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

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 t...

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Main Authors: Jan E Kammenga, Agnieszka Doroszuk, Joost A G Riksen, Esther Hazendonk, Laurentiu Spiridon, Andrei-Jose Petrescu, Marcel Tijsterman, Ronald H A Plasterk, Jaap Bakker
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-03-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC1808073?pdf=render
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spelling doaj-5e3d3876ddf249a98f0cc2d9a1f4e5032020-11-24T21:41:58ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042007-03-0133e3410.1371/journal.pgen.0030034A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.Jan E KammengaAgnieszka DoroszukJoost A G RiksenEsther HazendonkLaurentiu SpiridonAndrei-Jose PetrescuMarcel TijstermanRonald H A PlasterkJaap BakkerEctotherms 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.http://europepmc.org/articles/PMC1808073?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Jan E Kammenga
Agnieszka Doroszuk
Joost A G Riksen
Esther Hazendonk
Laurentiu Spiridon
Andrei-Jose Petrescu
Marcel Tijsterman
Ronald H A Plasterk
Jaap Bakker
spellingShingle Jan E Kammenga
Agnieszka Doroszuk
Joost A G Riksen
Esther Hazendonk
Laurentiu Spiridon
Andrei-Jose Petrescu
Marcel Tijsterman
Ronald H A Plasterk
Jaap Bakker
A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.
PLoS Genetics
author_facet Jan E Kammenga
Agnieszka Doroszuk
Joost A G Riksen
Esther Hazendonk
Laurentiu Spiridon
Andrei-Jose Petrescu
Marcel Tijsterman
Ronald H A Plasterk
Jaap Bakker
author_sort Jan E Kammenga
title A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.
title_short A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.
title_full A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.
title_fullStr A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.
title_full_unstemmed A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.
title_sort caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2007-03-01
description 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.
url http://europepmc.org/articles/PMC1808073?pdf=render
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