Аллельное разнообразие генов Vrn и контроль типа и скорости развития у пшениц
https://doi.org/10.18699/VJGB-23-108
Аннотация
Пшеница, являясь одной из трех основных продовольственных культур мира, занимает самый широкий ареал за счет адаптивности к разнообразным условиям возделывания. В обзоре рассматриваются полиморфизм и аллельная изменчивость генов Vrn (от англ. response to vernalization), контролирующих важнейшие адаптационные признаки пшениц – тип (яровость vs. озимость) и скорость развития у диких и возделываемых видов пшениц (род Triticum L.). Суммируется информация об аллельном разнообразии генов Vrn и обсуждается связь полиморфизмов этих генов на молекулярном уровне с их влиянием не только на признак «тип развития (яровость vs. озимость)», но и на признак «скороспелость (длина вегетационного периода яровых растений, ДВП)» у ди-, тетра- и гексаплоидных видов. Предпринята попытка связать полученную информацию о мутациях (полиморфизмах) доминантных аллелей генов Vrn с выраженностью наиболее важного с хозяйственной точки зрения признака «продолжительность ДВП (скороспелость)», которая ранее в обзорах не предпринималась. Рассматривается влияние мутаций (полиморфизмов) в последовательностях рецессивных генов vrn на признак «потребность в яровизации» у озимых форм растений пшениц и выполнена его формализация. Обсуждается эволюция озимости/яровости в роде Triticum. На основе выявленных полиморфизмов построена схема филогенетических взаимодействий аллелей генов Vrn и рассматриваются возможности расширения полиморфизма по доминантным генам Vrn и их аллелям за счет видов-сородичей и редко используемых алелей и перспективы селекции на изменение ДВП (скороспелости) для конкретных зон возделывания.
Об авторах
С. Э. СмоленскаяРоссия
Новосибирск
Н. П. Гончаров
Россия
Новосибирск
Список литературы
1. Adonina I.G., Goncharov N.P., Badaeva E.D., Sergeeva E.M., Petrash N.V., Salina E.A. (GAA)n microsatellite as an indicator of the A genome reorganization during wheat evolution and domestication. Comp. Cytogenet. 2015;9(4):533-547. DOI 10.3897/CompCytogen.v9i4.5120
2. Ausemus E.R., Herrington J.B., Reitz L.P., Worzella W.W. A summary of genetic studies in hexaploid and tetraploid wheats. J. Am. Soc. Agron. 1946;38:1082-1099
3. Barrett B., Bayram M., Kidwell K., Weber W.E. Identifying AFLP and microsatellite markers for vernalization response gene Vrn-B1 in hexaploid wheat using reciprocal mapping populations. Plant Breed. 2002;121(5):400-406. DOI 10.1046/j.1439-0523.2002.732319.x
4. Berezhnaya A., Kiseleva A., Leonova I., Salina E. Allelic variation analysis at the vernalization response and photoperiod genes in Russian wheat varieties identified two novel alleles of Vrn-B3. Biomolecules. 2021;11(12):1897. DOI 10.3390/biom11121897
5. Bonnin I., Rousset M., Madur D., Sourdille P., Dupuits C., Brunel D., Goldringer I. FT genome A and D polymorphisms are associated with the variation of earliness components in hexaploid wheat. Theor. Appl. Genet . 2008;116(3):383-394. DOI 10.1007/s00122-007-0676-0
6. Bulavka N.V. Inheritance of different requirements for vernalization in crossing winter varieties of bread wheat. Trudy po Pri klad noy Botanike, Genetike i Selektsii = Proceedings on Applied Botany, Genetics, and Breeding. 1984;85:37-42 (in Russian)
7. Catalogue of Varieties of Spring Soft Wheat by Genotypes of the Vrn Loci System (Sensitivity to Vernalization). Odessa: Plant Breeding and Genetics Institute, 1987 (in Russian)
8. Chen A., Li C., Hu W., Lau M.Y., Lin H., Rockwell N., Martin S.S., Jernstedt J., Lagarias K., Dubcovsky J. Phytochrome C plays a major role in the acceleration of wheat flowering under long-day photoperiod. Proc. Natl. Acad. Sci. USA. 2014;111(28):10037-10044. DOI 10.1073/pnas.1409795111
9. 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(1): 199. DOI 10.1186/1471-2229-13-199
10. Chen Y., Carver B.F., Wang S., Zhang F., Yan L. Genetic loci associated with stem elongation and winter dormancy release in wheat. Theor. Appl. Genet. 2009;118(5):881-889. DOI 10.1007/s00122-008-0946-5
11. Chen Y., Carver B.F., Wang S., Cao S., Yan L. Genetic regulation of developmental phases in winter wheat. Mol. Breed. 2010;26(4):573- 582. DOI 10.1007/s11032-010-9392-6
12. Chen Z., Cheng X., Chai L., Wang Z., Du D., Wang Z., Bian R., Zhao A., Xin M., Guo W., Hu Z., Peng H., Yao Y., Sun Q., Ni Z. Pleiotropic QTL influencing spikelet number and heading date in common wheat (Triticum aestivum L.). Theor. Appl. Genet. 2020;133(6):1825-1838. DOI 10.1007/s00122-020-03556-6
13. Chepurnov G.Yu., Blinov A.G. Effect of different alleles of the Vrn- A1 gene on the timing of heading in T. monococcum. In: Proceedings the 6th International Conference “Gene Pool and Plant Breeding” (GPB2022), Novosibirsk, November 23–25, 2022. Novosibirsk: Institute of Cytology and Genetics, 2022;206-209 (in Russian)
14. Chepurnov G.Y., Ovchinnikova Е.S., Blinov A., Chikida N.N., Belousova M.Kh., Goncharov N.P. Analysis of structural organization and expression of Vrn-D1 genes that control the growth habit (spring vs. winter) in Aegilops tauschii Coss. Plants. 2023;12(20):3596. DOI 10.3390/plants12203596
15. Chu C.-G., Tan C.T., Yu G.-T., Zhong S., Xu S.S., Yan L. A novel retrotransposon inserted in the dominant Vrn-B1 allele confers spring growth habit in tetraploid wheat (Triticum turgidum L.). G3. 2011;
16. (7):637-645. DOI 10.1534/g3.111.001131
17. Cockram J., Jones H., Leigh F.J., O’Sullivan D., Powell W., Laurie D.A., Greenland A.J. Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. J. Exp. Bot. 2007;58(6):1231-1244. DOI 10.1093/jxb/erm042
18. Dhillon T., Pearce S.P., Stockinger E.J., Distelfeld A., Li C., Knox A.K., Vashegyi I., Vagujfalvi A., Galiba G., Dubcovsky J. Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 connection. Plant Physiol. 2010;153(4):1846-1858. DOI 10.1104/pp.110.159079
19. Díaz A., Zikhali M., Turner A.S., Isaac P., Laurie D.A. Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PloS One. 2012;7(3):e33234. DOI 10.1371/journal.pone.0033234
20. Distelfeld A., Tranquilli G., Li C., Yan L., Dubcovsky J. Genetic and molecular characterization of the VRN2 loci in tetraploid wheat. Plant Physiol. 2009;149(1):245-257. DOI 10.1104/pp.108.129353
21. Dolgushin D.A. World Collection of Wheats against the Background of Vernalization. Moscow: Selkhozgiz Publ., 1935 (in Russian)
22. Dubcovsky J., Lijavetzky D., Appendino L., Tranquilli G. Comparative RFLP mapping of Triticum monococcum genes controlling vernalization requirement. Theor. Appl. Genet. 1998;97(5):968-975. DOI 10.1007/s001220050978
23. Dubcovsky J., Chen C., Yan L. Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol. Breed. 2005;15(4):395-407. DOI 10.1007/s11032-005-0084-6
24. 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(4):469-480. DOI 10.1007/s11103-005-4814-2
25. Efremova T.T., Chumanova E.V., Trubacheeva N.V., Arbuzova V.S., Pershina L.A., Belan I.A. Prevalence of VRN1 locus alleles among spring common wheat cultivars cultivated in Western Siberia. Russ. J. Genet. 2016;52(2):146-153. DOI 10.1134/S102279541601004X
26. 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):54-80. DOI 10.18699/LettersVJ-2023-9-09 (in Russian)
27. Faure S., Higgins J., Turner A., Laurie D.A. The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics. 2007; 176(1):599-609. DOI 10.1534/genetics.106.069500
28. Fayt V.I. Genetic system for the control of differences in vernalization duration in winter wheat. Tsitologiya i Genetika = Cytology and Genetics. 2003;37(5):69-76 (in Russian)
29. Fayt V.I. Genetic control of vernalization requirement duration of winter wheat cultivars. Ekologicheskaya Genetika = Ecological Genetics. 2006a;4(2):29-36 (in Russian)
30. Fayt V.I. Near-isogenic lines on the genes controlling differences in duration of vernalization in winter common wheat. Informatsionnyy Vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeding Scientists. 2006b;10(3):580-587 (in Russian)
31. Fayt V.I., Symonenko L.K., Mokanu N.V., Popova N.V. Chromosomal location of genes for vernalization requirement duration (Vrd ) in winter bread wheat. Russ. J. Genet. 2007;43(2):143-148. DOI 10.1134/S1022795407020081
32. Fayt V.І., Gubich O.Yu., Zelenіna G.A. Differences in the alternate varieties of soft wheat for Vrn-1 genes of development type. Plant Varieties Studying and Protection. 2018;14(2):160-169. DOI 10.21498/2518-1017.14.2.2018.134762 (in Russian)
33. Ferrándiz C., Gu Q., Martienssen R., Yanofsky M.F. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development. 2000;127(4):725-734. DOI 10.1242/dev.127.4.725
34. Flaksberger K.A. Wheat. Moscow; Leningrad: Selkhozgiz Publ., 1938 (in Russian)
35. Flood R.G., Halloran G.M. Genetics and physiology of vernalization response in wheat. Adv. Agron. 1986;39:87-125. DOI 10.1016/S0065-2113(08)60466-6
36. 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 VRN-1 are associated with spring growth habit in barley and wheat. Mol. Gen. Genomics. 2005;273(1):54-65. DOI 10.1007/s00438-004-1095-4
37. Fu Hao, Bohuslavskyi R.L. Inheritance of growth habit in einkorn wheat. Visnik Ukrains’kogo Tovaristva Genetikiv i Selekcioneriv. 2023;20(1-2):24-30. DOI 10.7124/visnyk.utgis.20.1-2.1510
38. Galiba G., Quarrie S.A., Sutka J., Morgounov A., Snape J.W. RFLP mapping of the vernalization (Vrn1) and frost resistance (Fr1) genes on chromosome 5A of wheat. Theor. Appl. Genet. 1995;90(7):1174-1179. DOI 10.1007/BF00222940
39. Genotypes of Accessions of Spring Soft Wheat by Genes Controlling the Habit of Development. Catalog of the World Collection of VIR. Issue 427. Leningrad: VNIIR, 1985 (in Russian)
40. Golovnina K.A., Kondratenko E.Ya., Blinov A.G., Goncharov N.P. Phylogeny of the A genome of wild and cultivated wheat species. Russ. J. Genet. 2009;45(11):1360-1367. DOI 10.1134/S1022795409110106
41. Golovnina K.A., Kondratenko E.Y., Blinov A.G., Goncharov N.P. Molecular characterization of vernalization loci VRN1 in wild and cultivated wheats. BMC Plant Biol. 2010;10(1):168. DOI 10.1186/1471-2229-10-168
42. Goncharov N.P. Genetic resources of wheat related species: The Vrn genes controlling growth habit (spring vs. winter). Euphytica. 1998; 100:371-376. DOI 10.1023/A:1018323600077
43. Goncharov N.P. Genetics of growth habit (spring vs winter) in common wheat: confirmation of the existence of dominant gene Vrn4. Theor. Appl. Genet. 2003;107(4):768-772. DOI 10.1007/s00122-003-1317-x
44. Goncharov N.P. Response to vernalization in wheat: its quantitative or qualitative nature. Cereal Res. Commun. 2004;32(3):323-330. DOI 10.1007/BF03543317
45. Goncharov N.P. Genus Triticum L. taxonomy: the present and the future. Plant Syst. Evol. 2011;295:1-11. DOI 10.1007/s00606-0110480-9
46. Goncharov N.P. Comparative Genetics of Wheats and their Related Species. 2nd edn. Novosibirsk: Acad. Publ. House “Geo”, 2012 (in Russian)
47. Goncharov N.P., Chikida N.N. Genetics of the growth habit in Aegi lops squarrosa L. Genetika (Moscow). 1995;31(3):343-346
48. Goncharov N.P., Gaidalenok R.F. Localization of genes controlling spherical grain and compact ear in Triticum antiquorum Heer ex Udacz. Russ. J. Genet. 2005;41(11):1262-1267. DOI 10.1007/s11177-005-0227-1
49. Goncharov N.P., Goncharov P.L. Methodical Bases of Plant Breeding. 3rd edn. Novosibirsk: Acad. Publ. House “Geo”, 2018 (in Russian)
50. 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):386-392
51. Goncharov N.P., Kondratenko E.Ja., Bannikova S.V., Konova lov A.A., Golovnina K.A. Comparative genetic analysis of diploid naked wheat Triticum sinskajae and the progenitor T. monococcum accession. Russ. J. Genet. 2007;43(11):1248-1256. DOI 10.1134/S1022795407110075
52. Gotoh T. Genetic studies on growth habit of some important spring wheat cultivars in Japan, with special reference to the identification of the spring genes involved. Japan. J. Breed. 1979;29(2):133-145. DOI 10.1270/jsbbs1951.29.133
53. Guo X., Wang Y., Meng L., Liu H., Yang L., Zhou Y., Zhang H. Distribution of the Vrn-D1b allele associated with facultative growth habit in Chinese wheat accessions. Euphytica. 2015;206:1-10. DOI 101007/s10681-015-1440-1
54. Gupalo P.I., Skripchinskiy V.V. Physiology of the Individual Development of Plants. Moscow: Kolos Publ., 1971 (in Russian)
55. International Wheat Genome Sequencing Consortium (IWGSC). Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science. 2018;361(6403):eaar7191. DOI 10.1126/science.aar7191
56. Ivaničová Z., Jakobson I., Reis D., Šafář J., Milec Z., Abrouk M., Doležel J., Järve K., Valárik M. Characterization of new allele influencing flowering time in bread wheat introgressed from Triticum militinae. New Biotechnol. 2016;33(5/B):718-727. DOI 10.1016/j.nbt.2016.01.008
57. Iwaki K., Nakagawa K., Kuno H., Kato K. Ecogeographical differentiation in East Asian wheat, revealed from the geographical variation of growth habit and Vrn genotype. Euphytica. 2000;111(2):137-143. DOI 10.1023/A:1003862401570
58. Iwaki K., Haruna S., Niwa T., Kato K. Adaptation and ecological differentiation in wheat with special reference to geographical variation of growth habit and Vrn genotype. Plant Breed. 2001;120(2):107114. DOI 10.1046/j.1439-0523.2001.00574.x
59. Iwaki K., Nishida J., Yanagisawa T., Yoshida H., Kato K. Genetic analysis of Vrn-B1 for vernalization requirement by using linked dCAPS markers in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 2002;104(4):571-576. DOI 10.1007/s00122-001-0769-0
60. Jin F.F., Wei L. The expression patterns of three VRN genes in common wheat (Triticum aestivum L.) in response to vernalization. Cereal Res. Commun. 2016;44(1):1-12. DOI 10.1556/0806.43.2015.041
61. Kato K. Chromosomal location of the genes for vernalization response, Vrn2 and Vrn4, in common wheat, Triticum aestivum L. Wheat Inf. Serv. 1993;76:53-53
62. Kippes N., Zhu J., Chen A., Vanzetti L., Lukaszewski A., Nishida H., Kato K., Dvorak J., Dubcovsky J. Fine mapping and epistatic interaction of the vernalization gene VRN-D4 in hexaploid wheat. Mol. Genet. Genomics. 2014;289(1):47-62. DOI 10.1007/s00438-0130788-y
63. Kippes N., Debernardi J.M., Vasquez-Gross H.A., Akpinar B.A., Budak H., Kato K., Chaod 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):E5401-E5410. DOI 10.1073/pnas.1514883112
64. 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(7):1417-1428. DOI 10.1007/s00122-016-2713-3
65. Kippes N., Guedira M., Lin L., Alvarez M.A., Brown-Guedira G.L., Dubcovsky J. Single nucleotide polymorphisms in a regulatory site of VRN-A1 first intron are associated with differences in vernalization requirement in winter wheat. Mol. Gen. Genomics. 2018; 293(5):1231-1243. DOI 10.1007/s00438-018-1455-0
66. Kiseleva A.A., Salina E.A. Genetic regulation of common wheat heading time. Russ. J. Genet. 2018;54(4):375-388. DOI 10.1134/S1022795418030067
67. Knott D.R. The inheritance of rust resistance: IV. Monosomic analysis of rust resistance and some other characters in six varieties of wheat including Gabo and Kenya farmer. Can. J. Plant Sci. 1959; 39(2):215-228. DOI 10.4141/cjps59-031
68. Konopatskaia I., Vavilova V., Kondratenko E.Ya., Blinov A., Goncharov N.P. Allelic variation of VRN1 gene in tetraploid wheat species with spring growth habit. BMC Plant Biol. 2016;16(Suppl. 3):244. DOI 10.1186/s12870-016-0924-z
69. Koval S.F., Goncharov N.P. Multiple allelism at VRN1 locus of common wheat. Acta Agr. Hung. 1998;46(2):113-119
70. Krasileva K.V., Vasquez-Gross H.A., Howell T., Bailey P., Paraiso F., Clissold L., Simmonds J., Ramirez-Gonzalez R.H., Wang X., Borrill P., Fosker C., Ayling S., Phillips A.L., Uauy C., Dubcovsky J. Uncovering hidden variation in polyploid wheat. Proc. Natl. Acad. Sci. USA. 2017;114(6):E913-E921. DOI 10.1073/pnas.1619 268114
71. Kumakov V.A. Principles of constructing optimum models (idiot ypes) of plant varieties. Sel’skokhozyaystvennaya Biologiya = Agricultural Biology. 1980;15(2):190-197 (in Russian)
72. Law C.N., Worland A.J., Giorgi B. The genetic control of ear-emergence time by chromosomes 5A and 5D of wheat. Heredity. 1976; 36(1):49-58. DOI 10.1038/hdy.1976.5
73. Li C., Dubcovsky J. Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J. 2008;55(4):543-554. DOI 10.1111/j.1365-313X.2008.03526.x
74. Likhenko I.E., Stasyuk A.I., Shcherban’ A.B., Zyryanova A.F., Likhenko N.I., Salina E.A. Analysis of the allelic variation of the Vrn-1 and Ppd-1 genes in Siberian early and medium early varieties of spring wheat. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2014;18(4/1):691-703 (in Russian)
75. Liu Y., He Z., Appels R., Xia X. Functional markers in wheat: current status and future prospects. Theor. Appl. Genet. 2012;125:1-10. DOI 10.1007/s00122-012-1829-3
76. Lysenko N.S., Kiseleva A.A., Mitrofanova O.P., Potokina E.K. Catalog of the world collection of VIR. Iss. 815. Common wheat. Molecular Testing of Vrn- and Ppd Gene Alleles in Breeding Varie ties Authorized for Use in the Russian Federation. St. Petersburg, 2014 (in Russian)
77. Makhoul M., Chawla H.S., Wittkop B., Stahl A., Voss-Fels K.P., Zetzsche H., Snowdon R.J., Obermeier C. Long-amplicon singlemolecule sequencing reveals novel, trait-associated variants of VERNALIZATION1 homoeologs in hexaploid wheat. Front. Plant Sci. 2022;13:942461. DOI 10.3389/fpls.2022.942461
78. McIntosh R.A. Catalogue of gene symbols for wheat. In: Proceedings of the Fourth International Wheat Genetics Symposium, Held at the University of Missouri, Columbia, Missouri, USA, August 6-11, 1973. Missouri, 1973;893-937
79. McIntosh R.A., Yamazaki Y., Dubcovsky J., Rogers J., Morris C., Appels R., Xia X.C. Catalogue of gene symbols for wheat. 2013. Retrieved from http://www.shigen.nig.ac.jp/wheat/komugi/genes/symbolClassList.jsp (accessed 20 Febr. 2023)
80. Milec Z., Tomková L., Sumíková T., Pánková K. A new multiplex PCR test for the determination of Vrn-B1 alleles in bread wheat (Triticum aestivum L.). Mol. Breed. 2012;30(1):317-323. DOI 10.1007/s11032-011-9621-7
81. Milec Z., Strejčková B., Šafář J. Contemplation on wheat vernalization. Front. Plant Sci. 2023;13:1093792. DOI 10.3389/fpls.2022. 1093792
82. Moiseeva E.A., Goncharov N.P. Genetic control of the spring habit in old local cultivars and landraces of common wheat from Siberia. Russ. J. Genet. 2007;43(4):369-375. DOI 10.1134/S1022795407040035
83. Murai K., Miyamae M., Kato H., Takumi S., Ogihara Y. WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol. 2003;44(12):1255-1265. DOI 10.1093/pcp/pcg171
84. Muterko A. Copy number variation and expression dynamics of the dominant Vernalization-A1a allele in wheat. Plant Mol. Biol. Rep. 2023;1-16. https://doi.org/10.1007/s11105-023-01406-5
85. Muterko A.F., Salina E.A. Analysis of the VERNALIZATION-A1 exon- 4 polymorphism in polyploid wheat. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2017;21(3): 323-333. DOI 10.18699/VJ16.19-o
86. Muterko A., Balashova I., Cockram J., Kalendar R., Sivolap Y. The new wheat vernalization response allele Vrn-D1s is caused by DNA transposon insertion in the first intron. Plant Mol. Biol. Rep. 2015;33:294-303. DOI 10.1007/s11105-014-0750-0
87. 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
88. Nédellec C., Ibanescu L., Bossy R., Sourdille P. WTO, an ontology for wheat traits and phenotypes in scientific publications. Genomics Inform. 2020;18(2): e14. DOI 10.5808/GI.2020.18.2.E14
89. Nishimura K., Moriyama R., Katsura K., Saito H., Takisawa R., Kitajima A., Nakazaki T. The early flowering trait of an emmer wheat accession (Triticum turgidum L. ssp. dicoccum) is associated with the cis-element of the Vrn-A3 locus. Theor. Appl. Genet. 2018;131(10): 2037-2053. DOI 10.1007/s00122-018-3131-5
90. Nishimura K., Handa H., Mori N., Kawaura K., Kitajima A., Nakazaki T. Geographical distribution and adaptive variation of VRN-A3 alleles in worldwide polyploid wheat (Triticum spp.) species collection. Planta. 2021;253(6):132. DOI 10.1007/s00425-021-03646-9
91. Nishiura A., Kitagawa S., Matsumura M., Kazama Y., Abe T., Mizuno N., Nasuda S., Murai K. An early-flowering einkorn wheat mutant with deletions of PHYTOCLOCK 1/LUX ARRHYTHMO and VERNALIZATION 2 exhibits a high level of VERNALIZATION 1 expression induced by vernalization. J. Plant Physiol. 2018;222: 28-38. DOI 10.1016/j.jplph.2018.01.002
92. Preston J.C., Kellogg E.A. Reconstructing the evolutionary history of pa ralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics. 2006;174(1):421-437. DOI 10.1534/genetics.106.057125
93. Pugsley A.T. Genetic studies of phasic development and their application to wheat breeding. In: Proceedings of the Third International Wheat Genetics Symposium, Australian Academy of Science, Canberra (5-9 August, 1968). Canberra: Australian Academy of Science, 1968;288-293
94. Pugsley A.T. A genetic analysis of the spring-winter habit of growth in wheat. Austr. J. Agr. Res. 1971;22(1):21-31. DOI 10.1071/AR9710021
95. Pugsley A.T. Additional genes inhibiting winter habit in wheat. Euphytica. 1972;21(3):547-552. DOI 10.1007/BF00039355
96. Pugsley A.T. The impact of plant physiology on Australian wheat breeding. Euphytica. 1983;32:743-748. https://doi.org/10.1007/BF00042154
97. Rigin B.V., Letifova M.S., Repina T.S. Comparative genetics of maturation rate of plant species of genus Triticum L. Genetika (Mosсow). 1994;30(10):1148-1154
98. Rigin B.V., Zuev E.V., Andreeva A.S., Matvienko I.I., Pyzhenkova Z.S. Comparative analysis of the inheritance of a high development rate in the Rimax and Rico lines of spring bread wheat (Triticum aestivum L.). Trudy po Prikladnoy Botanike, Genetike i Se lek tsii = Proceedings on Applied Botany, Genetics, and Breeding. 2021;182(2): 81-88. DOI 10.30901/2227-8834-2021-2-81-88 (in Russian)
99. 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
100. Santra D.K., Santra M., Allan R.E., Campbell K.G., Kidwell K.K. Genetic and molecular characterization of vernalization genes Vrn-A1, Vrn-B1, and Vrn-D1 in spring wheat germplasm from the Pacific Northwest region of the USA. Plant Breed. 2009;128(6):576-584. DOI 10.1111/j.1439-0523.2009.01681.x
101. Shcherban A.B., Salina E.A. Evolution of VRN-1 homoeologous loci in allopolyploids of Triticum and their diploid precursors. BMC Plant Biol. 2017;17(Suppl. 1):188. DOI 10.1186/s12870-017-1129-9
102. Shcherban A.B., Efremova T.T., Salina E.A. Identification of a new Vrn-B1 allele using two near-isogenic wheat lines with difference in heading time. Mol. Breed. 2012a;29(3):675-685. DOI 10.1007/s11032-011-9581-y
103. Shcherban A.B., Emtseva M.V., Efremova T.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. Commun. 2012b;40(3):351-361. DOI 10.1556/CRC.40.2012.3
104. Shcherban A.B., Khlestkina E.K., Efremova T.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(4-6):133-141. DOI 10.1007/s10709-013-9712-y
105. Shcherban A.B., 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):49-55. DOI 10.1111/pbr.12223
106. Shcherban A.B., Strygina K.V., 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(1):94. DOI 10.1186/s12870-015-0473-x
107. Shcherban A.B., Schichkina A.A., Salina E.A. The occurrence of spring forms in tetraploid Timopheevi wheat is associated with variation in the first intron of the VRN-A1 gene. BMC Plant Biol. 2016;16(3): 107-118. DOI 10.1186/s12870-016-0925-y
108. Shitsukawa N., Ikari C., Shimada S., Kitagawa S., Sakamoto K., Saito H., Ryuto H., Fukunishi N., Abe T., Takumi S., Nasuda S., Murai K. The einkorn wheat (Triticum monococcum) mutant, maintained vegetative phase, is caused by a deletion in the VRN1 gene. Genes Genet. Syst. 2007;82(2):167-170.
109. Singh M.P. Monosomic analysis in wheat. Heredity. 1967;22(4):591596. DOI 10.1038/hdy.1967.72
110. Smith L. Mutant and Linkage Studies in Triticum monococcum and T. aegilopoides. Columbia: University of Missouri, Agricultural Experiment Station, 1939
111. Smolenskaya S.E., Efimov V.М., Kruchinina Yu.V., Nemtsev B.F., Chepurnov G.Yu., Ovchinnikova E.S., Belan I.A., Zuev E.V., Zhou Chenxi, 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 (in Russian)
112. State Register of Selection Achievements Authorized for Use for Production Purposes. Vol. 1. Plant Varieties (official publication). Moscow: Rosinformagrotekh Publ., 2023 (in Russian)
113. Steinfort U., Trevaskis B., Fukai S., Bell K.L., Dreccer M.F. Vernalisation and photoperiod sensitivity in wheat: Impact on canopy development and yield components. Field Crops Res. 2017;201:108-121. DOI 10.1016/j.fcr.2016.10.012
114. Stelmakh A.F. Genetics of the habit of development and duration of the growing season of bread wheats. Selektsiya i Semenovodstvo (Kyiv) = Breeding and Seed Production (Kyiv).1981;48:8-15 (in Rus sian)
115. Stelmakh A.F. Genetic effects of the Vrn1-3 loci and the specific effect of the dominant Vrn3 allele on bread wheat. Tsitologiya i Genetika = Cytology and Genetics. 1987;21(4):278-286 (in Russian)
116. Stelmakh A.F. Geographic distribution of Vrn-genes in landraces and improved varieties of spring bread wheat. Euphytica. 1990;45:113118. DOI 10.1007/BF00033278
117. Stelmakh A.F. Genetic effects of Vrn genes on heading date and agronomic traits in bread wheat. Euphytica. 1993;65:53-60. DOI 10.1007/BF00022199
118. Stelmakh A.F., Avsenin V.I. Alien introgressions of spring habit dominant genes into bread wheat genomes. Euphytica. 1996;89:65-68. DOI 10.1007/BF00015720
119. Stelmakh A., Zolotova N., Fayt V. Genetic analysis of differences in duration vernalization requirement of winter bread wheat. Cereal Res. Commun. 2005;33(4):713-718. DOI 10.1556/CRC.33.2005.2- 3.139
120. Strejčková B., Milec Z., Holušová K., Cápal P., Vojtková T., Čegan R., Šafář J. In-depth sequence analysis of bread wheat VRN1 genes. Int. J. Mol. Sci. 2021;22:12284. DOI 10.3390/ijms222212284
121. 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 VERNALIZATION1 gene. Front. Plant Sci. 2023;13:1106164. DOI 10.3389/fpls.2022.1106164
122. 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 Aegilops tauschii Coss. Genes Genet. Syst. 2011;86(3):183-195. DOI 10.1266/ggs.86.183
123. Tan C., Yan L. Duplicated, deleted and translocated VRN2 genes in hexaploid wheat. Euphytica. 2016;208(2):277-284. DOI 10.1007/s10681-015-1589-7
124. Trevaskis B., Bagnall D.J., Ellis M.H., Peacock W.J., Dennis E.S. MADS box genes control vernalization-induced flowering in cereals. Proc. Natl. Acad. Sci. USA. 2003;100(22):13099-13104. DOI 10.1073/pnas.1635053100
125. Trevaskis B., Hemming M.N., Peacock W.J., Dennis E.S. HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol. 2006;140(4):1397-1405. DOI 10.1104/pp.105.073486
126. Tsunewaki K. Monosomic analysis of synthesized hexaploid wheats. Japan. J. Genet. 1962;37(2):155-168. DOI 10.1266/jjg.37.155
127. Tsunewaki K., Jenkins B.S. Monosomic and conventional gene analysis in common wheat. II. Growth habit and awnedness. Japan. J. Genet. 1961;46(11/12):428-443. DOI 10.1266/jjg.36.428
128. van Beem J., Mohler V., Lukman R., van Ginkel M., William M., Crossa J., Worland A.J. Analysis of genetic factors influencing the deve lopmental rate of globally important CIMMYT wheat cultivars. Crop Sci. 2005;45(5):2113-2119. DOI 10.2135/cropsci2004.0665
129. Würschum T., Boeven P.H., Langer S.M., Longin C.F., Leiser W.L. Multiply to conquer: copy number variations at Ppd-B1 and Vrn- A1 facilitate global adaptation in wheat. BMC Genet. 2015;16:96. https://doi.org/10.1186/s12863-015-0258-0
130. 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(10):6263-6268. DOI 10.1073_ pnas.0937399100
131. 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 down-regulated by vernalization. Science. 2004a;303(5664):1640-1644. DOI 10.1126/science.1094305
132. Yan L., Helguera M., Kato K., Fukuyama S., Sherman J., Dubcovsky J. Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor. Appl. Genet. 2004b;109(8):1677-1686. DOI 10.1007/s00122004-1796-4
133. Yan L., Fu D., Li C., Blechl A., Tranquilli G., Ramakrishna W., SanMeguel P., Bennetzen J.L., Echenique V., Dubcovsky J. The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Acad. Sci. USA. 2006;103(51):19581-19586. DOI 10.1073/pnas.0607142103
134. Zhang B., Wang X., Wang X., Ma L., Wang Z., Zhang X. Molecular characterize ation of a novel vernalization allele Vrn-B1d and its effect on heading time in Chinese wheat (Triticum aestivum L.) landrace Hongchunmai. Mol. Breed. 2018;38(10):127. DOI 10.1007/s11032-018-0870-6
135. Zhang J., Wang Y., Wu S., Yang J., Liu H., Zhou Y. A single nucleotide polymorphism at the Vrn-D1 promoter region in common wheat is associated with vernalization response. Theor. Appl. Genet. 2012; 125(8):1697-1704. DOI 10.1007/s00122-012-1946-z
136. Zhang X., Gao M., Wang S., Chen F., Cui D. Allelic variation at the vernalization and photoperiod sensitivity loci in Chinese winter wheat cultivars (Triticum aestivum L.). Front. Plant Sci. 2015;6:470. DOI 10.3389/fpls.2015.00470
137. Zhang X.K., Xiao Y.G., Zhang Y., Xia X.C., Dubcovsky J., He Z.H. Allelic variation at the vernalization genes Vrn-A1, Vrn-B1, Vrn-D1, and Vrn-B3 in Chinese wheat cultivars and their association with growth habit. Crop Sci. 2008;48(2):458-470. DOI 10.2135/cropsci2007.06.0355
138. Zotova L., Kurishbayev A., Jatayev S., Goncharov N.P., Shamambayeva N., Kashapov A., Nuralov A., Otemissova A., Sereda S., Shvidchenko V., Lopato S., Schramm C., Jenkins C., Soole K., Langridge P., Shavrukov Y. General transcription repressor gene, TaDr1, mediates expressions of TaVrn1 and TaFT1 controlling flowering in bread wheat under drought and slowly dehydration. Front. Genet. 2019;10:63. DOI 10.3389/fgene.2019.00063