Изучение изменчивости ДНК органелл аллоплазматических линий ячменя в эпоху высокопроизводительного секвенирования

Аллоплазматические линии являются подходящей моделью для изучения молекулярной коэволюции и взаимодействий между генетическими системами растительной клетки. C использованием MiSeqSystem (Illumina) были определены полногеномные последовательности ДНК органелл клетки -хлоропластов и митохондрий. ДНК органелл выделена из 12 образцов коллекции аллоплазматических линий ячменя с цитоплазмами Hordeumvulgaressp. spontaneum (H. spontaneum) и H. vulgaressp. vulgare (H. vulgare), а также из сортов ячменя доноров ядра. Разработан и верифицирован подход к анализу результатов NGS смесей хлоропластной и митохондриальной ДНК для сборки новых полных сиквенсов пла-стидных и митохондриальных геномов H. vulgare и H. spontaneum. Проведено сравнительное изучение изменчивости геномов органелл, локализованы полиморфные участки. Выделено восемь типов хпДНК и пять типов мтДНК. Полученная информация сопоставлена с результатами предыдущих исследований этих же линий методом полиморфизма длин рестрикционных фрагментов ДНК органелл. На основании сравнения полногеномных последовательностей хпДНК и мтДНК аллоплазматических линий и сортов доноров ядерных геномов пересмотрены полученные для них ранее данные по формированию признаков, связанных с продуктивностью. Семнадцать полиморфных локусов обнаружено в экзонах пластидных генов. Семь из них расположены в генах Ndh комплекса. Несинонимические замены нуклеотидов идентифицированы в генах matK, rpoCI, ndhK, ndhG, infA. Вероятно, некоторые SNP являются точками, где происходит эдитинг, о чем свидетельствуют позиции замены в кодоне и тип аминокислотной замены. Проведенное исследование открывает новые перспективы для изучения ядерно-цитоплазматических взаимодействий на примере аллоплазматических линий.

1. Batura F.N., Davydenko O.G., Kadyrov M.A. The substitution of cytoplasm in barley varieties and it breeding impact. Doklady AN BSSR = Reports of the Academy of Sciences of the BSSR. 1989; 33(7):657-659. (in Russian)

2. Birky C.W. Uniparental inheritance of organelle genes. Curr. Biol. 2008;18(16):R692-R695. https://doi.org/10.1016/j.cub.2008.06.049.

3. Bolger A.M., Lohse M., Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-2120. https://doi.org/10.1093/bioinformatics/btu170.

4. Clegg M.T., Brown A.N.D., Whitfeld P.R. Chloroplast DNA diversity in wild and cultivated barley: implication for genetic conservation. Genet. Res. 1984;4:339-343. https://doi.org/10.1017/S0016672300026112.

5. Daniell H., Lin C.S., Yu M., Chang W.J. Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 2016;17(1):134. https://doi.org/10.1186/s13059-016-1004-2.

6. Danilenko N.G., Davydenko O.G. Worlds of Organelle Genomes, Minsk: Tekhnalogiya Publ., 2003. (in Russian)

7. Fukasawa H. Nucleus substitution and restoration by means of successive backcrosses in wheat and its related genus Aegilops. Jpn. J. Bot. 1959;17:55-91.

8. Givnish T., Zuluaga A., Spalink D., Soto Gomez M., Lam V.K.Y., Saa-rela J.M., Sass C., Iles W.J.D., de Sousa D.J.L., Leebens-Mack J., Chris Pires J., Zomlefer W.B., Gandolfo M.A., Davis J.I., Stevenson D.W., dePamphilis C., Specht C.D., Graham S.W., Barrett C.F, Ane C. Monocot plastid phylogenomics, timeline, net rates of species diversification, the power of multi-gene analyses, and a functional model for the origin of monocots. Am. J. Bot. 2018;105(11):1888-1910. https://doi.org/10.1002/ajb2.1178.

9. Goloenko I.M., Davydenko O.G., Shimkevich A.M. The disturbance of splitting by nuclear marker genes in allo- and isoplasmic barley lines. Genetika = Genetics (Moscow). 2002;38(7):944-949. (in Russian)

10. Goloenko I.M., Teljatnicova A.A., Davydenko O.G. Some nuclei cytoplasmic combinations of barley substituted lines collection change the productivity characteristics. Barley Genet. Newsl. 2000;30:28-31.

11. Gornicki P., Zhu H., Wang J., Challa G., Zhang Z., Gill B., Li W. The chloroplast view of the evolution of polyploid wheat. New Phytolo-gist. 2014;204(3):704-714. https://doi.org/m.1111/nph.12931.

12. Hein A., Brenner S., Knoop V. Multifarious evolutionary pathways of a nuclear RNA editing factor: disjunctions in coevolution of DOT4 and its chloroplast target rpoC1eU488SL. Genome Biol. Evol. 2019; 11(3):798-813. https://doi.org/10.1093/gbe/evz032.

13. Hisano H., Tsujimura M., Yoshida H., Terachi T., Sato K. Mitochondrial genome sequences from wild and cultivated barley (Hordeum vulgare). BMC Genomics. 2016;17(1):824. https://doi.org/10.1186/s12864-016-3159-3.

14. Kihara H. Substitution of nucleus and its effects on genome manifestations. Cytologia. 1951;16:177-193. https://doi.org/10.1508/cytologia.16.177.

15. Krepak I.M., Davydenko O.G., Triboush S.O., Danilenko N.G. The creation of allo- and isoplasmic barley lines. In: Molecular-Genetic Markers in Plants: Abstracts of Int. Conf. Yalta, Nov. 11-15, 1996. Kiev: Agrarna Nauka Publ., 1996;74. (in Russian)

16. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078-2079. https://doi.org/10.1093/bioinformatics/btp352.

17. Lukhanina N.V., Siniauskaya M.G., Goloenko I.M., Davydenko O.G. Chloroplast microsatellites in barley: the reduction of variability spectrum in cultivated forms. Ekologicheskaya Genetika = Ecological Genetics. 2006;IV(1):17-21. (in Russian)

18. Maan S.S. Specificity of nucleo-cytoplasmic interactions in Triticum and Aegilops species. Wheat Inform. Service. 1979;50:71-79.

19. Maier R., Zeltz P., Kossel H., Bonnard G., Gualberto J., Grienenber-ger J. RNA editing in plant mitochondria and chloroplasts. Plant Mol. Biol. 1996;32(1-2):343-365. https://doi.org/10.1007/BF00039390.

20. Makarevich A., Pankratov O., Sinyavskaya M., Lukhanina N., Shym-kevich A., Liaudansky A., Goloenko I., Danilenko N., Davydenko O. NGS data processing method for the mixture of chloroplast and mitochondrial DNA of barley. In: Systems Biology and Bioinformatics (SBB-2018): The Tenth International Young Scientists School (27-31 Aug. 2018, Novosibirsk, Russia): Abstracts. Novosibirsk, 2018;29. https://doi.org/10.18699/SBB-2018-23.

21. Martin M., Sabater B. Plastid ndh genes in plant evolution. Plant Physiol. Biochem. 2010;48(8):636-645. https://doi.org/10.1016/j.plaphy.2010. 04.009.

22. Milne I., Stephen G., Bayer M., Cock P.J.A., Pritchard L., Cardle L., Shaw P.D., Marshall D. Using Tablet for visual exploration of second-generation sequencing data. Brief. Bioinformatics. 2013;14(2):193-202. https://doi.org/10.1093/bib/bbs012.

23. Mukai Y., Maan S.S., Panayotov I., Tsunewaki K. Comparative studies of the nucleus-cytoplasm hybrids of wheat produced by three research groups. In: Proc. 5th Int. Wheat Genet. Symp. 1978; 1: 282-292.

24. Nakamura Ch., Yamakawa S., Suzuki T. Recovery of normal photosynthesis and respiration in common wheat with Agropyron cytoplasms by telocentric Agropyron chromosomes. Theor. Appl. Genet. 1991;81:514-518. https://doi.org/10.1007/BF00219442.

25. Neale D.B., Saghai-Maroof M.A., Allard R.W., Zhang Q., Jorgensen R.A. Chloroplast DNA diversity in populations of wild and cultivated barley. Genetics. 1988;120(4):1105-1110.

26. Nock C.J., Waters D.L.E., Edwards M.A., Bowen S.G., Rice N., Cor-deiro G.M., Henry R.J. Chloroplast genome sequences from total DNA for plant identification. Plant Biotechnol. J. 2011;9:328-333. https://doi.org/10.1111/j.1467-7652.2010.00558.x.

27. Palilova A.N., Sylkova T.A. Formation of productivity in the new series of alloplasmic wheat lines under the influence of alien cytoplasm. Selskokhozyaistvennaya Biologiya = Agricultural Biology. 1987; 12:3-5. (in Russian)

28. Pankin A., von Korff M. Co-evolution of methods and thoughts in cereal domestication studies: a tale of barley (Hordeum vulgare). Curr. Opin. Plant Biol. 2017;36:15-21. https://doi.org/10.1016/j.pbi.2016.12.001.

29. Peredo E.L., King U.M., Les D.H. The plastid genome of Najas flexilis: adaptation to submersed environments is accompanied by the complete loss of the NDH complex in an aquatic angiosperm. PLoS One. 2013;8(7):e68591. https://doi.org/10.1371/journal.pone.0068591.

30. Provan J., Russell J.R., Booth A., Powell W. Polymorphic chloroplast simple sequence repeat primers for systematic and population studies in the genus Hordeum. Mol. Ecol. 1999;8(3):505-511. https://doi.org/10.1046/j.1365-294X.1999.00545.x.

31. Reboud X., Zeyl C. Organelle inheritance in plants. Heredity. 1994;72: 132-140. https://doi.org/10.1038/hdy.1994.19.

32. Roll-Mecak A., Shin B.S., Dever T.E., Burley S.K. Engaging the ribosome: universal IFs of translation. Trends Biochem. Sci. 2001;26: 705-709.

33. Rumeau D., Peltier G., Cournac L. Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 2007;30(9):1041-1051. https://doi.org/10.1111/j.1365-3040.2007.01675.x.

34. Russell J.R., Booth A., Fuller J.D., Baum M., Ceccarelli S., Grando S., Powell W. Patterns of polymorphism detected in the chloroplast and nuclear genomes of barley landraces sampled from Syria and Iordan. Theor. Appl. Genet. 2003;107(3):413-421. https://doi.org/10.1007/s00122-003-1261-9.

35. Sabater B. Evolution and function of the chloroplast. Current investigations and perspectives. Int. J. Mol. Sci. 2018;19(10):3095.

36. Saisho D., Purugganan M.D. Molecular phylogeography of domesticated barley traces expansion of agriculture in the Old World. Genetics. 2007;177(3):1765-1776. https://doi.org/10.1534/genetics.107.079491.

37. Saski C., Lee S.B., Fjellheim S., Guda C., Jansen R.K., Luo H., Tomkins J., Rognli O.A., Daniell H., Clarke J.L. Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes. Theor. Appl. Genet. 2007;115(4):571-590. https://doi.org/10.1007/s00122-007-0567-4.

38. Shikanai T. Chloroplast NDH: a different enzyme with a structure similar to that of respiratory NADH dehydrogenase. Biochim. Bio-phys. Acta. Bioenergetics. 2016;1857(7):1015-1022. https://doi.org/10.1016/j.bbabio.2015.10.013.

39. Sipahi H., Meydan H., Ozbek K. Genetic variation of barley germ-plasm from Turkey assessed by chloroplast microsatellite markers. Int. J. Biodivers. Conserv. 2013;5(11):775-781. https://doi.org/10.5897/IJBC2013.0613.

40. Sychjova I.M., Aksjonova H.A., Davydenko O.G. The effect of intraspecific cytoplasmic substitution on the frequency of chiasmata and sister chromatid exchanges and on marker gene segregation. In: Lel-ley T. (Ed.). Current Topics in Plant Cytogenetics Related to Plant Improvement. Wien: WUV-Universitatsverlag, 1998;168-174.

41. Takenaka M., Zehrmann A., Verbitskiy D., Hartel B., Brennicke A. RNA editing in plants and its evolution. Annu. Rev. Genet. 2013; 47(13):335-352. https://doi.org/10.1146/annurev-genet-111212-133519.

42. Triboush S.O., Danilenko N.G., Davydenko O.G. Method for isolation of chloroplast DNA and mitochondrial DNA from sunflower. Plant Mol. Biol. Rep. 1998;16:183-189. https://doi.org/10.1023/A:1007487806583.

43. Tsudzuki T., Wakasugi T., Sugiura M. Comparative analysis of RNA editing sites in higher plant chloroplasts. J. Mol. Evol. 2001;53: PMID: 32.pmid: 11675592.

44. Tsunewaki K. (Ed.). Genetic Diversity of the Cytoplasm in Triti-cum and Aegilops. Tokyo: Jpn. Soc. for the Promotion of Science, 1980.

45. Tsunewaki K. Genome-plasmon interactions in wheat. Jpn. J. Genet. 1993;68(1):1-34. https://doi.org/10.1266/jjg.68.1.

46. Tsunewaki K., Mori N., Takumi S. Experimental evolutionary studies on the genetic autonomy of the cytoplasmic genome “plasmon” in the Triticum (wheat)-Aegilops complex. Proc. Natl. Acad. Sci. USA. 2019;116(8):3082-3090. https://doi.org/10.1073/pnas.1817037116.

47. Tsunewaki K., Wang G.-Z., Matsuoka Y. Plasmon analysis of Triticum (wheat) and Aegilops. 2. Characterization and classification of 47 plasmons based on their effects on common wheat phenotype. Genes Genet. Syst. 2002;77(6):409-427. https://doi.org/10.1266/ggs.77.409.

48. Twyford A.D., Ness R.W. Strategies for complete plastid genome sequencing. Mol. Ecol. Resour. 2017;17(5):858-868. https://doi.org/10.1111/1755-0998.12626.