Генетические основы компактных форм у бахчевых культур

Генетическая основа компактности у различных сельскохозяйственных культур является областью активных исследований в последние годы. Было выявлено несколько генов, мутации в которых приводят к появлению карликового фенотипа растений. Понимание функций этих генов и механизмов, лежащих в основе карликовости у бахчевых культур, необходимо для разработки новых сортов с повышенной урожайностью и качеством плодов. В настоящей работе приведены актуальные данные о генах, мутации в которых ассоциированы с появлением компактного фенотипа у бахчевых культур, перечислены примеры мутантных компактных фенотипов и связанных с ними генов у таких представителей семейства Cucurbitaceae, как тыква крупноплодная (Cucurbita maxima Duch.), тыква твердокорая (Cucurbita pepo L.), тыква мускатная (Cucurbita moschata Duch.), арбуз (Citrullus lanatus (Thunb.) Matsum. & Nakai), дыня (Cucumis melo L.). В работе представлены современные данные о генетической и молекулярной основах формирования компактного фенотипа, а также молекулярные маркеры для выявления известных генов, связанных с уменьшением размера габитуса растений.

1. Anarjan M.B, Begum S., Bae I., Lee S. Mutation in the GA3ox gene governs short-internode characteristic in a Korean cucumber inbred line. Horticulture Environment and Biotechnology. 2023;64(3):485-495. DOI: 10.1007/s13580-022-00496-6

2. Azpiroz R., Wu Y., Locascio J.C., Feldmann K.A. An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. The Plant Cell. 1998;10(2):219-230. DOI: 10.1105/tpc.10.2.219

3. Bajguz A., Chmur M. Biosynthesis and inactivation of brassinosteroids in plants. In: R. Akula, G. Sirhindi (eds). Jasmonates and Brassinosteroids in Plants: Metabolism, Signaling, and Biotechnological Applications. Boca Raton, FL: CRC Press; 2022. p.1-22. DOI: 10.1201/9781003110651-1

4. Binenbaum J., Weinstain R., Shani E. Gibberellin localization and transport in plants. Trends in Plant Science. 2018;23(5):410-421. DOI: 10.1016/j.tplants.2018.02.005

5. Castorina G., Consonni G. The role of brassinosteroids in controlling plant height in Рoaceae: A genetic perspective. International Journal of Molecular Sciences. 2020;21(4):1191. DOI: 10.3390/ijms21041191

6. Chen Y., Fan X., Song W., Zhang Y., Xu G. Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnology Journal. 2012;10(2):139-149. DOI: 10.1111/j.1467-7652.2011.00637.x

7. Chen Y., Hou M., Liu L., Wu S., Shen Y., Ishiyama K. et al. The maize DWARF1 encodes a gibberellin 3-oxidase and is dual localized to the nucleus and cytosol. Plant Physiology. 2014;166(4):2028-2039. DOI: 10.1104/pp.114.247486

8. Chiang H.H., Hwang I., Goodman H.M. Isolation of the Arabidopsis GA4 locus. The Plant Cell. 1995;7(2):195-201. DOI: 10.1105/tpc.7.2.195

9. Chomkaeo N., Janphen K., Hinlo M., Petchara N., Struss D., Sakulsingharoj C. et al. A mutation in acceptor splice site of GA3ox homolog Cla015407 gene confers a dwarf phenotype in watermelon (Citrullus lanatus L.). Asia-Pacific Journal of Science and Technology. 2023;28(3):13. DOI: 10.14456/apst.2023.48

10. Ding W., Wang Y., Qi C., Luo Y., Wang C., Xu W. et al. Fine mapping identified the gibberellin 2-oxidase gene CpDw leading to a dwarf phenotype in squash (Cucurbita pepo L.). Plant Science. 2021;306:110857. DOI: 10.1016/j.plantsci.2021.110857

11. Dong W., Wu D., Li G., Wu D., Wang Z. Next-generation sequencing from bulked segregant analysis identifies a dwarfism gene in watermelon. Scientific Reports. 2018;8(1):2908. DOI: 10.1038/s41598-018-21293-1

12. Dong W., Wu D., Wang C., Liu Y., Wu D. Characterization of the molecular mechanism underlying the dwarfism of dsh mutant watermelon plants. Plant Science. 2021;313:111074. DOI: 10.1016/j.plantsci.2021.111074

13. Елацкова А.Г. Разнообразие коллекции тыквы и ее наследственный потенциал. Результаты и перспективы селекции. Труды по прикладной ботанике, генетике и селекции. 2019;180(2):77-82. DOI: 10.30901/2227-8834-2019-2-77-82

14. Елацкова А.Г. Выявление и создание исходного материала для селекции раннеспелых кустовых и короткоплетистых сортов мускатной тыквы (Cucurbita moschata Duch. ex Poir). Труды по прикладной ботанике, генетике и селекции. 2021;182(3):143-150. DOI: 10.30901/2227-8834-2021-3-143-150

15. Fagoaga C., Tadeo F.R., Iglesias D.J., Huerta L., Lliso I., Vidal A.M. et al. Engineering of gibberellin levels in citrus by sense and antisense overexpression of a GA 20-oxidase gene modifies plant architecture. Journal of Experimental Botanу. 2007;58(6):1407-1420. DOI: 10.1093/jxb/erm004

16. García-Hurtado N., Carrera E., Ruiz-Rivero O., López-Gresa M.P., Hedden P., Gong F. et al. The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. Journal of Experimental Botany. 2012;63(16):5803-5813. DOI: 10.1093/jxb/ers229

17. Geisler M., Blakeslee J.J., Bouchard R., Lee O.R., Vincenzetti V., Bandyopadhyay A. et al. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. The Plant Journal. 2005;44(2):179-194. DOI: 10.1111/j.1365-313X.2005.02519.x

18. Geisler M., Murphy A.S. The ABC of auxin transport: The role of p-glycoproteins in plant development. FEBS Letters. 2006;580(4):1094-1102. DOI: 10.1016/j.febslet.2005.11.054

19. Hedden P. Gibberellin metabolism and its regulation. Journal of Plant Growth Regulation. 2001;20(4):317-318. DOI: 10.1007/s003440010039

20. Hedden P. The current status of research on gibberellin biosynthesis. Plant and Cell Physiology. 2020;61(11):1832-1849. DOI: 10.1093/pcp/pcaa092

21. Hedden P. The genes of the Green Revolution. Trends in Genetics. 2003;19(1):5-9. DOI: 10.1016/S0168-9525(02)00009-4

22. Hou S., Niu H., Tao Q., Wang S., Gong Z., Li S. et al. A mutant in the CsDET2 gene leads to a systemic brassinosteriod deficiency and super compact phenotype in cucumber (Cucumis sativus L.). Theoretical and Applied Genetics. 2017;130(8):1693-1703. DOI: 10.1007/s00122-017-2919-z

23. Huang J., Tang D., Shen Y., Qin B., Hong L., You A. et al. Activation of gibberellin 2-oxidase 6 decreases active gibberellin levels and creates a dominant semi-dwarf phenotype in rice (Oryza sativa L.). Journal of Genetics and Genomics. 2010;37(1):23-36. DOI: 10.1016/S1673-8527(09)60022-9

24. Hwang J., Oh J., Kim Z., Staub J.E., Chung S.M., Park Y. Fine genetic mapping of a locus controlling short internode length in melon (Cucumis melo L.). Molecular Breeding. 2014;34(3):949-961. DOI: 10.1007/s11032-014-0088-1

25. Itoh H., Ueguchi-Tanaka M., Sentoku N., Kitano H., Matsuoka M., Kobayashi M. Cloning and functional analysis of two gibberellin 3beta-hydroxylase genes that are differently expressed during the growth of rice. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(15):8909-8914. DOI: 10.1073/pnas.141239398

26. Jang Y.J., Yun H.S., Rhee S.J., Seo M., Kim Y., Lee G.P. Exploring molecular markers and candidate genes responsible for watermelon dwarfism. Horticulture Environment and Biotechnology. 2020;61(1):173-182. DOI: 10.1007/s13580-020-00229-7

27. Kawai Y., Ono E., Mizutani M. Evolution and diversity of the 2-oxoglutarate-dependent dioxygenase superfamily in plants. The Plant Journal. 2014;78(2):328-343. DOI: 10.1111/tpj.12479

28. Kwon M., Choe S. Brassinosteroid biosynthesis and dwarf mutants. Journal of Plant Biology. 2005;48(1):1-15. DOI: 10.1007/BF03030559

29. Lange T., Hedden P., Graebe J.E. Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. Proceedings of the National Academy of Sciences of the United States of America. 1994;91(18):8552-8556. DOI: 10.1073/pnas.91.18.8552

30. Li Z., Zhang X., Zhao Y., Li Y., Zhang G., Peng Z. et al. Enhancing auxin accumulation in maize root tips improves root growth and dwarfs plant height. Plant Biotechnology Journal. 2018;16(1):86-99. DOI: 10.1111/pbi.12751

31. Mashilo J., Shimelis H., Ngwepe R.M. Genetic resources of bottle gourd (Lagenaria siceraria (Molina) Standl.] and citron watermelon (Citrullus lanatus var. citroides (L.H. Bailey) Mansf. ex Greb.) – implications for genetic improvement, product development and commercialization: A review. South African Journal of Botany. 2022;145:28-47. DOI: 10.1016/j.sajb.2021.10.013

32. Min Z., Hu X., Han X., Li Y., Li J., Wang D. et al. A novel singlebase mutation in GA3ox confers a Ga-deficient dwarf phenotype in pumpkin (Cucurbita moschata D.). SSRN; 2022. DOI: 10.2139/ssrn.3988095 Available from: https://papers.ssrn.com/sol3/papers.cfm?abstract_id=3988095 [accessed Jan. 17, 2023].

33. Mohr H.C., Sandhu M.S. Inheritance and morphological traits of a double recessive dwarf in watermelon, Citrullus lanatus (Thunb.) Mansf. Journal of the American Society for Horticultural Science. 1975;100(2):135-137. DOI: 10.21273/jashs.100.2.135

34. Mori M., Nomura T., Ooka H., Ishizaka M., Yokota T., Sugimoto K. et al. Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiology. 2002;130(3):1152-1161. DOI: 10.1104/pp.007179

35. Niki T., Nishijima T., Nakayama M., Hisamatsu T., OyamaOkubo N., Yamazaki H. et al. Production of dwarf lettuce by overexpressing a pumpkin gibberellin 20-oxidase gene. Plant Physiology. 2001;126(3):965-972. DOI: 10.1104/pp.126.3.965

36. Noh B. Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. The Plant Cell. 2001;13(11):2441-2454. DOI: 10.1105/tpc.13.11.2441

37. Oikawa T., Koshioka M., Kojima K., Yoshida H., Kawata M. A role of OsGA20ox1, encoding an isoform of gibberellin 20-oxidase, for regulation of plant stature in rice. Plant Molecular Biology. 2004;55(5):687-700. DOI: 10.1007/s11103-004-1692-y

38. Otani M., Meguro S., Gondaira H., Hayashi M., Saito M., Han D.S. et al. Overexpression of the gibberellin 2-oxidase gene from Torenia fournieri induces dwarf phenotypes in the liliaceous monocotyledon Tricyrtis sp. Journal of Plant Physiology. 2013;170(16):1416-1423. DOI: 10.1016/j.jplph.2013.05.002

39. Palme K., Dovzhenko A., Ditengou F.A. Auxin transport and gravitational research: perspectives. Protoplasma. 2006;229(2-4):175-181. DOI: 10.1007/s00709-006-0216-9

40. Paris H.S., Nerson H., Karchi Z. Genelics of internode length in melons. Journal of Heredity. 1984;75(5):403-406. DOI: 10.1093/oxfordjournals.jhered.a109965

41. Qin X., Liu J.H., Zhao W.S., Chen X.J., Guo Z.J., Peng Y.L. Gibberellin 20-oxidase gene OsGA20ox3 regulates plant stature and disease development in rice. Molecular Plant–Microbe Interactions. 2013;26(2):227-239. DOI: 10.1094/MPMI-05-12-0138-R

42. Rieu I., Ruiz-Rivero O., Fernandez-Garcia N., Griffiths J., Powers S.J., Gong F. et al. The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. The Plant Journal. 2008;53(3):488-504. DOI: 10.1111/j.1365-313X.2007.03356.x

43. Sasaki A., Ashikari M., Ueguchi-Tanaka M., Itoh H., Nishimura A., Swapan D. et al. A mutant gibberellin-synthesis gene in rice. Nature. 2002;416(6882):701-702. DOI: 10.1038/416701a

44. Schomburg F.M., Bizzell C.M., Lee D.J., Zeevaart J.A.D., Amasino R.M. Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. The Plant Cell. 2003;15(1):151-163. DOI: 10.1105/tpc.005975

45. Schwechheimer C. Gibberellin signaling in plants – the extended version. Frontiers in Plant Science. 2012;2:107. DOI: 10.3389/fpls.2011.00107

46. Shpak E.D., Berthiaume C.T., Hill E.J., Torii K.U. Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development. 2004;131(7):1491-1501. DOI: 10.1242/dev.01028

47. Spielmeyer W., Ellis M.H., Chandler P.M. Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(13):9043-9048. DOI: 10.1073/pnas.132266399

48. Strygina K.V., Elatskova A.G., Elatskov Yu.A., Tekhanovich G.A., Khlestkina E.K. Analysis of the genes that determine the dwarf form of watermelon Citrullus lanatus (Thunb.) Matsum. & Nakai in the VIR collection. Russian Journal of Genetics. 2022;58(12):1457-1472. DOI: 10.1134/S1022795422120134

49. Sun Y., Zhang H., Fan M., He Y., Guo P. A mutation in the intron splice acceptor site of a GA3ox gene confers dwarf architecture in watermelon (Citrullus lanatus L.). Scientific Reports. 2020;10(1):14915. DOI: 10.1038/s41598-020-71861-7

50. Теханович Г.А., Елацкова А.Г., Елацков Ю.А. Генетические источники для селекции кустовых и короткоплетистых сортов арбуза. Труды по прикладной ботанике, генетике и селекции. 2019;180(2):89-94. DOI: 10.30901/2227-8834-2019-2-89-94

51. Теханович Г.А., Елацкова А.Г., Елацков Ю.А. Исследования Н.И. Вавилова и его влияние на развитие интродукции, изучение коллекции и селекции бахчевых культур. Vavilovia. 2020;2(2):44-57. DOI: 10.30901/2658-3860-2019-2-44-57

52. Thomas S.G., Phillips A.L., Hedden P. Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proceedings of the National Academy of Sciences of the United States of America. 1999;96(8):4698-4703. DOI: 10.1073/pnas.96.8.4698

53. Titapiwatanakun B., Blakeslee J.J., Bandyopadhyay A., Yang H., Mravec J., Sauer M. et al. ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. The Plant Journal. 2009;57(1):27-44. DOI: 10.1111/j.1365-313X.2008.03668.x

54. Titapiwatanakun B., Murphy A.S. Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. Journal of Experimental Botany. 2009;60(4):1093-1107. DOI: 10.1093/jxb/ern240

55. Wang H., Li W., Qin Y., Pan Y., Wang X., Weng Y. et al. The cytochrome P450 gene CsCYP85A1 is a putative candidate for super compact-1 (Scp-1) plant architecture mutation in cucumber (Cucumis sativus L.). Frontiers in Plant Science. 2017;8:266. DOI: 10.3389/fpls.2017.00266

56. Wang Y., Zhao J., Lu W., Deng D. Gibberellin in plant height control: old player, new story. Plant Cell Reports. 2017;36(3):391-398. DOI: 10.1007/s00299-017-2104-5

57. Wei C., Zhu C., Yang L., Zhao W., Ma R., Li H. et al. A point mutation resulting in a 13 bp deletion in the coding sequence of Cldf leads to a GA-deficient dwarf phenotype in watermelon. Horticulture Research. 2019;6(1):132. DOI: 10.1038/s41438-019-0213-8

58. Wu T., Cao J., Qin Z., Du Y.L. Identification of a novel GA-related bush mutant in pumpkin (Cucurbita moschata Duchesne). Pakistan Journal of Botany. 2015;47(4):1359-1366.

59. Wu T., Cao J., Zhang Y. Comparison of antioxidant activities and endogenous hormone levels between bush and vine-type tropical pumpkin (Cucurbita moschata Duchesne). Scientia Horticulturae. 2008;116(1):27-33. DOI: 10.1016/j.scienta.2007.11.003

60. Xiang C., Duan Y., Li H., Ma W., Huang S., Sui X. et al. A high-density EST-SSR-based genetic map and QTL analysis of dwarf trait in Cucurbita pepo L. International Journal of Molecular Sciences. 2018;19(10):3140. DOI: 10.3390/ijms19103140

61. Xu X., Hu Q., Wang J., Wang X., Lou L., Xu J. et al. A 2-bp deletion in the protein kinase domain region of the ERECTAlike receptor kinase gene in cucumber results in short internode phenotype. Plant Science. 2023;327:111536. DOI: 10.1016/j.plantsci.2022.111536

62. Yamaguchi S. Gibberellin metabolism and its regulation. Annual Review of Plant Biology. 2008;59:225-251. DOI: 10.1146/annurev.arplant.59.032607.092804

63. Yang S., Zhang K., Zhu H., Zhang X., Yan W., Xu N. et al. Melon short internode (CmSi) encodes an ERECTA-like receptor kinase regulating stem elongation through auxin signaling. Horticulture Research. 2020;7(1):202. DOI: 10.1038/s41438-020-00426-6

64. Zhang G., Ren Y., Sun H., Guo S., Zhang F., Zhang J. et al. A highdensity genetic map for anchoring genome sequences and identifying QTLs associated with dwarf vine in pumpkin (Cucurbita maxima Duch.). BMC Genomics. 2015;16:1101. DOI: 10.1186/s12864-015-2312-8

65. Zhang M., Song M., Cheng F., Yang Z., Davoudi M., Chen J. et al. Identification of a putative candidate gene encoding 7-dehydrocholesterol reductase involved in brassinosteroids biosynthesis for compact plant architecture in Cucumber (Cucumis sativus L.). Theoretical and Applied Genetics. 2021;134(7):2023-2034. DOI: 10.1007/s00122-021-03802-5

66. Zhang M., Song M., Davoudi M., Cheng F., Yin J., Zha G. et al. The mutation of C-24 reductase, a key enzyme involved in brassinolide biosynthesis, confers a novel compact plant architecture phenotype to cucumber. Theoretical and Applied Genetics. 2022;135(8):2711-2723. DOI: 10.1007/s00122-022-04144-6

67. Zhang T., Liu J., Amanullah S., Ding Z., Cui H., Luan F. et al. Fine mapping of Cla015407 controlling plant height in watermelon. Journal of the American Society for Horticultural Science. 2021;146(3):196-205. DOI: 10.21273/JASHS04934-20

68. Zhang X., Hou X., Liu Y., Zheng L., Yi Q., Zhang H. et al. Maize brachytic2 (br2) suppresses the elongation of lower internodes for excessive auxin accumulation in the intercalary meristem region. BMC Plant Biology. 2019;19(1):589. DOI: 10.1186/s12870-019-2200-5

69. Zhao L., Yang X., Du H.L., Li M.M., Ding F.Q., Lv Q.X. et al. Reduced GA biosynthesis in GmRAV-transgenic tobacco causes the dwarf phenotype. Russian Journal of Plant Physiology. 2016;63(5):690-694. DOI: 10.1134/S1021443716050198

70. Zhu H., Zhang M., Sun S., Yang S., Li J., Li H. et al. A single nucleotide deletion in an ABC transporter gene leads to a dwarf phenotype in watermelon. Frontiers in Plant Science. 2019;10:1399. DOI: 10.3389/fpls.2019.01399