Integrating GWAS and Transcriptomics to Identify the Molecular Underpinnings of Thermal Stress Responses in Drosophila melanogaster

Authors

Melise C. Lecheta, University of KentuckyFollow
David N. Awde, University of KentuckyFollow
Thomas S. O’Leary, University of Vermont
Laura N. Unfried, University of KentuckyFollow
Nicholas A. Jacobs, University of KentuckyFollow
Miles H. Whitlock, University of KentuckyFollow
Eleanor McCabe, University of KentuckyFollow
Beck Powers, University of Vermont
Katie Bora, University of Vermont
James S. Waters, Providence College
Heather J. Axen, Salve Regina University
Seth Frietze, University of Vermont
Brent L. Lockwood, University of Vermont
Nicholas M. Teets, University of KentuckyFollow
Sara H. Cahan, University of Vermont

Abstract

Thermal tolerance of an organism depends on both the ability to dynamically adjust to a thermal stress and preparatory developmental processes that enhance thermal resistance. However, the extent to which standing genetic variation in thermal tolerance alleles influence dynamic stress responses vs. preparatory processes is unknown. Here, using the model species Drosophila melanogaster, we used a combination of Genome Wide Association mapping (GWAS) and transcriptomic profiling to characterize whether genes associated with thermal tolerance are primarily involved in dynamic stress responses or preparatory processes that influence physiological condition at the time of thermal stress. To test our hypotheses, we measured the critical thermal minimum (CT_min) and critical thermal maximum (CT_max) of 100 lines of the Drosophila Genetic Reference Panel (DGRP) and used GWAS to identify loci that explain variation in thermal limits. We observed greater variation in lower thermal limits, with CT_min ranging from 1.81 to 8.60°C, while CT_max ranged from 38.74 to 40.64°C. We identified 151 and 99 distinct genes associated with CT_min and CT_max, respectively, and there was strong support that these genes are involved in both dynamic responses to thermal stress and preparatory processes that increase thermal resistance. Many of the genes identified by GWAS were involved in the direct transcriptional response to thermal stress (72/151 for cold; 59/99 for heat), and overall GWAS candidates were more likely to be differentially expressed than other genes. Further, several GWAS candidates were regulatory genes that may participate in the regulation of stress responses, and gene ontologies related to development and morphogenesis were enriched, suggesting many of these genes influence thermal tolerance through effects on development and physiological status. Overall, our results suggest that thermal tolerance alleles can influence both dynamic plastic responses to thermal stress and preparatory processes that improve thermal resistance. These results also have utility for directly comparing GWAS and transcriptomic approaches for identifying candidate genes associated with thermal tolerance.

Document Type

Article

Publication Date

6-23-2020

Notes/Citation Information

Published in Frontiers in Genetics, v. 11, article 658, p. 1-17.

© 2020 Lecheta, Awde, O’Leary, Unfried, Jacobs, Whitlock, McCabe, Powers, Bora, Waters, Axen, Frietze, Lockwood, Teets and Cahan.

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

Digital Object Identifier (DOI)

https://doi.org/10.3389/fgene.2020.00658

Funding Information

This work was supported by the National Science Foundation grant OIA-1826689 to NT, BL, SF, JW, HA, and SC, Hatch Project 1010996 from the USDA National Institute of Food and Agriculture to NT. ML was partially supported by the National Science Foundation I/UCRC, The Center for Arthropod Management Technologies, under grant IIP-1821936, and by industry partners to NT.

Related Content

All datasets generated for this study are included in the article/Supplementary Material. Sequencing data have been deposited into the NCBI SRA database with accession Bioproject PRJNA612361.

Repository Citation

Lecheta, Melise C.; Awde, David N.; O’Leary, Thomas S.; Unfried, Laura N.; Jacobs, Nicholas A.; Whitlock, Miles H.; McCabe, Eleanor; Powers, Beck; Bora, Katie; Waters, James S.; Axen, Heather J.; Frietze, Seth; Lockwood, Brent L.; Teets, Nicholas M.; and Cahan, Sara H., "Integrating GWAS and Transcriptomics to Identify the Molecular Underpinnings of Thermal Stress Responses in Drosophila melanogaster" (2020). Entomology Faculty Publications. 194.
https://uknowledge.uky.edu/entomology_facpub/194