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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
ORCiD logo [1];  [2];  [2];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [10];  [11]; ORCiD logo [12];  [13];  [14]
  1. Skolkovo Inst. of Science and Technology, Moscow (Russia). Center for Data-Intensive Biomedicine and Biotechnology; Russian Academy of Sciences (RAS), Moscow (Russian Federation). Inst. for Information Transmission Problems (Kharkevich Inst.); Higher School of Economics, Moscow (Russia). Faculty of Computer Science
  2. Kazan Federal Univ., Kazan (Russia). Inst. of Fundamental Medicine and Biology
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Skolkovo Inst. of Science and Technology, Moscow (Russia). Center for Data-Intensive Biomedicine and Biotechnology; Russian Academy of Sciences (RAS), Moscow (Russian Federation). Inst. for Information Transmission Problems (Kharkevich Inst.)
  5. Johns Hopkins Univ., Baltimore, MD (United States). School of Medicine. Dept. of Oncology
  6. Skolkovo Inst. of Science and Technology, Moscow (Russia). Center for Data-Intensive Biomedicine and Biotechnology; Russian Academy of Sciences (RAS), Moscow (Russian Federation). Inst. for Information Transmission Problems (Kharkevich Inst.); Lomonosov Moscow State Univ., Moscow (Russia). A. N. Belozersky Institute of Physico-Chemical Biology
  7. Russian Academy of Sciences (RAS), Moscow (Russian Federation). Inst. for Information Transmission Problems (Kharkevich Inst.); Lomonosov Moscow State Univ., Moscow (Russia). A. N. Belozersky Institute of Physico-Chemical Biology; Lomonosov Moscow State Univ., Moscow (Russia). Faculty of Biology. Dept. of Genetics
  8. National Inst. of Agriculture and Food Research Organization, Tsukuba (Japan). Inst. of Agrobiological Sciences. Molecular Biomimetics Research Unit. Anhydrobiosis Research Group; Japan Society for the Promotion of Science, Tokyo (Japan); Fukushima College, Iwaki (Japan). National Inst. of Technology. Dept. of Applied Chemistry and Biochemistry
  9. National Inst. of Agriculture and Food Research Organization, Tsukuba (Japan). Inst. of Agrobiological Sciences. Molecular Biomimetics Research Unit. Anhydrobiosis Research Group
  10. The Univ. of Tokyo, Chiba (Japan).Graduate School of Frontier Sciences. Dept. of Integrated Biosciences
  11. National Inst. of Agriculture and Food Research Organization, Tsukuba (Japan). Inst. of Agrobiological Sciences. Molecular Biomimetics Research Unit. Anhydrobiosis Research Group; Tokyo Inst. of Technology, Yokohama (Japan). Center for Biological Resources and Informatics
  12. National Inst. of Agriculture and Food Research Organization, Tsukuba (Japan). Inst. of Agrobiological Sciences. Molecular Biomimetics Research Unit. Anhydrobiosis Research Group; The Univ. of Tokyo, Chiba (Japan).Graduate School of Frontier Sciences. Dept. of Integrated Biosciences
  13. Skolkovo Inst. of Science and Technology, Moscow (Russia). Center for Data-Intensive Biomedicine and Biotechnology; Russian Academy of Sciences (RAS), Moscow (Russian Federation). Inst. for Information Transmission Problems (Kharkevich Inst.); Higher School of Economics, Moscow (Russia). Faculty of Computer Science; Lomonosov Moscow State Univ., Moscow (Russia). Faculty of Bioengineering and Bioinformatics
  14. Kazan Federal Univ., Kazan (Russia). Inst. of Fundamental Medicine and Biology; RIKEN Innovation Center, Yokohama (Japan). Center for Life Science Technologies
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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. Finally, cooption of the heat shock regulatory system has been an important evolutionary mechanism for adaptation to desiccation in P. vanderplanki.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; Russian Science Foundation; KAKENHI; Ministry of Education, Culture, Sports, Science and Technology of Japan
Grant/Contract Number:
AC02-05CH11231; 17-44-07002; 14-50-00150; 15H05622; 23128512; 25128714; 25252060; 16K07308; 16K15073
OSTI ID:
1625008
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, Issue 10; ISSN 0027-8424
Publisher:
National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (8)

Staying young and fit? Ontogenetic and phylogenetic consequences of animal anhydrobiosis journal April 2019
The Multiplanetary Future of Plant Synthetic Biology journal July 2018
Consequences of HSF knockdown on gene expression during the heat shock response in Tigriopus californicus journal January 2020
Role of Intrinsic Disorder in Animal Desiccation Tolerance journal September 2018
Challenges during diapause and anhydrobiosis: Mitochondrial bioenergetics and desiccation tolerance: DIAPAUSE AND ANHYDROBIOSIS journal October 2018
Unlocking our understanding of intermittent rivers and ephemeral streams with genomic tools journal September 2021
Combined metabolome and transcriptome analysis reveals key components of complete desiccation tolerance in an anhydrobiotic insect journal July 2020
Slow release of oxygen from carbamide peroxide for promoting the proliferation of human brain microvascular endothelial cells under hypoxia journal January 2021

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
science & technology
desiccation tolerance
anhydrobiosis
RNA-seq
Polypedilum vanderplanki
heat shock