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Natural variation in the irld gene family affects starvation resistance in C. elegans

View ORCID ProfileAmy K. Webster, Rojin Chitrakar, Maya Powell, Jingxian Chen, Kinsey Fisher, Robyn Tanny, Lewis Stevens, Kathryn Evans, Angela Wei, Igor Antoshechkin, View ORCID ProfileErik C. Andersen, L. Ryan Baugh
doi: https://doi.org/10.1101/2021.06.07.447366
Amy K. Webster
1Department of Biology, Duke University, Durham, NC 27708, USA
5Institute of Ecology and Evolution, University of Oregon, Eugene, OR 97403, USA
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  • ORCID record for Amy K. Webster
Rojin Chitrakar
1Department of Biology, Duke University, Durham, NC 27708, USA
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Maya Powell
1Department of Biology, Duke University, Durham, NC 27708, USA
6Environment, Ecology, and Energy Program, University of North Carolina at Chapel Hill, Chapel Hill, NC 27514, USA
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Jingxian Chen
1Department of Biology, Duke University, Durham, NC 27708, USA
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Kinsey Fisher
1Department of Biology, Duke University, Durham, NC 27708, USA
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Robyn Tanny
2Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Lewis Stevens
2Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
7Tree of Life, Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
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Kathryn Evans
2Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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Angela Wei
1Department of Biology, Duke University, Durham, NC 27708, USA
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Igor Antoshechkin
3Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA
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Erik C. Andersen
2Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208, USA
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  • ORCID record for Erik C. Andersen
L. Ryan Baugh
1Department of Biology, Duke University, Durham, NC 27708, USA
4Center for Genomic and Computational Biology, Duke University, Durham, NC 27708, USA
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  • For correspondence: ryan.baugh@duke.edu
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Abstract

Starvation resistance is important to disease and fitness, but the genetic basis of its natural variation is unknown. We developed a synthetic-population (re)sequencing approach using molecular inversion probes (MIP-seq) to measure relative fitness during and after larval starvation in C. elegans. We applied this competitive assay to 100 genetically diverse, sequenced, wild strains, revealing natural variation in starvation resistance. We confirmed that the most starvation-resistant strains survive and recover from starvation better than the most starvation-sensitive strain, MY2147, using standard assays. We performed genome-wide association with the MIP-seq trait data and identified three quantitative trait loci (QTL) for starvation resistance. These QTL contain several members of the Insulin/EGF Receptor-L Domain (irld) family with sequence variation associated with variation in starvation resistance. We used genome editing to show that individual modification of four irld genes increases starvation resistance of MY2147. Modification of irld-39 and irld-52 together increases starvation resistance of the laboratory-reference strain N2. Increased starvation resistance of the irld-39; irld-52 double mutant depends on daf-16/FoxO, and these worms also show increased nuclear localization of DAF-16 during starvation. DAF-16/FoxO is a widely conserved transcriptional effector of insulin/IGF signaling (IIS), and these results suggest that IRLD proteins modify IIS. This work demonstrates efficacy of using MIP-seq to dissect a complex trait, identifies irld genes as natural modifiers of starvation resistance in C. elegans, and suggests that an expanded gene family affects a deeply conserved signaling pathway to alter a fitness-proximal trait.

Competing Interest Statement

The authors have declared no competing interest.

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Posted May 11, 2022.
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Natural variation in the irld gene family affects starvation resistance in C. elegans
Amy K. Webster, Rojin Chitrakar, Maya Powell, Jingxian Chen, Kinsey Fisher, Robyn Tanny, Lewis Stevens, Kathryn Evans, Angela Wei, Igor Antoshechkin, Erik C. Andersen, L. Ryan Baugh
bioRxiv 2021.06.07.447366; doi: https://doi.org/10.1101/2021.06.07.447366
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Natural variation in the irld gene family affects starvation resistance in C. elegans
Amy K. Webster, Rojin Chitrakar, Maya Powell, Jingxian Chen, Kinsey Fisher, Robyn Tanny, Lewis Stevens, Kathryn Evans, Angela Wei, Igor Antoshechkin, Erik C. Andersen, L. Ryan Baugh
bioRxiv 2021.06.07.447366; doi: https://doi.org/10.1101/2021.06.07.447366

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