Two Silene vulgaris copper transporters residing in different cellular compartments confer copper hypertolerance by distinct mechanisms when expressed in Arabidopsis thaliana

Yanbang Li, Mazhar Iqbal, Qianqian Zhang, Cornelis Spelt, Mattijs Bliek, Henk W.J. Hakvoort, Francesca M. Quattrocchio, Ronald Koes*, Henk Schat

*Corresponding author for this work

    Research output: Contribution to JournalArticleAcademicpeer-review

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    Abstract

    Silene vulgaris is a metallophyte of calamine, cupriferous and serpentine soils all over Europe. Its metallicolous populations are hypertolerant to zinc (Zn), cadmium (Cd), copper (Cu) or nickel (Ni), compared with conspecific nonmetallicolous populations. These hypertolerances are metal-specific, but the underlying mechanisms are poorly understood. We investigated the role of HMA5 copper transporters in Cu-hypertolerance of a S. vulgaris copper mine population. Cu-hypertolerance in Silene is correlated and genetically linked with enhanced expression of two HMA5 paralogs, SvHMA5I and SvHMA5II, each of which increases Cu tolerance when expressed in Arabidopsis thaliana. Most Spermatophytes, except Brassicaceae, possess homologs of SvHMA5I and SvHMA5II, which originate from an ancient duplication predating the appearance of spermatophytes. SvHMA5II and the A. thaliana homolog AtHMA5 localize in the endoplasmic reticulum and upon Cu exposure move to the plasma membrane, from where they are internalized and degraded in the vacuole. This resembles trafficking of mammalian homologs and is apparently an extremely ancient mechanism. SvHMA5I, instead, neofunctionalized and always resides on the tonoplast, likely sequestering Cu in the vacuole. Adaption of Silene to a Cu-polluted soil is at least in part due to upregulation of two distinct HMA5 transporters, which contribute to Cu hypertolerance by distinct mechanisms.

    Original languageEnglish
    Pages (from-to)1102-1114
    Number of pages13
    JournalNew Phytologist
    Volume215
    Issue number3
    Early online date16 Jun 2017
    DOIs
    Publication statusPublished - Aug 2017

    Funding

    We thank: Erik Manders and Ronald Breedijk (Center of Advanced Microscopy, University of Amsterdam) for advice and technical assistance with confocal microscopy; Teun Munnik (University of Amsterdam) for advice on the discussion; and Pengwei Wang (Durham University) for advice on the experiment of subcellular localization. Y.L. and Q.Z. were supported by a fellowship of the Chinese Scholarship Council. M.I. was supported by a fellowship of the Higher Education Commission (HEC), Pakistan.

    FundersFunder number
    China Scholarship Council
    Higher Education Commission, Pakistan

      Keywords

      • Arabidopsis thaliana
      • copper tolerance
      • heavy metal
      • HMA5
      • intracellular reallocation
      • P-ATPase
      • Silene vulgaris

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