Up-regulation of heat shock proteins is essential for cold survival during insect diapause

Abstract

Diapause, the dormancy common to overwintering insects, evokes a unique pattern of gene expression. In the flesh fly, most, but not all, of the fly's heat shock proteins (Hsps) are up-regulated. The diapause up-regulated Hsps include two members of the Hsp70 family, one member of the Hsp60 family (TCP-1), at least four members of the small Hsp family, and a small Hsp pseudogene. Expression of an Hsp70 cognate, Hsc70, is uninfluenced by diapause, and Hsp90 is actually down-regulated during diapause, thus diapause differs from common stress responses that elicit synchronous up-regulation of all Hsps. Up-regulation of the Hsps begins at the onset of diapause, persists throughout the overwintering period, and ceases within hours after the fly receives the signal to reinitiate development. The up-regulation of Hsps appears to be common to diapause in species representing diverse insect orders including Diptera, Lepidoptera, Coleoptera, and Hymenoptera as well as in diapauses that occur in different developmental stages (embryo, larva, pupa, adult). Suppressing expression of Hsp23 and Hsp70 in flies by using RNAi did not alter the decision to enter diapause or the duration of diapause, but it had a profound effect on the pupa's ability to survive low temperatures. We thus propose that up-regulation of Hsps during diapause is a major factor contributing to cold-hardiness of overwintering insects.cold tolerance ͉ overwintering ͉ stress proteins ͉ RNAi

Population dependent effects of photoperiod on diapause related physiological traits in an invasive beetle (Leptinotarsa decemlineata)

“…Heat shock proteins are molecular chaperones which assist in regulating the functionality of proteins during times of cellular stress (low/high pH or temperature for instance) (Lindquist 1986, Goto and Kimura 1998, Feder & Hoffmann 1999, Hochachka & Somero 2002. During diapause, several different heat shock proteins have been found to be up-regulated for long periods, in some cases the whole overwintering period (Denlinger 2002, Rinehart et al 2007, MacRae 2010. Also other stress related proteins, such as desiccation proteins have been found to be up-regulated during diapause (Graham et al 1996, Yocum 2003, Yocum et al 2011.…”

How insects survive the cold: molecular mechanisms—a review

“…In each case, the nature and extent of the shock is different. Cold shock is an unpredictable acute stress, whereas diapause is a programmed elongated chronic stress and HSPs have the necessary regulatory capacity to deal with all situations (Rinehart et al 2007). …”

“…Hsp 23 and Hsp70 are highly expressed during diapause, but not responsive to additional desiccation stresses, whilst in this state. Similarly, expression levels of smHsp, Hsp70 and Hsp90 are permanently upregulated in the larvae of Belgica antarctica and expression levels cannot be further enhanced under any type of desiccation stress (Hayward et al 2007). So there is potentially a trade-off in the cellular energetics for Hsp requirements.…”

“…This is supported by RNAi experiments using Hsp23 and Hsp70 in the flesh fly. Suppression of Hsp23 and HSP70 expression did not alter the decision to enter diapause or its duration, but had a profound effect on the pupa's ability to survive low temperatures and so is considered to be a major factor contributing to cold hardiness of overwintering insects (Rinehart et al 2007). …”

“…However, with microarrays and proteomics, there are now technologies for examining hundreds of genes/proteins at the same time. Indeed the continuing interest on diapause has expanded via a proteomics study comparing brain extracts of diapausing and nondiapusing flesh fly pupa (Li et al 2007). Thirty-seven diapauseunique or upregulated proteins were identified, of which, not surprisingly given previous studies, the HSPs predominated.…”