Molecular signatures of diapause in the Asian longhorned beetle: gene expression

Authors: Torson, Alex; BOWMAN, SUSAN - Natural Resources Canada; ROE, AMANDA - Natural Resources Canada; DOUCET, DANIEL - Natural Resources Canada; SINCLAIR, BRENT - University Of Western Ontario

Submitted to: Current Research in Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/8/2023
Publication Date: 3/14/2023
Citation: Torson, A.S., Roe, A.E., Doucet, D., Sinclair, B.J. 2023. Molecular signatures of diapause in the Asian longhorned beetle: gene expression. Current Research in Insect Science. https://doi.org/10.1016/j.cris.2023.100054.
DOI: https://doi.org/10.1016/j.cris.2023.100054

Interpretive Summary: Survival of harsh winter conditions dictates the success of many non-native insects. To survive winter, many insects enter a state of dormancy called diapause. The physiology of diapause has been well studied, but its regulatory mechanisms are still unknown. This knowledge gap limits our understanding of whether invasive species will thrive in new environments. In this study, we measured gene expression in five tissue types across several phases of diapause to answer two primary questions. First, we asked how gene expression varies among tissues during diapause. We provide evidence that gene expression in the brain and fat body varies from other tissue types, but there is a core set of genes regulating diapause common among all tissues. We then investigated how progress through diapause and changing temperatures affect gene expression. We observed differential expression of genes involved in growth and metabolism and identified new candidate genes involved in the regulation of diapause. This work increases the resolution at which we understand diapause regulation, identifies targets for cutting-edge pest management techniques such as RNAi, and provides a basis for genetic-based assessments of invasion risk in this important invasive species.

Technical Abstract: Surviving low temperature exposure during winter is an important factor dictating establishment and range expansion of insect pest species in temperate environments. To survive winter stress, many insects enter diapause, a programmed state of developmental arrest that is characterized by metabolic suppression and increased stress tolerance. The broad physiological changes that occur during diapause have been well studied, but less is known about the mechanisms that promote these phenotypes and how these physiological processes are partitioned and integrated among tissues. In this study, we measured tissue-specific transcriptomic changes during prepupal diapause in the Asian longhorned beetle, Anoplophora glabripennis. We sampled fat body, supraesophageal ganglia, midgut, hindgut, and Malpighian tubules for RNA-seq during four phases of larval diapause development: pre-diapause, diapause maintenance, post-diapause quiescence, and post-diapause development. We sought to answer three questions: 1) how does gene expression across diapause development vary within and among tissues; 2) how does the transcriptional regulation of diapause maintenance differ from that of post-diapause quiescence; and 3) how does low temperature modulate gene expression during diapause? We provide evidence of variable gene expression profiles among tissues; suggesting that some tissues may enter developmental/cellular arrest during diapause, but others like the fat body and brain may remain active. We found gene ontology enrichment in the fat body suggesting epigenetic reorganization during the diapause/post-diapause quiescence transition and observed a high degree of temperature-dependent gene expression during diapause maintenance, including within the insulin and TOR signaling pathways. Further, we identified suites of genes accounting disproportionate amount of the variance in gene expression among samples in this study: 10 of which being important in all tissues analyzed. Tissue-specific characterizations of the diapause phenotype in insects are rare, so these data will aid in increasing the resolution at which we understand the mechanisms governing diapause development in this important pest species.