ABSTRACT
KEY MESSAGE: Association analysis for ionomic concentrations of 20 elements identified independent genetic factors underlying the root and shoot ionomes of rice, providing a platform for selecting and dissecting causal genetic variants. Understanding the genetic basis of mineral nutrient acquisition is key to fully describing how terrestrial organisms interact with the non-living environment. Rice (Oryza sativa L.) serves both as a model organism for genetic studies and as an important component of the global food system. Studies in rice ionomics have primarily focused on above ground tissues evaluated from field-grown plants. Here, we describe a comprehensive study of the genetic basis of the rice ionome in both roots and shoots of 6-week-old rice plants for 20 elements using a controlled hydroponics growth system. Building on the wealth of publicly available rice genomic resources, including a panel of 373 diverse rice lines, 4.8 M genome-wide single-nucleotide polymorphisms, single- and multi-marker analysis pipelines, an extensive tome of 321 candidate genes and legacy QTLs from across 15 years of rice genetics literature, we used genome-wide association analysis and biparental QTL analysis to identify 114 genomic regions associated with ionomic variation. The genetic basis for root and shoot ionomes was highly distinct; 78 loci were associated with roots and 36 loci with shoots, with no overlapping genomic regions for the same element across tissues. We further describe the distribution of phenotypic variation across haplotypes and identify candidate genes within highly significant regions associated with sulfur, manganese, cadmium, and molybdenum. Our analysis provides critical insight into the genetic basis of natural phenotypic variation for both root and shoot ionomes in rice and provides a comprehensive resource for dissecting and testing causal genetic variants.
Subject(s)
Chromosome Mapping/methods , Chromosomes, Plant/genetics , Gene Expression Regulation, Plant , Oryza/genetics , Plant Proteins/metabolism , Plant Roots/genetics , Plant Shoots/genetics , Genome-Wide Association Study , Oryza/growth & development , Phenotype , Plant Proteins/genetics , Plant Roots/growth & development , Plant Shoots/growth & development , Quantitative Trait LociABSTRACT
Quantitative traits are important targets of both natural and artificial selection. The genetic architecture of these traits and its change during the adaptive process is thus of fundamental interest. The fate of the additive effects of variants underlying a trait receives particular attention because they constitute the genetic variation component that is transferred from parents to offspring and thus governs the response to selection. While estimation of this component of phenotypic variation is challenging, the increasing availability of dense molecular markers puts it within reach. Inbred plant species offer an additional advantage because phenotypes of genetically identical individuals can be measured in replicate. This makes it possible to estimate marker effects separately from the contribution of the genetic background not captured by genotyped loci. We focused on root growth in domesticated rice, Oryza sativa, under normal and aluminum (Al) stress conditions, a trait under recent selection because it correlates with survival under drought. A dense single nucleotide polymorphism (SNP) map is available for all accessions studied. Taking advantage of this map and a set of Bayesian models, we assessed additive marker effects. While total genetic variation accounted for a large proportion of phenotypic variance, marker effects contributed little information, particularly in the Al-tolerant tropical japonica population of rice. We were unable to identify any loci associated with root growth in this population. Models estimating the aggregate effects of all measured genotypes likewise produced low estimates of marker heritability and were unable to predict total genetic values accurately. Our results support the long-standing conjecture that additive genetic variation is depleted in traits under selection. We further provide evidence that this depletion is due to the prevalence of low-frequency alleles that underlie the trait.