zhang, X.Q., Comprehensive transcriptome analysis uncovers distinct expression patterns associated with early salinity stress in annual ryegrass (Lolium Multiflorum L.), Int. J. Mol. Sci., 2022, vol. 23, p. 3279. https://doi.org/10.3390/IJMS23063279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lin, L.K., Yuan, K.L., Huang, Y.D., Dong, H.Z., Qiao, Q.H., **ng, C.H., Huang, X.S., and Zhang, S.L., A WRKY transcription factor PbWRKY40 from Pyrus betulaefolia functions positively in salt tolerance and modulating organic acid accumulation by regulating PbVHA-B1 expression, Environ. Exp. Bot., 2022, vol. 196:104782. https://doi.org/10.1016/j.envexpbot.2022.104782

    Article  CAS  Google Scholar 

  31. Yan, J.W., Li, J., Zhang, H.P., Liu, Y., and Zhang, A.M., ZmWRKY104 positively regulates salt tolerance by modulating ZmSOD4 expression in maize, The Crop Journal, 2022, vol. 10, p. 555. https://doi.org/10.1016/j.envexpbot.2022.104782

    Article  CAS  Google Scholar 

  32. Yu, Y., Yu, M., Zhang, S.X., Song, T.Q., Zhang, M.F., Zhou, H.W., Wang, Y.K., **ang, J.S., and Zhang, X.K., Transcriptomic identification of wheat AP2/ERF transcription factors and functional characterization of TaERF-6-3A in response to drought and salinity stresses, Int. J. Mol. Sci., 2022, vol. 23, p. 3272. https://doi.org/10.3390/ijms23063272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhu, L., Li, S.L., Ouyang, M.Z., Yang, L.M., Sun, S.R., Wang, Y.J., Cai, X.X., Wu, G.X., and Li, Y.M., Overexpression of watermelon ClWRKY20 in transgenic Arabidopsis improves salt and low-temperature tolerance, Sci. Hortic. (Amsterdam, Neth.), 2022, vol. 295. https://doi.org/10.1016/j.scienta.2021.110848

    Book  Google Scholar 

  34. Yue, J., Tang, M.Q., Zhang, H., Luo, D.J., Cao, S., Hu, Y.L., Huang, Z., Wu, Q.J., Wu, X., Pan, J., Chen, C.N., Wang, C.J., and Chen, P., The transcription factor HcERF4 confers salt and drought tolerance in kenaf (Hibiscus cannabinus L.), Plant Cell, Tissue Organ Cult., 2022, vol. 150, p. 207. https://doi.org/10.1007/s11240-022-02260-1

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

We thank Transcriptome Sequencing Technology (Guangzhou, China) for the preliminary profiling of the transcriptome.

Funding

This work was performed with financial support from the National Natural Science Foundation of China (nos. 61971312 and 31800572).

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Authors and Affiliations

  1. College of Horticulture and Landscape Architecture, Tian** Agricultural University, 300392, Tian**, China

    H. Y. Zhang, A. Li & B. B. Cao

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  1. H. Y. Zhang
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  2. A. Li
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Contributions

Ai Li designed the experiments. Hanyang Zhang and Beibei Cao collected samples and performed the experiments. Hanyang Zhang and Ai Li drafted the manuscript and all authors revised it.

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Correspondence to A. Li.

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Zhang, H.Y., Li, A. & Cao, B.B. Physiological Changes and Transcriptome Analysis of Malus zumi in Response to Salt Stress. Russ J Plant Physiol 69, 150 (2022). https://doi.org/10.1134/S1021443722601641

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