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Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2

Nature Genetics volume 39, pages 896–900 (2007)Cite this article

Abstract

Most agronomic traits of importance, whether physiological (such as nutrient use efficiency) or developmental (such as flowering time), are controlled simultaneously by multiple genes and their interactions with the environment. Here, we show that variation in sulfate content between wild Arabidopsis thaliana accessions Bay-0 and Shahdara is controlled by a major quantitative trait locus that results in a strong interaction with nitrogen availability in the soil. Combining genetic and biochemical results and using a candidate gene approach, we have cloned the underlying gene, showing how a single–amino acid substitution in a key enzyme of the assimilatory sulfate reduction pathway, adenosine 5′-phosphosulfate reductase, is responsible for a decrease in enzyme activity, leading to sulfate accumulation in the plant. This work illustrates the potential of natural variation as a source of new alleles of known genes, which can aid in the study of gene function and metabolic pathway regulation. Our new insights on sulfate assimilation may have an impact on sulfur fertilizer use and stress defense improvement.

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Figure 1: Mapping and confirmation of the SO3.1 shoot sulfate content QTL.
Figure 2: Amino acid changes along the APR2 protein sequence detected within a core collection of 32 Arabidopsis thaliana accessions designed to represent a maximum of the total SNP diversity9.
Figure 3: Transgenic complementation test for SO3.1 QTL.
Figure 4: Quantitative complementation test for SO3.1 QTL.
Figure 5: Total adenosine 5′-phosphosulfate reductase (APR) activities.

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Acknowledgements

We thank J. Talbotec for taking care of the plants. We thank J. Chory, D. Weigel and T.P. Michael for discussions and comments on the manuscript. This work was supported by a European grant to F.D.-V. ('Natural' project number QLRT–2000–01097, 2002–2005). Research in S.K.'s laboratory at the John Innes Centre is supported by the Biotechnology and Biological Sciences Research Council (BBSRC).

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Authors and Affiliations

  1. Station de Génétique et Amélioration des Plantes (SGAP), Institut National de la Recherche Agronomique (INRA), Rte. de St. Cyr, Versailles, 78026, France

    Olivier Loudet & Christine Camilleri

  2. Laboratoire de Nutrition Azotée des Plantes (NAP), Institut National de la Recherche Agronomique (INRA), Rte. de St. Cyr, Versailles, 78026, France

    Vera Saliba-Colombani, Fanny Calenge, Virginie Gaudon & Françoise Daniel-Vedele

  3. John Innes Centre, Norwich Research Park, Colney, NR4 7UH, Norwich, UK

    Anna Koprivova, Kathryn A North & Stanislav Kopriva

Authors
  1. Olivier Loudet
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  2. Vera Saliba-Colombani
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  3. Christine Camilleri
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  4. Fanny Calenge
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  5. Virginie Gaudon
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  7. Kathryn A North
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  8. Stanislav Kopriva
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  9. Françoise Daniel-Vedele
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Contributions

O.L., S.K. and F.D.-V. conceived the experiments; O.L., V.S.-C., C.C., F.C., V.G., A.K., K.A.N. and S.K. performed the experiments; O.L., V.S.-C., C.C., S.K. and F.D.-V. analyzed the data and O.L., S.K. and F.D.-V. wrote the manuscript.

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Correspondence to Olivier Loudet.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Biochemical analysis of APR2 from Bay-0 and Shahdara. (PDF 26 kb)

Supplementary Fig. 2

Thiol content of Bay-0, Shahdara and HIF068. (PDF 43 kb)

Supplementary Table 1

Predicted QTL parameters for sulfate content in 'N+' (SO10) and 'N−' (SO3) environments in the Bay-0 × Shahdara RIL population. (PDF 11 kb)

Supplementary Table 2

Primers used in this study and described in the Methods. (PDF 10 kb)

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Loudet, O., Saliba-Colombani, V., Camilleri, C. et al. Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat Genet 39, 896–900 (2007). https://doi.org/10.1038/ng2050

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