Гены холодоустойчивости плодовых культур

Плодовые культуры – незаменимый источник необходимых нутриентов, макро- и микроэлементов, витаминов, органических кислот, антиоксидантов. Сегодня подавляющая часть предложения на рынке плодов обеспечивается зарубежными производителями. Замещение импорта и удовлетворение запроса населения Российской Федерации на потребление плодов силами отечественного агропромышленного комплекса невозможно без расширения географии посевных площадей, в том числе и в зоны рискованного земледелия, что требует выведения морозостойких (холодоустойчивых) сортов плодовых культур. Применение в селекционной работе современных биотехнологических и молекулярно-генетических методов позволит повысить рентабельность плодоводства за счет снижения сроков получения растений с требуемыми признаками и возможности комплексной оценки перспективности генотипов родительских форм.

В обзоре рассмотрены современные данные по генам устойчивости плодовых и ягодных культур к низким температурам, в том числе охарактеризованы гены, кодирующие ключевые рецепторы, сигнальные, эффекторные белки, факторы транскрипции у яблони, груши, персика, ананаса, земляники. Приведены известные механизмы их работы, активации, регуляции, описаны сигнальные каскады.

1. Акимов М.Ю., Макаров М.Н., Жбанова Е.В. Роль плодов и ягод в обеспечении человека жизненно важными биологически активными веществами. Достижения науки и техники АПК. 2019;33(2):56-60. DOI: 10.24411/0235-2451-2019-10214

2. Artus N.N., Uemura M., Steponkus P.L., Gilmour S.J., Lin C., Thomashow M.F. Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proceedings of the National Academy of Sciences of the United States of America. 1996;93(23):13404-13409. DOI: 10.1073/pnas.93.23.13404

3. Artlip T., McDermaid A., Ma Q., Wisniewski M. Differential gene expression in nontransgenic and transgenic “M.26ˮ apple overexpressing a peach CBF gene during the transition from eco-dormancy to bud break. Horticulture Research. 2019;6:86. DOI: 10.1038/s41438-019-0168-9

4. Baniulis D., Stepulaitiene I., Lukoseviciute V., Blazyte A., Stanys V., Rugienius R., Sasnauskas A. Accumulation of dehydrin-like proteins in pear (Pyrus communis L.) microshoots during cold acclimation. Žemdirbystė=Agriculture. 2012;99(3):293-298. Available from: https://zemdirbyste-agriculture.lt/99(3)tomas/99_3_tomas_str9.pdf [accessed Jun. 23, 2023].

5. Bolt S., Zuther E., Zintl S., Hincha D.K., Schmülling T. ERF105 is a transcription factor gene of Arabidopsis thaliana required for freezing tolerance and cold acclimation. Plant, Cell and Environment. 2016;40(1):108-120. DOI: 10.1111/pce.12838

6. Chai M., Cheng H., Yan M., Priyadarshani S.V.G.N., Zhang M., He Q., Huang Y., Chen F., Liu L., Huang X., Lai L., Chen H., Cai H., Qin Y. Identification and expression analysis of the DREB transcription factor family in pineapple (Ananas comosus (L.) Merr.). PeerJ. 2020;8:e9006. DOI: 10.7717/peerj.9006

7. Chen X., Li S., Zhang D., Han M., Jin X., Zhao C., Wang S., Xing L., Ma J., Ji J., An N. Sequencing of a wild apple (Malus baccata) genome unravels the differences between cultivated and wild apple species regarding disease resistance and cold tolerance. G3: Genes, Genomes, Genetics. 2019;9(7):2051-2060. DOI: 10.1534/g3.119.400245

8. Чиркова Т.В. Физиологические основы устойчивости растений. Санкт-Петербург: СПбГУ; 2002.

9. Чудинова Л.А., Орлова Н.В. Физиология устойчивости растений: учебное пособие к спецкурсу. Пермь; 2006.

10. Ding Y., Li H., Zhang X., Xie Q., Gong Z., Yang S. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Developmental Cell. 2015;32(3):278-289. DOI: 10.1016/j.devcel.2014.12.023

11. Dong M.A., Farre E.M., Thomashow M.F. Circadian CLOCK-ASSOCIATED 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(17):7241-7246. DOI: 10.1073/pnas.1103741108

12. Ерастенкова М.В., Тихонова Н.Г., Ухатова Ю.В. Изучение молекулярных механизмов устойчивости винограда (Vitis vinifera L.) к низкотемпературному стрессу. Биотехнология и селекция растений. [в печати] 2023. DOI: 10.30901/2658-6266-2023-4-o7

13. Eremina M., Unterholzner S.J., Rathnayake A.I., Castellanos M., Khan M., Kugler K.G., May S.T., Mayer K.F., Rozhon W., Poppenberger B. Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants. Proceedings of the National Academy of Sciences of the United States of America. 2016;113(40):E5982-E5991. DOI: 10.1073/pnas.1611477113

14. FAOSTAT. The Food and Agriculture Organization (FAO) of the United Nations. Domains: Production. Items: Aggregated. Fruit primary. Available from: https://www.fao.org/faostat/en/#data/QCL/visualize [accessed Sept. 11, 2023].

15. García Bañuelos M.L., Moreno L.V., Winzerling J., Orozco J.A., Gardea A.A. Winter metabolism in deciduous trees: mechanisms, genes and associated proteins. Revista Fitotecnia Mexicana. 2008;31(4);295-308. DOI: 10.35196/rfm.2008.4.295

16. Garcia-Bañuelos M.L., Gardea A.A, Winzerling J.J., Vazquez-Moreno L. Characterization of a Midwinter-expressed dehydrin (DHN) gene from apple trees (Malus domestica). Plant Molecular Biology Reporter. 2009;(27):476-487. DOI: 10.1007/s11105-009-0110-7

17. Geng J., Wei T., Wang Y., Huang X., Liu J.-H. Overexpression of PtrbHLH, a basic helix-loop-helix transcription factor from Poncirus trifoliata, confers enhanced cold tolerance in pummelo (Citrus grandis) by modulation of H2O2 level via regulating a CAT gene. Tree Physiology. 2019;39(12):2045-2054. DOI: 10.1093/treephys/tpz081

18. Guo C., Zhang J.Q., Peng T., Bao M.Z., Zhang J.W. Structural and expression analyses of three PmCBFs from Prunus mume. Biologia plantarum. 2014;58(2):247-255. DOI: 10.1007/s10535-014-0393-x

19. Guo X., Zhang L., Zhu J., Liu H., Wang A. Cloning and characterization of SiDHN, a novel dehydrin gene from Saussurea involucrata Kar. et Kir. that enhances cold and drought tolerance in tobacco. Plant Science. 2017;256:160-169. DOI: 10.1016/j.plantsci.2016.12.007

20. Huang X., Li K., Jin C., Zhang S. ICE1 of Pyrus ussuriensis functions in cold tolerance by enhancing PuDREBa transcriptional levels through interacting with PuHHP1. Scientific Reports. 2015;5:17620. DOI: 10.1038/srep17620

21. Hwarari D., Guan Y., Ahmad B., Movahedi A., Min T., Hao Z., Lu Y., Chen J., Yang L. ICE-CBF-COR signaling cascade and its regulation in plants responding to cold stress. International Journal of Molecular Sciences. 2022;23(3):1549. DOI: 10.3390/ijms23031549

22. Jiang B., Shi Y., Zhang X., Xin X., Qi L., Guo H., Li J., Yang S. PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America. 2017;114(32):E6695-E6702. DOI: 10.1073/pnas.1706226114

23. Jin C., Huang X.-S., Li K.-Q., Yin H., Li L.-T., Yao Z.-H., Zhang S.-L. Overexpression of a bHLH1 transcription factor of Pyrus ussuriensis confers enhanced cold tolerance and increases expression of stress-responsive genes. Frontiers in Plant Science. 2016;7:441. DOI: 10.3389/fpls.2016.00441

24. Koehler G, Weisel TJ, Randall S. Transcript expression analysis indicates distinct roles for dehydrin subclasses. Current Topics in Phytochemistry. 2007;8:73-83.

25. Koehler G., Wilson R., Goodpaster J.V., Sønsteby A., Lai X., Witzmann F.A., You J.-S., Rohloff J., Randall S.K., Alsheikh-Yousef M. Proteomic study of low temperature responses in strawberry cultivars (Fragaria × ananassa) that differ in cold tolerance. Plant Physiology. 2012;159(4):1787-1805. DOI: 10.1104/pp.112.198267

26. Куликов И.М., Марченко Л.А., Высоцкий В.А. Роль генетических коллекций в инновационном развитии садоводства России. Садоводство и виноградарство. 2016;(5):15-19. DOI: 10.18454/VSTISP.2016.5.3442

27. Lång V.; Palva E.T. The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Molecular Biology. 1992;20:951-962. DOI: 10.1007/BF00027165

28. Li X., Tao S., Wei S., Ming M., Huang X., Zhang S., Wu J. The mining and evolutionary investigation of AP2/ERF genes in pear (Pyrus). BMC Plant Biology. 2018;18:46. DOI: 10.1186/s12870-018-1265-x

29. Liang Y., Wang S., Zhao C., Ma X., Zhao Y., Shao J., Li Y., Li H., Song H., Ma H., Li H., Zhang B., Zhang L. Transcriptional regulation of bark freezing tolerance in apple (Malus domestica Borkh.). Horticulture Research. 2020;7:205. DOI: 10.1038/s41438-020-00432-8

30. Liu Y., Dang P., Liu L. He C. Cold acclimation by the CBF–COR pathway in a changing climate: lessons from Arabidopsis thaliana. Plant Cell Reports. 2019;38:511-519. DOI: 10.1007/s00299-019-02376-3

31. Miura K., Jin J.B., Lee J., Yoo C.Y., Stirm V., Miura T., Ashworth E.N., Bressan R.A., Yun D.J., Hasegawa P.M. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell. 2007;19(4):1403-1414. DOI: 10.1105/tpc.106.048397

32. Николаев М.В. Отклик рискованного земледелия на проявление аномальных погодно-климатических ситуаций в изменяющемся климате. Известия Русского географического общества. 2022;154(3):11-27. DOI: 10.31857/S0869607122030065

33. Novillo F., Medina J., Salinas J. Arabidopsis CBF1 and CBF3 have different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(52):21002-21007. DOI: 10.1073/pnas.0705639105

34. Owens L.C., Thomashow M.F., Hancock J.F., Iezzoni A.F. CBF1 orthologs in sour cherry and strawberry and the heterologous expression of CBF1 in strawberry. Journal of the American Society for Horticultural Science. 2002;127(4):489-494. DOI: 10.21273/JASHS.127.4.489

35. Samarina L.S., Malyukova L.S., Efremov A.M., Simonyan T.A., Matskiv A.O., Koninskaya N.G., Rakhmangulov R.S., Gvasaliya M.V., Malyarovskaya V.I., Ryndin A.V., Orlov Y.L., Tong W., Hanke M.-V. Physiological, biochemical and genetic responses of Caucasian tea (Camellia sinensis (L.) Kuntze) genotypes under cold and frost stress. PeerJ. 2020;8:e9787. DOI: 10.7717/peerj.9787

36. Song G-q., Gao X. Transcriptomic changes reveal gene networks responding to the overexpression of a blueberry DWARF AND DELAYED FLOWERING 1 gene in transgenic blueberry plants. BMC Plant Biology. 2017;17:106. DOI: 10.1186/s12870-017-1053-z

37. Туманов И.И. Физиология закаливания и морозостойкости. Москва: Наука; 1979.

38. Усманов И.Ю., Рахманкулова З.Ф., Кулагин А.Ю. Экологическая физиология растений: учебник. Москва: Логос; 2001.

39. Wang Z.-H., Tian J., Geng W.-J., Qin W., Turdi M. Characterization of CBF1, CBF2, CBF3, and CBF4 genes of Malus sieversii and analysis of their expression in different habitats. European Journal of Horticultural Science. 2017;82(2):81-89. DOI: 10.17660/eJHS.2017/82.2.3

40. Wisniewski M., Artlip T., Norelli J. Dealing with frost damage and climate change in tree fruit crops. New-York Fruit Quarterly. 2016;24(3):25-28.

41. Wisniewski M, Norelli J, Artlip T. Overexpression of a peach CBF gene in apple: a model for understanding the integration of growth, dormancy, and cold hardiness in woody plants. Frontiers in Plant Science. 2015;6:85. DOI: 10.3389/fpls.2015.00085

42. Xie Y., Chen P., Yan Y., Bao C., Li X., Wang L., Shen X., Li H., Liu X., Niu C., Zhu C., Fang N., Shao Y., Zhao T., Yu J., Zhu J., Xu L., Nocker S., Ma F., Guan Q. An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple. New Phytologist. 2018;218:201-218. DOI: 10.1111/nph.14952

43. Xiong L., Schumaker K.S., Zhu J.K. Cell signaling during cold, drought, and salt stress. Plant Cell. 2002;14 Suppl 1:S165-S183. DOI: 10.1105/tpc.000596

44. Yang X., Wang R., Hu Q., Li S., Mao X., Jing H., Zhao J., Hu G., Fu J., Liu C. DlICE1, a stress-responsive gene from Dimocarpus longan, enhances cold tolerance in transgenic Arabidopsis. Plant Physiology and Biochemistry. 2019;142:490-499. DOI: 10.1016/j.plaphy.2019.08.007

45. Yu D.J., Jun S.H., Park J., Kwon J.H., Lee H.J. Transcriptome analysis of genes involved in cold hardiness of peach tree (Prunus persica) shoots during cold acclimation and deacclimation. Genes. 2020;11(6):611. DOI: 10.3390/genes11060611

46. Zaikina E.A., Rumyantsev S.D., Sarvarova E.R., Kuluev B.R. Transcription factor genes involved in plant response to abiotic stress factors. Ecological Genetics. 2019;17(3):47-58. DOI: 10.17816/ecogen17347-58

47. Zalunskaitė I., Rugienius R., Vinskienė J., Bendokas V., Gelvonauskienė D., Stanys V. Expression of COR gene homologues in different plants during cold acclimation. Biologija. 2008;54(1):33-35. DOI: 10.2478/v10054-008-0007-7

48. Zhang B., Ma R., Guo L., Song Z., Yu M. Effects of exogenous salicylic acid on physiological traits and CBF gene expression in peach floral organs under freezing stress. Archives of Biological Sciences. 2017;69(4):585-592. DOI: 10.2298/ABS160816002Z

49. Zhao K., Zhou Y., Ahmad S., Yong X., Xie X., Han Y., Li Y., Sun L., Zhang Q. PmCBFs synthetically affect PmDAM6 by alternative promoter binding and protein complexes towards the dormancy of bud for Prunus mume. Scientific Reports. 2018;8:4527. DOI: 10.1038/s41598-018-22537-w

50. Zhao L., Gong X., Gao J., Dong H., Zhang S., Tao S., Huang X. Transcriptomic and evolutionary analyses of white pear (Pyrus bretschneideri) β-amylase genes reveal their importance for cold and drought stress responses. Gene. 2019;689:102-113. DOI: 10.1016/j.gene.2018.11.092

51. Zhao C., Liu X., He J., Xie Y., Xu Y., Ma F., Guan Q. Apple TIME FOR COFFEE contributes to freezing tolerance by promoting unsaturation of fatty acids. Plant Science. 2021;302:110695. DOI: 10.1016/j.plantsci.2020.110695

52. Zhu X., Li X., Chen W., Lu W., Mao J., Liu T. Molecular cloning, characterization and expression analysis of CpCBF2 gene in harvested papaya fruit under temperature stresses. Electronic Journal of Biotechnology. 2013;16(4):1-1. DOI: 10.2225/vol16-issue4-fulltext-1