Phosphorus (P) is a mineral nutrient essential for plant growth and development, but most P in the soil is unavailable for plants. To understand the genetic basis of P acquisition regulation, we performed genome-wide association studies (GWASs) on a diversity panel of Arabidopsis (Arabidopsis thaliana). Two primary determinants of P acquisition were considered, namely, phosphate (Pi)-uptake activity and PHOSPHATE TRANSPORTER 1 (PHT1) protein abundance. Association mapping revealed a shared significant peak on chromosome 5 (Chr5) where the PHT1;1/2/3 genes reside, suggesting a connection between the regulation of Pi-uptake activity and PHT1 protein abundance. Genes encoding transcription factors, kinases, and a metalloprotease associated with both traits were also identified. Conditional GWAS followed by statistical analysis of genotype-dependent PHT1;1 expression and transcriptional activity assays revealed an epistatic interaction between PHT1;1 and MYB DOMAIN PROTEIN 52 (MYB52) on Chr1. Further, analyses of F1 hybrids generated by crossing two subgroups of natural accessions carrying specific PHT1;1- and MYB52-associated single nucleotide polymorphisms (SNPs) revealed strong effects of these variants on PHT1;1 expression and Pi uptake activity. Notably, the soil P contents in Arabidopsis habitats coincided with PHT1;1 haplotype, emphasizing how fine-tuned P acquisition activity through natural variants allows environmental adaptation. This study sheds light on the complex regulation of P acquisition and offers a framework to systematically assess the effectiveness of GWAS approaches in the study of quantitative traits.
© The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists.