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Open Access Research article

Gene-environment and protein-degradation signatures characterize genomic and phenotypic diversity in wild Caenorhabditis elegans populations

Rita JM Volkers1, L Basten Snoek1, Caspara J van Hellenberg Hubar1, Renata Coopman2, Wei Chen3, Wentao Yang3, Mark G Sterken1, Hinrich Schulenburg3, Bart P Braeckman2 and Jan E Kammenga1*

Author Affiliations

1 Laboratory of Nematology, Wageningen University, Droevendaalsesteeg 1, Wageningen 6708PB, The Netherlands

2 Biology Department, Ghent University, Proeftuinstraat 86 N1, B-9000 Gent, Belgium

3 Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian Albrechts-Universitaet zu Kiel, Am Botanischen Garten 1-9, Kiel 24118, Germany

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BMC Biology 2013, 11:93  doi:10.1186/1741-7007-11-93

Published: 19 August 2013

Abstract

Background

Analyzing and understanding the relationship between genotypes and phenotypes is at the heart of genetics. Research on the nematode Caenorhabditis elegans has been instrumental for unraveling genotype-phenotype relations, and has important implications for understanding the biology of mammals, but almost all studies, including forward and reverse genetic screens, are limited by investigations in only one canonical genotype. This hampers the detection and functional analysis of allelic variants, which play a key role in controlling many complex traits. It is therefore essential to explore the full potential of the natural genetic variation and evolutionary context of the genotype-phenotype map in wild C. elegans populations.

Results

We used multiple wild C. elegans populations freshly isolated from local sites to investigate gene sequence polymorphisms and a multitude of phenotypes including the transcriptome, fitness, and behavioral traits. The genotype, transcriptome, and a number of fitness traits showed a direct link with the original site of the strains. The separation between the isolation sites was prevalent on all chromosomes, but chromosome V was the largest contributor to this variation. These results were supported by a differential food preference of the wild isolates for naturally co-existing bacterial species. Comparing polymorphic genes between the populations with a set of genes extracted from 19 different studies on gene expression in C. elegans exposed to biotic and abiotic factors, such as bacteria, osmotic pressure, and temperature, revealed a significant enrichment for genes involved in gene-environment interactions and protein degradation.

Conclusions

We found that wild C. elegans populations are characterized by gene-environment signatures, and we have unlocked a wealth of genotype-phenotype relations for the first time. Studying natural isolates provides a treasure trove of evidence compared with that unearthed by the current research in C. elegans, which covers only a diminutive part of the myriad of genotype-phenotype relations that are present in the wild.

Keywords:
Gene-environment interactions; Genotype-phenotype relations; Wild C. elegans strains; Transcriptomic diversity