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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Bibliographic Details
Main Authors: Miki, Taiki, Shinohara, Tsugumichi, Chafino, Silvia, Noji, Sumihare, Tomioka, Kenji
Other Authors: Japan Society for the Promotion of Science
Format: artículo biblioteca
Language:English
Published: National Academy of Sciences (U.S.) 2020-03-10
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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spelling 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.)
institution IBE ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-ibe-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IBE España
language English
topic Ymphal development
Photoperiod
Temperatures
Myo
Insulin/TOR signaling pathway
Ymphal development
Photoperiod
Temperatures
Myo
Insulin/TOR signaling pathway
spellingShingle 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
description 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
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