Evolutionary patterns of DNA base composition at polymorphic sites highlight the role of the environment in shaping barley and rice genomes

Insights into changes in genome base composition underlying crop domestication can be gained by using comparative genomics. With this approach, previous studies have reported that crop genomes during domestication accumulate more nucleotides adenine (A) and thymine (T) (termed as [AT]-increase) across polymorphic sites. However, the potential influence of the environment or its factors, for example, solar ultraviolet (UV) radiation and temperature, on the [AT]-increase has not been well elucidated. Here, we investigated the [AT]-increase in barley (Hordeum vulgare L.) and rice (Oryza sativa L.) and the association with natural environments, where accessions are distributed. With 12,798,376 and 2,861,535 single-nucleotide polymorphisms from 368 barley and 1375 rice accessions, respectively, we discovered that [AT] increases from wild accessions to improved cultivars, and genomic regions with larger [AT]-increase tend to have higher UV-related motif frequencies, suggesting solar UV radiation as a potential factor in driving genome variation. To link [AT] change with the geographic distribution, we gathered georeferenced accessions and examined their local environments. Interestingly, negative correlations between [AT] and environmental factors were observed (r = -0.39 similar to -0.75) and modern accessions with higher [AT] values, as compared with wild relatives, are from the environments with lower solar UV radiation or lower temperature. With [AT] and environmental factors as phenotypes, genome-wide association mapping identified three candidate genes that have the potential to contribute to [AT] variation under the effect of environmental conditions. Our findings provide genomic and environmental insights into evolutionary pattern of DNA base composition and underlying mechanisms. Barley and rice during domestication accumulate more nucleotides adenine (A) and thymine (T) at polymorphic sites within genomes. Genomic regions exhibiting a larger [AT]-increase tend to demonstrate higher frequencies of UV-related motif. The genome-wide [AT]-increase pattern is influenced by factors such as solar UV radiation and temperature. We identified three candidate genes that are associated with [AT] variation under environmental influence. Integration of environmental data with genome sequences allows for more comprehensive studies on crop adaptation. Crop evolution has resulted in significant changes in the traits of plants, making them more diverse and complex. These changes are driven by modifications in the genome. During the process of domestication, crops have shown an increase in nucleotides adenine (A) and thymine (T) in their genomes, known as [AT]-increase. To better understand how the environment impacts genome evolution, we investigated the environmental factors that contribute to [AT]-increase. Our research revealed that solar UV radiation and temperature, in addition to artificial selection, play significant roles in [AT]-increase. These findings highlight the connection between genome evolution patterns and the geographical environment, offering insights into how crops adapt to their surroundings. Furthermore, we provide a genomic perspective on environmental adaptation and shed light on the evolution of genomes in response to the environment.