Картирование локусов и генов, определяющих время колошения и созревания яровой мягкой пшеницы в условиях длинного дня, и оценка их влияния на урожайность

Продолжительность вегетационного периода оказывает значительное влияние на формирование урожая и является одной из важных характеристик сортов яровой мягкой пшеницы (Triticum aestivum L.). К основным межфазным периодам, влияющим на продолжительность вегетации, относятся время от всходов до колошения и от колошения до созревания. Для выявления генов и локусов, ассоциированных с этими признаками в условиях длинного дня, характерного для Западной Сибири, и оценки их влияния на структуру урожая мы провели картирование QTL с последующей оценкой признаков урожайности у линий, несущих различные аллели генов, определяющих скорость развития. В качестве картирующей популяции мы использовали растения F2, полученные от скрещивания контрастных по скорости развития сортов Обская 2 и Тулун 15. QTL анализ выявил новый локус на длинном плече хромосомы 7B, ассоциированный со временем созревания, и два локуса на хромосоме 2D и коротком плече хромосомы 7B, ассоциированных со временем колошения. Анализ генов, входящих в состав локусов, позволил выявить гены-кандидаты для признака «всходы–созревание», паттерны экспрессии которых соответствовали генам известного регулятора скорости созревания NAM-1. Локализация локусов для признака «всходы–колошение» позволила предположить, что они соответствуют известным генам Ppd-D1 и Vrn-B3. Анализ потомства линий с сочетанием аллелей Ppd-D1a и Vrn-B3a показал, что Ppd-D1a оказывает больший эффект на время колошения, чем Vrn-B3a, а сочетание этих двух аллелей приводит к наиболее раннему колошению, в среднем на пять дней раньше линий с аллелями Ppd-D1b и vrn-B3. Оценка признаков структуры урожая (количество и масса зерен с главного колоса и с растения, масса 1000 зерен) показала, что ген Ppd-D1 ассоциирован со всеми признаками на высоком уровне значимости, при этом в большинстве случаев аллель Ppd-D1a негативно влиял на урожайность. Ген Vrn-B3 влиял на признаки урожайности в меньшей степени по сравнению с Ppd-D1.

1. Alhabbar Z., Islam S., Yang R., Diepeveen D., Anwar M., Balotf S., Sultana N., Maddern R., She M., Zhang J., Ma W., Juhasz A. Associations of NAM-A1 alleles with the onset of senescence and nitrogen use efficiency under Western Australian conditions. Euphytica. 2018a;214(10):180. doi 10.1007/s10681-018-2266-4

2. Alhabbar Z., Yang R., Juhasz A., Xin H., She M., Anwar M., Sultana N., Diepeveen D., Ma W., Islam S. NAM gene allelic composition and its relation to grain-filling duration and nitrogen utilisation efficiency of Australian wheat. PLoS One. 2018b;13(10):e0205448. doi 10.1371/journal.pone.0205448

3. Beales J., Turner A., Griffiths S., Snape J.W., Laurie D.A. A PseudoResponse Regulator is misexpressed in the photoperiod insensitive Ppd-D1 a mutant of wheat (Triticum aestivum L.). Theor Appl Genet. 2007;115(5):721-733. doi 10.1007/s00122-007-0603-4

4. Belan I.A., Rosseeva L.P., Blokhina N.P., Grigoriev Y.P., Mukhina Y.V., Trubacheeva N.V., Pershina L.A. Resource potential of soft spring wheat varieties for the conditions of Western Siberia and Omsk region (analytical review). Agrarnaya Nauka Evro-Severo-Vostoka = Agric Science Euro-North-East. 2021;22(4):449-465. doi 10.30766/2072-9081.2021.22.4.449-465 (in Russian)

5. 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

6. Boden S.A., Cavanagh C., Cullis B.R., Ramm K., Greenwood J., Jean Finnegan E., Trevaskis B., Swain S.M. Ppd-1 is a key regulator of inflorescence architecture and paired spikelet development in wheat. Nat Plants. 2015;1(2):14016. doi 10.1038/nplants.2014.16

7. 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

8. Chen A., Li C., Hu W., Lau M.Y., Lin H., Rockwell N.C., Martin S.S., Jernstedt J.A., Lagarias J.C., 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 charac­ terization of vernalization and response genes in bread wheat from the Yellow and Huai Valley of China. BMC Plant Biol. 2013;13:199. doi 10.1186/1471-2229-13-199

10. Chen S., Wang J., Deng G., Chen L., Cheng X., Xu H., Zhan K. Interactive effects of multiple vernalization (Vrn-1)- and photoperiod (Ppd-1)-related genes on the growth habit of bread wheat and their association with heading and flowering time. BMC Plant Biol. 2018;18(1):374. doi 10.1186/s12870-018-1587-8

11. 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

12. Fu D., Szucs 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 Genet Genomics. 2005;273(1):54-65. doi 10.1007/s00438-004-1095-4

13. Guo Z., Song Y., Zhou R., Ren Z., Jia J. Discovery, evaluation and distribution of haplotypes of the wheat Ppd-D1 gene. New Phytol. 2010;185(3):841-851. doi 10.1111/j.1469-8137.2009.03099.x

14. Hagenblad J., Asplund L., Balfourier F., Ravel C., Leino M.W. Strong presence of the high grain protein content allele of NAM-B1 in Fennoscandian wheat. Theor Appl Genet. 2012;125(8):1677-1686. doi 10.1007/s00122-012-1943-2

15. Huang X.Q., Cloutier S., Lycar L., Radovanovic N., Humphreys D.G., Noll J.S., Somers D.J., Brown P.D. Molecular detection of QTLs for agronomic and quality traits in a doubled haploid population derived from two Canadian wheats (Triticum aestivum L.). Theor Appl Genet. 2006;113(4):753-766. doi 10.1007/s00122-006-0346-7

16. Iqbal M., Shahzad A., Ahmed I. Allelic variation at the Vrn-A1, Vrn-B1, Vrn-D1, Vrn-B3 and Ppd-D1a loci of Pakistani spring wheat cultivars. Electron J Biotechnol. 2011;14(1):1-8. doi 10.2225/vol14-issue1-fulltext-6

17. Kajimura T., Murai K., Takumi S. Distinct genetic regulation of flower­ ing time and grain-filling period based on empirical study of D-genome diversity in synthetic hexaploid wheat lines. Breed Sci. 2011; 61(2):130-141. doi 10.1270/jsbbs.61.130

18. Kamran A., Iqbal M., Navabi A., Randhawa H., Pozniak C., Spaner D. Earliness per se QTLs and their interaction with the photoperiod insensitive allele Ppd-D1a in the Cutler × AC Barrie spring wheat po­ pulation. Theor Appl Genet. 2013;126(8):1965-1976. doi 10.1007/s00122-013-2110-0

19. Kiseleva A.A., Eggi E.E., Koshkin V.A., Sitnikov M.N., Roder M., Salina E.A., Potokina E.K. Detection of genetic determinants that define the difference in photoperiod sensitivity of Triticum aestivum L. near-isogenic lines. Russ J Genet. 2014;50(7):701-711. doi 10.1134/S102279541405007X

20. Kiseleva A.A., Leonova I.N., Ageeva E.V., Likhenko I.E., Salina E.A. Identification of genetic loci for early maturity in spring bread wheat using the association analysis and gene dissection. PeerJ. 2023;11: e16109. doi 10.7717/peerj.16109

21. Kiss T., Balla K., Veisz O., Láng L., Bedő Z., Griffiths S., Isaac P., Karsai I. Allele frequencies in the VRN-A1, VRN-B1 and VRN-D1 vernalization response and PPD-B1 and PPD-D1 photoperiod sensitivity genes, and their effects on heading in a diverse set of wheat cultivars (Triticum aestivum L.). Mol Breed. 2014;34(2):297-310. doi 10.1007/s11032-014-0034-2

22. Kulwal P.L., Roy J.K., Balyan H.S., Gupta P.K. QTL mapping for growth and leaf characters in bread wheat. Plant Sci. 2003;164(2): 267-277. doi 10.1016/S0168-9452(02)00409-0

23. Li C., Lin H., Debernardi J.M., Zhang C., Dubcovsky J. GIGANTEA accelerates wheat heading time through gene interactions converging on FLOWERING LOCUS T1. Plant J. 2024;118(2):519-533. doi 10.1111/tpj.16622

24. Li W.L., Nelson J.C., Chu C.Y., Shi L.H., Huang S.H., Liu D.J. Chromosomal locations and genetic relationships of tiller and spike characters in wheat. Euphytica. 2002;125:357-366. doi 10.1023/A:1016069809977

25. 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 J Genet Breed. 2014;18(4/1):691-703 (in Russian)

26. Lundström M., Leino M.W., Hagenblad J. Evolutionary history of the NAM-B1 gene in wild and domesticated tetraploid wheat. BMC Genet. 2017;18(1):118. doi 10.1186/s12863-017-0566-7

27. Lysenko N.S., Kiseleva A.A., Mitrofanova O.P., Potokina E.K. VIR World Collection Catalogue. Iss. 815. Bread Wheat: Molecular Testing of the Vrn and Ppd Alleles in the Selection Varieties Approved for Use in the Russian Federation. St. Petersburg: VIR Publ., 2014 (in Russian)

28. May L., Van Sanford D.A. Selection for early heading and correlated response in maturity of soft red winter wheat. Crop Sci. 1992;32(1): 47-51. doi 10.2135/cropsci1992.0011183X003200010011x

29. McCartney C.A., Somers D.J., Humphreys D.G., Lukow O., Ames N., Noll J., Cloutier S., McCallum B.D. Mapping quantitative trait loci controlling agronomic traits in the spring wheat cross RL4452 × ‘AC Domain’. Genome. 2005;48(5):870-883. doi 10.1139/G05-055

30. Mester D., Ronin Y., Hu Y., Peng J., Nevo E., Korol A. Efficient multipoint mapping: making use of dominant repulsion-phase markers. Theor Appl Genet. 2003;107(6):1102-1112. doi 10.1007/s00122-003-1305-1

31. Milec Z., Valárik M., Bartoš J., Safář J. Can a late bloomer become an early bird? Tools for flowering time adjustment. Biotechnol Adv. 2014;32(1):200-214. doi 10.1016/j.biotechadv.2013.09.008

32. Mizuno N., Kinoshita M., Kinoshita S., Nishida H., Fujita M., Kato K., Murai K., Nasuda S. Loss-of-function mutations in three homoeo­ logous PHYTOCLOCK 1 genes in common wheat are associated with the extra-early flowering phenotype. PLoS One. 2016;11(10): e0165618. doi 10.1371/journal.pone.0165618

33. Mizuno N., Matsunaka H., Yanaka M., Nakata M., Nakamura K., Nakamaru A., Kiribuchi-Otobe C., Ishikawa G., Chono M., Hatta K., Fujita M., Kobayashi F. Allelic variations of Vrn-1 and Ppd-1 genes in Japanese wheat varieties reveal the genotype-environment interaction for heading time. Breed Sci. 2022;72(5):343-354. doi 10.1270/jsbbs.22017

34. Nishida H., Yoshida T., Kawakami K., Fujita M., Long B., Akashi Y., Laurie D.A., Kato K. Structural variation in the 5′ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time. Mol Breed. 2013;31(1):27-37. doi 10.1007/s11032-012-9765-0

35. Okada T., Jayasinghe J.E.A.R.M., Eckermann P., Watson-Haigh N.S., Warner P., Hendrikse Y., Baes M., … Albertsen M., Wolters P., Fleury D., Baumann U., Whitford R. Effects of Rht-B1 and Ppd-D1 loci on pollinator traits in wheat. Theor Appl Genet. 2019;132(7):1965-1979. doi 10.1007/s00122-019-03329-w

36. 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(22):16041. doi 10.3390/ijms242216041

37. Pearce S., Kippes N., ChenA., Debernardi J.M., Dubcovsky J. RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways. BMC Plant Biol. 2016; 16(1):141. doi 10.1186/s12870-016-0831-3

38. Perez-Lara E., Semagn K., Chen H., Iqbal M., N’Diaye A., Kamran A., Navabi A., Pozniak C., Spaner D. QTLs associated with agronomic traits in the Cutler × AC Barrie spring wheat mapping population using single nucleotide polymorphic markers. PLoS One. 2016;11(8):e0160623. doi 10.1371/journal.pone.0160623

39. Plaschke J., Ganal M.W., Röder M.S. Detection of genetic diversity in closely related bread wheat using microsatellite markers. Theor Appl Genet. 1995;91(6-7):1001-1007. doi 10.1007/BF00223912

40. Ramírez-González R.H., Borrill P., Lang D., Harrington S.A., Brinton J., Venturini L., Davey M., … Sharpe A.G., Paux E., Spannagl M., Bräutigam A., Uauy C. The transcriptional landscape of polyploid wheat. Science. 2018;361(6403):eaar6089. doi 10.1126/science.aar6089

41. Seki M., Chono M., Matsunaka H., Fujita M., Oda S., Kubo K., Kiribuchi-Otobe C., Kojima H., Nishida H., Kato K. Distribution of photoperiod-insensitive alleles Ppd-B1a and Ppd-D1a and their effect on heading time in Japanese wheat cultivars. Breed Sci. 2011;61(4): 405-412. doi 10.1270/jsbbs.61.405

42. 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. 2012;29(3):675-685. doi 10.1007/s11032-011-9581-y

43. Taria S., Arora A., Krishna H., Manjunath K.K., Kumar Sudhir, Singh B., Meena S., Malakondaiah A.C., Kousalya S., Padaria J.C., Singh P.K., Alam B., Kumar Sushil, Arunachalam A. Mapping of the QTLs governing stem-specific weight for stem reserve mobilisation in wheat (Triticum aestivum L.) under combined heat and drought stress. Plant Physiol Rep. 2025. doi 10.1007/s40502-025-00854-3

44. Wang J., Wen W., Hanif M., Xia X., Wang H., Liu S., Liu J., Yang L., Cao S., He Z. TaELF3-1DL, a homolog of ELF3, is associated with heading date in bread wheat. Mol Breed. 2016;36(12):161. doi 10.1007/s11032-016-0585-5

45. WhittalA., Kaviani M., Graf R., Humphreys G., NavabiA.Allelic varia­ tion of vernalization and photoperiod response genes in a diverse set of North American high latitude winter wheat genotypes. PLoS One. 2018;13(8):e0203068. doi 10.1371/journal.pone.0203068

46. Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer, 2016. doi 10.1007/978-3-319-24277-4

47. Wilhelm E.P., Turner A.S., Laurie D.A. Photoperiod insensitive PpdA1a mutations in tetraploid wheat (Triticum durum Desf.). Theor Appl Genet. 2009;118(2):285-294. doi 10.1007/s00122-008-0898-9

48. Worland A.J.J., Börner A., Korzun V., Li W.M.M., Petrovíc S., Sayers E.J.J. The influence of photoperiod genes on the adaptability of European winter wheats. Euphytica. 1998;100(1/3):385-394. doi 10.1023/A:1018327700985

49. Wu Y., Liu J., Hu G., Xue H., Xu H., Zhao C., Qin R., Cui F., Sun H. Functional analysis of the “Green Revolution” gene Photoperiod-1 and its selection trends during bread wheat breeding. Front Plant Sci. 2021;12:745411. doi 10.3389/fpls.2021.745411

50. 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. 2004;109(8):1677-1686. doi 10.1007/s00122-004-1796-4

51. Yan L., Fu D., Li C., Blechl A., Tranquilli G., Bonafede M., Sanchez A., Valarik M., Yasuda S., Dubcovsky J. The wheat and barley ver­ nalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA. 2006;103(51):19581-19586. doi 10.1073/pnas.0607142103

52. Yu M., Chen G.-Y., Pu Z.-E., Zhang L.-Q., Liu D.-C., Lan X.-J., Wei Y.-M., Zheng Y.-L. Quantitative trait locus mapping for growth duration and its timing components in wheat. Mol Breed. 2015; 35(1):44. doi 10.1007/s11032-015-0201-0

53. Zaitseva O.I., Lemesh V.A. Allelic composition in the Vrn-A1, Vrn-B1, and Vrn-B3 genes of double haploid lines of hexaploid triticale. Russ J Genet. 2015;51(7):653-660. doi 10.1134/S1022795415070145

54. 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

55. Zhang Y., Liu W.C., Li J., Wei H.T., Hu X.R., Li Y.J., Lu B.R., Yang W.Y. Distribution and selective effects of Vrn-A1, Vrn-B1, and Vrn-D1 genes in derivative varieties from four cornerstone breeding parents of wheat in China. Agric Sci China. 2010;9(10):1389-1399. doi 10.1016/S1671-2927(09)60230-3

56. Zikhali M., Wingen L.U., Griffiths S. Delimitation of the Earliness per se D1 (Eps-D1) flowering gene to a subtelomeric chromosomal deletion in bread wheat (Triticum aestivum). J Exp Bot. 2016;67(1): 287-299. doi 10.1093/jxb/erv458

57. Zou J., Semagn K., Iqbal M., N’Diaye A., Chen H., Asif M., Navabi A., Perez-Lara E., Pozniak C., Yang R.-C., Randhawa H., Spa­ ner D. Mapping QTLs controlling agronomic traits in the ‘Attila’ × ‘CDC Go’ spring wheat population under organic management using 90K SNP array. Crop Sci. 2017;57(1):365-377. doi 10.2135/cropsci2016.06.0459