Natural Variation in ATPS1 Isoform of ATP Sulfurylase Contributes to Control of Sulfate Levels in Arabidopsis

Sulfur is an essential macronutrient for all living organisms. Plants take up inorganic sulfate from the soil, reduce it and assimilate into bioorganic compounds, but part of this sulfate is stored in the vacuoles. In the first attempt to identify genes involved in control of sulfate content in the leaves we reported that a QTL for sulfate content in Arabidopsis was underlied by APR2 isoform of the key enzyme of sulfate assimilation, adenosine 5’-phosphosulfate reductase (APR; Loudet et al., 2007, Nat Genet 39, 896-900). To increase the knowledge on the control of this trait we cloned a second QTL from the same analysis. Surprisingly, the gene underlying this QTL encodes ATPS1 isoform of the enzyme ATP sulfurylase, which precedes APR in the sulfate assimilation pathway. Plants with Bay allele of ATPS1 accumulate lower steady state levels of ATPS1 transcript than those with Sha allele which leads to lower enzyme activity and ultimately accumulation of sulfate. Our results show that the transcript variation is controlled in cis. Examination of ATPS1 sequences of Bay-0 and Shahdara identified two deletions in the 1st intron and immediately downstream the gene in Bay-0 shared with multiple other Arabidopsis accessions. The average ATPS1 transcript levels are lower in these accessions than in those without the deletions, while sulfate levels are significantly higher. Thus, sulfate content in Arabidopsis is controlled by two genes encoding subsequent enzymes in sulfate assimilation pathway, but using different mechanisms, variation in amino acid sequence and variation in expression levels.