Phenotype

Sociology

Population

Genetic variation

Inbred strain

Biology

Gene

Genotype

Demography

Gene expression

Allele

Genetics

Quantitative trait locus

Genetic diversity

Nature

A multi-tissue gene expression resource representative of the genotypic and phenotypic diversity of modern inbred maize reveals the effect of rare alleles and evolutionary history on the regulation of gene expression. Karl Kremling, Edward Buckler and colleagues report a multi-tissue gene expression resource for maize that includes RNA-sequencing data on seven tissues from across 299 maize lines, which are representative of the genotypic and phenotypic diversity of modern inbred maize. The authors examined how gene expression is regulated, mapped expression quantitative trait loci and characterized the contribution of rare genetic variants to extremes in gene expression. They also show a correlation between cumulative deviation in the expression of the most highly expressed genes and seed-weight fitness. Here we report a multi-tissue gene expression resource that represents the genotypic and phenotypic diversity of modern inbred maize, and includes transcriptomes in an average of 255 lines in seven tissues. We mapped expression quantitative trait loci and characterized the contribution of rare genetic variants to extremes in gene expression. Some of the new mutations that arise in the maize genome can be deleterious; although selection acts to keep deleterious variants rare, their complete removal is impeded by genetic linkage to favourable loci and by finite population size1,2,3,4. Modern maize breeders have systematically reduced the effects of this constant mutational pressure through artificial selection and self-fertilization, which have exposed rare recessive variants in elite inbred lines5. However, the ongoing effect of these rare alleles on modern inbred maize is unknown. By analysing this gene expression resource and exploiting the extreme diversity and rapid linkage disequilibrium decay of maize6, we characterize the effect of rare alleles and evolutionary history on the regulation of expression. Rare alleles are associated with the dysregulation of expression, and we correlate this dysregulation to seed-weight fitness. We find enrichment of ancestral rare variants among expression quantitative trait loci mapped in modern inbred lines, which suggests that historic bottlenecks have shaped regulation. Our results suggest that one path for further genetic improvement in agricultural species lies in purging the rare deleterious variants that have been associated with crop fitness.

Dysregulation of expression correlates with rare-allele burden and fitness loss in maize