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      Caenorhabditis elegans Genomic Response to Soil Bacteria Predicts Environment-Specific Genetic Effects on Life History Traits

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          Abstract

          With the post-genomic era came a dramatic increase in high-throughput technologies, of which transcriptional profiling by microarrays was one of the most popular. One application of this technology is to identify genes that are differentially expressed in response to different environmental conditions. These experiments are constructed under the assumption that the differentially expressed genes are functionally important in the environment where they are induced. However, whether differential expression is predictive of functional importance has yet to be tested. Here we have addressed this expectation by employing Caenorhabditis elegans as a model for the interaction of native soil nematode taxa and soil bacteria. Using transcriptional profiling, we identified candidate genes regulated in response to different bacteria isolated in association with grassland nematodes or from grassland soils. Many of the regulated candidate genes are predicted to affect metabolism and innate immunity suggesting similar genes could influence nematode community dynamics in natural systems. Using mutations that inactivate 21 of the identified genes, we showed that most contribute to lifespan and/or fitness in a given bacterial environment. Although these bacteria may not be natural food sources for C. elegans, we show that changes in food source, as can occur in environmental disturbance, can have a large effect on gene expression, with important consequences for fitness. Moreover, we used regression analysis to demonstrate that for many genes the degree of differential gene expression between two bacterial environments predicted the magnitude of the effect of the loss of gene function on life history traits in those environments.

          Authors Summary

          Transcriptional profiling is often used to identify genes that are differentially regulated in response to different environments. These experiments assume that genes differentially expressed in response to different environments are functionally important and, furthermore, that the degree of differential gene expression is predictive of the magnitude of functional importance. In genetic experiments, function is inferred from analyzing the phenotypes of removing, reducing or altering gene function. However, to date, there has not been a specific test of how well the degree of differential gene expression between two (or more) environments is predictive of gene function. Here we identified C. elegans genes that were differentially expressed in response to different bacterial environments and determined the phenotypic differences of life history traits between these environments using mutant strains that compromised gene function. We found that differential gene expression is indeed predictive of functional importance of the identified genes in different environments. This observation has important implications for interpreting the results of transcriptional profiling experiments of populations of organisms in their native environments, where in many cases the genetic tools to disrupt gene function have not yet been fully developed or interfering with gene functions in nature may not be feasible.

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          Most cited references66

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          Regulation of aging and age-related disease by DAF-16 and heat-shock factor.

          A.-L. Hsu (2003)
          The Caenorhabditis elegans transcription factor HSF-1, which regulates the heat-shock response, also influences aging. Reducing hsf-1 activity accelerates tissue aging and shortens life-span, and we show that hsf-1 overexpression extends lifespan. We find that HSF-1, like the transcription factor DAF-16, is required for daf-2-insulin/IGF-1 receptor mutations to extend life-span. Our findings suggest this is because HSF-1 and DAF-16 together activate expression of specific genes, including genes encoding small heat-shock proteins, which in turn promote longevity. The small heat-shock proteins also delay the onset of polyglutamine-expansion protein aggregation, suggesting that these proteins couple the normal aging process to this type of age-related disease.
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            Structure and function of the soil microbial community in a long-term fertilizer experiment

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              The genetics of caloric restriction in Caenorhabditis elegans.

              Low caloric intake (caloric restriction) can lengthen the life span of a wide range of animals and possibly even of humans. To understand better how caloric restriction lengthens life span, we used genetic methods and criteria to investigate its mechanism of action in the nematode Caenorhabditis elegans. Mutations in many genes (eat genes) result in partial starvation of the worm by disrupting the function of the pharynx, the feeding organ. We found that most eat mutations significantly lengthen life span (by up to 50%). In C. elegans, mutations in a number of other genes that can extend life span have been found. Two genetically distinct mechanisms of life span extension are known: a mechanism involving genes that regulate dauer formation (age-1, daf-2, daf-16, and daf-28) and a mechanism involving genes that affect the rate of development and behavior (clk-1, clk-2, clk-3, and gro-1). We find that the long life of eat-2 mutants does not require the activity of DAF-16 and that eat-2; daf-2 double mutants live even longer than extremely long-lived daf-2 mutants. These findings demonstrate that food restriction lengthens life span by a mechanism distinct from that of dauer-formation mutants. In contrast, we find that food restriction does not further increase the life span of long-lived clk-1 mutants, suggesting that clk-1 and caloric restriction affect similar processes.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                June 2009
                June 2009
                5 June 2009
                : 5
                : 6
                : e1000503
                Affiliations
                [1 ]Ecological Genomics Institute, Kansas State University, Manhattan, Kansas, United States of America
                [2 ]Division of Biology, Kansas State University, Manhattan, Kansas, United States of America
                [3 ]Department of Plant Pathology, Kansas State University, Manhattan, Kansas, United States of America
                Stanford University Medical Center, United States of America
                Author notes

                Conceived and designed the experiments: JDC MAH. Performed the experiments: JDC BCC. Analyzed the data: JDC KLJ TCT. Contributed reagents/materials/analysis tools: KLJ. Wrote the paper: JDC MAH.

                Article
                08-PLGE-RA-1765R2
                10.1371/journal.pgen.1000503
                2684633
                19503598
                8886cc1d-8c7b-481f-be98-72f9a0b543ff
                Coolon et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 2 January 2009
                : 4 May 2009
                Page count
                Pages: 12
                Categories
                Research Article
                Ecology/Global Change Ecology
                Genetics and Genomics/Functional Genomics
                Genetics and Genomics/Gene Discovery
                Genetics and Genomics/Gene Expression
                Immunology/Innate Immunity

                Genetics
                Genetics

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