Cargando…

Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki

Polypedilum vanderplanki is a striking and unique example of an insect that can survive almost complete desiccation. Its genome and a set of dehydration–rehydration transcriptomes, together with the genome of Polypedilum nubifer (a congeneric desiccation-sensitive midge), were recently released. Her...

Descripción completa

Detalles Bibliográficos
Autores principales: Mazin, Pavel V., Shagimardanova, Elena, Kozlova, Olga, Cherkasov, Alexander, Sutormin, Roman, Stepanova, Vita V., Stupnikov, Alexey, Logacheva, Maria, Penin, Aleksey, Sogame, Yoichiro, Cornette, Richard, Tokumoto, Shoko, Miyata, Yugo, Kikawada, Takahiro, Gelfand, Mikhail S., Gusev, Oleg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5877948/
https://www.ncbi.nlm.nih.gov/pubmed/29463761
http://dx.doi.org/10.1073/pnas.1719493115
_version_ 1783310794464690176
author Mazin, Pavel V.
Shagimardanova, Elena
Kozlova, Olga
Cherkasov, Alexander
Sutormin, Roman
Stepanova, Vita V.
Stupnikov, Alexey
Logacheva, Maria
Penin, Aleksey
Sogame, Yoichiro
Cornette, Richard
Tokumoto, Shoko
Miyata, Yugo
Kikawada, Takahiro
Gelfand, Mikhail S.
Gusev, Oleg
author_facet Mazin, Pavel V.
Shagimardanova, Elena
Kozlova, Olga
Cherkasov, Alexander
Sutormin, Roman
Stepanova, Vita V.
Stupnikov, Alexey
Logacheva, Maria
Penin, Aleksey
Sogame, Yoichiro
Cornette, Richard
Tokumoto, Shoko
Miyata, Yugo
Kikawada, Takahiro
Gelfand, Mikhail S.
Gusev, Oleg
author_sort Mazin, Pavel V.
collection PubMed
description Polypedilum vanderplanki is a striking and unique example of an insect that can survive almost complete desiccation. Its genome and a set of dehydration–rehydration transcriptomes, together with the genome of Polypedilum nubifer (a congeneric desiccation-sensitive midge), were recently released. Here, using published and newly generated datasets reflecting detailed transcriptome changes during anhydrobiosis, as well as a developmental series, we show that the TCTAGAA DNA motif, which closely resembles the binding motif of the Drosophila melanogaster heat shock transcription activator (Hsf), is significantly enriched in the promoter regions of desiccation-induced genes in P. vanderplanki, such as genes encoding late embryogenesis abundant (LEA) proteins, thioredoxins, or trehalose metabolism-related genes, but not in P. nubifer. Unlike P. nubifer, P. vanderplanki has double TCTAGAA sites upstream of the Hsf gene itself, which is probably responsible for the stronger activation of Hsf in P. vanderplanki during desiccation compared with P. nubifer. To confirm the role of Hsf in desiccation-induced gene activation, we used the Pv11 cell line, derived from P. vanderplanki embryo. After preincubation with trehalose, Pv11 cells can enter anhydrobiosis and survive desiccation. We showed that Hsf knockdown suppresses trehalose-induced activation of multiple predicted Hsf targets (including P. vanderplanki-specific LEA protein genes) and reduces the desiccation survival rate of Pv11 cells fivefold. Thus, cooption of the heat shock regulatory system has been an important evolutionary mechanism for adaptation to desiccation in P. vanderplanki.
format Online
Article
Text
id pubmed-5877948
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-58779482018-04-02 Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki Mazin, Pavel V. Shagimardanova, Elena Kozlova, Olga Cherkasov, Alexander Sutormin, Roman Stepanova, Vita V. Stupnikov, Alexey Logacheva, Maria Penin, Aleksey Sogame, Yoichiro Cornette, Richard Tokumoto, Shoko Miyata, Yugo Kikawada, Takahiro Gelfand, Mikhail S. Gusev, Oleg Proc Natl Acad Sci U S A PNAS Plus Polypedilum vanderplanki is a striking and unique example of an insect that can survive almost complete desiccation. Its genome and a set of dehydration–rehydration transcriptomes, together with the genome of Polypedilum nubifer (a congeneric desiccation-sensitive midge), were recently released. Here, using published and newly generated datasets reflecting detailed transcriptome changes during anhydrobiosis, as well as a developmental series, we show that the TCTAGAA DNA motif, which closely resembles the binding motif of the Drosophila melanogaster heat shock transcription activator (Hsf), is significantly enriched in the promoter regions of desiccation-induced genes in P. vanderplanki, such as genes encoding late embryogenesis abundant (LEA) proteins, thioredoxins, or trehalose metabolism-related genes, but not in P. nubifer. Unlike P. nubifer, P. vanderplanki has double TCTAGAA sites upstream of the Hsf gene itself, which is probably responsible for the stronger activation of Hsf in P. vanderplanki during desiccation compared with P. nubifer. To confirm the role of Hsf in desiccation-induced gene activation, we used the Pv11 cell line, derived from P. vanderplanki embryo. After preincubation with trehalose, Pv11 cells can enter anhydrobiosis and survive desiccation. We showed that Hsf knockdown suppresses trehalose-induced activation of multiple predicted Hsf targets (including P. vanderplanki-specific LEA protein genes) and reduces the desiccation survival rate of Pv11 cells fivefold. Thus, cooption of the heat shock regulatory system has been an important evolutionary mechanism for adaptation to desiccation in P. vanderplanki. National Academy of Sciences 2018-03-06 2018-02-20 /pmc/articles/PMC5877948/ /pubmed/29463761 http://dx.doi.org/10.1073/pnas.1719493115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle PNAS Plus
Mazin, Pavel V.
Shagimardanova, Elena
Kozlova, Olga
Cherkasov, Alexander
Sutormin, Roman
Stepanova, Vita V.
Stupnikov, Alexey
Logacheva, Maria
Penin, Aleksey
Sogame, Yoichiro
Cornette, Richard
Tokumoto, Shoko
Miyata, Yugo
Kikawada, Takahiro
Gelfand, Mikhail S.
Gusev, Oleg
Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki
title Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki
title_full Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki
title_fullStr Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki
title_full_unstemmed Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki
title_short Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki
title_sort cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid polypedilum vanderplanki
topic PNAS Plus
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5877948/
https://www.ncbi.nlm.nih.gov/pubmed/29463761
http://dx.doi.org/10.1073/pnas.1719493115
work_keys_str_mv AT mazinpavelv cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT shagimardanovaelena cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT kozlovaolga cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT cherkasovalexander cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT sutorminroman cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT stepanovavitav cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT stupnikovalexey cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT logachevamaria cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT peninaleksey cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT sogameyoichiro cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT cornetterichard cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT tokumotoshoko cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT miyatayugo cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT kikawadatakahiro cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT gelfandmikhails cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki
AT gusevoleg cooptionofheatshockregulatorysystemforanhydrobiosisinthesleepingchironomidpolypedilumvanderplanki