piRNAs Regulated by Mitochondria Variation Linked With Reproduction and Aging in Caenorhabditis elegans

In Caenorhabditis elegans, the binding of Piwi protein to a non-coding RNA form, called piRNA, has been found to be important to both reproductive and aging processes. As the biosynthesis of piRNA is modulated by mitochondrial function, it is likely that the interaction between mitochondrial functio...

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Main Authors: Zuobin Zhu, Ying Li, Mengyu Liang, Lei Wang, Liang Wang, Joshua D. Rizak, Conghui Han, Wenda Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-03-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2020.00190/full
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author Zuobin Zhu
Ying Li
Mengyu Liang
Lei Wang
Liang Wang
Joshua D. Rizak
Conghui Han
Conghui Han
Wenda Zhang
Wenda Zhang
Wenda Zhang
author_facet Zuobin Zhu
Ying Li
Mengyu Liang
Lei Wang
Liang Wang
Joshua D. Rizak
Conghui Han
Conghui Han
Wenda Zhang
Wenda Zhang
Wenda Zhang
author_sort Zuobin Zhu
collection DOAJ
description In Caenorhabditis elegans, the binding of Piwi protein to a non-coding RNA form, called piRNA, has been found to be important to both reproductive and aging processes. As the biosynthesis of piRNA is modulated by mitochondrial function, it is likely that the interaction between mitochondrial function and piRNA expression plays an unknown, yet important, role in reproductive and aging processes because both processes are known to be affected by declines in mitochondrial quality and activity. While the relationship between reproduction and longevity is not characterized in full, the optimality theory of aging and the disposable soma theory suggest that a trade-off between energy and resources is needed for reproductive and aging maintenance. In this study, the influence of mitochondrial variations, via a respiratory chain complex IV (COX1) polymorphism, on piRNA expression was examined in relation to the reproductive and aging outcomes of C. elegans. The COX1 polymorphism in mitochondria was found to affect the number of piRNAs expressed, the development of germ cells, and the length of the lifespan of the nematodes. Interestingly, more than two-thirds of the piRNA expression changes associated with the mitochondrial variation were found to also be affected by age. A gene ontology analysis of the altered piRNA species found that the piRNAs affected by mitochondrial variation and age were linked to genes known to have roles in reproductive and developmental function. Moreover, a piRNA-lncRNA-mRNA regulatory network based on the differential expression patterns of piRNA related to the mitochondrial variation was constructed to further identify potential gene targets with functional interactions. Similarly, this network identified genes involved in reproduction, development, and aging processes. These findings provide new insight into understanding how mitochondrial variations may regulate piRNA expression and may influence the underlying molecular mechanisms that affect reproduction and aging.
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spelling doaj.art-dff5dc10ccef42f69063d2529a2e396b2022-12-21T23:56:46ZengFrontiers Media S.A.Frontiers in Genetics1664-80212020-03-011110.3389/fgene.2020.00190517968piRNAs Regulated by Mitochondria Variation Linked With Reproduction and Aging in Caenorhabditis elegansZuobin Zhu0Ying Li1Mengyu Liang2Lei Wang3Liang Wang4Joshua D. Rizak5Conghui Han6Conghui Han7Wenda Zhang8Wenda Zhang9Wenda Zhang10Department of Genetics, Xuzhou Medical University, Xuzhou, ChinaMedical Technology School of Xuzhou Medical University, Xuzhou, ChinaDepartment of Bioinformatics, School of Medical Informatics and Engineering, Clinical College of Xuzhou Medical University, Xuzhou, ChinaDepartment of Histology and Embryology, Xuzhou Medical University, Xuzhou, ChinaDepartment of Biochemistry, Xuzhou Medical University, Xuzhou, ChinaR.A.S. Innovation, Regina, SK, CanadaDepartment of Clinical Medicine, Xuzhou Medical University, Xuzhou, ChinaDepartment of Urology, Xuzhou Central Hospital, Xuzhou, ChinaDepartment of Genetics, Xuzhou Medical University, Xuzhou, ChinaDepartment of Clinical Medicine, Xuzhou Medical University, Xuzhou, ChinaDepartment of Urology, Xuzhou Central Hospital, Xuzhou, ChinaIn Caenorhabditis elegans, the binding of Piwi protein to a non-coding RNA form, called piRNA, has been found to be important to both reproductive and aging processes. As the biosynthesis of piRNA is modulated by mitochondrial function, it is likely that the interaction between mitochondrial function and piRNA expression plays an unknown, yet important, role in reproductive and aging processes because both processes are known to be affected by declines in mitochondrial quality and activity. While the relationship between reproduction and longevity is not characterized in full, the optimality theory of aging and the disposable soma theory suggest that a trade-off between energy and resources is needed for reproductive and aging maintenance. In this study, the influence of mitochondrial variations, via a respiratory chain complex IV (COX1) polymorphism, on piRNA expression was examined in relation to the reproductive and aging outcomes of C. elegans. The COX1 polymorphism in mitochondria was found to affect the number of piRNAs expressed, the development of germ cells, and the length of the lifespan of the nematodes. Interestingly, more than two-thirds of the piRNA expression changes associated with the mitochondrial variation were found to also be affected by age. A gene ontology analysis of the altered piRNA species found that the piRNAs affected by mitochondrial variation and age were linked to genes known to have roles in reproductive and developmental function. Moreover, a piRNA-lncRNA-mRNA regulatory network based on the differential expression patterns of piRNA related to the mitochondrial variation was constructed to further identify potential gene targets with functional interactions. Similarly, this network identified genes involved in reproduction, development, and aging processes. These findings provide new insight into understanding how mitochondrial variations may regulate piRNA expression and may influence the underlying molecular mechanisms that affect reproduction and aging.https://www.frontiersin.org/article/10.3389/fgene.2020.00190/fullC. elegansmitochondriapiRNAreproductionaging
spellingShingle Zuobin Zhu
Ying Li
Mengyu Liang
Lei Wang
Liang Wang
Joshua D. Rizak
Conghui Han
Conghui Han
Wenda Zhang
Wenda Zhang
Wenda Zhang
piRNAs Regulated by Mitochondria Variation Linked With Reproduction and Aging in Caenorhabditis elegans
Frontiers in Genetics
C. elegans
mitochondria
piRNA
reproduction
aging
title piRNAs Regulated by Mitochondria Variation Linked With Reproduction and Aging in Caenorhabditis elegans
title_full piRNAs Regulated by Mitochondria Variation Linked With Reproduction and Aging in Caenorhabditis elegans
title_fullStr piRNAs Regulated by Mitochondria Variation Linked With Reproduction and Aging in Caenorhabditis elegans
title_full_unstemmed piRNAs Regulated by Mitochondria Variation Linked With Reproduction and Aging in Caenorhabditis elegans
title_short piRNAs Regulated by Mitochondria Variation Linked With Reproduction and Aging in Caenorhabditis elegans
title_sort pirnas regulated by mitochondria variation linked with reproduction and aging in caenorhabditis elegans
topic C. elegans
mitochondria
piRNA
reproduction
aging
url https://www.frontiersin.org/article/10.3389/fgene.2020.00190/full
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