Abstract

Simple SummaryIn metropolitan Seoul and its vicinity, cicadas of the species Hyalessa fuscata living in warmer areas could tolerate the heat better than those living in cooler areas, but genetic mechanisms involved in better heat tolerance remained unclear. In this study, we examined differences in gene expression of cicadas living in a warm urban area, a cool urban area and a suburban area in three experimental treatments: no heating, 10 min heating and heating until the cicadas lost their mobility. Cicadas from the warm urban area changed their gene expressions the most. Activated genes were mostly related to heat shock, energy metabolism, and detoxification. These results suggested that under heat stress, cicadas inhabiting warm areas could differentially express genes to increase their thermal tolerance. In metropolitan Seoul, populations of the cicada Hyalessa fuscata in hotter urban heat islands (“high UHIs”) exhibit higher thermal tolerance than those in cooler UHIs (“low UHIs”). We hypothesized that heat stress may activate the expression of genes that facilitate greater thermal tolerance in high-UHI cicadas than in those from cooler areas. Differences in the transcriptomes of adult female cicadas from high-UHI, low-UHI, and suburban areas were analyzed at the unheated level, after acute heat stress, and after heat torpor. No noticeable differences in unheated gene expression patterns were observed. After 10 min of acute heat stress, however, low-UHI and suburban cicadas expressed more heat shock protein genes than high-UHI counterparts. More specifically, remarkable changes in the gene expression of cicadas across areas were observed after heat torpor stimulus, as represented by a large number of up- and downregulated genes in the heat torpor groups compared with the 10 min acute heat stress and control groups. High-UHI cicadas expressed the most differentially expressed genes, followed by the low-UHI and suburban cicadas. There was a notable increase in the expression of heat shock, metabolism, and detoxification genes; meanwhile, immune-related, signal transduction, and protein turnover genes were downregulated in high-UHI cicadas versus the other cicada groups. These results suggested that under heat stress, cicadas inhabiting high-UHIs could rapidly express genes related to heat shock, energy metabolism, and detoxification to protect cells from stress-induced damage and to increase their thermal tolerance toward heat stress. The downregulation of apoptosis mechanisms in high-UHI cicadas suggested that there was less cellular damage, which likely contributed to their high tolerance of heat stress.

Highlights

  • Insects are poikilotherms whose body temperature changes with the ambient temperature

  • Three groups of cicadas were examined: the control or unheated group consisted of those cicadas that were not exposed to any heat stress; the 10 min and heat torpor groups refer to those exposed to 10 min of acute heat stress and experienced the heat torpor condition, respectively

  • We focused on genes that were implicated in six biological functions to further understand the overall biology of the transcriptional responses of cicadas to heat stress, namely, heat shock proteins, antioxidants and detoxification, energy metabolism, intracellular immune response, signal transduction pathways, and programmed cell death

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Summary

Introduction

Insects are poikilotherms whose body temperature changes with the ambient temperature. Heat shock proteins (Hsps) are highly conserved heat response proteins in both prokaryotes and eukaryotes [1,12,15,16,17], and their role in heat tolerance was studied in detail [18,19] Hsp families encompass both constitutive and heat-inducible members [18]. When exposed to high temperatures, Hsps protect cells and organisms from temperature impairments by counteracting the accumulation of aberrant proteins. They mediate proper protein folding, repair denatured proteins, bind to unfolded proteins to prevent inappropriate protein–protein interactions or clustering of non-native conformations, and degrade or remove abnormal proteins from the cell [12,13,18,23,24,25,26]. The abundance of Hsps increases [11], suggesting that Hsps enhance an organism’s thermotolerance [27,28]

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