Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae.

Temperature sensation guides animals to avoid temperature extremes and to seek their optimal temperatures. The larval stage of Drosophila development has a dramatic effect on temperature preference. While early-stage Drosophila larvae pursue a warm temperature, late-stage larvae seek a significantly...

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Main Authors: Jordan J Tyrrell, Jackson T Wilbourne, Alisa A Omelchenko, Jin Yoon, Lina Ni
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-04-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009499&type=printable
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author Jordan J Tyrrell
Jackson T Wilbourne
Alisa A Omelchenko
Jin Yoon
Lina Ni
author_facet Jordan J Tyrrell
Jackson T Wilbourne
Alisa A Omelchenko
Jin Yoon
Lina Ni
author_sort Jordan J Tyrrell
collection DOAJ
description Temperature sensation guides animals to avoid temperature extremes and to seek their optimal temperatures. The larval stage of Drosophila development has a dramatic effect on temperature preference. While early-stage Drosophila larvae pursue a warm temperature, late-stage larvae seek a significantly lower temperature. Previous studies suggest that this transition depends on multiple rhodopsins at the late larval stage. Here, we show that early-stage larvae, in which dorsal organ cool cells (DOCCs) are functionally blocked, exhibit similar cool preference to that of wild type late-stage larvae. The molecular thermoreceptors in DOCCs are formed by three members of the Ionotropic Receptor (IR) family, IR21a, IR93a, and IR25a. Early-stage larvae of each Ir mutant pursue a cool temperature, similar to that of wild type late-stage larvae. At the late larval stage, DOCCs express decreased IR proteins and exhibit reduced cool responses. Importantly, late-stage larvae that overexpress IR21a, IR93a, and IR25a in DOCCs exhibit similar warm preference to that of wild type early-stage larvae. These data suggest that IR21a, IR93a, and IR25a in DOCCs navigate early-stage larvae to avoid cool temperatures and the reduction of these IR proteins in DOCCs results in animals remaining in cool regions during the late larval stage. Together with previous studies, we conclude that multiple temperature-sensing systems are regulated for the transition of temperature preference in fruit fly larvae.
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publishDate 2021-04-01
publisher Public Library of Science (PLoS)
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spelling doaj-art-242a229aca8143bc98afdd4c54f0c5452025-08-20T02:55:32ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-04-01174e100949910.1371/journal.pgen.1009499Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae.Jordan J TyrrellJackson T WilbourneAlisa A OmelchenkoJin YoonLina NiTemperature sensation guides animals to avoid temperature extremes and to seek their optimal temperatures. The larval stage of Drosophila development has a dramatic effect on temperature preference. While early-stage Drosophila larvae pursue a warm temperature, late-stage larvae seek a significantly lower temperature. Previous studies suggest that this transition depends on multiple rhodopsins at the late larval stage. Here, we show that early-stage larvae, in which dorsal organ cool cells (DOCCs) are functionally blocked, exhibit similar cool preference to that of wild type late-stage larvae. The molecular thermoreceptors in DOCCs are formed by three members of the Ionotropic Receptor (IR) family, IR21a, IR93a, and IR25a. Early-stage larvae of each Ir mutant pursue a cool temperature, similar to that of wild type late-stage larvae. At the late larval stage, DOCCs express decreased IR proteins and exhibit reduced cool responses. Importantly, late-stage larvae that overexpress IR21a, IR93a, and IR25a in DOCCs exhibit similar warm preference to that of wild type early-stage larvae. These data suggest that IR21a, IR93a, and IR25a in DOCCs navigate early-stage larvae to avoid cool temperatures and the reduction of these IR proteins in DOCCs results in animals remaining in cool regions during the late larval stage. Together with previous studies, we conclude that multiple temperature-sensing systems are regulated for the transition of temperature preference in fruit fly larvae.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009499&type=printable
spellingShingle Jordan J Tyrrell
Jackson T Wilbourne
Alisa A Omelchenko
Jin Yoon
Lina Ni
Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae.
PLoS Genetics
title Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae.
title_full Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae.
title_fullStr Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae.
title_full_unstemmed Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae.
title_short Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae.
title_sort ionotropic receptor dependent cool cells control the transition of temperature preference in drosophila larvae
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009499&type=printable
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AT jacksontwilbourne ionotropicreceptordependentcoolcellscontrolthetransitionoftemperaturepreferenceindrosophilalarvae
AT alisaaomelchenko ionotropicreceptordependentcoolcellscontrolthetransitionoftemperaturepreferenceindrosophilalarvae
AT jinyoon ionotropicreceptordependentcoolcellscontrolthetransitionoftemperaturepreferenceindrosophilalarvae
AT linani ionotropicreceptordependentcoolcellscontrolthetransitionoftemperaturepreferenceindrosophilalarvae