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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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Positions of QTL Associated with Body Size and the Slope of the TRBQTL for body size at different temperatures (12 °C [dotted line] and 24 °C [dashed line]) [26] and the slope of the TRB (solid line) at Chromosomes III and IV. Triangles are the peak of the QTL and the horizontal bars are CIs. Values near the bars represent the likelihood ratio values. Only those parts of the chromosomes are shown where QTLs were detected.
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pgen-0030034-g002: Positions of QTL Associated with Body Size and the Slope of the TRBQTL for body size at different temperatures (12 °C [dotted line] and 24 °C [dashed line]) [26] and the slope of the TRB (solid line) at Chromosomes III and IV. Triangles are the peak of the QTL and the horizontal bars are CIs. Values near the bars represent the likelihood ratio values. Only those parts of the chromosomes are shown where QTLs were detected.

Mentions: Figure 2 shows the detected QTLs associated with the slope of the TRB. Two QTLs on Chromosome IV were associated with a negative effect on the slope of the TRB and were linked to CB alleles. The distal QTL at Chromosome IV showed pleiotropy or linkage for body size at 24 °C (additive effect of 4%). We aimed to identify the gene(s) controlling the QTL at Chromosome IV with a peak at marker pkP4095 at 12 cM, because this QTL was uniquely associated with TRB (hence we named it the TRB-locus) and not with body size itself at 12 °C or 24 °C. This locus had a relatively large additive effect of 34% of the total standard deviation and explained 11% of the among-RIL variance. Introgression of a CB segment spanning the TRB-locus into an N2 background confirmed the QTL analysis. Phenotyping of NIL WN17–9 carrying an ~6-cM region of the TRB locus revealed no significant body-size difference between low and high temperature (Figure 3). Three other QTLs on Chromosome III increased the slope and each of these QTLs was linked to N2 alleles and showed a pleiotropic or close linkage effect for body size at 12 °C [26].


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)

Positions of QTL Associated with Body Size and the Slope of the TRBQTL for body size at different temperatures (12 °C [dotted line] and 24 °C [dashed line]) [26] and the slope of the TRB (solid line) at Chromosomes III and IV. Triangles are the peak of the QTL and the horizontal bars are CIs. Values near the bars represent the likelihood ratio values. Only those parts of the chromosomes are shown where QTLs were detected.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-0030034-g002: Positions of QTL Associated with Body Size and the Slope of the TRBQTL for body size at different temperatures (12 °C [dotted line] and 24 °C [dashed line]) [26] and the slope of the TRB (solid line) at Chromosomes III and IV. Triangles are the peak of the QTL and the horizontal bars are CIs. Values near the bars represent the likelihood ratio values. Only those parts of the chromosomes are shown where QTLs were detected.
Mentions: Figure 2 shows the detected QTLs associated with the slope of the TRB. Two QTLs on Chromosome IV were associated with a negative effect on the slope of the TRB and were linked to CB alleles. The distal QTL at Chromosome IV showed pleiotropy or linkage for body size at 24 °C (additive effect of 4%). We aimed to identify the gene(s) controlling the QTL at Chromosome IV with a peak at marker pkP4095 at 12 cM, because this QTL was uniquely associated with TRB (hence we named it the TRB-locus) and not with body size itself at 12 °C or 24 °C. This locus had a relatively large additive effect of 34% of the total standard deviation and explained 11% of the among-RIL variance. Introgression of a CB segment spanning the TRB-locus into an N2 background confirmed the QTL analysis. Phenotyping of NIL WN17–9 carrying an ~6-cM region of the TRB locus revealed no significant body-size difference between low and high temperature (Figure 3). Three other QTLs on Chromosome III increased the slope and each of these QTLs was linked to N2 alleles and showed a pleiotropic or close linkage effect for body size at 12 °C [26].

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