Abstract
Gene duplication is a major mechanism facilitating adaptation to changing environments. From recent genomic analyses, the acquisition of zinc hypertolerance and hyperaccumulation characters discriminating Arabidopsis halleri from its zinc sensitive/non-accumulator closest relatives Arabidopsis lyrata and Arabidopsis thaliana was proposed to rely on duplication of genes controlling zinc transport or zinc tolerance. Metal Tolerance Protein 1 (MTP1) is one of these genes. It encodes a Zn2+/H+ antiporter involved in cytoplasmic zinc detoxification and thus in zinc tolerance. MTP1 was proposed to be triplicated in A. halleri, while it is present in single copy in A. thaliana and A. lyrata. Two of the three AhMTP1 paralogues were shown to co-segregate with zinc tolerance in a BC1 progeny from a cross between A. halleri and A. lyrata. In this work, the MTP1 family was characterized at both the genomic and functional levels in A. halleri. Five MTP1 paralogues were found to be present in A. halleri, AhMTP1-A1, -A2, -B, -C, and -D. Interestingly, one of the two newly identified AhMTP1 paralogues was not fixed at least in one A. halleri population. All MTP1s were expressed, but transcript accumulation of the paralogues co-segregating with zinc tolerance in the A. halleri X A. lyrata BC1 progeny was markedly higher than that of the other paralogues. All MTP1s displayed the ability to functionally complement a Saccharomyces cerevisiæ zinc hypersensitive mutant. However, the paralogue showing the least complementation of the yeast mutant phenotype was one of the paralogues co-segregating with zinc tolerance. From our results, the hypothesis that pentaplication of MTP1 could be a major basis of the zinc tolerance character in A. halleri is strongly counter-balanced by the fact that members of the MTP1 family are likely to experience different evolutionary fates, some of which not concurring to increase zinc tolerance.
Highlights
Adaptation of an organism to a challenging environment entails dramatic modifications in cellular, physiological, and regulatory processes
Halleri, a BAC library [21] was screened with a labelled full length AhMTP1 probe obtained by PCR using primers designed from the published A. halleri Metal Tolerance Protein 1 (MTP1) mRNA sequence (AJ556183 accession)
With the aim to better understand the adaptive evolutionary processes leading to zinc hyperaccumulation and tolerance in A. halleri, we characterised the AhMTP1 gene family, which had been proposed to play a role in the control of these traits [14,17]
Summary
Adaptation of an organism to a challenging environment entails dramatic modifications in cellular, physiological, and regulatory processes. The absence of gene duplications is thought to severely limit the plasticity for a genome or species in adapting to a challenging environment [2]. Because selective constraints can be relaxed on duplicated genes initially underlying a same function, degenerative mutations can occur and result in the loss of function for one of the gene copies, creating a pseudogene (non-functionalization). A new advantageous mutation can occur and confer a new function to one of the gene copy (neo-functionalization). Rather than one gene duplicate retaining the original function and the others either degrading or evolving new functions, the original function of the single-copy gene may be partitioned among the duplicates (subfunctionalization). Whereas orthologues in different species are usually expected to share similar functions, paralogues within a genome could have no or different functions
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