Genome-wide association mapping for grain manganese in rice (Oryza sativa L.) using a multi-experiment approach

Authors: RUANG-AREERATE, PANTHITA - University Of Aberdeen; TRAVIS, ANTHONY - University Of Aberdeen; Pinson, Shannon; TARPLEY, LEE - Texas A&M Agrilife; Eizenga, Georgia; GUERINOT, MARY LOU - Dartmouth College; SALT, DAVID - Dartmouth College; DOUGLAS, ALEX - University Of Aberdeen; PRICE, ADAM - University Of Aberdeen; NORTON, GARETH - University Of Aberdeen

Submitted to: Heredity
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/2/2020
Publication Date: 11/24/2020
Citation: Ruang-Areerate, P., Travis, A.J., Pinson, S.R., Tarpley, L., Eizenga, G.C., Guerinot, M., Salt, D.E., Douglas, A., Price, A.H., Norton, G.J. 2020. Genome-wide association mapping for grain manganese in rice (Oryza sativa L.) using a multi-experiment approach. Heredity. https://doi.org/10.1038/s41437-020-00390-w.
DOI: https://doi.org/10.1038/s41437-020-00390-w

Interpretive Summary: The grain mineral content of rice is important for human nutrition, especially when rice contributes a high percentage of calories in subsistence diets. One of the essential elements in human nutrition is manganese. In plants, manganese deficiency is common when plants are grown in water-logged soils, such as rice growing in flooded paddies. Also, when animals forage on manganese-deficient plants, the animals suffer nutritionally. We evaluated the grain manganese content of 389 rice varieties grown in four different production environments. Using 5.2 million DNA markers, we identified regions on rice chromosomes 3 and 7 that had six and three potential genes, respectively, affecting the accumulation and concentration of manganese in rice grains by either modifying the rate of manganese uptake by roots or transport of manganese between the tissues in the rice plant. A subsequent statistical analysis, combining the three flooded paddy environments revealed four new regions on chromosomes 2, 8, 9 and 12, with each region containing one major gene associated with manganese uptake or transport. In summary, this study revealed six chromosome regions containing 14 potential genes from which molecular markers could be developed for use in rice varietal development programs focused on enhancing the nutritional value of rice, as well as enhancing plant health. Understanding the interaction of the genes associated with the complex processes of uptake and transport in the plant, and deposition of manganese in the rice grain, is crucial to breeding rice varieties that are nutritionally dense and improve plant health.

Technical Abstract: Rice (Oryza sativa L.) is an important crop in terms of the calorie contribution to the global human diet. Manganese (Mn) is an essential trace element for rice plants and commonly contributes to animal nutrition when consumed as a forage or grain crop; however, the understanding of the genes controlling natural variation in Mn in crop plants is limited. Genome-wide association study (GWAS) is a statistically powerful approach for identifying genetic loci and genes related to complex traits. In this study, the integration of two GWAS approaches was used to increase the power of the analysis for identifying valuable quantitative trait loci (QTLs) and candidate genes responsible for the concentration of grain Mn across 389 diverse rice cultivars grown in Arkansas and Texas, USA in multiple years, for a total of four different location/year/irrigation treatment environments. QTLs were initially identified using the mean grain-Mn per each of the four environments that were scanned individually against three SNP datasets of different marker densities (44K, 700K, and 5.2 M SNPs across the rice genome). For each environment, use of denser marker maps identified QTLs that were not revealed from analyses using less-dense SNP sets. The 5.2M SNP analyses identified regions on chromosomes 3 and 7 as containing genes impacting grain Mn in two or more of the four environments. To further increase the power of QTL detection, trait data from the three similarly flooded studies were combined to create a multi-experiment trait estimate per genotype. New Mn QTLs were identified on chromosomes 2, 8, 9 and 12 that were not found in individual experiments. Thirteen total candidate genes were identified underlying these QTLs related to grain Mn, indicating it is a complex trait with multiple controlling genes. This demonstrates the utilization of multi-experiment GWAS analysis based on high SNP density genotypes for a collection of diverse rice accessions identifies a large number of QTLs and candidate genes associated with the grain Mn concentration. Dense marker maps and the multi-experiment approach should be used to expedite genomic breeding programs in rice and other crops that are considering QTLs and genes associated with complex traits in natural populations.