Пшениця є стратегічною зерновою культурою у світі, яка відіграє провідну роль у харчовому забезпеченні людства. Незважаючи на загалом зростаючу тенденцію її виробництва, кліматичні зміни, що призводять до температурних перепадів, непередбачуваних опадів або посух, значно позначаються на її врожайності. Для попередження негативного впливу змін кліматичних умов на продуктивність цієї культури необхідна розробка інноваційних технологій покращення стійкості пшениці до абіотичних стресів. РНК-інтерференція (РНКі) є новим потенційним інструментом для селекції пшениці шляхом впровадження малих некодувальних послідовностей РНК із можливістю глушіння експресії генів специфічним для послідовності способом. Здатність до зниження експресії конкретного гена забезпечує можливість набуття нової характеристики елімінацією або накопиченням певних сполук в рослинах, що приводить до біохімічних або фенотипних змін, яких не мають вихідні рослини. У даному огляді літератури представлено сучасні уявлення про роль мікроРНК (міРНК), які є регуляторами експресії генів інгібуванням трансляції їх мРНК-мішеней через комплементарне зв’язування і розщеплення, у відповіді рослин пшениці на абіотичні стреси. Коротко представлено основні етапи механізму глушіння генів, опосередкованих міРНК. Детально описано особливості їхнього біогенезу, способи дії та розповсюдження. Розглянуто ідентифіковані міРНК пшениці, що реагують на абіотичні стреси, та їх передбачувані гени-мішені. Наводяться приклади диференційної експресії міРНК за стресової дії посухи, засолення і температурних чинників.
Ключові слова: Triticum aestivum L., пшениця, РНК-інтерференція, міРНК, стійкість до абіотичних стресів
Повний текст та додаткові матеріали
У вільному доступі: PDFЦитована література
1. Shewry, P.R. (2009). Wheat. J. Exp. Bot., 60, No. 6, pp. 1537-1553. https://doi.org/10.1093/jxb/erp058
2. Shiferaw, B., Smale, M., Braun, H., Duveiller, E., Reynolds, M. & Muricho, G. (2013). Crops that feed the world 10. Past successes and future challenges to the role played by wheat in global food security. Food Sec., 5, No. 3, pp. 291-317. https://doi.org/10.1007/s12571-013-0263-y
3. Budak, H., Hussain, B., Khan, Z., Ozturk, N.Z. & Ullah, N. (2015a). From genetics to functional genomics: improvement in drought signaling and tolerance in wheat. Front Plant Sci., 6, 1012. https://doi.org/10.3389/fpls.2015.01012
4. Nowsherwan, I., Shabbir, G., Malik, S.I. & Ilyas, M. (2018). Effect of drought stress on different physiological traits in bread wheat. J. Agricult., 16, No. 1, pp. 1-6. https://doi.org/10.3329/sja.v16i1.37418
5. Mickelbart, M.V., Hasegawa, P.M. & Bailey-Serres J. (2015). Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat. Rev. Genet., 16, pp. 237-251. https://doi.org/10.1038/nrg3901
6. Alptekin, B., Langridge, P. & Budak, H. (2017). Abiotic stress miRNomes in the Triticeae. Funct. Int. Genom., 17, pp. 145-170. https://doi.org/10.1007/s10142-016-0525-9
7. Kapoor, D., Bhardwaj, S., Landi, M., Sharma, A., Ramakrishnan, M. & Sharma, A. (2020). The impact of drought in plant metabolism: how to exploit tolerance mechanisms to increase crop production. Appl. Sci., 10, No. 16, 5692. https://doi.org/10.3390/app10165692
8. Zhang, B. (2015). MicroRNA: a new target for improving plant tolerance to abiotic stress. J. Exp. Bot., 66, pp. 1749-1761. https://doi.org/10.1093/jxb/erv013
9. Akpinar, B.A., Avsar, B., Lucas, S.J. & Budak, H. (2012). Plant abiotic stress signaling. Plant Sign. Behav., 7, No. 11, pp. 1450-1455. https://doi.org/10.4161/psb.21894
10. Budak, H., Kantar, M., Bulut, R. & Akpinar, B.A. (2015b). Stress responsive miRNAs and isomiRs in cereals. Plant Sci., 235, pp. 1-13. https://doi.org/10.1016/j.plantsci.2015.02.008
11. Fletcher, S.J., Reeves, P.T., Hoang, B.T. & Mitter, N.A. (2020). Perspective on RNAi-based biopesticides. Front. Plant Sci., 11, e00051. https://doi.org/10.3389/fpls.2020.00051
12. Liu, S., Geng, S., Li, A., Mao, Y. & Mao, L. (2021). RNAi technology for plant protection and its application in wheat. aBIOTECH, 2, pp. 365-374. https://doi.org/10.1007/s42994-021-00036-3
13. Bharathi, J., Anandan, R., Benjamin, L., Muneer, S. & Prakash, M. (2023). Recent trends and advances of RNA interference (RNAi) to improve agricultural crops and enhance their resilience to biotic and abiotic stresses. Plant Physiol. Biochem. J., 194, pp. 600-618. https://doi.org/10.1016/j.plaphy.2022.11.035
14. Kumar, K., Gambhir, G., Dass, A., Tripathi, A.K., Singh, A., Jha, A.K., Yadava, P., Choudhary, M. & Rakshit, S. (2020). Genetically modified crops: current status and future prospects. Planta, 251, No. 4, 91. https://doi.org/10.1007/s00425-020-03372-8
15. Hern«ndez-Soto, A. & ChacЩn-Cerdas, R. (2021). RNAi crop protection advances. Int. J. Mol. Sci., 22, No. 22, 12148. https://doi.org/10.3390/ijms222212148
16. Bilir, љ., GШl, D., Hong, Y., McDowell, J.M. & TШr, M. (2022). Small RNA-based plant protection against diseases. Front. Plant Sci., 13, 951097. https://doi.org/10.3389/fpls.2022.951097
17. Halder, K., Chaudhuri, A., Abdin, M.Z. & Datta, A. (2023). Tweaking the small non-coding RNAs to improve desirable traits in plant. Int. J. Mol. Sci., 24, 3143. https://doi.org/10.3390/ijms24043143
18. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E. & Mello, C.C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nat. J., 391, No. 6669, pp. 806-811. https://doi.org/10.1038/35888
19. Qi, T., Guo, J., Liu, P., He, F., Wan, C., Islam, M., Tyler, B.M., Kang, Z. & Guo, J. (2019a). Stripe rust effector PstGSRE1 disrupts nuclear localization of ROS-promoting transcription factor TaLOL2 to defeat ROS-induced defense in wheat. Mol. Plant, 12, No. 12, pp. 1624-1638. https://doi.org/10.1016/j.molp.2019.09.010
20. Abdellatef, E., Kamal, N.M. & Tsujimoto, H. (2021). Tuning beforehand: a foresight on RNA interference (RNAi) and in vitro-derived dsRNAs to enhance crop resilience to biotic and abiotic stresses. Int. J. Mol. Sci., 22, No. 14, 7687. https://doi.org/10.3390/ijms22147687
21. Akbar, S., Wei, Y. & Zhang, M.-Q. (2022). RNA interference: promising approach to combat plant viruses. Int. J. Mol. Sci., 23, No. 10, 5312. https://doi.org/10.3390/ijms23105312
22. Dubrovna, O.V., Mykhalska, S.I. & Komisarenko, A.G. (2023). Use of RNA interference technology for improving economically valuable traits of cereal crops. Cytol. Genet., 57, No. 6, pp. 587-610. https://doi.org/10.3103/S0095452723060026
23. Rajam, M.V. (2020). RNA silencing technology: A boon for crop improvement. J. Biosci., 45, No. 1, pp. 1-5. https://doi.org/10.1007/s12038-020-00082-x
24. Rodrigues, T.B. & Petrick, J.S. (2020). Safety considerations for humans and other vertebrates regarding agricultural uses of externally applied RNA molecules. Front. Plant Sci., 11, 407. https://doi.org/10.3389/fpls.2020.00407
25. Kaur, R., Choudhury, A., Chauhan, S., Ghosh, A., Tiwari, R. & Rajam, M. (2021). RNA interference and crop protection against biotic stresses. Physiol. Mol. Biol. Plants, 27, No. 10, pp. 2357-2377. https://doi.org/10.1007/s12298-021-01064-5
26. Mezzetti, B., Smagghe, G., Arpaia, S. & Christiaens, O. (2020). RNAi: what is its position in agriculture? J. Pest. Sci., 93, No. 4, pp. 1125-1130. https://doi.org/10.1007/s10340-020-01238-2
27. Barro, F., Iehisa, J.C., Gimѕnez, M.J., GarcHa-Molina, M.D., Ozuna, C.V., Comino, I., Sousa, C. & Gil-Humanes, J. (2016). Targeting of prolamins by RNAi in bread wheat: effectiveness of seven silencing-fragment combinations for obtaining lines devoid of coeliac disease epitopes from highly immunogenic gliadins. Plant Biotechnol. J., 14, No. 3, pp. 986-996. https://doi.org/10.1111/pbi.12455
28. Gasparis, S., KaYa, M., Przyborowski, M., Orczyk, W. & Nadolska-Orczyk, A. (2017). Artificial microRNA-based specific gene silencing of grain hardness genes in polyploid cereals appeared to be not stable over transgenic plant generations. Front. Plant Sci., 9, No. 7, 02017. https://doi.org/10.3389/fpls.2016.02017
29. Qi, T., Guo, J., Peng, H., Liu, P., Kang, Z. & Guo, J. (2019). Host-induced gene silencing: a powerful strategy to control diseases of wheat and barley. Int. J. Mol. Sci., 20, No. 1, 206. https://doi.org/10.3390/ijms20010206
30. Wang, M., Wu, L., Mei, Y., Zhao, Y., Ma, Z., Zhang, X. & Chen, Y. (2020). Host-induced gene silencing of multiple genes of Fusarium graminearum enhances resistance to Fusarium head blight in wheat. Plant Biotechnol. J., 18, No. 12, pp. 2373-2375. https://doi.org/10.1111/pbi.13401
31. Dutta, T.K., Papolu, P.R., Singh, D., Sreevathsa, R. & Rao, U. (2020). Expression interference of a number of Heterodera avenae conserved genes perturbs nematode parasitic success in Triticum aestivum. Plant Sci., 301, e110670. https://doi.org/10.1016/j.plantsci.2020.110670
32. Gupta, O.P., Meena, N.L., Sharma, I. & Sharma, P. (2014). Differential regulation of microRNAs in response to osmotic, salt and cold stresses in wheat. Mol. Biol. Rep., 41, pp. 4623-4629. https://doi.org/10.1007/s11033-014-3333-0
33. Bai, Q., Wang, X., Chen, X., Shi, G., Liu, Z., Guo, C. & Xiao, K. (2018). Wheat miRNA Taemir408 acts as an essential mediator in plant tolerance to Pi deprivation and salt stress via modulating stress-associated physiological processes. Front. Plant Sci., 18, No. 9, 499. https://doi.org/10.3389/fpls.2018.00499
34. Banerjee, P. (2020). Plant abiotic stress responses and microRNAs. Adv. Agricult., pp. 109-118. https://doi.org/10.30954/NDP-advagr.2020.6
35. Zeeshan, M., Qiu, C.W., Naz, S., Cao, F. & Wu, F. (2021). Genome-wide discovery of mirnas with differential expression patterns in responses to salinity in the two contrasting wheat cultivars. Int. J. Mol. Sci., 22, No. 22, 12556. https://doi.org/10.3390/ijms222212556
36. Brosnan, C.A. & Voinnet, O. (2009). The long and the short of noncoding RNAs. Curr. Opin. Cell Biol., 21, No. 3, pp. 416-425. https://doi.org/10.1016/j.ceb.2009.04.001
37. D'Ario, M., Griffiths-Jones, S. & Kim, M. (2017). Small RNAs: big impact on plant development. Trends Plant Sci., 22, No. 12, pp. 1056-1068. https://doi.org/10.1016/j.tplants.2017.09.009
38. Song, X., Li, Y., Cao, X. & Qi, Y. (2019). MicroRNAs and their regulatory roles in plant-environment interactions. Ann. Rev. Plant Biol., 70, pp. 489-525. https://doi.org/10.1146/annurev-arplant-050718-100334
39. Lee, R.C., Feinbaum, R.L. & Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, No. 5, pp. 843-854. https://doi.org/10.1016/0092-8674(93)90529-Y
40. Yu, Y., Zhang, Y., Chen, X. & Chen, Y. (2019). Plant noncoding RNAs: hidden players in development and stress responses. Ann. Rev. Cell Develop. Biol., 35, pp. 407-431. https://doi.org/10.1146/annurev-cellbio-100818-125218
41. Budak, H. & Akpinar, B.A. (2015). Plant miRNAs: biogenesis, organization and origins. Funct. Int. Genom., 15, No. 5, pp. 523-531. https://doi.org/10.1007/s10142-015-0451-2
42. Zhang, B. & Wang, Q. (2016). MicroRNA, a new target for engineering new crop cultivars. Bioengineered, 7, No. 1, pp. 7-10. https://doi.org/10.1080/21655979.2016.1141838
43. Li, C. & Zhang, B. (2016). MicroRNAs in control of plant development. J. Cell. Physiol., 231, No. 2, pp. 303-313. https://doi.org/10.1002/jcp.25125
44. Bhogireddy, S., Mangrauthia, S., Kumar, R., Pandey, A., Singh, S., Jain, A., Budak, H., Varshney, R. & Kudapa, H. (2021). Regulatory non-coding RNAs: a new frontier in regulation of plant biology. Funct. Int. Gen., 21, pp. 313-330. https://doi.org/10.1007/s10142-021-00787-8
45. Sunkar, R., Li, Y.F. & Jagadeeswaran, G. (2012). Functions of microRNAs in plant stress responses. Trends Plant Sci., 17, No. 4, pp. 196-203. https://doi.org/10.1016/j.tplants.2012.01.010
46. Skopelitis, D.S., Hill, K., Klesen, S., Marco, C.F., von Born, P., Chitwood, D. H. & Timmermans, C.P.M. (2018). Gating of miRNA movement at defined cell-cell interfaces governs their impact as positional signals. Nature Comm., 9, No. 1, 3107. https://doi.org/10.1038/s41467-018-05571-0
47. Deng, P., Muhammad, S., Cao, M. & Wu, L. (2018). Biogenesis and regulatory hierarchy of phased small interfering RNAs in plants. Plant Biotechnol. J., 16, No. 5, pp. 965-975. https://doi.org/10.1111/pbi.12882
48. Fahim, M., Millar, A.A., Wood, C.C. & Larkin, P.J. (2012). Resistance to wheat streak mosaic virus generated by expression of an artificial polycistronic microRNA in wheat. Plant Biotechnol. J., 10, No. 2, pp. 150-163. https://doi.org/10.1111/j.1467-7652.2011.00647.x
49. Feng, H. Wang, B., Zhang, Q., Fu, Y., Huang, L., Wang, X. & Kang, Z. (2015). Exploration of microRNAs and their targets engaging in the resistance interaction between wheat and stripe rust. Front. Plant Sci., 6, 469. https://doi.org/10.3389/fpls.2015.00469
50. Jiao, J. & Peng, D. (2018). Wheat MicroRNA1023 suppresses invasion of Fusarium graminearum via targeting and silencing FGSG_03101. J. Plant Int., 13, No. 1, pp. 514-521. https://doi.org/10.1080/17429145.2018.1528512
51. Kantar, M., Lucas, S.J. & Budak, H. (2011b). Drought stress. Molecular genetics and genomics approaches. Adv. Bot. Res., 57, pp. 445-493. https://doi.org/10.1016/B978-0-12-387692-8.00013-8
52. Feng, H., Zhang, Q., Wang, Q., Wang, X., Liu, J. & Li, M. (2013). Target of tae-miR408, a chemocyanin-like protein gene (TaCLP1), plays positive roles in wheat response to high-salinity, heavy cupric stress and stripe rust. Plant Mol. Biol., 83, No. 4-5, pp. 433-443. https://doi.org/10.1007/s11103-013-0101-9
53. Tang, Z., Zhang, L., Xu, C., Yuan, S., Zhang, F., Zheng, Y. & Zhao, C. (2012). Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic malesterile line by deep sequencing. Plant Physiol., 159, No. 2, pp. 721-738. https://doi.org/10.1104/pp.112.196048
54. Akpinar, B.A., Kantar, M. & Budak, H. (2015). Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct. Int. Genom., 15, No. 5, pp. 587-598. https://doi.org/10.1007/s10142-015-0453-0
55. Liu, H., Searle, I.R., Watson-Haigh, N.S., Baumann, U., Mather, D.E., Able, A.J. & Able, J.A. (2015). Genome-wide identification of microRNAs in leaves and the developing head of four durum genotypes during water deficit stress. PLoS ONE, 10, No. 11, e0142799. https://doi.org/10.1371/journal.pone.0142799
56. Liu, H., Able, A.J. & Able, J.A. (2016). Water-deficit stress-responsive microRNAs and their targets in four durum wheat genotypes. Funct. Int. Genom., 17, pp. 237-251. https://doi.org/10.1007/s10142-016-0515-y
57. Budak, H., Khan, Z. & Kantar, M. (2015c). History and current status of wheat miRNAs using next-generation sequencing and their roles in development and stress. Brief. Funct. Genom., 14, No. 3, pp. 189-198. https://doi.org/10.1093/bfgp/elu021
58. Kantar, M., Lucas, S.J. & Budak, H. (2011a). miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta, 233, pp. 471-484. https://doi.org/10.1007/s00425-010-1309-4
59. Ma, X., Xin, Z., Wang, Z., Yang, Q., Guo, S., Guo, X., Cao, L. & Lin, T. (2015). Identification and comparative analysis of differentially expressed miRNAs in leaves of two wheat (Triticum aestivum L.) genotypes during dehydration stress. BMC Plant Biol., 15, 21. https://doi.org/10.1186/s12870-015-0413-9
60. Pandey, R., Joshi, G., Bhardwaj, A.R., Agarwal, M. & Katiyar-Agarwal, S.A. (2014). Comprehensive genome-wide study on tissue specific and abiotic stress-specific miRNAs in Triticum aestivum. PLoS ONE, 9, No. 4, e95800. https://doi.org/10.1371/journal.pone.0095800
61. Li, Y.-F., Zheng, Y., Jagadeeswaran, G. & Sunkar, R. (2013). Characterization of small RNAs and their target genes in wheat seedlings using sequencing based approaches. Plant Sci., 203-204, pp. 17-24. https://doi.org/10.1016/j.plantsci.2012.12.014
62. Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M. Luo, L. & Notes, A. (2010). Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J. Exp. Bot., 61, No. 15, pp. 4157-4168. https://doi.org/10.1093/jxb/erq237
63. Sunkar, R., Girke, T., Jain, P.K. & Zhu, J.-K. (2005). Cloning and characterization of microRNAs from rice. Plant Cell, 17, No. 5, pp. 1397-1411. https://doi.org/10.1105/tpc.105.031682
64. Hua, Y., Zhang, C., Shi, W. & Chen, H. (2019). High-throughput sequencing reveals microRNAs and their targets in response to drought stress in wheat (Triticum aestivum L.). Biotechnol. Biotechnol. Equipment, 33, pp. 465-471. https://doi.org/10.1080/13102818.2019.1586586
65. Lu, W., Li, J., Liu, F., Gu, J., Guo, C., Xu, L., Zhang, H. & Xiao, K. (2011). Expression pattern of wheat miRNAs under salinity stress and prediction of salt-inducible miRNAs targets. Front. Agricult. China, 5, pp. 413-422. https://doi.org/10.1007/s11703-011-1133-z
66. Zhao, B., Ge, L., Liang, R., Li, W., Ruan, K., Lin, H. & Jin, Y. (2009). Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol. Biol., 10, 29. https://doi.org/10.1186/1471-2199-10-29
67. Wang, B., Fei Sun, Y., Son, N., Wei, J., Wang, X., Feng, H., Yin, Z. & Kang, Z. (2014). MicroRNAs involving in cold, wounding and salt stresses in Triticum aestivum L. Plant Physiol. Biochem., 80, pp. 90-96. https://doi.org/10.1016/j.plaphy.2014.03.020
68. Xin, M., Wang, Y., Yao, Y., Xie, C., Peng, H., Ni, Z. & Sun, Q. (2010). Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol., 10, 123. https://doi.org/10.1186/1471-2229-10-123
69. Kumar, R.R., Pathak, H., Sharma, S.K., Kala, Y.K., Nirjal, M.K., Singh, G.P., Goswami, S. & Rai, R.D. (2015). Novel and conserved heat-responsive microRNAs in wheat (Triticum aestivum L.). Funct. Int. Genom., 15, No. 3, pp. 323-348. https://doi.org/10.1007/s10142-014-0421-0
70. Wang, Y., Sun, F., Cao, H., Peng, H., Ni, Z., Sun, Q. & Yao, Y. (2012). TamiR159 directed wheat TaGAMYB cleavage and its involvement in anther development and heat response. PLoS ONE, 7, No. 11, e48445. https://doi.org/10.1371/journal.pone.0048445
71. Goswami, S., Kumar, R.R. & Rai, R.D. (2014). Heat-responsive microRNAs regulate the transcription factors and heat shock proteins in modulating thermo stability of starch biosynthesis enzymes in wheat (Triticum aestivum L.) under the heat stress. Aust. J. Crop Sci., 8, No. 5, pp. 697-705.
72. Ragupathy, R., Ravichandran, S., Mahdi, M.S.R., Huang, D., Reimer, E., Domaratzki, M. & Cloutier, S. (2016). Deep sequencing of wheat sRNA transcriptome reveals distinct temporal expression pattern of miRNAs in response to heat, light and UV. Sci. Rep., 6, pp. 1-15. https://doi.org/10.1038/srep39373
73. Ravichandran, S., Ragupathy, R., Edwards, T., Domaratzki, M. & Cloutier, S. (2019). MicroRNA-guided regulation of heat stress response in wheat. BMC Genom., 20, No. 1, 488. https://doi.org/10.1186/s12864-019-5799-6
74. Al-Ashkar, I., Al-Suhaibani, N., Abdella, K., Sallam, M., Alotaibi, M. & Seleiman, M.F. (2021). Combining genetic and multidimensional analyses to identify interpretive traits related to water shortage tolerance as an indirect selection tool for detecting genotypes of drought tolerance in wheat breeding. Plants, 10, No. 5, 931. https://doi.org/10.3390/plants10050931
75. Hasanuzzaman, M., Bhuyan, M., Zulfiqar, F., Raza, A., Mohsin, S.M., Mahmud, J.A., Fujita, M. & Fotopoulos, V. (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants, 9, No. 8, 681. https://doi.org/10.3390/antiox9080681
76. Wasaya, A., Manzoor, S., Yasir, T.A., Sarwar, N., Mubeen, K., Ismail, I.A., Raza, A., Rehman, A., Hossain, A. & EL Sabagh, A. (2021). Evaluation of fourteen bread wheat (Triticum aestivum L.) genotypes by observing gas exchange parameters, relative water and chlorophyll content, and yield attributes under drought stress. Sustainability, 13, No. 9, 4799. https://doi.org/10.3390/su13094799
77. Al-Ashkar, I., Alderfasi, A., El-Hendawy, S., Al-Suhaibani, N., El-Kafafi, S. & Seleiman, M.F. (2019). Detecting salt tolerance in doubled haploid wheat lines. Agronomy, 9, No. 4, 211. https://doi.org/10.3390/agronomy9040211
78. Ferdous, J., Hussain, S.S. & Shi, B.J. (2015). Role of microRNAs in plant drought tolerance. Plant Biotechnol. J., 13, pp. 293-305. https://doi.org/10.1111/pbi.12318
79. Yin, F., Gao, J., Liu, M., Qin, C., Zhang, W., Yang, A., Xia, M., Zhang, Z., Shen, Y., Lin, H., Luo, C. & Pan, G. (2014). Genomewide analysis of water-stress-responsive microRNA expression profile in tobacco roots. Funct. Int. Genom., 14, No. 2, pp. 319-332. https://doi.org/10.1007/s10142-014-0365-4
80. Jung, I.L., Ryu, M., Cho, S.K., Shah, P., Lee, J.H., Bae, H., Kim, I.G. & Yang, S.W. (2015). Cesium toxicity alters MicroRNA processing and AGO1 expressions in Arabidopsis thaliana. PLoS ONE, 10, No. 5, e0125514. https://doi.org/10.1371/journal.pone.0125514
81. Covarrubias, A.A. & Reyes, J.L. (2010). Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs. Plant, Cell, Environm., 33, No. 4, pp. 481-489. https://doi.org/10.1111/j.1365-3040.2009.02048.x
82. Budak, H., Kantar, M. & Kurtoglu, K.Y. (2015). Drought tolerance in modern and wild wheat. Sci. World J., 548246. https://doi.org/10.1155/2013/548246
83. Ding, Y., Tao, Y. & Zhu, C. (2013). Emerging roles of microRNAs in the mediation of drought stress response in plants. J. Exp. Bot., 64, No. 11, pp. 3077-3086. https://doi.org/10.1093/jxb/ert164
84. Akdogan, G., Tufekci, E.D., Uranbey, S. & Unver, T. (2016). miRNA-based drought regulation in wheat. Funct. Int. Genom., 16, No. 3, pp. 221-233. https://doi.org/10.1007/s10142-015-0452-1
85. Nemati, F., Ghanati, F., Ahmadi Gavlighi, H. & Sharifi, M. (2018). Comparison of sucrose metabolism in wheat seedlings during drought stress and subsequent recovery. Biol. Plant., 62, pp. 595-599. https://doi.org/10.1007/s10535-018-0792-5
86. Kazan, K. (2017). The multitalented mediator25. Front. Plant Sci., 8, 999. https://doi.org/10.3389/fpls.2017.00999
87. Guilfoyle, T.J. & Hagen, G. (2007). Auxin response factors. Curr. Opin. Plant Biol., 10, No. 5, pp. 453-460. https://doi.org/10.1016/j.pbi.2007.08.014
88. Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K. & Shinozaki, K.Y. (2012). NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta, 1819, No. 2, pp. 97-103. https://doi.org/10.1016/j.bbagrm.2011.10.005
89. Zeeshan, M., Lu, M., Sehar, S., Holford, P. & Wu, F. (2020). Comparison of biochemical, anatomical, morphological, and physiological responses to salinity stress in wheat and barley genotypes deferring in salinity tolerance. Agronomy, 10, No. 1, 127. https://doi.org/10.3390/agronomy10010127
90. Parihar, P., Singh, S., Singh, R., Singh, V.P. & Prasad, S.M. (2015). Effect of salinity stress on plants and its tolerance strategies: a review. Environ. Sci. Pollut. Res., 22, No. 6, pp. 4056-4075. https://doi.org/10.1007/s11356-014-3739-1
91. Deinlein, U., Stephan, A.B., Horie, T., Luo, W., Xu, G. & Schroeder, J. (2014). Plant salt-tolerance mechanisms. Trends. Plant Sci., 19, No. 6, pp. 371-379. https://doi.org/10.1016/j.tplants.2014.02.001
92. Hamamoto, S., Horie, T., Hauser, F. Deinlein, U., Schroeder, J.I. & Uozumi, N. (2015). HKT transporters mediate salt stress resistance in plants: from structure and function to the field. Curr. Opin. Biotechnol., 32, pp. 113-120. https://doi.org/10.1016/j.copbio.2014.11.025
93. Islam, W., Waheed, A., Naveed, H. & Zeng, F. (2022). MicroRNAs mediated plant responses to salt stress. Cells, 11, No. 18, 2806. https://doi.org/10.3390/cells11182806
94. Liu, H.H., Tian, X., Li, Y-J., Wu, C-Ai. & Zheng, C.C. (2008). Microarray-based analysis of stressregulated microRNAs in Arabidopsis thaliana. RNA, 14, No. 5, pp. 836-843. https://doi.org/10.1261/rna.895308
95. Eren, H., Pekmezci, M. Y., Okay, S., Turktas, M., Inal, B., Ilhan, E., Atak, M., Erayman, M. & Unver, T. (2015). Hexaploid wheat (Triticum aestivum) root miRNome analysis in response to salt stress. Ann. Appl. Biol., 167, No. 2, pp. 208-216. https://doi.org/10.1111/aab.12219
96. Deng, X., Hu, W., Wei, S., Zhou, S., Zhang, F., Han, J., Chen, L., Li, Y., Feng, J., Fang, B., Luo, Q., Li, S., Liu, Y., Yang, G. & He, G. (2013). TaCIPK29, a CBL-Interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco. PLoS ONE, 8, No. 7, e69881. https://doi.org/10.1371/journal.pone.0069881
97. Schlenker, W. & Roberts, M.J. (2009). Nonlinear temperature effects indicate severe damages to U.S. crop yields under climate change. Proc. Natl. Acad. Sci. USA, 106, No. 37, pp. 15594-15598. https://doi.org/10.1073/pnas.0906865106
98. Hatfield, J.L. & Prueger, J.H. (2015). Temperature extremes: effect on plant growth and development. Weather Clim Extrem., 10, pp. 4-10. https://doi.org/10.1016/j.wace.2015.08.001
99. Bita, C.E. & Gerats, T. (2013). Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stresstolerant crops. Front. Plant Sci., 4, 273. https://doi.org/10.3389/fpls.2013.00273
100. Hasanuzzaman, M., Nahar, K., Alam, M.M., Roychowdhury, R. & Fujita, M. (2013). Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci., 14, No. 5, pp. 9643-9684. https://doi.org/10.3390/ijms14059643
101. Liu, J., Feng, L., Li, J. & He, Z. (2015b). Genetic and epigenetic control of plant heat responses. Front. Plant Sci., 6, 267. https://doi/org/10.3389/fpls.2015.00267 https://doi.org/10.3389/fpls.2015.00267
102. Jiang, S., Lu, Y., Li, K., Lin, L., Zheng, H., Yan, F. & Chen, J. (2014). Heat shock protein 70 is necessary for Rice stripe virus infection in plants. Mol. Plant Pathol., 15, No. 9, pp. 907-917. https://doi.org/10.1111/mpp.12153
103. Zuo, Z-F., He, W., Li, J., Mo, B. & Liu, L. (2021). Small RNAs: The essential regulators in plant thermotolerance. Front. Plant Sci., 12, 726762. https://doi.org/10.3389/fpls.2021.726762
104. Sun, L., Wen, J., Peng, H., Yao, Y., Hu, Z., Ni, Z., Sun, Q. & Xin, M. (2022). The genetic and molecular basis for improving heat stress tolerance in wheat. aBIOTECH, 3, pp. 25-39. https://doi.org/10.1007/s42994-021-00064-z
105. Kumar, D., Singh, D., Kanodia, P., Prabhu, K.V., Kumar, M. & Mukhopadhyay, K. (2014a). Discovery of novel leaf rust responsive microRNAs in wheat and prediction of their target genes. J. Nucleic Acids, 570176. https://doi.org/10.1155/2014/570176
106. Song, J.B., Gao, S., Wang, Y., Li, B.W., Zhang, Y.L. & Yang, Z.M. (2016). miR394 and its target gene LCR are involved in cold stress response in Arabidopsis. Plant Gene, 5, pp. 56-64. https://doi.org/10.1016/j.plgene.2015.12.001
107. Akpinar, B.A. & Budak, H. (2016). Dissecting miRNAs in wheat D genome progenitor, Aegilops tauschii. Front. Plant Sci., 7, pp. 1-17.