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
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.
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.
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.
Patade, V.Y. and Suprasanna, P., Radiation induced in vitro mutagenesis for sugarcane improvement, Sugar. Tech., 2008, vol. 10, no. 1, pp. 14—19.
Acquaah, G., Principles of Plant Genetics and Breeding, Wiley, 2012.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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
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.
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
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.
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.
Langridge, P. and Fleury, D., Making the most of ‘omics’ for crop breeding, Trends Biotechnol., 2011, vol. 29, no. 1, pp. 33—40.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Li, H. and Durbin, R., Fast and accurate short read alignment with Burrows—Wheeler transform, Bioinformatics, 2009, vol. 25, no. 14, pp. 1754—1760.
Li, H., Handsaker, B., Wysoker, A., et al., The sequence alignment/map format and SAMtools, Bioinformatics., 2009, vol. 25, no. 16, pp. 2078—2079.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Ahloowalia, B.S. and Maluszynski, M., Induced mutations—a new paradigm in plant breeding, Euphytica, 2001, vol. 188, no. 2, pp. 167—173.
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.
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.
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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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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DOI: https://doi.org/10.1134/S1022795420060149