Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect
Insects living in the temperate zone enter a physiological state of arrested or slowed development to overcome an adverse season, such as winter. Developmental arrest, called diapause, occurs at a species-specific developmental stage, and embryonic and pupal diapauses have been extensively studied in mostly holometabolous insects. Some other insects overwinter in the nymphal stage with slow growth for which the mechanism is poorly understood. Here, we show that this nymphal period of slow growth is regulated by temperature and photoperiod through separate pathways in the cricket Modicogryllus siamensis. The former regulates the growth rate, at least in part, through the insulin / target of rapamycin (TOR) signaling pathway. Lower temperature down-regulates the expression of insulin-like peptide (Ms’Ilp) and Target of rapamycin (Ms’Tor) genes to slow down the growth rate without affecting the number of molts. The latter regulates the number of molts independent of temperature. Short days increase the number of molts through activation of the juvenile hormone (JH) pathway and down-regulation of myoglianin (Ms’myo), a member of the TGFβ family, which induces adult metamorphosis. In contrast, long days regulate Ms’myo expression to increase during the fifth to sixth instar to initiate adult metamorphosis. When Ms’myo expression is suppressed, juvenile hormone O-methyl transferase (Ms’jhamt) was up-regulated and increased molts to prolong the nymphal period even under long-day conditions. The present findings suggested that the photoperiod regulated Ms’myo, and the JH signaling pathway and the temperature-controlled insulin/TOR pathway cooperated to regulate nymphal development for overwintering to achieve seasonal adaptation of the life cycle in M. siamensis.
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Language: | English |
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National Academy of Sciences (U.S.)
2020-03-10
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Subjects: | Ymphal development, Photoperiod, Temperatures, Myo, Insulin/TOR signaling pathway, |
Online Access: | http://hdl.handle.net/10261/218833 http://dx.doi.org/10.13039/501100001691 |
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dig-ibe-es-10261-2188332021-12-28T15:43:17Z Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect Miki, Taiki Shinohara, Tsugumichi Chafino, Silvia Noji, Sumihare Tomioka, Kenji Japan Society for the Promotion of Science Ymphal development Photoperiod Temperatures Myo Insulin/TOR signaling pathway Insects living in the temperate zone enter a physiological state of arrested or slowed development to overcome an adverse season, such as winter. Developmental arrest, called diapause, occurs at a species-specific developmental stage, and embryonic and pupal diapauses have been extensively studied in mostly holometabolous insects. Some other insects overwinter in the nymphal stage with slow growth for which the mechanism is poorly understood. Here, we show that this nymphal period of slow growth is regulated by temperature and photoperiod through separate pathways in the cricket Modicogryllus siamensis. The former regulates the growth rate, at least in part, through the insulin / target of rapamycin (TOR) signaling pathway. Lower temperature down-regulates the expression of insulin-like peptide (Ms’Ilp) and Target of rapamycin (Ms’Tor) genes to slow down the growth rate without affecting the number of molts. The latter regulates the number of molts independent of temperature. Short days increase the number of molts through activation of the juvenile hormone (JH) pathway and down-regulation of myoglianin (Ms’myo), a member of the TGFβ family, which induces adult metamorphosis. In contrast, long days regulate Ms’myo expression to increase during the fifth to sixth instar to initiate adult metamorphosis. When Ms’myo expression is suppressed, juvenile hormone O-methyl transferase (Ms’jhamt) was up-regulated and increased molts to prolong the nymphal period even under long-day conditions. The present findings suggested that the photoperiod regulated Ms’myo, and the JH signaling pathway and the temperature-controlled insulin/TOR pathway cooperated to regulate nymphal development for overwintering to achieve seasonal adaptation of the life cycle in M. siamensis. This study was supported in part by the grant from the Japan Society for the Promotion of Science (23370033) (to K.T.). Peer reviewed 2020-08-28T10:42:47Z 2020-08-28T10:42:47Z 2020-03-10 artículo http://purl.org/coar/resource_type/c_6501 Proceedings of the National Academy of Sciences of the USA 117(10): 5525-5531 (2020) 0027-8424 http://hdl.handle.net/10261/218833 10.1073/pnas.1922747117 1091-6490 http://dx.doi.org/10.13039/501100001691 32098850 en https://doi.org/10.1073/pnas.1922747117 Sí none National Academy of Sciences (U.S.) |
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Ymphal development Photoperiod Temperatures Myo Insulin/TOR signaling pathway Ymphal development Photoperiod Temperatures Myo Insulin/TOR signaling pathway |
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Ymphal development Photoperiod Temperatures Myo Insulin/TOR signaling pathway Ymphal development Photoperiod Temperatures Myo Insulin/TOR signaling pathway Miki, Taiki Shinohara, Tsugumichi Chafino, Silvia Noji, Sumihare Tomioka, Kenji Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect |
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Insects living in the temperate zone enter a physiological state of arrested or slowed development to overcome an adverse season, such as winter. Developmental arrest, called diapause, occurs at a species-specific developmental stage, and embryonic and pupal diapauses have been extensively studied in mostly holometabolous insects. Some other insects overwinter in the nymphal stage with slow growth for which the mechanism is poorly understood. Here, we show that this nymphal period of slow growth is regulated by temperature and photoperiod through separate pathways in the cricket Modicogryllus siamensis. The former regulates the growth rate, at least in part, through the insulin / target of rapamycin (TOR) signaling pathway. Lower temperature down-regulates the expression of insulin-like peptide (Ms’Ilp) and Target of rapamycin (Ms’Tor) genes to slow down the growth rate without affecting the number of molts. The latter regulates the number of molts independent of temperature. Short days increase the number of molts through activation of the juvenile hormone (JH) pathway and down-regulation of myoglianin (Ms’myo), a member of the TGFβ family, which induces adult metamorphosis. In contrast, long days regulate Ms’myo expression to increase during the fifth to sixth instar to initiate adult metamorphosis. When Ms’myo expression is suppressed, juvenile hormone O-methyl transferase (Ms’jhamt) was up-regulated and increased molts to prolong the nymphal period even under long-day conditions. The present findings suggested that the photoperiod regulated Ms’myo, and the JH signaling pathway and the temperature-controlled insulin/TOR pathway cooperated to regulate nymphal development for overwintering to achieve seasonal adaptation of the life cycle in M. siamensis. |
author2 |
Japan Society for the Promotion of Science |
author_facet |
Japan Society for the Promotion of Science Miki, Taiki Shinohara, Tsugumichi Chafino, Silvia Noji, Sumihare Tomioka, Kenji |
format |
artículo |
topic_facet |
Ymphal development Photoperiod Temperatures Myo Insulin/TOR signaling pathway |
author |
Miki, Taiki Shinohara, Tsugumichi Chafino, Silvia Noji, Sumihare Tomioka, Kenji |
author_sort |
Miki, Taiki |
title |
Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect |
title_short |
Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect |
title_full |
Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect |
title_fullStr |
Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect |
title_full_unstemmed |
Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect |
title_sort |
photoperiod and temperature separately regulate nymphal development through jh and insulin/tor signaling pathways in an insect |
publisher |
National Academy of Sciences (U.S.) |
publishDate |
2020-03-10 |
url |
http://hdl.handle.net/10261/218833 http://dx.doi.org/10.13039/501100001691 |
work_keys_str_mv |
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