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...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2019-01-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1007423 |
| _version_ | 1818348753782833152 |
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| author | Qing-Wei Meng Qing-Yu Xu Tao-Tao Zhu Lin Jin Kai-Yun Fu Wen-Chao Guo Guo-Qing Li |
| author_facet | Qing-Wei Meng Qing-Yu Xu Tao-Tao Zhu Lin Jin Kai-Yun Fu Wen-Chao Guo Guo-Qing Li |
| author_sort | Qing-Wei Meng |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-13T17:55:04Z |
| format | Article |
| id | doaj.art-0aa5b04c23ed47e68524f5b8a4f399eb |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-13T17:55:04Z |
| publishDate | 2019-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-0aa5b04c23ed47e68524f5b8a4f399eb2022-12-21T23:36:24ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042019-01-01151e100742310.1371/journal.pgen.1007423Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae.Qing-Wei MengQing-Yu XuTao-Tao ZhuLin JinKai-Yun FuWen-Chao GuoGuo-Qing LiMany 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.https://doi.org/10.1371/journal.pgen.1007423 |
| spellingShingle | Qing-Wei Meng Qing-Yu Xu Tao-Tao Zhu Lin Jin Kai-Yun Fu Wen-Chao Guo Guo-Qing Li Hormonal signaling cascades required for phototaxis switch in wandering Leptinotarsa decemlineata larvae. PLoS Genetics |
| 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 |
| url | https://doi.org/10.1371/journal.pgen.1007423 |
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