The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Physiology and Gene Expression Analysis of Tomato (Solanum lycopersicum L.) Exposed to Combined-Virus and Drought Stresses

  • Samra Mirzayeva (Institute of Molecular Biology & Biotechnologies, Ministry of Science and Education of Azerbaijan Republic) ;
  • Irada Huseynova (Institute of Molecular Biology & Biotechnologies, Ministry of Science and Education of Azerbaijan Republic) ;
  • Canan Yuksel Ozmen (Biotechnology Institute, Ankara University) ;
  • Ali Ergul (Biotechnology Institute, Ankara University)
  • Received : 2023.07.20
  • Accepted : 2023.09.06
  • Published : 2023.10.01
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Abstract

Crop productivity can be obstructed by various biotic and abiotic stresses and thus these stresses are a threat to universal food security. The information on the use of viruses providing efficacy to plants facing growth challenges owing to stress is lacking. The role of induction of pathogen-related genes by microbes is also colossal in drought-endurance acquisition. Studies put forward the importance of viruses as sustainable means for defending plants against dual stress. A fundamental part of research focuses on a positive interplay between viruses and plants. Notably, the tomato yellow leaf curl virus (TYLCV) and tomato chlorosis virus (ToCV) possess the capacity to safeguard tomato host plants against severe drought conditions. This study aims to explore the combined effects of TYLCV, ToCV, and drought stress on two tomato cultivars, Money Maker (MK, UK) and Shalala (SH, Azerbaijan). The expression of pathogen-related four cellulose synthase gene families (CesA/Csl) which have been implicated in drought and virus resistance based on gene expression analysis, was assessed using the quantitative real-time polymerase chain reaction method. The molecular tests revealed significant upregulation of Ces-A2, Csl-D3,2, and Csl-D3,1 genes in TYLCV and ToCV-infected tomato plants. CesA/Csl genes, responsible for biosynthesis within the MK and SH tomato cultivars, play a role in defending against TYLCV and ToCV. Additionally, physiological parameters such as "relative water content," "specific leaf weight," "leaf area," and "dry biomass" were measured in dual-stressed tomatoes. Using these features, it might be possible to cultivate TYLCV-resistant plants during seasons characterized by water scarcity.

Keywords

Acknowledgement

This research was financially supported by a grant from the Islamic Development Bank (ISDB) "Postdoc" Scholarship programme, Scholarship No.: 600047690 (2022). This research was conducted under the supervision of Professor Dr. Ali Ergul at Ankara University, Institute of Biotechnology, located in Ankara, Turkey. We extend our sincere gratitude to Professor Dr. Ali Ergul for his guidance and support throughout the study. Additionally, we would like to express our appreciation for the provision of laboratory space and the necessary chemical reagents, which greatly contributed to the successful completion of this work.

References

  1. Aboul-Maaty, N. A.-F. and Oraby, H. A.-S. 2019. Extraction of high-quality genomic DNA from different plant orders applying a modified CTAB-based method. Bull. Natl. Res. Centre 43:25.
  2. Aguilar, E., Cutrona, C., Del Toro, F. J., Vallarino, J. G., Osorio, S., Perez-Bueno, M. L., Baron, M., Chung, B.-N., Canto, T. and Tenllado, F. 2017. Virulence determines beneficial tradeoffs in the response of virus-infected plants to drought via induction of salicylic acid. Plant Cell Environ. 40:2909-2930. https://doi.org/10.1111/pce.13028
  3. Berges, S. E., Vile, D., Yvon, M., Masclef, D., Dauzat, M. and van Munster, M. 2021. Water deficit changes the relationships between epidemiological traits of Cauliflower mosaic virus across diverse Arabidopsis thaliana accessions. Sci. Rep. 11:24103.
  4. Brown, R. K., Wyatt, H., Price, J. F. and Kelly, F. J. 1996. Pulmonary dysfunction in cystic fibrosis is associated with oxidative stress. Eur. Respir. J. 9:334-339. https://doi.org/10.1183/09031936.96.09020334
  5. Burn, J. E., Hocart, C. H., Birch, R. J., Cork, A. C. & Williamson, R. E. 2002. Functional analysis of the cellulose synthase genes CesA1, CesA2, and CesA3 in Arabidopsis. Plant Physiol. 129:797-807.
  6. Cevik, B., Kivrak, H. and Sahin-Cevik, M. 2019. Development of a graft inoculation method and a real-time RT-PCR assay for monitoring tomato chlorosis virus infection in tomato. J. Virol. Methods 265:1-8. https://doi.org/10.1016/j.jviromet.2018.12.004
  7. Chen, T., Lv, Y., Zhao, T., Li, N., Yang, Y., Yu, W., He, X., Liu, T. and 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:e80816.
  8. Chen, Z., Hong, X., Zhang, H., Wang, Y., Li, X., Zhu, J.-K. and Gong, Z. 2005. Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J. 43:273-283. https://doi.org/10.1111/j.1365-313X.2005.02452.x
  9. Choe, S., Choi, B., Kang, J.-H. and Seo, J.-K. 2021. Tolerance to tomato yellow leaf curl virus in transgenic tomato overexpressing a cellulose synthase-like gene. Plant Biotechnol. J. 19:657-659. https://doi.org/10.1111/pbi.13539
  10. Chu, Z., Chen, H., Zhang, Y., Zhang, Z., Zheng, N., Yin, B., Yan, H., Zhu, L., Zhao, X., Yuan, M., Zhang, X. and Xie, Q. 2007. Knockout of the AtCESA2 gene affects microtubule orientation and causes abnormal cell expansion in Arabidopsis. Plant Physiol. 143:213-224. https://doi.org/10.1104/pp.106.088393
  11. Corrales-Gutierrez, M., Medina-Puche, L., Yu, Y., Wang, L., Ding, X., Luna, A. P, Bejarano, E. R., Castillo, A. G. and Lozano-Duran, R. 2020. The C4 protein from the geminivirus tomato yellow leaf curl virus confers drought tolerance in Arabidopsis through an ABA-independent mechanism. Plant Biotechnol. J. 18:1121-1123. https://doi.org/10.1111/pbi.13280
  12. Czosnek, H. 2021. Tomato yellow leaf curl viruses (Geminiviridae). In: Encyclopedia of virology, eds. by D. H. Bamford and M. Zuckerman, 4th ed., pp. 768-777. Elsevier, Amsterdam, The Netherlands.
  13. Dai, H., Cheng, L., Zhu, X., Liu, Y. and Zhao, J. 2017. Coinfections of Tomato chlorosis virus and Tomato yellow leaf curl virus transmitted by tobacco whitefly Bemisia tabaci to different tomato varieties. J. Plant Prot. 44:453-459.
  14. Dastogeer, K. M., Chakraborty, A., Sarker, M. S. A. and Akter, M. A. 2020. Roles of fungal endophytes and viruses in mediating drought stress tolerance in plants. Int. J. Agric. Biol. 24:1497-1512.
  15. Desbiez, C., Verdin, E., Moury, B., Lecoq, H., Millot, P., Wipf-Scheibel, C., Mirzayeva, S., Sultanova, N., Balakishiyeva, G., Mammadov, A., Kheyr-Pour, A. and Huseynova, I. 2019. Prevalence and molecular diversity of the main viruses infecting cucurbit and solanaceous crops in Azerbaijan. Eur. J. Plant Pathol. 153:359-369. https://doi.org/10.1007/s10658-018-1562-0
  16. Dovas, C., Katis, N. I. and Avgelis, A. D. 2002. Multiplex detection of criniviruses associated with epidemics of a yellowing disease of tomato in Greece. Plant Dis. 86:1345-1349. https://doi.org/10.1094/PDIS.2002.86.12.1345
  17. Espinoza, C., Medina, C., Somerville, S. and Arce-Johnson, P. 2007. Senescence-associated genes induced during compatible viral interactions with grapevine and Arabidopsis. J. Exp. Bot. 58:3197-3212. https://doi.org/10.1093/jxb/erm165
  18. Fiallo-Olive, E. and Navas-Castillo, J. 2019. Tomato chlorosis virus, an emergent plant virus still expanding its geographical and host ranges. Mol. Plant Pathol. 20:1307-1320. . https://doi.org/10.1111/mpp.12847
  19. Food and Agriculture Organization of the United Nations. 2020. The FAO Statistical Database-Agriculture. URL http://faostat3.fao.org/faostatgateway/go/to/download/Q/QC/E [9 January 2021].
  20. Foyer, C. H., Valadier, M. H., Migge, A. and Becker, T. W. 1998. Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiol. 117:283-292. https://doi.org/10.1104/pp.117.1.283
  21. Fullana-Pericas, M., Ponce, J., Conesa, M. A., Juan, A., Ribas-Carbo, M. and Galmes, J. 2018. Changes in yield, growth and photosynthesis in a drought-adapted Mediterranean tomato landrace (Solanum lycopersicum 'Ramellet') when grafted onto commercial rootstocks and Solanum pimpinellifolium. Sci. Hortic. 233:70-77. https://doi.org/10.1016/j.scienta.2018.01.045
  22. Gargallo-Garriga, A., Sardans, J., Perez-Trujillo, M., Rivas-Ubach, A., Oravec, M., Vecerova, K., Urban, O., Jentsch, A., Kreyling, J., Beierkuhnlein, C., Parella, T. and Penuelas, J. 2014. Opposite metabolic responses of shoots and roots to drought. Sci. Rep. 4:6829.
  23. Garrett, K. A., Dendy, S. P., Frank, E. E., Rouse, M. N. and Travers, S. E. 2006. Climate change effects of plant disease: genomes to ecosystems. Annu. Rev. Phytopathol. 44:489-509. https://doi.org/10.1146/annurev.phyto.44.070505.143420
  24. Gonzalez, R., Butkovic, A., Escaray, F. J., Martinez-Latorre, J., Melero, I., Perez-Parets, E., Gomez-Cadenas, A., Carrasco, P. and Elena, S. F. 2021. Plant virus evolution under strong drought conditions results in a transition from parasitism to mutualism. Proc. Natl. Acad. Sci. U. S. A. 118:e2020990118.
  25. Grunzweig, J. M., Katan, J., Ben-Tal, Y. and Rabinowitch, H. D. 1999. The role of mineral nutrients in the increased growth response of tomato plants in solarized soil. Plant Soil 206:21-27. https://doi.org/10.1023/A:1004321118896
  26. Hancinsky, R., Mihalik, D., Mrkvova, M., Candresse, T. and Glasa, M. 2020. Plant viruses infecting Solanaceae family members in the cultivated and wild environments: a review. Plants 9:667.
  27. Heidari, P., Ahmadizadeh, M., Izanlo, F. and Nussbaumer, T. 2019. In silico study of the CESA and CSL gene family in Arabidopsis thaliana and Oryza sativa: focus on post-translation modifications. Plant Gene 19:100189.
  28. Hosseini, S. A., Zamani, G. R., Yaghub, Z. M. and Khayyat, M. 2018. Effects of Cucumber mosaic virus infection and drought tolerance of tomato plants under greenhouse conditions: preliminary results. J. Berry Res. 8:129-136. https://doi.org/10.3233/JBR-170285
  29. Hu, H., Zhang, R., Feng, S., Wang, Y., Wang, Y., Fan, C., Li, Y., Liu, Z., Schneider, R., Xia, T., Ding, S.-Y., Persson, S. and Peng, L. 2018. Three AtCesA6-like members enhance biomass production by distinctively promoting cell growth in Arabidopsis. Plant Biotechnol. J. 16:976-988. https://doi.org/10.1111/pbi.12842
  30. Hull, R. 2002. Matthews' plant virology. 4th ed. Academic Press, San Diego, CA, USA. 1056 pp.
  31. Khan, S. H., Khan, A., Litaf, U., Shah, A. S., Khan, M. A., Bilal, M. and Ali, M. U. 2015. Effect of drought stress on Tomato cv. Bombino. J. Food Process. Technol. 6:7.
  32. Klay, I., Pirrello, J., Riahi, L., Bernadac, A., Cherif, A., Bouzayen, M. and Bouzid, S. 2014. Ethylene response factor Sl-ERF.B.3 is responsive to abiotic stresses and mediates salt and cold stress response regulation in tomato. Scientific World Journal 2014:167681.
  33. Krishna, R., Ansari, W. A., Soumia, P. S., Yadav, A., Jaiswal, D. K., Kumar, S., Singh, A. K., Singh, M. and Verma, J. P. 2022. Biotechnological interventions in tomato (Solanum lycopersicum) for drought stress tolerance: achievements and future prospects. BioTech 11:48.
  34. Landrein, B. and Hamant, O. 2013. How mechanical stress controls microtubule behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J. 75:324-338. https://doi.org/10.1111/tpj.12188
  35. Le Gall, H., Philippe, F., Domon, J.-M., Gillet, F., Pelloux, J. and Rayon, C. 2015. Cell wall metabolism in response to abiotic stress. Plants 4:112-166. https://doi.org/10.3390/plants4010112
  36. Lee, H., Kim, M.-K., Choi, H.-S., Kang, J.-H., Ju, H.-J. and Seo, J.-K. 2017. Efficient transmission and propagation of tomato chlorosis virus by simple single-leaflet grafting. Plant Pathol. J. 33:345-349. https://doi.org/10.5423/PPJ.NT.02.2017.0039
  37. Lesk, C., Rowhani, P. and Ramankutty, N. 2016. Influence of extreme weather disasters on global crop production. Nature 529:84-87. https://doi.org/10.1038/nature16467
  38. Li, T., Huang, Y., Xu, Z.-S., Wang, F. and Xiong, A.-S. 2019. Salicylic acid-induced differential resistance to the Tomato yellow leaf curl virus among resistant and susceptible tomato cultivars. BMC Plant Biol. 19:173.
  39. Liang, G., Bu, J., Zhang, S., Jing, G., Zhang, G. and Liu, X. 2018. Effects of drought stress on the photosynthetic physiological parameters of Populus×euramericana 'Neva'. J. For. Res. 30:409-416. https://doi.org/10.1007/s11676-018-0667-9
  40. Liang, G., Liu, J., Zhang, J. And Guo, J. 2020. Effects of drought stress on photosynthetic and physiological parameters of tomato. J. Am. Soc. Hortic. Sci. 145:12-17. https://doi.org/10.21273/JASHS04725-19
  41. Livak, K. J. and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  42. Louro, D., Accotto, G. and Vaira, A. M. 2000. Occurrence and diagnosis of Tomato chlorosis virus in Portugal. Eur. J. Plant Pathol. 106:589-592. https://doi.org/10.1023/A:1008738130592
  43. Macedo, M. A., Inoue-Nagata, A. K., Silva, T. N. Z., Freitas, D. M. S., Rezende, J. A. M., Barbosa, J. C., Michereff-Filho, M., Nascimento, A. R., Lourencao, A. and Filho, A. B. 2019. Temporal and spatial progress of the diseases caused by the Crinivirus tomato chlorosis virus and the Begomovirus tomato severe rugose virus in tomatoes in Brazil. Plant Pathol. 68:72-84. https://doi.org/10.1111/ppa.12920
  44. Mackie, A. E., Barbetti, M. J., Rodoni, B., McKirdy, S. J. and Jones, R. A. C. 2019. Effects of a potato spindle tuber viroid tomato strain on the symptoms, biomass, and yields of classical indicator and currently grown potato and tomato cultivars. Plant Dis. 103:3009-3017. https://doi.org/10.1094/PDIS-02-19-0312-RE
  45. Malinovsky, F. G., Fangel, J. U. and Willats, W. G. T. 2014. The role of the cell wall in plant immunity. Front. Plant Sci. 5:178.
  46. Marchant, W. G., Gautam, S., Hutton, S. F. and Srinivasan, R. 2020. Tomato yellow leaf curl virus-resistant and -susceptible tomato genotypes similarly impact the virus population genetics. Front. Plant Sci. 11:599697.
  47. Martinez-Culebras, P., Font, I. and Jorda, C. 2001. A rapid PCR method to discriminate between Tomato yellow leaf curl virus isolates. Ann. Appl. Biol. 139:251-257. https://doi.org/10.1111/j.1744-7348.2001.tb00401.x
  48. Mayek-Perez, N., Garcia-Espinosa, R., Lopez-Casteneda, C., Acosta-Gallegos, J. A. and Simpson, J. 2002. Water relations, histopathology and growth of common bean (Phaseolus vulgaris L.) during pathogenesis of Macrophomina phaseolina under drought stress. Physiol. Mol. Plant Pathol. 60:185-195. https://doi.org/10.1006/pmpp.2001.0388
  49. McElrone, A. J., Sherald, J. L. and Forseth, I. N. 2001. Effects of water stress on symptomatology and growth of Parthenocissus quinquefolia infected by Xylella fastidiosa. Plant Dis. 85:1160-1164. https://doi.org/10.1094/PDIS.2001.85.11.1160
  50. McLaughlin, M. R. and Windham, G. L. 1996. Effects of peanut stunt virus, Meloidogyne incognita, and drought on growth and persistence of white clover. Phytopathology 86:1105-1111. https://doi.org/10.1094/Phyto-86-1105
  51. Milc, J., Bagnaresi, P., Aragona, M., Valente, M. T., Biselli, C., Infantino, A., Francia, E. and Pecchioni, N. 2019. Comparative transcriptome profiling of the response to Pyrenochaeta lycopersici in resistant tomato cultivar Mogeor and its background genotype-susceptible Moneymaker. Funct. Integr. Genomics 19:811-826. https://doi.org/10.1007/s10142-019-00685-0
  52. Mishra, R., Shteinberg, M., Shkolnik, D., Anfoka, G., Czosnek, H. and Gorovits, R. 2022. Interplay between abiotic (drought) and biotic (virus) stresses in tomato plants. Mol. Plant Pathol. 23:475-488. https://doi.org/10.1111/mpp.13172
  53. Moriones, E. and Navas-Castillo, J. 2000. Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Res. 71:123-134. https://doi.org/10.1016/S0168-1702(00)00193-3
  54. Narciso, J., Oane, R. H., Kumar, A. and Kohli, A. 2010. Cellulose synthase as a major candidate gene in the large effect QTL for rice yield under drought stress. Philip. J. Crop Sci. 35:7.
  55. Ong, S. N., Taheri, S., Othman, R. Y. and Teo, C. H. 2020. Viral disease of tomato crops (Solanum lycopesicum L.): an overview. J. Plant Dis. Prot. 127:725-739. https://doi.org/10.1007/s41348-020-00330-0
  56. Orfanidou, C. G., Pappi, P. G., Efthimiou, K. E., Katis, N. I. and Maliogka, V. I. 2016. Transmission of Tomato chlorosis virus (ToCV) by Bemisia tabaci biotype Q and evaluation of four weed species as viral sources. Plant Dis. 100: 2043-2049. https://doi.org/10.1094/PDIS-01-16-0054-RE
  57. Papayiannis, L. C., Harkoua, I. S., Markou, Y. M., Demetriou, C. N. and Katis, N. I. 2011. Rapid discrimination of Tomato chlorosis virus, Tomato infectious chlorosis virus and co-amplification of plant internal control using real-time RT-PCR. J. Virol. Methods 176:53-59. https://doi.org/10.1016/j.jviromet.2011.05.036
  58. Patane, C., Cosentino, S. L., Romano, D. and Toscano, S. 2022. Relative water content, proline, and antioxidant enzymes in leaves of long shelf-life tomatoes under drought stress and rewatering. Plants 11:3045.
  59. Pathirana, R. and McKenzie, M. J. 2005. A modified green-grafting technique for large-scale virus indexing of grapevine (Vitis vinifera L.). Sci. Hortic. 107:97-102. https://doi.org/10.1016/j.scienta.2005.06.002
  60. Poudel, M., Mendes, R., Costa, L. A. S., Bueno, C. G., Meng, Y., Folimonova, S. Y., Garrett, K. A. and Martins, S. J. 2021. The role of plant-associated bacteria, fungi, and viruses in drought stress mitigation. Front. Microbiol. 12:743512.
  61. Prasch, C. M. and Sonnewald, U. 2013. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol. 162:1849-1866. https://doi.org/10.1104/pp.113.221044
  62. Rivarez, M. P. S., Vucurovic, A., Mehle, N., Ravnikar, M. and Kutnjak, D. 2021. Global advances in tomato virome research: current status and the impact of high-throughput sequencing. Front. Microbiol. 12:671925.
  63. Rukundo, P., Betaw, H. G., Ngailo, S. and Balcha, F. 2014. Assessment of drought stress tolerance in root and tuber crops. Afr. J. Plant Sci. 8:214-224. https://doi.org/10.5897/AJPS2014.1169
  64. Sakya, A. T., Sulistyaningsih, E., Indradewa, D. and Purwanto, B. H. 2018. Physiological characters and tomato yield under drought stress. IOP Conf. Ser. Earth Environ. Sci. 200:012043. https://doi.org/10.1088/1755-1315/200/1/012043
  65. Sand, B. E., Vile, D., Vazquez-Rovere, C., Blanc, S., Yvon, M., Bediee, A., Rolland, G., Dauzat, M. and van Munster, M. 2018. Interactions between drought and plant genotype change epidemiological traits of cauliflower mosaic virus. Front. Plant Sci. 9:703.
  66. Seo, J.-K., Kim, M.-K., Kwak, H.-R., Choi, H.-S., Nam, M., Choe, J., Choi, B., Han, S.-J., Kang, J.-H. and Jung, C. 2018. Molecular dissection of distinct symptoms induced by tomato chlorosis virus and tomato yellow leaf curl virus based on comparative transcriptome analysis. Virology 516:1-20. https://doi.org/10.1016/j.virol.2018.01.001
  67. Shackel, B. 1991. Usability: context, framework, definition, design and evaluation. In: Human factors for informatics usability, eds. by B. Shackel and S. Richardson, pp. 21-37. Cambridge University Press, Cambridge, UK.
  68. Siniga Geroge, S., Jatoi, S. A. and Siddiqui, S. U. 2013. Genotypic differences against peg simulated drought stress in tomato. Pak. J. Bot. 45:1551-1556.
  69. Sofy, A. R., Sofy, M. R., Hmed, A. A., Dawoud, R. A., Alnaggar, A. E.-A. M., Soliman, A. M. and El-Dougdoug, N. K. 2021. Ameliorating the adverse effects of Tomato mosaic tobamovirus infecting tomato plants in Egypt by boosting immunity in tomato plants using zinc oxide nanoparticles. Molecules 26:1337.
  70. Somerville, C. 2006. Cellulose synthesis in higher plants. Annu. Rev. Cell Dev. Biol. 22:53-78. https://doi.org/10.1146/annurev.cellbio.22.022206.160206
  71. Song, X., Xu, L., Yu, J., Tian, P., Hu, X., Wang, Q. and Pan, Y. 2019. Genome-wide characterization of the cellulose synthase gene superfamily in Solanum lycopersicum. Gene 688:71-83. https://doi.org/10.1016/j.gene.2018.11.039
  72. Tahi, H., Wahbi, S., Wakrim, R., Aganchich, B., Serraj, R. and Centritto, M. 2007. Water relations, photosynthesis, growth and water-use efficiency in tomato plants subjected to partial rootzone drying and regulated deficit irrigation. Plant Biosyst. 141:265-274. https://doi.org/10.1080/11263500701401927
  73. Tambussi, E. A., Nogues, S. and Araus, J. L. 2005. Ear of durum wheat under water stress: water relations and photosynthetic metabolisms. Planta 221:446-458. https://doi.org/10.1007/s00425-004-1455-7
  74. Torres-Ruiz, J. M., Diaz-Espejo, J., Perez-Martin, A. and Hernandez-Santana, A. 2015. Role of hydraulic and chemical signals in leaves, stems and roots in the stomatal behaviour of olive trees under water stress and recovery conditions. Tree Physiol. 35:415-424. https://doi.org/10.1093/treephys/tpu055
  75. Verdin, E., Desbiez, C., Wipf-Scheibel, C., Gognalons, P., KheyrPour, A., Gronenborn, B., Mirzayeva, S., Sultanova, N., Mammadov, A. and Huseynova, I. 2018. First report of tomato yellow leaf curl virus infecting tomato in Azerbaijan. J. Plant Pathol. 100:335.
  76. Waititu, J. K., Zhang, X., Chen, T., Zhang, C., Zhao, Y. and Wang, H. 2021. Transcriptome analysis of tolerant and susceptible maize cultivars reveals novel insights about the molecular mechanisms underlying drought responses in leaves. Int. J. Mol. Sci. 22:6980.
  77. Wang, J., Li, J., Lin, W., Deng, B., Lin, L., Lv, X., Hu, Q., Liu, K., Fatima, M., He, B., Qiu, D. And Ma, X. 2023. Genome-wide identification and adaptive evolution of CesA/Csl superfamily among species with different life forms in Orchidaceae. Front. Plant Sci. 13:994679.
  78. Wang, S., Yin, Y., Ma, Q., Tang, X., Hao, D. and Xu, Y. 2012. Genome-scale identification of cell-wall related genes in Arabidopsis based on co-expression network analysis. BMC Plant Biol. 12:138.
  79. Wei, K.-K., Li, J., Ding, T.-B., Liu, T.-X. and Chu, D. 2019. Transmission characteristics of Tomato chlorosis virus (ToCV) by Bemisia tabaci MED and its effects on host preference of vector whitefly. J. Integr. Agric. 18:2107-2114. https://doi.org/10.1016/S2095-3119(18)62080-5
  80. Xu, P., Chen, F., Mannas, J. P., Feldman, T., Sumner, L.W. and Roossinck, M. J. 2008. Virus infection improves drought tolerance. New Phytol. 180:911-921. https://doi.org/10.1111/j.1469-8137.2008.02627.x
  81. Yan, B. and Wang, G. 2013. The development situation and countermeasure of reclaimed water reuse in Zhanjiang City Guangdong Province. Ecol. Sci. 32:668-672.
  82. Zhang, X., Tan, J., Wen, M. and Miao, Z. 2019. Systematic identification and functional study of CesA family in maize. J. Northwest A & F Univ. Nat. Sci. Ed. 47:45-53.
  83. Zhou, R., Yu, X., Ottosen, C.-O., Rosenqvist, E., Zhao, L., Wang, Y., Yu, W., Zhao, T. and Wu, Z. 2017. Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol. 17:24.