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

Abstract

SignificanceAnhydrobiosis is an ametabolic state found in several organisms that can survive extreme desiccation. It is of practical interest because its application to other systems might allow room temperature preservation of cells, tissues, or organs in the dry state. The insect Polypedilum vanderplanki is the most complex animal that can enter anhydrobiosis. Proteins responsible for desiccation tolerance in P. vanderplanki are relatively well studied, but little is known about mechanisms underlying their induction during desiccation. Here, we show that the heat shock transcription factor regulatory network was coopted during the evolution of P. vanderplanki to activate many known desiccation-protective genes, including genes encoding late embryogenesis abundant (LEA) proteins.

Identification of a master transcription factor and a regulatory mechanism for desiccation tolerance in the anhydrobiotic cell line Pv11

“…We performed motif enrichment analysis to detect the transcription factor-binding elements enriched in the upstream regions of the genes in each module (CLOVER [25], randomization Inferred transcriptional regulatory network obtained by integration of those of trehalose pretreatment and rehydration. Each rectangular node refers to a transcription factor gene with the ID defined in the previous study [19]. Genes differentially expressed in trehalose pretreatment (yellow), in rehydration (blue), and both treatments (green) are shown.…”

“…Although various genes related to desiccation tolerance have been detected and molecular mechanisms for the anhydrobiosis of P. vanderplanki have been inferred [9][10][11][12][13][14][15][16][17][18], the transcription factors and regulatory mechanisms that drive the expression of these genes have not been clarified. Mazin et al revealed that heat shock factor (HSF) has a substantial role in regulation of these genes [19]; the HSF-binding element is enriched in the enhancers of anhydrobiosisrelated genes. In Pv11 cells, HSF knock-down significantly decreases transcription of the genes for the antioxidant protein thioredoxin (TRX), a LEA protein, and trehalose-6-phosphate phosphatase, but not that of other anhydrobiosis-related genes [19].…”

“…Mazin et al revealed that heat shock factor (HSF) has a substantial role in regulation of these genes [19]; the HSF-binding element is enriched in the enhancers of anhydrobiosisrelated genes. In Pv11 cells, HSF knock-down significantly decreases transcription of the genes for the antioxidant protein thioredoxin (TRX), a LEA protein, and trehalose-6-phosphate phosphatase, but not that of other anhydrobiosis-related genes [19]. This knock-down does not completely suppress cell proliferation after rehydration, and some cells are able to recover.…”

Staying young and fit? Ontogenetic and phylogenetic consequences of animal anhydrobiosis

“…Gaertn., Meyer and Scherb., 1802, in response to drying and in the course of the rehydration phase (O'Mahony & Oliver, ). It has been recently shown for the sleeping chironomid Polypedilum vanderplanki Hinton, 1951 that an important strategy is also the presence of a regulatory network able to activate different desiccation‐protective genes (Mazin et al ., ).…”

Challenges during diapause and anhydrobiosis: Mitochondrial bioenergetics and desiccation tolerance

“…Targeting to multiple subcellular compartments, including mitochondria, likely accounts for some of this apparent redundancy . It has been recently demonstrated that expression of LEA proteins and other selected desiccation‐induced genes are under control of the heat shock transcription activator system . Finally, the phylogenetic distribution across selected animal phyla (nematodes, rotifers, tardigrades, arthropods) is difficult to explain by traditional vertical gene transfer, and evidence is mounting for the involvement of horizontal gene transfer from bacteria and fungi .…”