The effect of T. aestivum chromosomes 1A and 1D on fertility of alloplasmic recombinant (H. vulgare)-T. aestivum lines depending on cytonuclear compatibility

The effect of T. aestivum L. chromosomes 1A and 1D on fertility of recombinant bread wheat allolines of the same origin carrying the cytoplasm of barley H. vulgare L. and different levels of cytonuclear compatibility was studied. Alloline L-56 included mainly fully sterile (FS) and partially sterile (PS) plants, alloline L-57 included partially fertile (PF) plants and line L-58 included fertile (F) ones. Analysis of morphobiological traits and pollen painting indicated complete or partial male sterility in plants of allolines L-56 and L-57. To differentiate genotypes with cytonuclear coadaptation and genotypes with cytonuclear incompatibility, PCR analysis of the 18S/5S mitochondrial (mt) repeat was performed. Heteroplasmy (simultaneous presence of barley and wheat mtDNA copies) was found in FS, PS, PF and some F plants, which was associated with a violation of cytonuclear compatibility. Wheattype homoplasmy (hm) was detected in the majority of the fertile plants, which was associated with cytonuclear coadaptation. The allolines used as maternal genotypes were crossed with wheat-rye substitution lines 1R(1A) and 1R(1D). In F1, all plants of PF×1R(1A) and PF×1R(1D) combinations were fertile, and in F2, a segregation close to 3 (fertile) : 1 (sterile) was observed. These results showed for the first time that chromosomes 1A and 1D carry one dominant Rf gene, which controls the restoration of male fertility of bread wheat carrying the cytoplasm of H. vulgare. All plants of F1 combinations FS×1R(1A), FS×1R(1D), PS×1R(1A), PS×1R(1D) were sterile, which indicates that a single dose of genes localized on wheat chromosomes 1A or 1D is not enough to restore male fertility in FS and PS plants. All plants of hybrid combinations F(hm)×1R(1A) and F(hm)×1R(1D) in both F1 and F2 were fertile, that is, fertility of allolines with cytonuclear coadaptation does not depend on wheat chromosomes 1A and 1D. 

1. Aksyonova E., Sinyavskaya M., Danilenko N., Pershina L., Nakamura C., Davydenko O. Heteroplasmy and paternally oriented shift of the organellar DNA composition in barley-wheat hybrids during backcrosses with wheat parents. Genome. 2005;48(5):761-769. DOI 10.1139/g05-049

2. Atienza S.G., Martin A., Peechioni N., Platani C., Cattivelli L. The nuclear-cytoplasmic interaction controls carotenoid content in wheat. Euphytica. 2008;159:325-331. DOI 10.1007/s10681-007-9511-6

3. Badaeva E.D., Pershina L.A., Bil’danova L.L. Cytogenetic analysis of alloplasmic recombinant lines (H. vulgare)-T. aestivum unstable in fertility and viability. Russ. J. Genet. 2006;42(2):140-149. DOI 10.1134/S1022795406020074

4. Barnard-Kubow K.B., McCoy M.A., Galloway L.F. Biparental chloroplast inheritance leads to rescue from cytonuclear incompatibility. New Phytol. 2016;213(3):1466-1476. DOI 10.1111/nph.14222

5. Belan I.A., Rosseeva L.P., Blokhina N.P., Mukhina Y.V., Trubacheeva N.V., Pershina L.A. The use of double haploid lines is an acceleration of breeding process in creating varieties of spring bread wheat. In: Abstracts from the Int. Conf. “Advanced Technologies in Agricultural Production: People, digital, environment (AgroProd 2021)”. Omsk, 2021;128-133 (in Russian)

6. Bohra A., Jha U.C., Adhimoolam P., Bisht D., Sing N.P. Cytoplasmic male sterility (CMS) in hybrid breeding in field crops. Plant Cell Rep. 2016;35(5):967-993. DOI 10.1007/s00299-016-1949-3

7. Buloychik A.A., Voluevich E.A., Mikhno A.M. Genome and plasmon effects on expression of the defeated genes of resistance to brown rust in wheat. Tsitologiya i Genetika = Cytology and Genetics. 2002; 36(2):11-19 (in Russian)

8. Coulthart M.B., Spencer D.F., Gray M.W. Comparative analysis of a recombining-repeat-sequence family in the mitochondrial genomes of wheat (Triticum aestivum L.) and rye (Secale cereale L.). Curr. Genet. 1993;23(3):255-264. DOI 10.1007/BF00351504

9. Crosatti C., Quansah L., Maré C., Giusti L., Roncaglia E., Atienz S.G., Cattivelli L., Fait A. Cytoplasmic genome substitution in wheat affects the nuclear-cytoplasmic cross-talk leading to transcript and metabolite alterations. BMC Genomics. 2013;14:868-889. DOI 10.1186/1471-2164-14-868

10. Current Protocols in Molecular Biology. Greene Publishing Associates. N.Y.: Wiley Interscience, 1987

11. Gupta P.K., Balyan H.S., Gahlaut V., Saripalli G., Pal B., Basnet B.R., Joshi A.K. Hybrid wheat: past, present and future. Theor. Appl. Genet. 2019;132(9):2463-2483. DOI 10.1007/s00122-019-03397-y

12. Hattori N., Kitagawa K., Takumi S., Nakamura C. Mitochondrial DNA heteroplasmy in wheat, Aegilops and their nucleus-cytoplasm hybrids. Genetics. 2002;160(4):1619-1630. DOI 10.1093/genetics/160.4.1619

13. Hohn C.E., Lukaszewski A.J. Engineering the 1BS chromosome arm in wheat to remove the Rf multi locus restoring male fertility in cytoplasms of Aegilops kotschyi, Ae. uniaristata and Ae. mutica. Theor. Appl. Genet. 2016;129(9):1769-1774. DOI 10.1007/s00122-016-2738-7

14. Islam M.S., Studer B., Møller I.M., Asp T. Genetics and biology of cytoplasmic male sterility and its applications in forage and turf grass breeding. Plant Breed. 2014;133(3):299-312. DOI 10.1111/pbr.12155

15. Kawaura K., Saeki A., Masumura T., Morita S., Ogihara Y. Heteroplasmy and expression of mitochondrial genes in alloplasmic and euplasmic wheat. Genes Genet. Syst. 2011;86(4):249-255. DOI 10.1266/ggs.86.249

16. Klimushina M.V., Divashuk M.G., Mokhammed T.A.K., Semenov O.G., Karlov G.I. Analysis of allelic state of genes responsible for baking properties in allocytoplasmic wheat hybrids. Russ. J. Genet. 2013; 49(5):530-538. DOI 10.1134/S1022795413050074

17. Liu C.G., Wu Y.W., Hou H., Zhang C., Zhang Y., McIntosh R.A. Value and utilization of alloplasmic common wheats with Aegilops crassa cytoplasm. Plant Breed. 2002;121(5):407-410. DOI 10.1046/j.1439-0523.2002.755374.x

18. Liu Y., Tang L., Xu Q., Ma D., Zha M., Sun J., Chen W. Experimental and genomic evidence for the indica-type cytoplasmic effect in Oryza sativa L. ssp. japonica. J. Integr. Agric. 2016;15(10):2183- 2191. DOI 10.1016/S2095-3119(15)61190-X

19. Martin A.C., Atienza S.G., Ramírez M.C., Barro F., Martín A. Molecular and cytological characterization of an extra acrocentric chromosome that restores male fertility of wheat in the msH1 CMS system. Theor. Appl. Genet. 2010;121(6):1093-1101. DOI 10.1007/s00122-010-1374-x

20. Noyszewski A.K., Ghavami F., Alnemer L.M., Soltani A., Gu Y.Q., Huo N., Meinhardt S., Penny M.A., Kianian P.M.A., Kianian S.F. Accelerated evolution of the mitochondrial genome in an alloplasmic line of durum wheat. BMC Genomics. 2014;15(1):67. DOI 1471-2164/15/67

21. Pershina L.A., Numerova O.M., Belova L.I., Devyatkina E.P. Biotechnological and cytogenetic aspects of producing new wheat genotypes using hybrids. Euphytica. 1998;100(1-3):239-244. DOI 10.1023/A:1018312408312

22. Pershina L.A., Devyatkina E.P., Trubacheeva N.V., Kravtsova L.A., Dobrovol’skaya O.B. Characterization of fertility restoration in alloplasmic lines derived from hybridization of self-fertilized of spring of barley–wheat (Hordeum vulgare L. × Triticum aestivum L.) amphiploid with common wheat varieties Saratovskaya 29 and Pyrotrix 28. Russ. J. Genet. 2012;48(12):1184-1190. DOI 10.1134/S1022795412120101

23. Pershina L.A., Belova L.I., Trubacheeva N.V., Osadсhaya T.S., Shumny V.K., Belan I.A., Rosseeva L.P., Nemchenko V.V., Abakumov S.N. Alloplasmic recombinant lines (H. vulgare)-T. aestivum with 1RS.1BL translocation: initial genotypes for production of common wheat varieties. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2018;22(5):544-552. DOI 10.18699/VJ18.393]

24. Pershina L., Trubacheeva N., Badaeva E., Belan I., Rosseeva L. Study of androgenic plant families of alloplasmic introgression lines (H. vulgare)–T. aestivum and the use of sister DH lines in breeding. Plants. 2020;9(6):764-816. DOI 10.3390/plants9060764

25. Rafee V.V., Lalitha R., Remadevi A.K., Lekshmi M., Premachandran M.N. Substitution of cytoplasm of sugarcane with that of the wild grass Erianthus arundinaceus. Gregor Mendel Found. J. 2010; 1(1&2):16-22

26. Shchapova A.I., Kravtzova L.A. The production of wheat-rye substitution line by using the Giemsa staining technique. Cereal Res. Commun. 1982;10(1):33-39

27. Sinha P., Tomar S.M., Vinod, Singh V.K., Balyan H.S. Genetic analysis and molecular mapping of a new fertility restorer gene Rf8 for Triticum timopheevi cytoplasm in wheat (Triticum aestivum L.) using SSR markers. Genetica. 2013;141(10-12):431-441. DOI 10.1007/s10709-013-9742-5

28. Soltani A., Kumar A., Mergoum M., Pirseyedi S.M., Hegstad J.B., Mazaheri M., Kianian S.F. Novel nuclear-cytoplasmic interaction in wheat (Triticum aestivum) induces vigorous plants. Funct. Integr. Genom. 2016;16(2):171-182. DOI 10.1007/s10142-016-0475-2

29. Takenaka S., Yamamoto R., Nakamura C. Differential and interactive effects of cytoplasmic substitution and seed aging on submergence stress response in wheat (Triticum aestivum L.). Biotechnol. Biotechnol. Equip. 2019;33(1):75-85. DOI 10.1080/13102818.2018.1549960

30. Talukder S.K., Vara Prasad P.V., Todd T., Babar M.A., Poland J., Bowden R., Fritz A. Effect of cytoplasmic diversity on post anthesis heat tolerance in wheat. Euphytica. 2015;204:383-394. DOI 10.1007/s10681-014-1350-7

31. Tao D., Xu P., Zhou J., Deng X., Li J., Deng W., Yang J., Yang G., Li Q., Hu F. Cytoplasm affects grain weight and filled-grain ratio in indica rice. BMC Genet. 2011;12:53. DOI 10.1186/1471-2156-12-53

32. Trubacheeva N.V., Kravtsova L.A., Devyatkina E.P., Efremova T.T., Sinyavskaya M.G., Shumny V.K., Pershina L.A. Heteroplasmic and homoplasmic states of mitochondrial and chloroplast DNA regions in progenies of distant common wheat hybrids of different origins. Russ. J. Genet. Appl. Res. 2012;2(6):494-500. DOI 10.1134/S20790 59712060147

33. Trubacheeva N.V., Divashuk M.G., Chernook A.G., Belan I.A., Rosseeva L.P., Pershina L.A. The effect of chromosome arm 1BS on the fertility of alloplasmic recombinant lines in bread wheat with the Hordeum vulgare cytoplasm. Plants. 2021;10(6):1120. DOI 10.3390/plants10061120

34. Tsukamoto N., Asakura N., Hattori N., Takumi S., Mori N., Nakamura C. Identification of paternal mitochondrial DNA sequences in the nucleus-cytoplasm hybrid of tetraploidand hexaploid wheat with D and D2 plasmon from Aegilops species. Curr. Genet. 2000; 38(4):208-217. DOI 10.1007/s002940000153

35. Tsunewaki K. Plasmon analysis as the counterpart of genome analysis. In: Jauhar P.P. (Ed.) Methods of Genome Analysis in Plants. Boca Raton: CRC Press, 1996;271-299. http://pi.lib.uchicago.edu/1001/cat/bib/2607056

36. Tsunewaki K. Fine mapping of the first multi fertility restoring gene, Rf multi, of wheat for three Aegilops plasmons, using 1BS 1RS recombinant lines. Theor. Appl. Genet. 2015;128(4):723-732. DOI 10.1007/s00122-015-2467-3

37. Yang J., Zhang M., Yu J. Mitochondrial retrograde regulation tuning fork in nuclear genes expressions of higher plants. J. Genet. Genomics. 2008;35(2):65-71. DOI 10.1016/S1673-8527(08)60010-7

38. Zhang Q., Sodmergen. Why does biparental plastid inheritance revive in angiosperms? J. Plant Res. 2010;123(2):201-206. DOI 10.1007/s10265-009-0291-z