Vol. 64 No. 2 (2025)
Articles

Cellulose synthase gene expression profile and physiological responses of tomato cultivars exposed to virus and salt stresses

Samra MİRZAYEVA
Institute of Molecular Biology & Biotechnologies, Ministry of Science and Education of Azerbaijan Republic, Baku, Azerbaijan
Irada HUSEYNOVA
Institute of Molecular Biology & Biotechnologies, Ministry of Science and Education of Azerbaijan Republic, Baku, Azerbaijan
İbraim Özer ELİBÜYÜK
Faculty of Agriculture, Department of Plant protection, Ankara University, Ankara, Türkiye
Canan YÜKSEL ÖZMEN
Biotechnology Institute, Ankara University, Ankara, Türkiye
Ali ERGÜL
Biotechnology Institute, Ankara University, Ankara, Türkiye

Published 2025-09-12

Keywords

  • Solanum lycopersicum L.,
  • tomato yellow leaf curl virus,
  • tomato chlorosis virus,
  • cellulose synthase genes,
  • qRT-PCR

How to Cite

[1]
MİRZAYEVA S., I. HUSEYNOVA, İbraim Özer ELİBÜYÜK, C. YÜKSEL ÖZMEN, and ERGÜL A., “Cellulose synthase gene expression profile and physiological responses of tomato cultivars exposed to virus and salt stresses”, Phytopathol. Mediterr., vol. 64, no. 2, pp. 229–244, Sep. 2025.

Funding data

Abstract

Plants are exposed to adverse growth conditions, and have developed mechanisms to adapt and survive under abiotic and biotic stresses. The plant’s response to the combined effects of biotic and abiotic stress represents a highly complex phenomenon, involving intricate interactions between the host plant and associated pathogens, further modulated by the intensity, duration, and type of environmental stressors. Tomato production can be severely affected by tomato yellow leaf curl virus (TYLCV) and tomato chlorosis virus (ToCV), and salt stress inhibits tomato crop productivity, although molecular regulation controlling tomato resistance to salt stress remains unclear. The cellulose synthase (Ces) and cellulose synthase-like (Csl) gene families control biosynthesis of cellulose and hemicellulose in plant cell walls, and Ces/Csl genes are also involved in resistance against abiotic and biotic stresses, including those from viruses and salt. To gain understanding of the molecular basis of combined viruses (TYLCV/ToCV) and salt stresses on the tomato cultivars Money Maker and Yegana, comparative analyses of four cellulose synthase genes (CesA/Csl) were carried out using Quantitative Reverse Transcription Polymerase Chain Reaction (RT -qPCR). Tomato physiological parameters, including relative water content, specific leaf weight, leaf area, and dry biomass, were also assessed. CesA/Csl genes (Ces-A2, Csl-D3,2, Csl-D3,1, Csl-H1) were up-regulated in virus-infected plants. These genes, associated with the biosynthesis of CesA/Csl genes are probably pivotal in defense mechanisms against TYLCV/ToCV. Relative water content in plants subjected to combined ToCV and salt stresses were similar to those observed in non-inoculated controls. Congruence between the outcomes of these analyses and physiological studies indicates that the Yegana tomato cultivar may be as sensitive to these stresses as the Money Maker cultivar. This research emphasizes the importance of up-regulating specific genes, namely Csl-D3,1, Csl-D3,2, and Ces-A2, to confer host resistance to the complex effects of salt and virus stresses. This study will facilitate development of stress-resistant tomato plants, and contribute to elucidating the molecular mechanisms of CesA/Csl genes in abiotic and biotic stress situations.

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References

  1. Abd El Rahman H., Nasr-Eldin M. A., Abo-Elmaaty S. A., Abdelwahed M. A., ElHefnawi M., El Fiky A. M., Soliman, E. R., 2024. Partial Genome Detection, Characterization of TYLCV (MZ546492) Infecting tomato plants and sirna sequences detection for alternative control strategy. Egyptian Journal of Botany 64(1): 211–223. https://doi.org/10.21608/ejbo.2023.208980.2321 DOI: https://doi.org/10.21608/ejbo.2023.208980.2321
  2. Aboul-Maaty N., Oraby H., 2019. Extraction of high-quality genomic DNA from different plant orders applying a modified CTAB-based method. Bulletin of the National Research Centre 43(1): 25–35. https://doi.org/10.1186/s42269-019-0066-1 DOI: https://doi.org/10.1186/s42269-019-0066-1
  3. Alam M.S., Tester M., Fiene G., Mousa M.A., 2021. Early growth stage characterization and the biochemical responses for salinity stress in tomato. Plants 10(4): 712. https://doi.org/10.3390/plants10040712 DOI: https://doi.org/10.3390/plants10040712
  4. Bacha H., Tekaya M., Drine S., Guasmi F., Touil L., Enneb H., Triki T., Cheour F., … Ferchichi A., 2017. Impact of salt stress on morpho-physiological and biochemical parameters of Solanum lycopersicum cv. Microtom leaves. South African Journal of Botany 108(1): 364–369. https://doi.org/10.1016/j.sajb.2016.08.018 DOI: https://doi.org/10.1016/j.sajb.2016.08.018
  5. Botto C.S., Mati S., Moine A., Chitarra W., Nerva L., D’Errico C., Pagliarani C., … Noris Emanuela., 2023. Tomato yellow leaf curl sardinia virus ıncreases drought tolerance of tomato. International Journal Molecular Sciences 24(3): 2893–2909. https://doi.org/10.3390/ijms24032893. DOI: https://doi.org/10.3390/ijms24032893
  6. Brown R., Wyatt H., Price J., Kelly F., 1996. Pulmonary dysfunction in cystic fibrosis is associated with oxidative stress. European Respiratory Journal 9(5): 334–339. https://10.1183/09031936.96.09020334 DOI: https://doi.org/10.1183/09031936.96.09020334
  7. Cao S., Cheng H., Zhang J., Aslam M., Yan M., … Qin Y., 2019. Genome-wide ıdentification, expression pattern analysis and evolution of the Ces/Csl gene superfamily in pineapple (Ananas comosus). Plants 8(11): 275. https://doi.org/10.3390/plants8080275 DOI: https://doi.org/10.3390/plants8080275
  8. Chantreau M., Chabbert B., Billiard S., Hawkins S., Neutelings G., 2015. Functional analyses of cellulose synthase genes in flax (Linum usitatissimum) by virus‐induced gene silencing. Plant Biotechnology Journal 13(9): 1312–1324. https://doi.org/10.1111/pbi.12350. DOI: https://doi.org/10.1111/pbi.12350
  9. Chen T., Lv Y., Zhao T., Li N., Yang Y., … Zhang B., 2013. Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PloS One 8(11): e80816. https:// doi.org/10.1371/journal.pone.0080816 DOI: https://doi.org/10.1371/journal.pone.0080816
  10. Chinnaraja C., Ramkissoon A., Ramsubhag A., Jayaraj J., 2016. First report of Tomato yellow leaf curl virus infecting tomatoes in Trinidad. Plant Diseases 100(4): 1958. https://doi.org/10.1094/PDIS-04-16-0446-PDN DOI: https://doi.org/10.1094/PDIS-04-16-0446-PDN
  11. Choe S., Choi B., Kang J.H., Seo J.K., 2021. Tolerance to tomato yellow leaf curl virus in transgenic tomato overexpressing a cellulose synthase-like gene. Plant Biotechnology Journal 19(4): 657–659. https://doi.org/10.1111/pbi.13539 DOI: https://doi.org/10.1111/pbi.13539
  12. Çevik B., Kıvrak H., Şahin-Çevik M., 2019. Development of a graft inoculation method and a real-time RT-PCR assay for monitoring Tomato chlorosis virus infection in tomato. Journal of Virological Methods 265(5): 1–8. https://doi.org/10.1016/j.jviromet.2018.12.004 DOI: https://doi.org/10.1016/j.jviromet.2018.12.004
  13. Dabravolski S.A., and Isayenkov S.V., 2023. The regulation of plant cell wall organisation under salt stress. Frontiers in Plant Science 14(1): 1118313. https://doi.org/10.3389/fpls.2023.1118313 DOI: https://doi.org/10.3389/fpls.2023.1118313
  14. Desbiez C., Verdin E., Moury B., Lecoq H., Millot P., … Huseynova I., 2018. Prevalence and molecular diversity of the main viruses infecting Cucurbit and Solanaceous crops in Azerbaijan. European Journal of Plant Pathology 153(2): 1–11. https://link.springer.com/article/10.1007%2Fs10658-018-1562-0
  15. Devkar V., Thirumalaikumar V. P., Xue G.-P., Vallarino J. G., Turečková V., … Balazadeh S.,2020. Multifaceted regulatory function of tomato SlTAF1 in the response to salinity stress. New Phytology 225(4): 1681–1698. https://doi.org/10.1111/nph.16247 DOI: https://doi.org/10.1111/nph.16247
  16. Diouf I.A., Derivot L., Bitton F., Pascual L., Causse M., 2018. Water deficit and salinity stress reveal many specific qtl for plant growth and fruit quality traits in tomato. Environmental and Experimental Botany 9(6): 279. https://doi.org/10.3389/fpls.2018.00279 DOI: https://doi.org/10.3389/fpls.2018.00279
  17. Dovas C., Katis N., Avgelis A., 2002 Multiplex detection of criniviruses associated with epidemics of a yellowing disease of tomato in Greece. Plant Disease 86(12): 1345–1349. https://doi.org/10.1094/PDIS.2002.86.12.1345 DOI: https://doi.org/10.1094/PDIS.2002.86.12.1345
  18. Elsharkawy M.M., El-Okkiah S., Elsadany A.Y., Bedier M.Y., Omara R.I., …Abdelkhalek A., 2022. Systemic resistance induction of tomato plants against tomato mosaic virus by microalgae. Egyptian Journal of Biological Pest Control 32(1): 1–7. https://doi.org/10.1186/s41938-022-00538-2 DOI: https://doi.org/10.1186/s41938-022-00538-2
  19. Endler A., Kesten C., Schneider R., Zhang Y., Ivakov A., … Persson S., 2014. Alfalfa cellulose synthase gene expression under abiotic stress: a hitchhiker’s guide to RT-qPCR Normalization. PLoS One 162(6): 1353–1364. https://doi.org/10.1371/journal.pone.0103808
  20. Endler A., Kesten C., Schneider R., Zhang Y., Ivakov A., … Persson S., 2015. A mechanism for sustained cellulose synthesis during salt stress. Cell 162(6): 1353–1364. https://doi.org/10.1371/journal.pone.0103808 DOI: https://doi.org/10.1016/j.cell.2015.08.028
  21. FAO 2011. The state of the world’s land and water resources for Food and Agriculture (SOLAW)—managing systems at risk. Abingdon: Food and Agriculture Organization of the United Nations and Earthscan.
  22. FAOSTAT 2022. Crops and livestock products. Available at: https://www.fao.org/faostat/en/#data/QCL.
  23. Fiallo‐Olivé E., Navas‐Castillo J., 2019. Tomato chlorosis virus, an emergent plant virus still expanding its geographical and host ranges. Molecular Plant Pathology 20(9): 1307–1320. https://doi.org/10.1111/mpp.12847 DOI: https://doi.org/10.1111/mpp.12847
  24. Fidan H., Sarıkaya P., 2020. Virus diseases in eggplant (Solanum melongena) cultivation in Antalya province. Mediterranean Agricultural Sciences 33(1): 27–35. https://doi.org/10.29136/mediterranean.642226 (in Turkish) DOI: https://doi.org/10.29136/mediterranean.642226
  25. Gao W., Wang Z., Dong C., Wei K., Chen Y., Qiu Z., Wang., X., 2024. Screening resistant germplasms and quantitative trait locus mapping of resistance to Tomato chlorosis virus. International Journal of Molecular Sciences 26(5): 2060. https://doi.org/10.21203/rs.3.rs-4235788/v1 DOI: https://doi.org/10.3390/ijms26052060
  26. Gharsallah C., Fakhfakh H., Grubb D., Gorsane. F., 2016. Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants 8(1): plw055. https://doi.org/10.1093/aobpla/plw055 DOI: https://doi.org/10.1093/aobpla/plw055
  27. Gharsallah C., Gharsallah S., Werghi S., Mehrez M., Fakhfakh H., Gorsane F., 2020. Tomato contrasting cultivars responses under combined salinity and viral stresses. Physiology and Molecular Biology of Plants 26(7): 1411–1424. https://doi.org/10.1007/s12298-020-00835-w. DOI: https://doi.org/10.1007/s12298-020-00835-w
  28. Grünzweig J., Katan J., Ben-Tal Y., Rabinowitch H., 1999. The role of mineral nutrients in the increased growth response of tomato plants in solarized soil. Plant and Soil 206(1): 21–27. https://doi.org/10.1023/A:1004321118896 DOI: https://doi.org/10.1023/A:1004321118896
  29. Guo M., Wang X.-S., Guo H.-D., Bai S.-Y., Khan A., … Li J.-S., 2022. Tomato salt tolerance mechanisms and their potential applications for fighting salinity: A review. Frontiers in Plant Science 13(1): 949541. https://doi.org/10.3389/fpls.2022.949541 DOI: https://doi.org/10.3389/fpls.2022.949541
  30. Hoagland D.R., Arnon D.I., 1950. The water culture method for growing plants without soil. California Agricultural Experimental Station Circular, University of California, Berkeley 347(2): 1–32. https://doi.org/10.1371/journal.pone.0103808 DOI: https://doi.org/10.1371/journal.pone.0103808
  31. Hosseini S., Reza Z., Mostafa Y., Khayyat M., 2018. Effects of Cucumber Mosaic Virus infection and drought tolerance of tomato plants under greenhouse conditions: Preliminary results. Journal of Berry Research 8(3): 1–8. https://doi.org/10.3233/JBR-170285 DOI: https://doi.org/10.3233/JBR-170285
  32. Hu H., Zhang R., Feng S., Wang Y., Wang Y., … Peng L., 2018. Three AtCesA6-like members enhance biomass production by distinctively promoting cell growth in Arabidopsis. Plant Biotechnology Journal 16(5): 976–988. https://doi.org/10.1111/pbi.12842 DOI: https://doi.org/10.1111/pbi.12842
  33. Huang H., Zhao S., Chen J., Li T., Guo G., Xu M., Liao X. 2022. Genome-wide identification and functional analysis of Cellulose synthase gene superfamily in Fragaria vesca. Frontiers in Plant Science 13(1): 1044029. DOI: https://doi.org/10.3389/fpls.2022.1044029
  34. Huang Y., Ma H.-Y., Huang W., Wang F., Xu Z-S., Xiong A.-S., 2016. Comparative proteomic analysis provides novel insight into the interaction between resistant vs susceptible tomato cultivars and TYLCV infection. BMC Plant Biology 16(1): 162. https://doi.org/10.1186/S12870-016-0819-Z DOI: https://doi.org/10.1186/s12870-016-0819-z
  35. Ibrahim A.M., 2018. Salt tolerance of some tomato (Solanum lycoversicum L.) cultivars for salinity under controlled conditions. American Journal of Plant Physiology 13(2): 58–64. https://doi.org/10.3923/ajpp.2018.58.64 DOI: https://doi.org/10.3923/ajpp.2018.58.64
  36. Jin F.M., Song J., Xue J., Sun H.B., Zhang Y., Wang S., Wang Y.H., 2020. Successful generation of anti-ToCV and TYLCV transgenic tomato plants by RNAi. Biology of Plant 64(1): 490–496. https://doi.org/10.32615/bp.2020.069 DOI: https://doi.org/10.32615/bp.2020.069
  37. Jones R. A., Naidu R. A., 2019. Global dimensions of plant virus diseases: current status and future perspectives. Annual Review of Virology 6(1): 387–409. https://doi.org/10.1146/annurev-virology-092818-015606 DOI: https://doi.org/10.1146/annurev-virology-092818-015606
  38. Kesten C., Menna A., Sanchez-Rodrıguez C., 2017. Regulation of cellulose synthesis in response to stress. Current Opinion in Plant Biology 40(3): 106–113. https:// doi.org/10.1016/j.pbi.2017.08.010 DOI: https://doi.org/10.1016/j.pbi.2017.08.010
  39. Klay I., Pirrello J., Riahi L., Bernadac A., Cherif A., Bouzayen M., Bouzid S., 2014. Ethylene response factor Sl-ERF.B.3 ıs responsive to abiotic stresses and mediates salt and cold stress response regulation in tomato. Scientific World Journal 1(1): 12. https://doi.org/10.1155/2014/167681 DOI: https://doi.org/10.1155/2014/167681
  40. Kusvuran S., Kiran S., Ellialtioglu S. S., 2016. Antioxidant enzyme activities and abiotic stress tolerance relationship in vege crops. In: Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives. (A. K. Shanker, C. Shanker, ed.). InTech 8(12): 481–506. https://doi.org/10.5772/62235 DOI: https://doi.org/10.5772/62235
  41. Kwon S. J., Lee Y. J., Cho Y. E., Byun H. S., Seo J. K., 2024. Engineering of stable infectious cDNA constructs of a fluorescently tagged tomato chlorosis virus. Virology 16(1): 125. https://doi.org/10.1038/ijir.2012.45 DOI: https://doi.org/10.1016/j.virol.2024.110010
  42. Le Gall., Philippe F., Domon J., Gillet F., Pelloux J., Rayon C., 2015. Cell wall metabolism in response to abiotic stress. Plants 4(1): 112–166. https://doi.org/10.3390/plants4010112 DOI: https://doi.org/10.3390/plants4010112
  43. Lee H., Kim M., Choi H., Kang J., Ju H., Seo J., 2017. Efficient transmission and propagation of tomato chlorosis virus by simple single-leaflet grafting. Plant Pathology Journal 33(3): 345–349. https://doi.org/10.5423/PPJ.NT.02.2017.0039 DOI: https://doi.org/10.5423/PPJ.NT.02.2017.0039
  44. Li N., Wu X., Zhuang W., Xia L., Chen Y., Wu C., et al., 2021. Tomato and lycopene and multiple health outcomes: Umbrella review. Food Chemistry 343(3): 128396. https://doi.org/10.1016/j.foodchem.2020.128396 DOI: https://doi.org/10.1016/j.foodchem.2020.128396
  45. Li T., Huang Y., Xu Z.S., Wang F., Xiong A.S., 2019. Salicylic acid-induced differential resistance to the tomato yellow leaf curl virus among resistant and susceptible tomato cultivars. BMC Plant Biology 19(1): 173. https://doi.org/10.1186/s12870-019-1784-0 DOI: https://doi.org/10.1186/s12870-019-1784-0
  46. Livak K., Schmittgen T., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4): 402–408. https://doi.org/10.1006/meth.2001.1262 DOI: https://doi.org/10.1006/meth.2001.1262
  47. Louro D., Accotto G., Vaira A., 2000. Occurrence and diagnosis of tomato chlorosis virus in portugal. European Journal of Plant Pathology 106(6): 589–592. https://doi.org/10.1023/A:1008738130592 DOI: https://doi.org/10.1023/A:1008738130592
  48. Maach M., Baghour M., Akodad M., Gálvez F.J., Sánchez M.E., … Rodríguez-Rosales M.P., 2020. Overexpression of LeNHX4 improved yield, fruit quality and salt tolerance in tomato plants (Solanum lycopersicum L.). Molecular Biology Reports 47(4): 4145–4153. https://doi.org/10.1007/s11033-020-05499-z DOI: https://doi.org/10.1007/s11033-020-05499-z
  49. Maach M., Rodríguez-Rosales M., Venema K., Akodad M., Moumen A., Skalli A., Baghour M., 2021. Improved yield, fruit quality, and salt resistance in tomato co-overexpressing LeNHX2 and SlSOS2 genes. Physiology and Molecular Biology of Plants 27(4): 703–712. https://doi.org/10.1007/s12298-021-00974-8 DOI: https://doi.org/10.1007/s12298-021-00974-8
  50. Maksup S., Sengsai S., Laosuntisuk K., Asayot J., Pongprayoon W., 2020. Physiological responses and the expression of cellulose and lignin associated genes in Napier grass hybrids exposed to salt stress. Acta Physiologiae Plantarum 42(7): 1–12. https://doi.org/10.1007/s11738-020-03092-2 DOI: https://doi.org/10.1007/s11738-020-03092-2
  51. Malinovsky F., Fangel J., Willats W., 2014. The role of the cell wall in plant immunity. Frontiers in Plant Science 5(6): 178–190. https://doi.org/10.3389/fpls.2014.00178 DOI: https://doi.org/10.3389/fpls.2014.00178
  52. Martínez-Culebras P., Font I., Jordá C., 2001. A rapid PCR method to discriminate between tomato yellow leaf curl virus isolates. Annals of Applied Biology 139(2): 251–257. https://doi.org/10.1111/j.1744-7348.2001.tb00401.x DOI: https://doi.org/10.1111/j.1744-7348.2001.tb00401.x
  53. Metwally R., Shereen S., 2023. Alleviation of the adverse effects of NaCl stress on tomato seedlings (Solanum lycopersicum L.) by Trichoderma viride through the antioxidative defense system. Botanical Studies 64(4): 1–18. https://doi.org/10.1186/s40529-023-00368-x DOI: https://doi.org/10.1186/s40529-023-00368-x
  54. Milc J., Bagnaresi P., Aragona M., Valente M.T., Biselli C., … Pecchioni N., 2019. Comparative transcriptome profiling of the response to Pyrenochaeta lycopersici in resistant tomato cultivar Mogeor and its background cultivar-susceptible Moneymaker. Functional & Integrative Genomics 19(5): 811–826. https://doi.org/10.1007/s10142-019-00685-0 DOI: https://doi.org/10.1007/s10142-019-00685-0
  55. Mirzayeva S., Huseynova I., Özmen C.Y., Ergül A., 2023. Physiology and gene expression analysis of tomato (Solanum lycopersicum L.) exposed to combined-virus and drought stresses. Plant Pathology Journal 39(5): 466–485. https://doi.org/10.5423/PPJ.OA.07.2023.0103 DOI: https://doi.org/10.5423/PPJ.OA.07.2023.0103
  56. Moriones E., Navas-Castillo J., 2000. Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Research 71(2): 2123–2134. https://doi.org/10.1016/S0168-1702(00)00193-3 DOI: https://doi.org/10.1016/S0168-1702(00)00193-3
  57. Mugiira R.B., Arama P.F., Macharia J.M., Gichimu B.M., 2011. Antibacterial activity of foliar fertilizer formulations and their effect on ice nucleation activity of Pseudomonas syringae pv garcae Van Hall; the causal agent of Bacterial Blight of Coffee. International Journal of Agricultural Research 6(7): 550–561. https://doi.org/10.3923/ijar.2011.550.561 DOI: https://doi.org/10.3923/ijar.2011.550.561
  58. Nahar K., Hasanuzzaman M., Alam M., Rahman A., Suzuki T., Fujita M., 2016. Polyamine and nitric oxide crosstalk: Antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology and Environmental Safety 126(1): 245–255. https://doi.org/10.1016/j.ecoenv.2015.12.026 DOI: https://doi.org/10.1016/j.ecoenv.2015.12.026
  59. Ong S.N., Taheri S., Othman R.Y., Teo C.H., 2020. Viral disease of tomato crops (Solanum lycopesicum L.): an overview. Journal of Plant Diseases and Protection 127(10): 725–739. https://doi.org/10.1007/s41348-020-00330-0 DOI: https://doi.org/10.1007/s41348-020-00330-0
  60. Parvin K., Hasanuzzaman M., Bhuyan M., Nahar K., Mohsin S.M., Fujita M., 2019. Comparative physiological and biochemical changes in tomato (Solanum lycopersicum L.) under salt stress and recovery: Role of antioxidant defense and glyoxalase systems. Antioxidants 8(9): 350. https://doi.org/10.3390/antiox8090350 DOI: https://doi.org/10.3390/antiox8090350
  61. Parvin K., Nahar K., Hasanuzzaman M., Bhuyan M.B., Mohsin S.M., Fujita M., 2020. Exogenous vanillic acid enhances salt tolerance of tomato: Insight into plant antioxidant defense and glyoxalase systems. Plant Physiology and Biochemistry 150(1): 109–120. https://doi.org/10.1016/j.plaphy.2020.02.030 DOI: https://doi.org/10.1016/j.plaphy.2020.02.030
  62. Patanè C., Cosentino S., Romano D., Toscano S., 2022. Relative water content, proline, and antioxidant enzymes in leaves of long shelf-life tomatoes under drought stress and rewatering. Plants 11(22): 3045–3046. https://doi.org/10.3390/plants11223045 DOI: https://doi.org/10.3390/plants11223045
  63. Peng X., Pang H., Abbas M., Yan X., Dai X., Li Y., Li Q., 2019. Characterization of Cellulose synthase-like D (CSLD) family revealed the involvement of PtrCslD5 in root hair formation in Populus trichocarpa. Scientific Reports 9(1): 1452. https://doi.org/10.1038/s41598-018-36529-3 DOI: https://doi.org/10.1038/s41598-018-36529-3
  64. Raziq A., Wang Y., Mohi Ud Din A., Sun J., Shu S., Guo S., 2022. A comprehensive evaluation of salt tolerance in tomato (Var. Ailsa Craig): responses of physiological and transcriptional changes in RBOH’s and ABA biosynthesis and signalling genes. International Journal of Molecular Science 23(3): 1603. https://doi.org/10.3390/ijms23031603. DOI: https://doi.org/10.3390/ijms23031603
  65. Renau-Morata B., Molina R.V., Carrillo L.J., Cebolla-Cornejo J., Sánchez-Perales M.,… Nebauer S.G., 2017. Ectopic expression of CDF3 genes in tomato enhances biomass production and yield under salinity stress conditions. Frontiers in Plant Science 3(13): 660–678. https://doi.org/10.3389/fpls.2017.00660 DOI: https://doi.org/10.3389/fpls.2017.00660
  66. Roșca M., Mihalache G., Stoleru V., 2023. Tomato responses to salinity stress: From morphological traits to genetic changes. Frontiers in Plant Science 14(1): 1118383. https://doi.org/10.3389/fpls.2023.1118383 DOI: https://doi.org/10.3389/fpls.2023.1118383
  67. Sandy C.J., Gosling S.D., Koelkebeck T., 2014. Psychometric com-parison of automated versus rational methods of scale abbreviation: Anillustration using a brief measure of values. Journal of Individual Differences 35(4): 221–235. https://doi.org/10.1027/1614-0001/a000144 DOI: https://doi.org/10.1027/1614-0001/a000144
  68. Savy D., Cozzolino V., Vinci G., Verrillo M., Aliberti A., … Piccolo A., 2022. Fertilisation with compost mitigates salt stress in tomato by affecting plant metabolomics and nutritional profiles. Chemical and Biological Technologies in Agriculture 9(1): 12–30. https://doi.org/10.1186/s40538-022-00373-5 DOI: https://doi.org/10.1186/s40538-022-00373-5
  69. Seo J.K., Kim M.K., Kwak H.R., Choi H.S., Nam M., … C. Jung, 2018. Molecular dissection of distinct symptoms induced by tomato chlorosis virus and tomato yellow leaf curl virus based on comparative transcriptome analysis. Virology 516(1): 1–20. https://doi.org/10.1186/s40538-022-00373-5 DOI: https://doi.org/10.1016/j.virol.2018.01.001
  70. Shafi A., Gill T., Zahoor I., Ahuja P.S., Sreenivasulu Y., Kumar S., Singh A.K., 2019. Ectopic expression of SOD and APX genes in Arabidopsis alters metabolic pools and genes related to secondary cell wall cellulose biosynthesis and improve salt tolerance. Molecular Biology Reports 46(2): 1985–2002. https://doi.org/10.1007/s11033-019-04648-3 DOI: https://doi.org/10.1007/s11033-019-04648-3
  71. Sharif R., Liu P., Wang D., Jin Z., Uzair U., Yadav V., Li Y., 2021. Genome-wide characterisation and expression analysis of cellulose synthase genes superfamily under various environmental stresses in Cucumis sativus L. New Zealand Journal of Crop and Horticultural Science 49(3): 127–150. https://doi.org/10.1080/01140671.2021.1926291 DOI: https://doi.org/10.1080/01140671.2021.1926291
  72. Song X., Xu L., Yu J., Tian P., Hu X., Wang Q., Pan Y., 2019. Genome-wide characterization of the cellulose synthase gene superfamily in Solanum lycopersicum. Gene 688(10): 71–83. https://doi.org/10.1016/j.gene.2018.11.039 DOI: https://doi.org/10.1016/j.gene.2018.11.039
  73. Tabein S., 2021. Evaluation of two nontransformative approaches in triggering RNAi against tomato yellow leaf curl virus. Plant Protection (Scientific Journal of Agriculture) 44(4): 77–88. https://doi.org/10.22055/ppr.2021.17177
  74. Tambussi E., Nogués S., Araus J., 2005. Ear of durum wheat under water stress: water relations and photosynthetic metabolisms. Planta 221(3): 446–458. https://doi.org/10.1007/s00425-004-1455-7 DOI: https://doi.org/10.1007/s00425-004-1455-7
  75. Tanveer M., Shahzad B., Sharma A., Khan E.A., 2019. 24-Epibrassinolide application in plants: An implication for improving drought stress tolerance in plants. Plant Physiology and Biochemistry 135(2): 295–303. https://doi.org/10.1016/j.plaphy.2018.12.013. DOI: https://doi.org/10.1016/j.plaphy.2018.12.013
  76. Terada N., Sanada A., Koshio K., Habibi N., Sediquim N., 2021. Effects of salinity on growth, physiological and biochemical responses of tomato. Journal of the International Society for Southeast Asian Agricultural Sciences 27(2): 14–28. https://doi.org/10.1007/s10811-018-1619-7 DOI: https://doi.org/10.1007/s10811-018-1619-7
  77. Tiwari S., Lata C., Chauhan P., Nautiyal C., 2016. Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiology and Biochemistry 99(1): 108–117. https://doi.org/10.1016/j.plaphy.2015.11.001 DOI: https://doi.org/10.1016/j.plaphy.2015.11.001
  78. Ueda A., Yamamoto-Yamane Y., Takabe T., 2007. Salt stress enhances proline utilization in the apical region of barley roots. Biochemical and Biophysical Research Communications 355(1): 61–66. https:// doi.org/10.1016/j.bbrc.2007.01.098 DOI: https://doi.org/10.1016/j.bbrc.2007.01.098
  79. Verdin E., Desbiez C., Wipf-Scheibel C., Gognalons P., Kheyr-Pour A… Huseynova I., 2018. First report of tomato yellow leaf curl virus infecting tomato in Azerbaijan. Journal of Plant Pathology 100(2): 335. https://doi.org/10.1007/s42161-018-0050-x DOI: https://doi.org/10.1007/s42161-018-0050-x
  80. Wang W., Cai L., Long Z., Zhang X., Zhao F., 2021. Effects of non-uniform salt stress on growth, yield, and quality of tomato. Journal of the International Society for Southeast Asian Agricultural Sciences 27(5): 545–556. https://doi.org/10.1080/00380768.2021.1966834 DOI: https://doi.org/10.1080/00380768.2021.1966834
  81. Wang J., Li J., Lin W., Deng B., Lin L., … Ma X., 2022. Genome-wide identification and adaptive evolution of CesA/Csl superfamily among species with different life forms in Orchidaceae. Frontiers in Plant Science 13(1): 994679. https://doi.org/10.3389/fpls.2022.994679 DOI: https://doi.org/10.3389/fpls.2022.994679
  82. Zelm E., Zhang Y, Testerink C., 2020. Salt Tolerance Mechanisms of Plants. Annual Review of Plant Biology 71(1): 403–433. https://doi.org/10.1146/annurev-arplant-050718-100005. DOI: https://doi.org/10.1146/annurev-arplant-050718-100005
  83. Zeng C., Liu L., Wang B., Wu X., Zhou Y., 2011. Physiological effects of exogenous nitric oxide on Brassica juncea plants under NaCl stress. Biology of Plants 55(2): 345–348. https://doi.org/10.1007/s10535-011-0051-5 DOI: https://doi.org/10.1007/s10535-011-0051-5
  84. Zhang H., Sonnewald U., 2017. Differences and commonalities of plant responses to single and combined stresses. The Plant Journal 90(5): 839–855. https://doi.org/10.1111/tpj.13557 DOI: https://doi.org/10.1111/tpj.13557
  85. Zhang S.S., Sun L., Dong X., Lu S.J., Tian W., Liu J.X., 2016. Cellulose synthesis genes CESA6 and CSI1 are important for salt stress in Arabidopsis. Journal of Integrative Plant Biology 58(7): 623–626. https://doi.org/10.1111/jipb.12442 DOI: https://doi.org/10.1111/jipb.12442
  86. Zhao S., Zhang Q., Liu M., Zhou H., Ma C., Wang P., 2021. Regulation of plant responses to salt stress. International Journal of Molecular Science 22(9): 4609. https://doi.org/10.3390/ijms22094609 DOI: https://doi.org/10.3390/ijms22094609
  87. Zhou R., Yu X., Ottosen C.-O., Rosenqvist E., Zhao L., … Wu Z., 2017. Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biology 17(1): 24. https://doi.org/10.1186/s12870-017-0974-x DOI: https://doi.org/10.1186/s12870-017-0974-x
  88. Zheng M., Liu X., Lin J., Liu X., Wang Z., … Ni Z., 2019. Histone acetyltransferase GCN 5 contributes to cell wall integrity and salt stress tolerance by altering the expression of cellulose synthesis genes. The Plant Journal 97(3): 587–602. https://doi.org/10.1111/tpj.14144 DOI: https://doi.org/10.1111/tpj.14144