Deciphering Proteomic Signatures of Early Diapause in Nasonia

Abstract

Insect diapause is an alternative life-history strategy used to increase longevity and survival in harsh environmental conditions. Even though some aspects of diapause are well investigated, broader scale studies that elucidate the global metabolic adjustments required for this remarkable trait, are rare. In order to better understand the metabolic changes during early insect diapause, we used a shotgun proteomics approach on early diapausing and non-diapausing larvae of the recently sequenced hymenopteran model organism Nasonia vitripennis. Our results deliver insights into the molecular underpinnings of diapause in Nasonia and corroborate previously reported diapause-associated features for invertebrates, such as a diapause-dependent abundance change for heat shock and storage proteins. Furthermore, we observed a diapause-dependent switch in enzymes involved in glycerol synthesis and a vastly changed capacity for protein synthesis and degradation. The abundance of structural proteins and proteins involved in protein synthesis decreased with increasing diapause duration, while the abundance of proteins likely involved in diapause maintenance (e.g. ferritins) increased. Only few potentially diapause-specific proteins were identified suggesting that diapause in Nasonia relies to a large extent on a modulation of pre-existing pathways. Studying a diapause syndrome on a proteomic level rather than isolated pathways or physiological networks, has proven to be an efficient and successful avenue to understand molecular mechanisms involved in diapause.

Gene expression, metabolic regulation and stress tolerance during diapause

“…Identifying the switches and the extent to which they are shared between organisms are central questions in the study of diapause. Although answers remain elusive, it is known that genes characteristic of reproductive growth are down-regulated during diapause, while other genes, often termed diapause-specific, are up-regulated, and the expression of still others is either not altered or changes intermittently [3,[10][11][12][13][14]. Gene expression and progress through diapause are likely to be influenced by signaling pathways, many of which are receptor responsive and perceive extracellular factors, whether generated by other cells or as a physical signal originating in the environment, the best studied being for Caenorhabditis and Drosophila [8,[15][16][17].…”

“…This approach is complemented by the establishment of expressed sequence tag (EST) libraries [49][50][51][52] and the application of methodologies permitting multiple-gene analysis in single experiments such as proteomics [12,39,53], suppressive subtractive hybridization [11,14,38,54] and microarray analysis [13,55], these often coupled with PCR-based quantification and probing of northern blots. The result is an expanding list of mRNAs and proteins that increase, decrease or are unchanged during diapause.…”

“…All diapause organisms exhibit one or more properties, in varying degrees of intensity, which enable survival upon exposure to harsh environments and permit the mixing of genes from temporally separated populations. This review demonstrates underlying similarities between diapauses in organisms that may otherwise appear unrelated and that diapause in different organism is often characterized by shared properties expressed in varying intensities Responding to external and internal factors, the parasitic solitary wasp Nasonia vitripennis undergoes maternally induced developmental diapause, with the last larval instar entering dormancy prior to pupation [12]. Non-gel shotgun proteomics revealed the exclusive synthesis of only a few proteins during early Nasonia diapause, but differences were observed in the abundance of proteins concerned with fat and sugar metabolism, results reminiscent of diapause in other invertebrates.…”

“…The changes in Hsp90 may reflect increased signaling activity as cells return to pre-diapause activity [82,116]. In comparison, N. vitripennis Hsp90 protein decays as larval diapause progresses [12]. Diapause is induced in pupae of the flesh fly S. crassipalpis via failure of the brain to promote ecdysteroid production [58].…”

Maternal and nourishment factors interact to influence offspring developmental trajectories in social wasps

“…Exposure to artificial drumming significantly decreased gyne-biased gene expression of hsp90a in WR individuals to levels similar to those of FR individuals. In Nasonia wasps, an increase in expression of hsp90a corresponds to early stages of diapause [36]. If we consider expression of hsp90a as an indicator of a diapause phenotype [29], our results suggest antennal drumming could inhibit diapauseassociated gene expression.…”