Abstract

Quantitative genetic analysis has long been used to study how natural variation of genotype can influence an organism's phenotype. While most studies have focused on genetic determinants of phenotypic average, it is rapidly becoming understood that stochastic noise is genetically determined. However, it is not known how many traits display genetic control of stochastic noise nor how broadly these stochastic loci are distributed within the genome. Understanding these questions is critical to our understanding of quantitative traits and how they relate to the underlying causal loci, especially since stochastic noise may be directly influenced by underlying changes in the wiring of regulatory networks. We identified QTLs controlling natural variation in stochastic noise of glucosinolates, plant defense metabolites, as well as QTLs for stochastic noise of related transcripts. These loci included stochastic noise QTLs unique for either transcript or metabolite variation. Validation of these loci showed that genetic polymorphism within the regulatory network alters stochastic noise independent of effects on corresponding average levels. We examined this phenomenon more globally, using transcriptomic datasets, and found that the Arabidopsis transcriptome exhibits significant, heritable differences in stochastic noise. Further analysis allowed us to identify QTLs that control genomic stochastic noise. Some genomic QTL were in common with those altering average transcript abundance, while others were unique to stochastic noise. Using a single isogenic population, we confirmed that natural variation at ELF3 alters stochastic noise in the circadian clock and metabolism. Since polymorphisms controlling stochastic noise in genomic phenotypes exist within wild germplasm for naturally selected phenotypes, this suggests that analysis of Arabidopsis evolution should account for genetic control of stochastic variance and average phenotypes. It remains to be determined if natural genetic variation controlling stochasticity is equally distributed across the genomes of other multi-cellular eukaryotes.

Highlights

  • Almost all phenotypes are not fixed within species but instead exhibit significant levels of variation among individuals that is controlled by quantitative genetic loci

  • Understanding how genetic variation controls phenotypic variation is a fundamental goal of biology in both modern medicine and agriculture

  • Utilizing Arabidopsis, we tested this hypothesis at a genomic level by mapping quantitative trait loci for stochastic noise in global transcriptomics, plant defense metabolism, circadian clock oscillation, and flowering time within a single non-stressful environment

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Summary

Introduction

Almost all phenotypes are not fixed within species but instead exhibit significant levels of variation among individuals that is controlled by quantitative genetic loci. An ultimate goal of research on the basis of quantitative genetic variation is to generate a sufficient level of understanding to be able to predict phenotypic range of a species based on knowledge of that species’ genetic variation. These efforts are complicated because phenotypic diversity is typically under polygenic control and can involve complex interactions with numerous factors including, but not limited to, the environment, development, epistatic interactions between genes, and potential higher-order interaction among these factors [1,2]. If these polymorphisms are frequent in number, heritable and discrete from loci altering mean phenotpyes they can lead to an inability to fully describe the variance within any phenotype using current statistical approaches that focus solely upon the mean phenotype

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