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Characterization of γ-Radiation-Induced DNA Polymorphisms in the M1 Population of the Japonica Rice Variety Gaogengnuo by Whole-Genome Resequencing

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Abstract

Radiation has been widely used for rice germplasm innovation. The molecular mechanisms by which radiation induces mutations at the genome level require further investigation. To determine the pattern of DNA polymorphisms induced by radiation in the M1 population, we performed whole-genome sequencing of the rice cultivar Gaogengnuo, which was subjected to two 60Co γ-radiation doses, generating the 300 Gy group and the 400 Gy group (11.2 Gy min–1). A total of 356,314 and 588.414 single nucleotide polymorphisms (SNPs), 73,495 and 95,807 insertion/deletion polymorphisms (InDels), 9075 and 8852 structural variations and 5100 and 4252 copy number variations were identified in the 300 Gy group and 400 Gy group, respectively, based on the Nipponbare genome. Through an integrative analysis of resequencing data, we identified 609,209 SNPs and 67,885 InDels that differed between the 300 Gy and Gaogengnuo groups and 632,745 SNPs and 69,899 InDels that differed between the 400 Gy and Gaogengnuo groups. We also detected 2682 homozygous SNPs and 2988 homozygous InDels that were present in the Gaogengnuo, 300 Gy and 400 Gy groups. Gene Ontology clustering showed that the mutated genes in the 300 Gy and 400 Gy groups were classified into two main categories, molecular function and biological process, suggesting that genes associated with molecular functions and biological processes were susceptible to γ-radiation.

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REFERENCES

  1. Bughio, H.R., Asad, M.A., Arain, M.A., et al., Genetic improvement of an indigenous aromatic variety ‘Jajai 77’ through mutagenesis, Plant Mut.Rep., 2010, vol. 2, no. 2, pp. 40—44.

    Google Scholar 

  2. Chung, H.J. and Liu, Q., Molecular structure and physicochemical properties of potato and bean starches as affected by γ-irradiation, Int. J. Biol. Macromol., 2010, vol. 47, no. 2, pp. 214—222.

    CAS  PubMed  Google Scholar 

  3. Semon, S.F.A., Developments in breeding and techniques within the community plant variety rights fruit sector, Acta. Hortic., 2004, vol. 2, no. 663, pp. 707—711.

    Google Scholar 

  4. Patade, V.Y. and Suprasanna, P., Radiation induced in vitro mutagenesis for sugarcane improvement, Sugar. Tech., 2008, vol. 10, no. 1, pp. 14—19.

    CAS  Google Scholar 

  5. Acquaah, G., Principles of Plant Genetics and Breeding, Wiley, 2012.

    Google Scholar 

  6. Kronenberg, A. and Little, J.B., Molecular characterization of thymidine kinase mutants of human cells induced by densely ionizing radiation, Mutat. Res., 1989, vol. 211, no. 2, pp. 215—224.

    CAS  PubMed  Google Scholar 

  7. Novák, F. J., Afza, R., Van, D. M., et al., Mutation induction by gamma irradiation of in vitro cultured shoot tips of banana and plantain (Musa cvs), Trop. Agric., 1990, vol. 67, no. 1, pp. 21—28.

    Google Scholar 

  8. Bae, C. H., Abe, T., Matsuyama, T., et al., Regulation of chloroplast gene expression is affected in ali, a novel tobacco albino mutant, Ann. Bot., 2001, vol. 88, no. 4, part 1, pp. 545—553.

  9. Lawton-Rauh, A., Robichaux, R.H. and Purugganan, M.D., Diversity and divergence patterns in regulatory genes suggest differential gene flow in recently derived species of the Hawaiian silversword alliance adaptive radiation (Asteraceae), Mol. Ecol., 2007, vol. 16, no. 19, pp. 3995—4013.

    CAS  PubMed  Google Scholar 

  10. Lai, J., Li, R., Xu, X., et al., Genome-wide patterns of genetic variation among elite maize inbred lines, Nat. Genet., 2010, vol. 42, no. 11, pp. 1027—1030.

    CAS  PubMed  Google Scholar 

  11. Lam, H.M., Xu, X., Liu, X., et al., Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection, Nat. Genet., 2010, vol. 42, no. 12, pp. 1053—1061.

    CAS  PubMed  Google Scholar 

  12. Xie, W.B., Feng, Q., Yu, H.H., et al., Parent-independent genotyping for constructing an ultrahigh-density linkage map based on population sequencing, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 23, pp. 10578—10583.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Zheng, L.Y., Guo, X.S., He, B., et al., Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor), Genome Biol., 2011, vol. 12, no. 11, p. R114.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Huang, X., Kurata, N., Wei, X., et al., A map of rice genome variation reveals the origin of cultivated rice, Nature, 2012, vol. 490, no. 7421, pp. 497—501.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. McCouh, S.R., Zhao, K., Wright, M., et al., Development of genome-wide SNP assays for rice, Breed. Sci., 2010, vol. 60, no. 5, pp. 524—535.

    Google Scholar 

  16. Muñoz-Amatriaín, M., Eichten, S.R., Wicker, T., et al., Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome, Genome Biol., 2013, vol. 14, no. 6, p. R58.

    PubMed  PubMed Central  Google Scholar 

  17. DeBolt, S., Copy number variation shapes genome diversity in Arabidopsis over 24 immediate family generational scales, Genome Biol. Evol., 2010, vol. 2, pp. 441—453. https://doi.org/10.1093/gbe/evq033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cheng, Z.X., Lin, C.J., Lin, T.X., et al., Genome-wide analysis of radiation-induced mutations in rice (Oryza sativa L. ssp. indica), Mol. BioSyst., 2014, vol. 10, no. 4, pp. 795—805.

    CAS  PubMed  Google Scholar 

  19. Wallace, J.G., Bradbury, P.J., Zhang, N., et al., Association mapping across numerous traits reveals patterns of functional variation in maize, PLoS Genet, 2014, vol. 10, no. 12. e1004845

    PubMed  PubMed Central  Google Scholar 

  20. Collard, B.C. and Mackill, D.J., Marker-assisted selection: an approach for precision plant breeding in the twenty-first century, Philos. Trans. R. Soc., B, 2008, vol. 363, no. 1491, pp. 557—572.

  21. Ganal, M.W., Altmann, T. and Roder, MS., SNP identification in crop plants, Curr. Opin. Plant Biol., 2009, vol. 2, no. 12, pp. 211—217.

    Google Scholar 

  22. Langridge, P. and Fleury, D., Making the most of ‘omics’ for crop breeding, Trends Biotechnol., 2011, vol. 29, no. 1, pp. 33—40.

    CAS  PubMed  Google Scholar 

  23. Schmid, K.J., Sorensen, T.R., Stracke, R., et al., Large-scale identification and analysis of genome-wide single nucleotide polymorphisms for mapping in Arabidopsis thaliana,Genome Res. 2003, vol. 13, no. 6, pp. 1250—1257.

    PubMed  PubMed Central  Google Scholar 

  24. Feltus, F.A., Wan, J., Schulze, S.R., et al., An SNP resource for rice genetics and breeding based on subspecies indica and japonica genome alignments, Genome Res., 2004, vol. 14, no. 9, pp. 1812—1819.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Ossowski, S., Schneeberger, K., Clark, R.M., et al., Sequencing of natural strains of Arabidopsis thaliana with short reads, Genome Res., 2008, vol. 18, no. 12, pp. 2024—2033.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Gore, M.A., Chia, J.M., Elshire, R.J., et al., A first-generation haplotype map of maize, Science, 2009, vol. 326, no. 5956, pp. 1115—1117.

    CAS  PubMed  Google Scholar 

  27. Clark, R.M., Schweikert, G., Toomajian, C., et al., Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana,Science, 2007, vol. 317, no. 5836, pp. 338—342.

    CAS  PubMed  Google Scholar 

  28. McNally, K.L., Childs, K.L., Bohnert, R., et al., Genome-wide SNP variation reveals relationships among landraces and modern varieties of rice, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, no. 30, pp. 12273—12278.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Huang, X., Wei, X., Sang, T., et al., Genome-wide association studies of 14 agronomic traits in rice landraces, Nat. Genet., 2010, vol. 42, no. 11, pp. 961—967.

    CAS  PubMed  Google Scholar 

  30. Kump, K.L., Bradbury, P.J., Wisser, R.J., et al., Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population, Nat. Genet., 2011, vol. 43, no. 2, pp. 163—168.

    CAS  PubMed  Google Scholar 

  31. Wang, L., Hao, L., Li, X., et al., SNP deserts of Asian cultivated rice: genomic regions under domestication, J. Evol. Biol., 2009, vol. 22, no. 4, pp. 751—761.

    CAS  PubMed  Google Scholar 

  32. Heerwaarden, J. V., Doebley, J., Briggs, W.H., et al., Genetic signals of origin, spread, and introgression in a large sample of maize landraces, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, no. 3, pp. 1088—1092.

    PubMed  Google Scholar 

  33. Zhang, L., Cheng, Z., Qin, R., et al., Identification and characterization of an epi-allele of FIE1 reveals a regulatory linkage between two epigenetic marks in rice, Plant Cell, 2012, vol. 24, no. 11, pp. 4407—4421.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Li, H. and Durbin, R., Fast and accurate short read alignment with Burrows—Wheeler transform, Bioinformatics, 2009, vol. 25, no. 14, pp. 1754—1760.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Li, H., Handsaker, B., Wysoker, A., et al., The sequence alignment/map format and SAMtools, Bioinformatics., 2009, vol. 25, no. 16, pp. 2078—2079.

    PubMed  PubMed Central  Google Scholar 

  36. Chen, K., Wallis, J.W., McLellan, M.D., et al., Break Dancer: an algorithm for high-resolution mapping of genomic structural variation, Nat. Methods, 2009, vol. 6, no. 9, pp. 677—681.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Abyzov, A., Urban, A.E., Snyder M., and Gerstein, M., CNVnator: an approach to discover, genotype, and characterize typical and atypical CNVs from family and population genome sequencing, Genome Res., 2011, vol. 6, no. 21, pp. 974—984.

    Google Scholar 

  38. Wang, K., Li, M., and Hakonarson, H., ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data, Nucleic. Acids. Res., 2010, vol. 16, no. 38. e164.

    Google Scholar 

  39. Krzywinski, M., Schein, J., Birol, I., et al., Circos: an information aesthetic for comparative genomics, Genome Res., 2009, vol. 9, no. 19, pp. 1639—1645.

    Google Scholar 

  40. Cheng, W., Liu, F., Li, M., et al., Variation detection based on next-generation sequencing of type Chinese 1 strains of Toxoplasma gondii with different virulence from China, BMC Genomics, 2015, vol. 16, no. 888, pp. 1—9.

    Google Scholar 

  41. Young, M.D., Wakefield, M.J., Smyth, G.K., and Oshlack, A., Gene ontology analysis for RNA-seq: accounting for selection bias, Genome Biol., 2010, vol. 11, no. 2, p. R58.

    Google Scholar 

  42. Subbaiyan, G.K., Waters, D.L., Katiyar, S.K., et al., Genome-wide DNA polymorphisms in elite indica rice inbreds discovered by whole genome sequencing, Plant Biotechnol., 2011, vol. 10, no. 6, pp. 623—634.

    Google Scholar 

  43. Jain, M., Moharana, K.C., Shankar, R., et al., Genome-wide discovery of DNA polymorphisms in rice cultivars with contrasting drought and salinity stress response and their functional relevance, Plant Biotechnol., 2014, vol. 12, no. 2, pp. 253—264.

    CAS  Google Scholar 

  44. Fu, C.Y., Liu, W.G., Liu, D.L., et al., Genome-wide DNA polymorphism in the indica rice varieties RGD-7S and Taifeng B as revealed by whole genome re-sequencing, Genome, 2016, vol. 32, no. 59, pp. 197—207.

    Google Scholar 

  45. Yu, P., Wang, C., Xu, Q., et al., Detection of copy number variations in rice using array based comparative genomic hybridization, BMC Genomics, 2011, vol. 12, no. 372, pp. 1—8.

    Google Scholar 

  46. Glessner, J.T., Smith, A.V., Panossian, S., et al., Copy number variations in alternative splicing gene networks impact lifespan, PLoS One, 2013, vol. 8, no. 1. e53846.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Frenkel, F.E. and Korotkov, E.V., Using triplet periodicity of nucleotide sequences for finding potential reading frame shifts in genes, DNA Res., 2009, vol. 16, no. 2, pp. 105—114.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Ahloowalia, B.S. and Maluszynski, M., Induced mutations—a new paradigm in plant breeding, Euphytica, 2001, vol. 188, no. 2, pp. 167—173.

    Google Scholar 

  49. Chung, H.J. and Liu, Q., Effect of γ irradiation on molecular structure and physicochemical properties of corn starch, J. Food Sci., 2009, vol. 74, no. 5, pp. 353—361.

    Google Scholar 

  50. Han, J.A. and Lim, S.T., Effect of γ-irradiation on pasting and emulsification properties of octenyl succinylated rice starches, Carbohydr. Polym., 2012, vol. 90, no. 4, pp. 1480—1485.

    CAS  PubMed  Google Scholar 

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Funding

This work was financially supported by the National Key Research and Development Program of China (2016YFD0102013), the Agricultural Innovation Fund of Hunan Province (2017JC52 and 2017QN28), and the Natural Science Foundation of Hunan Province (2019JJ50427) and the Natural Science Foundation of China (11205055).

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Correspondence to X. M. Peng or Zh. Yang.

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The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Zhang, L., Sun, P.Y., Xie, H.K. et al. Characterization of γ-Radiation-Induced DNA Polymorphisms in the M1 Population of the Japonica Rice Variety Gaogengnuo by Whole-Genome Resequencing. Russ J Genet 56, 693–705 (2020). https://doi.org/10.1134/S1022795420060149

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