Влияние аллельных вариантов гена Vrn-A1 на длину вегетационного периода у Triticum dicoccoides

Длина (продолжительность) вегетационного периода является одним из ключевых хозяйственно важных признаков зерновых культур. У пшениц основное влияние на него оказывают гены Vrn, контролирующие тип (яровость vs. озимость) и скорость развития растений. В настоящей работе по признаку «тип развития» изучено 137 образцов дикой полбы Triticum dicoccoides (Körn. ex Aschers. et Graebn.) Schweinf., среди которых выявлено 39 яровых. Методом секвенирования у яровых образцов установлены нуклеотидные последовательности промоторной области гена Vrn-A1. Идентифицировано пять аллельных вариантов: Vrn-A1b.1, Vrn-A1b.2, Vrn-A1b.4, Vrn-A1d, Vrn-A1u. Три яровых образца, PI355457, PI190919 и PI560817 T. dicoccoides, содержали одновременно два аллеля гена Vrn-A1: Vrn-A1d и не описанный ранее аллельный вариант, обозначенный авторами как Vrn-A1b.8. Промоторная область этого аллеля имела несколько делеций относительно интактного варианта, одна из ко торых захватывала 8 п. н. VRN-бокса. В контролируемых условиях теплицы у образцов была определена длина вегетационного периода и методом 2B-PLS анализа (two-block partial least squares analysis) оценена связь между аллельными вариантами гена Vrn-A1 и длиной вегетационного периода яровых образцов T. dicoccoides. Коэффициент корреляции (r) между этими признаками составил 0.534. Был рассчитан также коэффициент корреляции между длиной вегетационного периода растений и регионами происхождения образцов (r = 0.478). Показано, что образцы, имеющие одинаковые аллели гена Vrn-A1 и происходящие из одного региона, могут значитель но отличаться между собой по длине вегетационного периода. Наличие фенотипических различий при одина ковом аллельном составе гена Vrn-A1 указывает на вклад иных наследственных факторов, локализованных в геномах этих образцов, что обусловливает их ценность в качестве новых источников генетических ресурсов, способствующих расширению биоразнообразия сортов возделываемых видов пшениц.

1. Afshari-Behbahanizadeh S., Puglisi D., Esposito S., De Vita P. Allelic variations in vernalization (Vrn)genes in Triticum spp. Genes. 2024; 15:251. doi 10.3390/genes15020251

2. Badaeva E.D., Davoyan R.O., Tereshchenko N.A., Lyalina E.V., Zoshchuk S.A., Goncharov N.P. Cytogenetic features of intergeneric amphydiploids and genome-substituted forms of wheat. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2024;28(7):716730. doi 10.18699/VJGB-24-80

3. Chen A., Dubcovsky J. Wheat TILLING mutants show that the vernalization gene Vrn1 downregulates the flowering repressor Vrn2 in leaves but is not essential for flowering. PLoS Genet. 2012;8:e1003134. doi 10.1371/journal.pgen.1003134

4. Chen F., Gao M., Zhang J., Zuo A., Shang X., Cui D. Molecular characterization of vernalization and response genes in bread wheat from the Yellow and Huai Valley of China. BMC Plant Biol. 2013;13:199. doi 10.1186/1471222913199

5. Chepurnov G., Ovchinnikova E., Blinov A., Chikida N., Belousova M., Goncharov N.P. Analysis of the structural organization and expression of the Vrn-D1 gene controlling growth habit (spring vs. winter) in Aegilops tauschii Coss. Plants. 2023;12:3596. doi 10.3390/plants12203596

6. Chhuneja P., Arora J.K., Kaur P., Kaur S., Singh K. Characterization of wild emmer wheat Triticum dicoccoides germplasm for vernalization alleles. J Plant Biochem Biotechnol. 2015;24:249253. doi 10.1007/s1356201402817

7. Chumanova E., Efremova T. Marker-assisted development of wheat lines of the winter cultivar Bezostaya 1 and the effects of interaction between alleles of Vrn-A1L and Vrn-B1 loci on heading time. Cereal Res Commum. 2024;52(4):1287-1298. doi 10.1007/s4297602300478z

8. Distelfeld A., Li C., Dubcovsky J. Regulation of flowering in temperate cereals. Curr Opin Plant Biol. 2009a;12:178-184. doi 10.1016/j.pbi.2008.12.010

9. Distelfeld A., Tranquilli G., Li C., Yan L., Dubcovsky J. Genetic and molecular characterization of the Vrn2 loci in tetraploid wheat. Plant Physiol. 2009b;149:245-257. doi 10.1104/pp.108.129353

10. Dong P., Wei Y.-M., Chen G.-Y., Li W., Wang J.-R., Nevo E., Zheng Y.-L. Sequencerelated amplified polymorphism (SRAP) of wild emmer wheat (Triticum dicoccoides) in Israel and its ecological association. Biochem Syst Ecol. 2010;38(1):111. doi 10.1016/j.bse.2009.12.015

11. Dubcovsky J., Loukoianov A., Fu D., Valarik M., Sanchez A., Yan L. Effect of photoperiod on the regulation of wheat vernalization genes Vrn1 and Vrn2. Plant Mol Biol. 2006;60:469-480. doi 10.1007/s1110300548142

12. Efremova T.T., Chumanova E.V. Stages of growth and development of wheat and their importance in the formation of productivity elements. Pisma v Vavilovskii Zhurnal Genetiki i Selektsii = Letters to Vavilov Journal of Genetics and Breeding. 2023;9(2):5480. doi 10.18699/LettersVJ2023909 (inRussian)

13. Feng K., Nie X., Cui L., Deng P., Wang M., Song W. Genome-wide identification and characterization of salinity stressresponsive miRNAs in wild emmer wheat (Triticum turgidum ssp. dicoccoides). Genes. 2017;8:156. doi 10.3390/genes8060156

14. Flood R.G., Halloran G.M. Genetics and physiology of vernalization response in wheat. Adv Agron. 1986;39:87125. doi 10.1016/S00652113(08)604666

15. Fu D., Szűcs P., Yan L., Helguera M., Skinner J.S., Von Zitzewitz J., Hayes P.M., Dubcovsky J. Large deletions within the first intron in Vrn1 are associated with spring growth habit in barley and wheat.

16. Mol Genet Genomics. 2005;273:5465. doi 10.1007/s004380041095-4

17. Golovnina K.A., Kondratenko E., Blinov A.G., Goncharov N.P. Molecular characterization of vernalization loci Vrn1 in wild and cultivated wheats. BMC Plant Biol. 2010;10:168. doi 10.1186/1471-2229-10-168

18. Goncharov N.P. Genetic resources of wheat related species: the Vrn genes controlling growth habit (spring vs. winter). Euphytica. 1998; 100:371376. doi 10.1023/A:1018323600077

19. Goncharov N.P. Response to vernalization in wheat: its quantitative or qualitative nature. Cereal Res Commun. 2004a;32:323330. doi 10.1007/BF03543317

20. Goncharov N.P. Genetics of growth habit (spring vs. winter) in tetraploid wheats: production and analysis of near-isogenic lines. Hereditas. 2004b;130:125130. doi 10.1111/j.16015223.1999.00125.x

21. Goncharov N.P. Shitova I.P. The inheritance of growth habit in old local varieties and landraces of hexaploid wheat. Russ J Genet. 1999;35(4):386392 Goncharov N.P., Plotnikov K.O., Chepurnov G.Y., Kamenev I.A., Nemtsev B.F., Smolenskaya S.E., Blinov A.G. Global warming and the genetics of wheat type and rate of development. Vestnik Tomskogo Gosudarstvennogo Universiteta. Biologiya = Tomsk State University Journal of Biology. 2025;69:68-75. doi 10.17223/19988591/69/8 (in Russian)

22. Grogan S.M., Brown-Guedira G., Haley S.D., McMaster G.S., Reid S.D., Smith J., Byrne P.F. Allelic variation in developmental genes and effects on winter wheat heading date in the U.S. great plains. PLoS One. 2016;11:e0152852. doi 10.1371/journal.pone.0152852

23. Hemming M.N., Peacock W.J., Dennis E.S., Trevaskis B. Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol. 2008;147:355366. doi 10.1104/pp.108.116418

24. Kamran A., Iqbal M., Spaner D. Flowering time in wheat (Triticum aestivum L.): a key factor for global adaptability. Euphytica. 2014; 197:1-26. doi 10.1007/s10681-014-1075-7

25. Kato K., Mori Y., Beiles A., Nevo E. Geographical variation in heading traits in wild emmer wheat, Triticum dicoccoides. I. Variation in vernalization response and ecological differentiation. Theor Appl Genet. 1997;95:546-552. doi 10.1007/s001220050595

26. Kato K., Tanizoe C., Beiles A., Nevo E. Geographical variation in heading traits in wild emmer wheat, Triticum dicoccoides. II. Variation in heading date and adaptation to diverse ecogeographical conditions. Hereditas. 1998;128(1):3339. doi 10.1111/j.16015223.1998.00033.x

27. Kippes N., Zhu J., Chen A., Vanzetti L., Lukaszewski A., Nishida H., Kato K., Dvorak J., Dubcovsky J. Fine mapping and epistatic interactions of the vernalization gene Vrn-D4 in hexaploid wheat. Mol Gen Genomics. 2014;289:47-62. doi 10.1007/s004380130788y

28. Kippes N., Debernardi J.M., Vasquez-Gross H.A., Akpinar B.A., Budak H., Kato K., Chao S., Akhunov E., Dubcovsky J. Identification of the Vernalization 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia. Proc Natl Acad Sci USA. 2015;112(39):E5401E5410. doi 10.1073/pnas.151488311

29. Kippes N., Chen A., Zhang X., Lukaszewski A.J., Dubcovsky J. Development and characterization of a spring hexaploid wheat line with no functional Vrn2 genes. Theor Appl Genet. 2016;129:1417-1428. doi 10.1007/s0012201627133

30. Kiss T., Horváth Á.D., Cseh A., Berki Z., Balla K., Karsai I. Molecular genetic regulation of the vegetative–generative transition in wheat from an environmental perspective. Ann Bot. 2025;135(4):605628. doi 10.1093/aob/mcae174

31. Konopatskaia I., Vavilova V., Kondratenko E.Ya., Blinov A., Goncharov N.P. Vrn1 genes variability in tetraploid wheat species with a spring growth habit. BMC Plant Biol. 2016;16:244. doi 10.1186/s12870-016-0924-z

32. Lack H.W., Van Slageren M. The discovery, typification and rediscovery of wild emmer wheat, Triticum turgidum subsp. dicoccoides (Poaceae). Willdenowia. 2020;50(2):207-216. doi 10.3372/wi.50.50206

33. Law C.N., Worland A.J. Genetic analysis of some flowering time and adaptive traits in wheat. New Phytol. 1997;137(1):1928. doi 10.1046/j.14698137.1997.00814.x

34. Liang Y., Zhang D.-Y., Ouyang S., Xie J., Wu Q., Wang Z., Cui Y., … Dvorak J., Huo N., Sun Q., Gu Y.-Q., Liu Z. Dynamic evolution of resistance gene analogs in the orthologous genomic regions of powdery mildew resistance gene MlIW170 in Triticum dicoccoides and Aegilops tauschii. Theor Appl Genet. 2015;128:1617-1629. doi 10.1007/s0012201525367

35. Muterko A., Kalendar R., Salina E. Novel alleles of the VERNALIZATION1 genes in wheat are associated with modulation of DNA curvature and flexibility in the promoter region. BMC Plant Biol. 2016;16(Suppl.1):9. doi 10.1186/s12870-015-0691-2

36. Nevo E. Genetic resources of wild emmer, Triticum dicoccoides, for wheat improvement in the third millennium. Isr J Plant Sci. 2001; 49(1):77-92. doi 10.1560/XJQN9T4HVTL3CDXU

37. Novoselskaya-Dragovich A.Yu., Fisenko A.V., Konovalov F.A., Lyapunova O.A., Kudryavtsev A.M., Badaeva E.D., Goncharov N.P. Assessment of genetic diversity of tetraploid wheat Triticum dicoccum Schrank ex Schübl. based on long terminal repeat (LTR) retro transposon integration sites and C-banding analysis. Genet Resour Crop Evol. 2025;72:88198839. doi 10.1007/s10722-025-02487-9

38. Ouyang S., Zhang D., Han J., Zhao X., Cui Y., Song W., Huo N., … Ling H.-Q., Luo M., Gu Y., Sun Q., Liu Z. Fine physical and genetic mapping of powdery mildew resistance gene MlIW172 originating from wild emmer (Triticum dicoccoides). PLoS One. 2014;9:e100160. doi 10.1371/journal.pone.0100160

39. Özkan H., Willcox G., Graner A., Salamini F., Kilian B. Geographic distribution and domestication of wild emmer wheat (Triticum dicoccoides). Genet Resour Crop Evol. 2011;58:1153. doi 10.1007/s10722-010-9581-5

40. Palomino C., Cabrera A. Evaluation of the allelic variations in vernalisation (Vrn1) and photoperiod (PPD1) genes and genetic diversity in a spanish spelt wheat collection. Int J Mol Sci. 2023;24:16041. doi 10.3390/ijms242216041

41. Plotnikov K.O., Klimenko A.I., Ovchinnikova E.S., Lashin S.A., Goncharov N.P. Analysis of the effects of the Vrn1 and Ppd-1 alleles on adaptive and agronomic traits in common wheat (Triticum aestivum L.). Plants. 2024;13:1453. doi 10.3390/plants13111453

42. Qiu L., Liu N., Wang H., Shi X., Li F., Zhang Q., Wang W., Guo W., Hu Z., Li H., Ma J., Sun Q., Xie C. Fine mapping of a powdery mildew resistance gene MlIW39 derived from wild emmer wheat (Triticum turgidum ssp. dicoccoides). Theor Appl Genet. 2021;134: 2469-2479. doi 10.1007/s0012202103836-9

43. Rivera D., Ferrer-Gallego P., Obón C., Alcaraz F., Laguna E., Goncharov N.P., Kislev M. Fossil or non-fossil: a case study in the archaeological wheat Triticum parvicoccum (Poaceae: Triticeae). Genes.2025;16(3):274. doi 10.3390/genes16030274

44. Rohlf F.J., Corti M. Use of two-block partial least-squares to study covariation in shape. Syst Biol. 2000;49:740753. doi 10.1080/106351500750049806

45. Royo C., Dreisigacker S., Soriano J.M., Lopes M.S., Ammar K., Villegas D. Allelic variation at the vernalization response (Vrn-1) and photoperiod sensitivity (Ppd-1) genes and their association with the development of durum wheat landraces and modern cultivars. Front Plant Sci. 2020;11:838. doi 10.3389/fpls.2020.00838

46. Saidou M., Wang C., Alam Md.A., Chen C., Ji W. Genetic analysis of powdery mildew resistance gene using SSR markers in common wheat originated from wild emmer (Triticum dicoccoides Thell). Turkish J Field Crops. 2015;21:10. doi 10.17557/tjfc.83589

47. Sela H., Ezrati S., Ben-Yehuda P., Manisterski J., Akhunov E., Dvorak J., Breiman A., Korol A. Linkage disequilibrium and association analysis of stripe rust resistance in wild emmer wheat (Triticum turgidum ssp. dicoccoides) population in Israel. Theor Appl Genet. 2014;127:24532463. doi 10.1007/s0012201423895

48. Shcherban A., Salina E.A. Evolution of Vrn1 homoeologous loci in allopolyploids of Triticum and their diploid precursors. BMC Plant Biol. 2017;17:188. doi 10.1186/s12870-017-1129-9

49. Shcherban A., Emtseva M., Efremova T. Molecular genetical characterization of vernalization genes Vrn-A1, Vrn-B1 and Vrn-D1 in spring wheat germplasm from Russia and adjacent regions. Cereal Res

50. Commun. 2012a;40:351361. doi 10.1556/CRC.40.2012.3.4

51. Shcherban A., Efremova T., Salina E.A. Identification of a new Vrn-B1 allele using two near isogenic wheat lines with difference in heading time. Mol Breed. 2012b;29:675-685. doi 10.1007/s110320119581-y

52. Shcherban A., Khlestkina E., Efremova T., Salina E.A. The effect of two differentially expressed wheat Vrn-B1 alleles on the heading time is associated with structural variation in the first intron. Genetica. 2013;141(46):133141. doi 10.1007/s107090139712y

53. Shcherban A., Börner A., Salina E.A. Effect of Vrn-1 and Ppd D1 genes on heading time in European bread wheat cultivars. Plant Breed. 2015a;134(1):4955. doi 10.1111/pbr.12223

54. Shcherban A., Strygina K., Salina E.A. Vrn-1 gene-associated prerequisites of spring growth habit in wild tetraploid wheat T. dicoccoides and the diploid A genome species. BMC Plant Biol. 2015b;15:94. doi 10.1186/s128700150473x

55. Smolenskaya S.E., Goncharov N.P. Allelic diversity of the Vrn genes and the control of growth habit and earliness in wheat. Vavi lovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2023;27(8):933946. doi 10.18699/VJGB23108

56. Smolenskaya S.E., Efimov V.M., Kruchinina Y.V., Nemtsev B.F., Chepurnov G.Y., Ovchinnikova Е.Y., Belan I.A., Zuev E.V., Chenxi Zhou, Piskarev V.V., Goncharov N.P. Earliness and morphotypes of common wheat cultivars of Western and Eastern Siberia. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2022;26(7):662-674. doi 10.18699/VJGB-22-81

57. Soresi D., Zappacosta D., Garayalde A., Irigoyen I., Basualdo J., Carrera A. A valuable QTL for Fusarium head blight resistance from Triticum turgidum L. ssp. dicoccoides has a stable expression in durum wheat cultivars. Cereal Res Commun. 2017;45:234247. doi 10.1556/0806.45.2017.007

58. Soresi D., Bagnaresi P., Crescente J.M., Díaz M., Cattivelli L., Vanzetti L., Carrera A. Genetic characterization of a fusarium head blight resistance QTL from Triticum turgidum ssp. dicoccoides. Plant Mol Biol Rep. 2021;39:710726. doi 10.1007/s11105-020-01277-0

59. Stelmakh A.F. Genetic systems regulating flowering response in wheat. Euphytica.1998;100(13):359369. doi 10.1023/A:1018374116006

60. Strejčková B., Mazzucotelli E., Čegan R., Milec Z., Brus J., Çakır E., Mastrangelo A.M., Özkan H., Šafář J. Wild emmer wheat, the progenitor of modern bread wheat, exhibits great diversity in the Ver

61. nalization1 gene. Front Plant Sci. 2023;13:1106164. doi 10.3389/fpls.2022.1106164

62. Takumi S., Koyama K., Fujiwara K., Kobayashi F. Identification of a large deletion in the first intron of the Vrn-D1 locus, associated with loss of vernalization requirement in wild wheat progenitor Aegi lops tauschii Coss. Genes Genet Syst. 2011;86:183195. doi 10.1266/ggs.86.183

63. Trevaskis B., Hemming M.N., Dennis E.S., Peacock W.J. The molecular basis of vernalizationinduced flowering in cereals. Trends Plant Sci. 2007;12:352357. doi 10.1016/j.tplants.2007.06.010

64. Würschum T., Langer S.M., Longin C.F.H., Tucker M.R., Leiser W.L. A three component system incorporating Ppd-D1, copy number variation at Ppd-B1, and numerous small effect quantitative trait

65. loci facilitates adaptation of heading time in winter wheat cultivars of worldwide origin. Plant Cell Environ. 2018;41:1407-1416. doi 10.1111/pce.13167

66. Xue F., Ji W., Wang C., Zhang H., Yang B. High-density mapping and marker development for the powdery mildew resistance gene PmAS846 derived from wild emmer wheat (Triticum turgidum var.

67. dicoccoides). Theor Appl Genet. 2012;124:1549-1560. doi 10.1007/s00122-012-1809-7

68. Yan L., Loukoianov A., Tranquilli G., Helguera M., Fahima T., Dubcovsky J. Positional cloning of the wheat vernalization gene Vrn1 Proc Natl Acad Sci USA. 2003;100:62636268. doi 10.1073/pnas.0937399100

69. Yan L., Helguera M., Kato K., Fukuyama S., Sherman J., Dubcovsky J. Allelic variation at the Vrn1 promoter region in polyploid wheat. Theor Appl Genet. 2004a;109:1677-1686. doi 10.1007/s001220041796-4

70. Yan L., Loukoianov A., Blechl A., Tranquilli G., Ramakrishna W., SanMiguel P., Bennetzen J.L., Echenique V., Dubcovsky J. The wheat Vrn2 gene is a flowering repressor downregulated by vernalization. Science. 2004b;303:16401644. doi 10.1126/science.1094305

71. Yan L., Fu D., Li C., Blechl A., Tranquilli G., Bonafede M., Sanchez A., Valarik M., Yasuda S., Dubcovsky J. The wheat and barley vernali zation gene Vrn3 is an orthologue of FT. Proc Natl Acad Sci USA. 2006;103:1958119586. doi 10.1073/pnas.060714210

72. Zhang B., Guo Y., Fan Q., Li R., Chen D., Zhang X. Characterization and distribution of novel alleles of the vernalization gene Vrn-A1 in Chinese wheat (Triticum aestivum L.) cultivars. Crop J. 2023;11:852862. doi 10.1016/j.cj.2022.10.002

73. Zhang H., Zhang L., Wang C., Wang Y., Zhou X., Lv S., Liu X., Kang Z., Ji W. Molecular mapping and marker development for the Triticum dicoccoides – derived stripe rust resistance gene YrSM139-1B in

74. bread wheat cv. Shaanmai 139. Theor Appl Genet. 2016;129:369376. doi 10.1007/s0012201526337