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A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.

Kammenga JE, Doroszuk A, Riksen JA, Hazendonk E, Spiridon L, Petrescu AJ, Tijsterman M, Plasterk RH, Bakker J - PLoS Genet. (2007)

Bottom Line: We found that the Caenorhabditis elegans wild-type N2 complied with the temperature-size rule, whereas wild-type CB4856 defied it.Homology modelling predicts that F96L reduces TRA-3 activity by destabilizing the DII-A domain.These findings provide a novel step toward the molecular understanding of the temperature-size rule, which has puzzled biologists for decades.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Nematology, Wageningen University, Wageningen, The Netherlands. Jan.Kammenga@wur.nl

ABSTRACT
Ectotherms rely for their body heat on surrounding temperatures. A key question in biology is why most ectotherms mature at a larger size at lower temperatures, a phenomenon known as the temperature-size rule. Since temperature affects virtually all processes in a living organism, current theories to explain this phenomenon are diverse and complex and assert often from opposing assumptions. Although widely studied, the molecular genetic control of the temperature-size rule is unknown. We found that the Caenorhabditis elegans wild-type N2 complied with the temperature-size rule, whereas wild-type CB4856 defied it. Using a candidate gene approach based on an N2 x CB4856 recombinant inbred panel in combination with mutant analysis, complementation, and transgenic studies, we show that a single nucleotide polymorphism in tra-3 leads to mutation F96L in the encoded calpain-like protease. This mutation attenuates the ability of CB4856 to grow larger at low temperature. Homology modelling predicts that F96L reduces TRA-3 activity by destabilizing the DII-A domain. The data show that size adaptation of ectotherms to temperature changes may be less complex than previously thought because a subtle wild-type polymorphism modulates the temperature responsiveness of body size. These findings provide a novel step toward the molecular understanding of the temperature-size rule, which has puzzled biologists for decades.

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The tra-3 N2 Allele Makes CB Grow Larger at Low TemperatureWe measured body size in transgenic CB strains carrying the N2 allele of tra-3. Average values are shown for four to five independently derived strains of CB(gfp and tra-3(+)) and CB(gfp). The transgenic strains grew significantly larger at low temperature (t-test, n = 39, p < 0.0001). Bars are standard deviation.
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pgen-0030034-g005: The tra-3 N2 Allele Makes CB Grow Larger at Low TemperatureWe measured body size in transgenic CB strains carrying the N2 allele of tra-3. Average values are shown for four to five independently derived strains of CB(gfp and tra-3(+)) and CB(gfp). The transgenic strains grew significantly larger at low temperature (t-test, n = 39, p < 0.0001). Bars are standard deviation.

Mentions: We next asked whether the N2 version of the tra-3 gene could transform CB to have a larger body size at low temperature. Therefore we carried out a transgenic assay in which tra-3 from N2 was transferred to the CB background. We exposed independently derived strains of CB(gfp) (control strains) and CB(gfp and tra-3(+)) to 12 °C and 24 °C. Figure 5 shows that the N2 phenotype was rescued in CB(gfp and tra-3(+)) because it grew 24% larger at the low temperature. CB(gfp) retained the CB phenotype because it did not grow larger at low temperature.


A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.

Kammenga JE, Doroszuk A, Riksen JA, Hazendonk E, Spiridon L, Petrescu AJ, Tijsterman M, Plasterk RH, Bakker J - PLoS Genet. (2007)

The tra-3 N2 Allele Makes CB Grow Larger at Low TemperatureWe measured body size in transgenic CB strains carrying the N2 allele of tra-3. Average values are shown for four to five independently derived strains of CB(gfp and tra-3(+)) and CB(gfp). The transgenic strains grew significantly larger at low temperature (t-test, n = 39, p < 0.0001). Bars are standard deviation.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1808073&req=5

pgen-0030034-g005: The tra-3 N2 Allele Makes CB Grow Larger at Low TemperatureWe measured body size in transgenic CB strains carrying the N2 allele of tra-3. Average values are shown for four to five independently derived strains of CB(gfp and tra-3(+)) and CB(gfp). The transgenic strains grew significantly larger at low temperature (t-test, n = 39, p < 0.0001). Bars are standard deviation.
Mentions: We next asked whether the N2 version of the tra-3 gene could transform CB to have a larger body size at low temperature. Therefore we carried out a transgenic assay in which tra-3 from N2 was transferred to the CB background. We exposed independently derived strains of CB(gfp) (control strains) and CB(gfp and tra-3(+)) to 12 °C and 24 °C. Figure 5 shows that the N2 phenotype was rescued in CB(gfp and tra-3(+)) because it grew 24% larger at the low temperature. CB(gfp) retained the CB phenotype because it did not grow larger at low temperature.

Bottom Line: We found that the Caenorhabditis elegans wild-type N2 complied with the temperature-size rule, whereas wild-type CB4856 defied it.Homology modelling predicts that F96L reduces TRA-3 activity by destabilizing the DII-A domain.These findings provide a novel step toward the molecular understanding of the temperature-size rule, which has puzzled biologists for decades.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Nematology, Wageningen University, Wageningen, The Netherlands. Jan.Kammenga@wur.nl

ABSTRACT
Ectotherms rely for their body heat on surrounding temperatures. A key question in biology is why most ectotherms mature at a larger size at lower temperatures, a phenomenon known as the temperature-size rule. Since temperature affects virtually all processes in a living organism, current theories to explain this phenomenon are diverse and complex and assert often from opposing assumptions. Although widely studied, the molecular genetic control of the temperature-size rule is unknown. We found that the Caenorhabditis elegans wild-type N2 complied with the temperature-size rule, whereas wild-type CB4856 defied it. Using a candidate gene approach based on an N2 x CB4856 recombinant inbred panel in combination with mutant analysis, complementation, and transgenic studies, we show that a single nucleotide polymorphism in tra-3 leads to mutation F96L in the encoded calpain-like protease. This mutation attenuates the ability of CB4856 to grow larger at low temperature. Homology modelling predicts that F96L reduces TRA-3 activity by destabilizing the DII-A domain. The data show that size adaptation of ectotherms to temperature changes may be less complex than previously thought because a subtle wild-type polymorphism modulates the temperature responsiveness of body size. These findings provide a novel step toward the molecular understanding of the temperature-size rule, which has puzzled biologists for decades.

Show MeSH
Related in: MedlinePlus