Adaptive differences in gene expression associated with heavy metal tolerance in the soil arthropod Orchesella cincta

D. Roelofs, T.K.S. Janssens, M.J.T.N. Timmermans, B. Nota, A.G.H. Mariën, Z. Bochdanovits, B. Ijlstra, N.M. van Straalen

Research output: Contribution to journalArticleAcademicpeer-review

78 Citations (Scopus)

Abstract

Field-selected tolerance to heavy metals has been reported for Orchesella cincta (Arthropoda: Collembola) populations occurring at metal-contaminated mining sites. This tolerance correlated with heritable increase in metal excretion efficiency, less pronounced cadmium (Cd)-induced growth reduction and overexpression of the metallothionein gene. We applied transcriptomics to determine differential gene expression caused by this abiotic stress in reference and Cd-tolerant populations. Many cDNAs responded to Cd exposure in the reference population. Significantly fewer clones were Cd responsive in tolerant animals. Analysis of variance revealed transcripts that interact between Cd exposure and population. Hierarchical cluster analysis of these clones identified two major groups. The first one contained cDNAs that were up-regulated by Cd in the reference culture but non-responsive or down-regulated in tolerant animals. This cluster was also characterized by elevated constitutive expression in the tolerant population. Gene ontology analysis revealed that these cDNAs were involved in structural integrity of the cuticle, anti-microbial defence, calcium channel-blocking, sulphur assimilation and chromatin remodelling. The second group consisted of cDNAs down-regulated in reference animals but not responding or slightly up-regulated in tolerant animals. Their functions involved carbohydrate metabolic processes, Ca(2+)-dependent stress signalling, redox state, proteolysis and digestion. The reference population showed a strong signature of stress-induced genome-wide perturbation of gene expression, whereas the tolerant animals maintained normal gene expression upon Cd exposure. We confirmed the micro-evolutionary processes occurring in soil arthropod populations and suggest a major contribution of gene regulation to the evolution of a stress-adapted phenotype.

Original languageEnglish
Pages (from-to)3227-3239
Number of pages13
JournalMolecular ecology
Volume18
Issue number15
Early online date27 Jul 2009
DOIs
Publication statusPublished - Aug 2009

Keywords

  • Adaptation, Physiological
  • Animals
  • Arthropods
  • Cadmium
  • Cluster Analysis
  • DNA, Complementary
  • Evolution, Molecular
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Journal Article
  • Oligonucleotide Array Sequence Analysis
  • Research Support, Non-U.S. Gov't
  • Sequence Analysis, DNA
  • Soil
  • Soil Pollutants
  • Stress, Physiological

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