Research Paper

Genomic Prediction of Arsenic Tolerance and Grain Yield in Rice: Contribution of Trait-Specific Markers and Multi-Environment Models

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  • 1Institute of Genetic Improvement and Adaptation of Mediterranean and Tropical Plants, French Agricultural Research and International Cooperation Organization, Montpellier F-34398, France
    2University of Montpellier, National Research Institute for Agriculture, Food and Environment, French Agricultural Research and International Cooperation Organization, Montpellier SupAgro, Montpellier 34090, France
    3School of Biological Sciences, University of Aberdeen, Aberdeen AB24 3UU, Scotland

Received date: 2020-03-10

  Accepted date: 2020-10-12

  Online published: 2021-05-28

Abstract

Many rice-growing areas are affected by high concentrations of arsenic (As). Rice varieties that prevent As uptake and/or accumulation can mitigate As threats to human health. Genomic selection is known to facilitate rapid selection of superior genotypes for complex traits. We explored the predictive ability (PA) of genomic prediction with single-environment models, accounting or not for trait-specific markers, multi-environment models, and multi-trait and multi-environment models, using the genotypic (1600K SNPs) and phenotypic (grain As content, grain yield and days to flowering) data of the Bengal and Assam Aus Panel. Under the base-line single-environment model, PA of up to 0.707 and 0.654 was obtained for grain yield and grain As content, respectively; the three prediction methods (Bayesian Lasso, genomic best linear unbiased prediction and reproducing kernel Hilbert spaces) were considered to perform similarly, and marker selection based on linkage disequilibrium allowed to reduce the number of SNP to 17K, without negative effect on PA of genomic predictions. Single-environment models giving distinct weight to trait-specific markers in the genomic relationship matrix outperformed the base-line models up to 32%. Multi-environment models, accounting for genotype × environment interactions, and multi-trait and multi-environment models outperformed the base-line models by up to 47% and 61%, respectively. Among the multi-trait and multi-environment models, the Bayesian multi-output regressor stacking function obtained the highest predictive ability (0.831 for grain As) with much higher efficiency for computing time. These findings pave the way for breeding for As-tolerance in the progenies of biparental crosses involving members of the Bengal and Assam Aus Panel. Genomic prediction can also be applied to breeding for other complex traits under multiple environments.

Cite this article

Ahmadi Nourollah, Cao Tuong-Vi, Frouin Julien, J. Norton Gareth, H. Price Adam . Genomic Prediction of Arsenic Tolerance and Grain Yield in Rice: Contribution of Trait-Specific Markers and Multi-Environment Models[J]. Rice Science, 2021 , 28(3) : 268 -278 . DOI: 10.1016/j.rsci.2021.04.006

References

[1] Ahmadi N, Bartholomé J, Cao T V, Grenier C. 2020. Genomic selection in rice: Empirical results and implications for breeding. In: Kang M J. Quantitative Genetics, Genomics and Plant Breeding. 2nd edn. CAB International.
[2] Asoro F G, Newell M A, Beavis W D, Scott M P, Jannink J L. 2011. Accuracy and training population design for genomic selection on quantitative traits in elite North American oats. Plant Genom, 4(2): 132?144.
[3] Bassi F M, Bentley A R, Charmet G, Ortiz R, Crossa J. 2015. Breeding schemes for the implementation of genomic selection in wheat ( Triticum spp.). Plant Sci, 242: 23-36.
[4] ben Hassen M, Cao T V, Bartholomé J, Orasen G, Colombi C, Rakotomalala J, Razafinimpiasa L, Bertone C, Biselli C, Volante A, Desiderio F, Jacquin L, Vale G, Ahmadi N. 2017. Rice diversity panel provides accurate genomic predictions for complex traits in the progenies of biparental crosses involving members of the panel. Theor Appl Genet, 131(2): 417?435.
[5] ben Hassen M, Bartholomé J, Valè G, Cao T V, Ahmadi N. 2018. Genomic prediction accounting for genotype by environment interaction offers an effective framework for breeding simultaneously for adaptation to an abiotic stress and performance under normal cropping conditions in rice. G3, 8(7): 2319?2332.
[6] Bernardo R, Yu J M. 2007. Prospects for genome-wide selection for quantitative traits in maize. Crop Sci, 47(3): 1082?1090.
[7] Bhandari A, Bartholomé B, Cao T V, Kumari N, Frouin J, Kumar A, Ahmadi N. 2019. Selection of trait-specific markers and multi-environment models improve genomic predictive ability in rice. PLoS One, 14(5): e0208871.
[8] Brammer H, Ravenscroft P. 2009. Arsenic in groundwater: A threat to sustainable agriculture in South and South-east Asia. Environ Int, 35(3): 647?654.
[9] Cuevas J, Crossa J, Soberanis V, Pérez-Elizalde S, Pérez-Rodríguez P, de Los Campos G, Montesinos-Lopez O A, Burgueno J. 2016. Genomic prediction of genotype × environment interaction kernel regression models. Plant Genom, 9(3): 1?20.
[10] Cuevas J, Crossa J, Montesinos-López O A, Burgueño J, Pérez- Rodríguez P, de Los Campos G. 2017. Bayesian genomic prediction with genotype × environment interaction kernel models. G3, 7(1): 41?53.
[11] Dasgupta T, Hossain S A, Meharg A A, Price A H. 2004. An arsenate tolerance gene on chromosome 6 of rice. New Phytol, 163(1): 45?49.
[12] Frouin J, Labeyrie A, Boisnard A, Sacchi G A, Ahmadi N. 2019. Genomic prediction offers the most effective marker assisted breeding approach for ability to prevent arsenic accumulation in rice grains. PLoS One, 14(6): e0217516.
[13] Gianola D, van Kaam J B C H M. 2008. Reproducing kernel hilbert spaces regression methods for genomic assisted prediction of quantitative traits. Genetics, 178(4): 2289?2303.
[14] Habier D, Fernando R L, Dekkers J C M. 2009. Genomic selection using low-density marker panels. Genetics, 182(1): 343?353.
[15] Heffner E L, Sorrells M E, Jannink J L. 2009. Genomic selection for crop improvement. Crop Sci, 49(1): 1?12.
[16] Kuramata M, Abe T, Kawasaki A, Ebana K, Shibaya T, Yano M, Lshikawa S. 2013. Genetic diversity of arsenic accumulation in rice and QTL analysis of methylated arsenic in rice grains. Rice, 6(3): 2?10.
[17] Lopez-Cruz M, Crossa J, Bonnett D, Dreisigacker S, Poland J, Jannink J L, Singh R P, Autrique E, de los Campos G. 2015. Increased prediction accuracy in wheat breeding trials using a marker × environment interaction genomic selection model. G3, 5(4): 569?582.
[18] Lorenz A J, Chao S, Asoro G F, Heffner L F, Hayashi T, Iwata H, Smith K P, Sorrells M E, Jannink J L. 2011. Genomic selection in plant breeding: Knowledge and prospects. Adv Agron, 110: 77?123.
[19] Meuwissen T H E, Hayes B J, Goddard M E. 2001. Prediction of total genetic value using genome-wide dense marker maps. Genetics, 157(4): 1819?1829.
[20] Montesinos-Lopez O A, Montesinos-Lopez A, Crossa J, Toledo F H, Perez-Hernandez O, Eskridge K M, Rutkoski J. 2016. A genomic Bayesian multi-trait and multi-environment model. G3, 6(9): 2725?2744.
[21] Montesinos-López O A, Montesinos-López A, Luna-Vázquez F J, Toledo F H, Pérez-Rodríguez P, Lillemo M, Crossa J. 2019. An R package for Bayesian analysis of multi-environment and multi-trait multi-environment data for genome-based prediction. G3, 9(5): 1355?1369.
[22] Norton G J, Duan G L, Dasgupta T, Islam M R, Lei M, Zhu Y G, Deacon C M, Moran A C, Islam S, Zhao F J, Stroud J L, McGrath S P, Feldmann J, Price A H, Meharg A A. 2009. Environmental and genetic control of arsenic accumulation and speciation in rice grain: Comparing a range of common cultivars grown in contaminated sites across Bangladesh, China and India. Environ Sci Technol, 43: 8381?8386.
[23] Norton G J, Deacon C M, Xiong L Z, Huang S Y, Meharg A A, Price A H. 2010. Genetic mapping of the rice ionome in leaves and grain: Identification of QTLs for 17 elements including arsenic, cadmium, iron and selenium. Plant Soil, 329: 139?153.
[24] Norton G J, Pinson S R M, Alexander J, Mckay S, Hansen H, Duan G L, Islam M R, Islam S, Stroud J, Zhao F J, McGrath S P, Zhu Y G, Lahner B, Yakubova E, Guerinot M L, Tarpley L, Eizenga G C, Salt D E, Mcharg A A, Price A H. 2012a. Variation in grain arsenic assessed in a diverse panel of rice(Oryza sativa) grown in multiple sites. New Phytol, 193: 650?664.
[25] Norton G J, Duan G L, Lei M, Zhu Y G, Meharg A A, Price A H. 2012b. Identification of quantitative trait loci for rice grain element composition on an arsenic impacted soil: Influence of flowering time on genetic loci. Ann Appl Biol, 161(1): 46-56.
[26] Norton G T, Douglas A, Lahner B, Yakubova E, Guerinot M L, Pinson S R, Tarpley L, Eizenga G, McGrath S P, Zhao F J, Islam M R, Islam S, Duan G L, Zhu Y G, Salt D E, Meharg A A, Price A H. 2014. Genome wide association mapping of grain arsenic, copper, molybdenum and zinc in rice ( Oryza sativa L.) grown at four international field sites. PLoS One, 9(2): e89685.
[27] Norton G J, Shafaei M, Travis A J, Deacon C M, Danku J, Pond D, Cochrane N, Lockhart K, Salt D, Zhang H, Dodd I C, Hossain M, Islam M R, Price A H. 2017a. Impact of alternate wetting and drying on rice physiology, grain production, and grain quality. Field Crops Res, 205: 1?13.
[28] Norton G J, Travis A J, Danku J M C, Salt D E, Hossain M, Islam M R, Price A H. 2017b. Biomass and elemental concentrations of 22 rice cultivars grown under alternate wetting and drying conditions at three field sites in Bangladesh. Food Energy Secur, 6(3): 98-112.
[29] Norton G J, Travis A J, Douglas A, Fairley S, de Paiva Alves E, Ruang-areerate P, Naredo M E B, McNally K L, Hossain M, Islam M R, Price A H. 2018. Genome wide association mapping of grain and straw biomass traits in the rice Bengal and Assam Aus panel (BAAP) grown under alternate wetting and drying and permanently flooded irrigation. Front Plant Sci, 9: 1223.
[30] Norton G J, Travis A J, Talukdar P, Hossain M, Islam M R, Douglas A, Price A H. 2019. Genetic loci regulating arsenic content in rice grains when grown flooded or under alternative wetting and drying irrigation. Rice, 12: 54.
[31] Park T, Casella G. 2008. The bayesian lasso. J Am Stat Assoc, 103: 681?686.
[32] Pérez P, de los Campos G. 2014. Genome-wide regression and prediction with the BGLR statistical package. Genetics, 198(2): 483?495.
[33] Rahman M A, Hasegawa H, Rahman M M, Islam M N, Miah M A M, Tasmen A. 2007. Effect of arsenic on photosynthesis, growth and yield of five widely cultivated rice ( Oryza sativa L.) varieties in Bangladesh. Chemosphere, 67(6): 1072-1079.
[34] Sempéré G, Pétel A, Rouard M, Frouin J, Hueber Y, de Bellis F, Larmande P. 2019. Gigwa-v2 extended and improved genotype investigator. Giga Sci, 8(5): giz051.
[35] Spyromitros-Xioufis E, Tsoumakas G, Groves W, Vlahavas I. 2016. Multi-target regression via input space expansion: Treating targets as inputs. Mach Learn, 104: 55-98.
[36] Stroud J L, Norton G J, Islam M R, Dasgupta T, White R P, Price A H, Meharg A A, McGrath S P, Zhao F J. 2011. The dynamics of arsenic in four paddy fields in the Bengal Deltas. Environ Pollut, 159(4): 947?953.
[37] Tibshirani R. 1996. Regression shrinkage and selection via the lasso: A retrospective. J Roy Stat Soc, 58(1): 267?288.
[38] Van Raden P M. 2008. Efficient methods to compute genomic predictions. J Dairy Sci, 91(11): 4414?4423.
[39] Veerkamp R F, Bouwman A C, Schrooten C, Calus M P L. 2016. Genomic prediction using preselected DNA variants from a GWAS with whole genome sequence data in Holstein-Friesian cattle. Genet Sel Evol, 48(1): 95.
[40] Zavala Y J, Duxbury J M. 2008. Arsenic in rice: I. Estimating normal levels of total arsenic in rice grain. Environ Sci Technol, 42(10): 3856-3860.
[41] Zhang M, Pinson S R M, Tarpley L, Huang X Y, Lahner B, Yakubova E, Baxter L, Guerinot M L, Salt D E. 2014. Mapping and validation of quantitative trait toci associated with concentration of 16 elements in unmilled rice grain. Theor Appl Genet, 127(1): 137?165.
[42] Zhang Z, Ober U, Erbe M, Zhang H, Gao N, He J L, Li J Q, Simianer H. 2014. Improving the accuracy of whole genome prediction for complex traits using the results of genome wide association studies. PLoS One, 9(3): e93017.
[43] Zhong S Q, Dekkers J C M, Fernando R L, Jannink J L. 2009. Factors affecting accuracy from genomic selection in populations derived from multiple inbred lines: A barley case study. Genetics, 182(1): 355?364.
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