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Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae

Many animals exploit several niches sequentially during their life cycles, a fitness referred to as ontogenetic niche shift (ONS). To successfully accomplish ONS, transition between development stages is often coupled with changes in one or more primitive, instinctive behaviors. Yet, the underlining...

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Autores principales: Meng, Qing-Wei, Xu, Qing-Yu, Zhu, Tao-Tao, Jin, Lin, Fu, Kai-Yun, Guo, Wen-Chao, Li, Guo-Qing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6336328/
https://www.ncbi.nlm.nih.gov/pubmed/30615614
http://dx.doi.org/10.1371/journal.pgen.1007423
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author Meng, Qing-Wei
Xu, Qing-Yu
Zhu, Tao-Tao
Jin, Lin
Fu, Kai-Yun
Guo, Wen-Chao
Li, Guo-Qing
author_facet Meng, Qing-Wei
Xu, Qing-Yu
Zhu, Tao-Tao
Jin, Lin
Fu, Kai-Yun
Guo, Wen-Chao
Li, Guo-Qing
author_sort Meng, Qing-Wei
collection PubMed
description Many animals exploit several niches sequentially during their life cycles, a fitness referred to as ontogenetic niche shift (ONS). To successfully accomplish ONS, transition between development stages is often coupled with changes in one or more primitive, instinctive behaviors. Yet, the underlining molecular mechanisms remain elusive. We show here that Leptinotarsa decemlineata larvae finish their ONS at the wandering stage by leaving the plant and pupating in soil. At middle wandering phase, larvae also switch their phototactic behavior, from photophilic at foraging period to photophobic. We find that enhancement of juvenile hormone (JH) signal delays the phototactic switch, and vise verse. Moreover, RNA interference (RNAi)-aided knockdown of LdPTTH (prothoracicotropic hormone gene) or LdTorso (PTTH receptor gene) impairs avoidance response to light, a phenotype nonrescuable by 20-hydroxyecdysone. Consequently, the RNAi beetles pupate at the soil surface or in shallow layer of soil, with most of them failing to construct pupation chambers. Furthermore, a combination of depletion of LdPTTH/LdTorso and disturbance of JH signal causes no additive effects on light avoidance response and pupation site selection. Finally, we establish that TrpA1 (transient receptor potential (TRP) cation channel) is necessary for light avoidance behavior, acting downstream of PTTH. We conclude that JH/PTTH cascade concomitantly regulates metamorphosis and the phototaxis switch, to drive ONS of the wandering beetles from plant into soil to start the immobile pupal stage.
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spelling pubmed-63363282019-01-30 Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae Meng, Qing-Wei Xu, Qing-Yu Zhu, Tao-Tao Jin, Lin Fu, Kai-Yun Guo, Wen-Chao Li, Guo-Qing PLoS Genet Research Article Many animals exploit several niches sequentially during their life cycles, a fitness referred to as ontogenetic niche shift (ONS). To successfully accomplish ONS, transition between development stages is often coupled with changes in one or more primitive, instinctive behaviors. Yet, the underlining molecular mechanisms remain elusive. We show here that Leptinotarsa decemlineata larvae finish their ONS at the wandering stage by leaving the plant and pupating in soil. At middle wandering phase, larvae also switch their phototactic behavior, from photophilic at foraging period to photophobic. We find that enhancement of juvenile hormone (JH) signal delays the phototactic switch, and vise verse. Moreover, RNA interference (RNAi)-aided knockdown of LdPTTH (prothoracicotropic hormone gene) or LdTorso (PTTH receptor gene) impairs avoidance response to light, a phenotype nonrescuable by 20-hydroxyecdysone. Consequently, the RNAi beetles pupate at the soil surface or in shallow layer of soil, with most of them failing to construct pupation chambers. Furthermore, a combination of depletion of LdPTTH/LdTorso and disturbance of JH signal causes no additive effects on light avoidance response and pupation site selection. Finally, we establish that TrpA1 (transient receptor potential (TRP) cation channel) is necessary for light avoidance behavior, acting downstream of PTTH. We conclude that JH/PTTH cascade concomitantly regulates metamorphosis and the phototaxis switch, to drive ONS of the wandering beetles from plant into soil to start the immobile pupal stage. Public Library of Science 2019-01-07 /pmc/articles/PMC6336328/ /pubmed/30615614 http://dx.doi.org/10.1371/journal.pgen.1007423 Text en © 2019 Meng et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Meng, Qing-Wei
Xu, Qing-Yu
Zhu, Tao-Tao
Jin, Lin
Fu, Kai-Yun
Guo, Wen-Chao
Li, Guo-Qing
Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae
title Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae
title_full Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae
title_fullStr Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae
title_full_unstemmed Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae
title_short Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae
title_sort hormonal signaling cascades required for phototaxis switch in wandering leptinotarsa decemlineata larvae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6336328/
https://www.ncbi.nlm.nih.gov/pubmed/30615614
http://dx.doi.org/10.1371/journal.pgen.1007423
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