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

Pavel V. Mazin, Elena Shagimardanova, Olga Kozlova, Alexander Cherkasov, Roman Sutormin, Vita V. Stepanova, Alexey Stupnikov, Maria Logacheva, Aleksey Penin, Yoichiro Sogame, Richard Cornette, Shoko Tokumoto, Yugo Miyata, Takahiro Kikawada, Mikhail S. Gelfand, Oleg Gusev

    Research output: Contribution to journalArticlepeer-review

    24 Citations (Scopus)

    Abstract

    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.

    Original languageEnglish
    Pages (from-to)E2477-E2486
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume115
    Issue number10
    DOIs
    Publication statusPublished - 6 Mar 2018

    Keywords

    • Anhydrobiosis
    • Desiccation tolerance
    • Heat shock
    • Polypedilum vanderplanki
    • RNA-seq

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