Natural Genetic Variation Shapes Root System Responses to Phytohormones in Arabidopsis

Abstract

Plants adjust their architecture by modulating organ growth. This ability is largely dependent on phytohormones. While many genes involved in phytohormone pathways have been identified, it remains unclear to which extent and how these pathways are modulated in non-reference strains and whether this is relevant for local adaptation. Here we assess variation of root traits in response to perturbations of the auxin, cytokinin, and abscisic acid pathways in 192 Arabidopsis accessions. We identify common response patterns, uncover the extent of their modulation by specific genotypes, and find that the Col-0 reference accession is not a good representative of the species in this regard. We conduct GWAS and identify 114 significant associations, most of them relating to ABA treatment. The numerous ABA candidate genes are not enriched for known ABA associated genes indicating that we largely uncovered unknown players. We then study two associated regions in detail and identify the CRF3 gene as a modulator of multiple hormone pathways. Finally, we show that natural variation in root traits is significantly associated with climate parameters relevant for local adaption in Arabidopsis thaliana and that, in particular, ABA regulated lateral root traits are likely to be relevant for adaptation to soil moisture.\n\nAuthor SummaryThe root system is a key component for plant survival and productivity. Apart from anchoring the plant, its architecture determines which parts of the soil are foraged for water and nutrients, and it serves as an interface for interaction with microbes and other soil organisms. Plant hormones play crucial roles in the development of root system architecture and its plasticity. However, while there is substantial natural variation of root architectures, it is not clear to which extent genetic variation in hormone related pathways contribute. Using the model species Arabidopsis thaliana we quantitatively explore the breadth of natural variation in plant hormone responses to three major plant hormones: auxin, cytokinin, and abscisic acid. The Col-0 reference strain can be quite different from a large proportion of the natural accessions of the species, illustrating a severe caveat of relying on a single reference strain in model species and drawing generalizations from it. Using GWAS, we further identify a large number of loci underlying the variation of responses to plant hormones, in particular to abscisic acid, find links between local adaptation and root responses to hormones, and finally using mutants for GWAS candidate genes, identify novel players involved in regulating hormone responses.