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The study of organelle DNA variability in alloplasmic barley lines in the NGS era

https://doi.org/10.18699/VJ19.589

Abstract

Alloplasmic lines are a suitable model for studying molecular coevolution and interrelations between genetic systems of plant cells. Whole chloroplast (cp) and mitochondrial (mt) genome sequences were obtained by the MiSeq System (Illumina). Organelle DNA samples were prepared from a set of 12 alloplasmic barley lines with different cytoplasms of Hordeum vulgare ssp. spontaneum and H. vulgare ssp. vulgare, as well as from their paternal varieties. A bioinformatic approach for analysis of NGS data obtained on an organellar DNA mix has been developed and verified. A comparative study of Hordeum organelle genomes' variability and disposition of polymorphic loci was conducted. Eight types of chloroplast DNA and 5 types of mitochondrial DNA were distinguished for the barley sample set examined. These results were compared with the previous data of a restriction fragment length polymorphism (RFLP) study of organelle DNAs for the same material. Formerly established data about a field evaluation of alloplasmic barley lines were revised in the light of information about organelle genomes gained after NGS. Totally 17 polymorphic loci were found at exons of chloroplast genomes. Seven of the SNPs were located in the genes of the Ndh complex. The nonsynonymous changes of nucleotides were detected in the matK, rpoCI, ndhK, ndhG and infA genes. Some of the SNPs detected are very similar in codon position and in the type of amino acid substitution to the places where RNA editing can occur. Thus, these results outline new perspectives for the future study of nuclear-cytoplasmic interactions in alloplasmic lines.

About the Authors

M. G. Siniauskaya
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


A. M. Makarevich
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


I. M. Goloenko
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


V. S. Pankratov
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


A. D. Liaudanski
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


N. G. Danilenko
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


N. V. Lukhanina
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


A. M. Shimkevich
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


O. G. Davydenko
Institute of Genetics and Cytology, National Academy of Sciences of Belarus
Belarus
Minsk


References

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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 10.1186/s12864-016-3159-3.

14. Kihara H. Substitution of nucleus and its effects on genome manifestations. Cytologia. 1951;16:177-193. DOI 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. DOI 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. DOI 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. DOI 10.18699/SBB-2018-23.

21. Martin M., Sabater B. Plastid ndh genes in plant evolution. Plant Physiol. Biochem. 2010;48(8):636-645. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 10.1046/j.1365-294X.1999.00545.x.

31. Reboud X., Zeyl C. Organelle inheritance in plants. Heredity. 1994;72: 132-140. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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. DOI 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: 327-332.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. DOI 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. DOI 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. DOI 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. DOI 10.1111/1755-0998.12626.


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