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Drosophila melanogaster Y Chromosome Genes Affect Male Sensitivity to Microbial Infections

SIMPLE SUMMARY: This manuscript focuses on the protein-encoding genes of the Drosophila melanogaster Y chromosome and their role in immunity. Since their discovery, these genes have mainly been studied for their role(s) in male fertility, such as spermatogenesis. Two previously published papers have...

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Autores principales: Bartolo, Gloria, Gonzalez, Leandra O., Levitin, Anastasia, Martchenko Shilman, Mikhail
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7824794/
https://www.ncbi.nlm.nih.gov/pubmed/33466347
http://dx.doi.org/10.3390/insects12010030
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author Bartolo, Gloria
Gonzalez, Leandra O.
Levitin, Anastasia
Martchenko Shilman, Mikhail
author_facet Bartolo, Gloria
Gonzalez, Leandra O.
Levitin, Anastasia
Martchenko Shilman, Mikhail
author_sort Bartolo, Gloria
collection PubMed
description SIMPLE SUMMARY: This manuscript focuses on the protein-encoding genes of the Drosophila melanogaster Y chromosome and their role in immunity. Since their discovery, these genes have mainly been studied for their role(s) in male fertility, such as spermatogenesis. Two previously published papers have linked the polymorphism within the Y chromosome and immunity. Currently, there is no research article to our knowledge that has studied the effect of the individual genes of the Y chromosome on fly immunity. Here, we aim to address the lack of immunity-related knowledge of Y chromosome genes by determining the effect of many of these genes on male sensitivity to microbial infections. We challenged loss-of-function gene mutants with bacterial and fungal pathogens orally and observed any significant fly survival changes. We discovered several genes affecting male sensitivity to both bacterial and fungal infections. While most of the Y chromosome genes were found to reduce sensitivity, we found one gene increases sensitivity to fungal infection. Because several genes were found to increase male sensitivity to microbial infections, inhibitors for such genes could be introduced in areas where fruit flies are pests. Amid declining bee populations, Diptera pollinators could be protected from fungal infections with Y-gene inhibitors. ABSTRACT: The genders of Drosophila melanogaster vary in their sensitivities to microbial pathogens. While many of the immunity-related genes are located on the X chromosome, the polymorphisms within the Y chromosome were also shown to affect the immunity of flies. In this study, we investigated the necessity of individual genes on the Y chromosome (Y-genes) for male sensitivity to microbes. We identified several Y-genes whose genetic inactivation either increases or decreases the sensitivity of males to gastrointestinal infections with fungal Saccharomyces cerevisiae and bacterial Serratia liquefaciens. Specifically, the loss of function mutations in fly kl-5 and Ppr-Y Y-genes lead to increased and decreased sensitivity of males to fungal challenge, respectively, compared to female sensitivity. In contrast, mutations in Drosophila Pp1-Y1, kl-5, kl-3, Ppr-Y, CCY, and FDY Y-genes lead to increased sensitivity of males to bacterial infection, compared to females. Moreover, while these Y-genes are necessary, the Y chromosome is not sufficient for the sensitivity of males to microbes, since the sensitivity of XXY females to fungal and bacterial challenges was not different from the sensitivity of wild-type female flies, compared to males. This study assigns a new immunity-related function to numerous Y-genes in D. melanogaster.
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spelling pubmed-78247942021-01-24 Drosophila melanogaster Y Chromosome Genes Affect Male Sensitivity to Microbial Infections Bartolo, Gloria Gonzalez, Leandra O. Levitin, Anastasia Martchenko Shilman, Mikhail Insects Article SIMPLE SUMMARY: This manuscript focuses on the protein-encoding genes of the Drosophila melanogaster Y chromosome and their role in immunity. Since their discovery, these genes have mainly been studied for their role(s) in male fertility, such as spermatogenesis. Two previously published papers have linked the polymorphism within the Y chromosome and immunity. Currently, there is no research article to our knowledge that has studied the effect of the individual genes of the Y chromosome on fly immunity. Here, we aim to address the lack of immunity-related knowledge of Y chromosome genes by determining the effect of many of these genes on male sensitivity to microbial infections. We challenged loss-of-function gene mutants with bacterial and fungal pathogens orally and observed any significant fly survival changes. We discovered several genes affecting male sensitivity to both bacterial and fungal infections. While most of the Y chromosome genes were found to reduce sensitivity, we found one gene increases sensitivity to fungal infection. Because several genes were found to increase male sensitivity to microbial infections, inhibitors for such genes could be introduced in areas where fruit flies are pests. Amid declining bee populations, Diptera pollinators could be protected from fungal infections with Y-gene inhibitors. ABSTRACT: The genders of Drosophila melanogaster vary in their sensitivities to microbial pathogens. While many of the immunity-related genes are located on the X chromosome, the polymorphisms within the Y chromosome were also shown to affect the immunity of flies. In this study, we investigated the necessity of individual genes on the Y chromosome (Y-genes) for male sensitivity to microbes. We identified several Y-genes whose genetic inactivation either increases or decreases the sensitivity of males to gastrointestinal infections with fungal Saccharomyces cerevisiae and bacterial Serratia liquefaciens. Specifically, the loss of function mutations in fly kl-5 and Ppr-Y Y-genes lead to increased and decreased sensitivity of males to fungal challenge, respectively, compared to female sensitivity. In contrast, mutations in Drosophila Pp1-Y1, kl-5, kl-3, Ppr-Y, CCY, and FDY Y-genes lead to increased sensitivity of males to bacterial infection, compared to females. Moreover, while these Y-genes are necessary, the Y chromosome is not sufficient for the sensitivity of males to microbes, since the sensitivity of XXY females to fungal and bacterial challenges was not different from the sensitivity of wild-type female flies, compared to males. This study assigns a new immunity-related function to numerous Y-genes in D. melanogaster. MDPI 2021-01-05 /pmc/articles/PMC7824794/ /pubmed/33466347 http://dx.doi.org/10.3390/insects12010030 Text en © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Bartolo, Gloria
Gonzalez, Leandra O.
Levitin, Anastasia
Martchenko Shilman, Mikhail
Drosophila melanogaster Y Chromosome Genes Affect Male Sensitivity to Microbial Infections
title Drosophila melanogaster Y Chromosome Genes Affect Male Sensitivity to Microbial Infections
title_full Drosophila melanogaster Y Chromosome Genes Affect Male Sensitivity to Microbial Infections
title_fullStr Drosophila melanogaster Y Chromosome Genes Affect Male Sensitivity to Microbial Infections
title_full_unstemmed Drosophila melanogaster Y Chromosome Genes Affect Male Sensitivity to Microbial Infections
title_short Drosophila melanogaster Y Chromosome Genes Affect Male Sensitivity to Microbial Infections
title_sort drosophila melanogaster y chromosome genes affect male sensitivity to microbial infections
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7824794/
https://www.ncbi.nlm.nih.gov/pubmed/33466347
http://dx.doi.org/10.3390/insects12010030
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