Diverse phosphate and auxin transport loci distinguish phosphate tolerant from sensitive Arabidopsis accessions

Phosphorus is an essential element for plant growth often limiting agroecosystems. To identify genetic determinants of performance under variable phosphate supply, we conducted genome-wide-association studies on five highly predictive phosphate starvation response traits in 200 Arabidopsis (Arabidopsis thaliana) accessions. Phosphate concentration in phosphate-limited organs had the strongest, and primary root length had the weakest genetic component. Of 70 trait-associated candidate genes, 17 responded to phosphate withdrawal. The PHOSPHATE TRANSPORTER1 gene cluster on chromosome 5 comprised PHT1;1, PHT1;2 and PHT1;3 with known impact on phosphorus status. A second locus featured uncharacterized endomembrane-associated auxin efflux carrier encoding PIN-LIKES7 (PILS7) which was more strongly suppressed in phosphate-limited roots of phosphate-starvation sensitive accessions. In the Col-0 background, phosphate uptake and organ growth were impaired in both phosphate-limited pht1;1 and two pils7 T-DNA insertion mutants, while phosphate-limited pht1;2 had higher biomass and pht1;3 was indistinguishable from wild type. Copy number variation at the PHT1 locus with loss of the PHT1;3 gene and smaller scale deletions in PHT1;1 and PHT1;2 predicted to alter both protein structure and function suggest diversification of PHT1 is a key driver for adaptation to phosphorus limitation. Haplogroup analysis revealed a phosphorylation site in the protein encoded by the PILS7 allele from stress-sensitive accessions as well as additional auxin-responsive elements in the promoter of the ‘stress tolerant’ allele. The former allele’s inability to complement the pils7-1 mutant in the Col-0 background implies the presence of a kinase signaling loop controlling PILS7 activity in accessions from phosphorus-rich environments, while survival in phosphorus-poor environments requires fine-tuning of stress-responsive root auxin signaling.