title: Variation in sulfur and selenium accumulation is controlled by naturally occurring isoforms of the key sulfur assimilation enzyme ADENOSINE 5'-PHOSPHOSULFATE REDUCTASE2 across the Arabidopsis species range.
abstract: Natural variation allows the investigation of both the fundamental functions of genes and their role in local adaptation. As one of the essential macronutrients, sulfur is vital for plant growth and development and also for crop yield and quality. Selenium and sulfur are assimilated by the same process, and although plants do not require selenium, plant-based selenium is an important source of this essential element for animals. Here, we report the use of linkage mapping in synthetic F2 populations and complementation to investigate the genetic architecture of variation in total leaf sulfur and selenium concentrations in a diverse set of Arabidopsis (Arabidopsis thaliana) accessions. We identify in accessions collected from Sweden and the Czech Republic two variants of the enzyme ADENOSINE 5'-PHOSPHOSULFATE REDUCTASE2 (APR2) with strongly diminished catalytic capacity. APR2 is a key enzyme in both sulfate and selenate reduction, and its reduced activity in the loss-of-function allele apr2-1 and the two Arabidopsis accessions Hodonín and Shahdara leads to a lowering of sulfur flux from sulfate into the reduced sulfur compounds, cysteine and glutathione, and into proteins, concomitant with an increase in the accumulation of sulfate in leaves. We conclude from our observation, and the previously identified weak allele of APR2 from the Shahdara accession collected in Tadjikistan, that the catalytic capacity of APR2 varies by 4 orders of magnitude across the Arabidopsis species range, driving significant differences in sulfur and selenium metabolism. The selective benefit, if any, of this large variation remains to be explored.
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: Dai-Yin
authors.initials: DY
authors.lastname: Chao
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: Patrycja
authors.initials: P
authors.lastname: Baraniecka
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: John
authors.initials: J
authors.lastname: Danku
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: Anna
authors.initials: A
authors.lastname: Koprivova
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: Brett
authors.initials: B
authors.lastname: Lahner
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: Hongbing
authors.initials: H
authors.lastname: Luo
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: Elena
authors.initials: E
authors.lastname: Yakubova
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: Brian
authors.initials: B
authors.lastname: Dilkes
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.).
authors.forename: Stanislav
authors.initials: S
authors.lastname: Kopriva
authors.affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom (D.-Y.C., J.D., D.E.S.);Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom (P.B., A.K., S.K.); andDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., H.L., E.Y., B.D.) david.salt@abdn.ac.uk.
authors.forename: David E
authors.initials: DE
authors.lastname: Salt
mesh_terms: D019943:Amino Acid Substitution; D017360:Arabidopsis / Q000235:genetics* / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D018153:Czech Republic; D005787:Gene Frequency; D014644:Genetic Variation; D055106:Genome-Wide Association Study; D007527:Isoenzymes / Q000235:genetics / Q000378:metabolism; D050862:Oxidoreductases Acting on Sulfur Group Donors / Q000235:genetics / Q000378:metabolism*; D010641:Phenotype; D018515:Plant Leaves / Q000378:metabolism; D018520:Plant Shoots / Q000378:metabolism; D030821:Plants, Genetically Modified; D012643:Selenium / Q000378:metabolism*; D013431:Sulfates / Q000378:metabolism; D013455:Sulfur / Q000378:metabolism*; D013548:Sweden
chemical_list: D029681:Arabidopsis Proteins; D007527:Isoenzymes; D013431:Sulfates; D013455:Sulfur; D050862:Oxidoreductases Acting on Sulfur Group Donors; C522406:APR2 protein, Arabidopsis; D012643:Selenium