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Abstract Nitrogen is an essential element required for plant growth and productivity. Understanding the mechanisms and natural genetic variation underlying nitrogen use in plants will facilitate the engineering of plant nitrogen use to maximize crop productivity while minimizing environmental costs. To understand the scope of natural variation that may influence nitrogen use, we grew 1,135 Arabidopsis thaliana natural genotypes on two nitrogen sources, nitrate and ammonium, and measured both developmental and defense metabolite traits. By using different environments and focusing on multiple traits, we identified a wide array of different nitrogen responses. These responses are associated with numerous genes, most of which were not previously associated with nitrogen responses. Only a small portion of these genes appear to be shared between environments or traits, while most are predominantly specific to a developmental or defense trait under a specific nitrogen source. Finally, by using a large population, we were able to identify unique nitrogen responses, such as preferring ammonium or nitrate, which appear to be generated by combinations of loci rather than a few large-effect loci. This suggests that it may be possible to obtain novel phenotypes in complex nitrogen responses by manipulating sets of genes with small effects rather than solely focusing on large-effect single gene manipulations. 

Summary Processes affecting rates of sequence polymorphism are fundamental to the evolution of gene duplicates. The relationship between gene activity and sequence polymorphism can influence the likelihood that functionally redundant gene copies are co‐maintained in stable evolutionary equilibria vs other outcomes such as neofunctionalization.Here, we investigate genic variation in epigenome‐associated polymorphism rates inArabidopsis thalianaand consider whether these affect the evolution of gene duplicates. We compared the frequency of sequence polymorphism and patterns of genetic differentiation between genes classified by exon methylation patterns: unmethylated (unM), gene‐body methylated (gbM), and transposon‐like methylated (teM) states, which reflect divergence in gene expression.We found that the frequency of polymorphism was higher in teM (transcriptionally repressed, tissue‐specific) genes and lower in gbM (active, constitutively expressed) genes. Comparisons of gene duplicates were largely consistent with genome‐wide patterns – gene copies that exhibit teM accumulate more variation, evolve faster, and are in chromatin states associated with reduced DNA repair.This relationship between expression, the epigenome, and polymorphism may lead to the breakdown of equilibrium states that would otherwise maintain genetic redundancies. Epigenome‐mediated polymorphism rate variation may facilitate the evolution of novel gene functions in duplicate paralogs maintained over evolutionary time.