DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna

Abstract The cladoceran crustacean Daphnia has long been a model of energy allocation studies due to its important position in the trophic cascade of freshwater ecosystems. However, the loci for controlling energy allocation between life history traits still remain unknown. Here, we report CRISPR/Ca...

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Autores principales:	Nhan Duc Nguyen, Tomoaki Matsuura, Yasuhiko Kato, Hajime Watanabe
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/eedd9464399a4d73801a3c27a3a65d10
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spelling	oai:doaj.org-article:eedd9464399a4d73801a3c27a3a65d102021-12-02T18:17:53ZDNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna10.1038/s41598-021-86578-42045-2322https://doaj.org/article/eedd9464399a4d73801a3c27a3a65d102021-04-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-86578-4https://doaj.org/toc/2045-2322Abstract The cladoceran crustacean Daphnia has long been a model of energy allocation studies due to its important position in the trophic cascade of freshwater ecosystems. However, the loci for controlling energy allocation between life history traits still remain unknown. Here, we report CRISPR/Cas-mediated target mutagenesis of DNA methyltransferase 3.1 (DNMT3.1) that is upregulated in response to caloric restriction in Daphnia magna. The resulting biallelic mutant is viable and did not show any change in growth rate, reproduction, and longevity under nutrient rich conditions. In contrast, under starved conditions, the growth rate of this DNMT3.1 mutant was increased but its reproduction was reciprocally reduced compared to the wild type when the growth and reproduction activities competed during a period from instar 4 to 8. The life span of this mutant was significantly shorter than that of the wild type. We also compared transcriptomes between DNMT3.1 mutant and wild type under nutrient-rich and starved conditions. Consistent with the DNMT3.1 mutant phenotypes, the starved condition led to changes in the transcriptomes of the mutant including differential expression of vitellogenin genes. In addition, we found upregulation of the I am not dead yet (INDY) ortholog, which has been known to shorten the life span in Drosophila, explaining the shorter life span of the DNMT3.1 mutant. These results establish DNMT3.1 as a key regulator for life span and energy allocation between growth and reproduction during caloric restriction. Our findings reveal how energy allocation is implemented by selective expression of a DNMT3 ortholog that is widely distributed among animals. We also infer a previously unidentified adaptation of Daphnia that invests more energy for reproduction than growth under starved conditions.Nhan Duc NguyenTomoaki MatsuuraYasuhiko KatoHajime WatanabeNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Nhan Duc Nguyen Tomoaki Matsuura Yasuhiko Kato Hajime Watanabe DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna
description	Abstract The cladoceran crustacean Daphnia has long been a model of energy allocation studies due to its important position in the trophic cascade of freshwater ecosystems. However, the loci for controlling energy allocation between life history traits still remain unknown. Here, we report CRISPR/Cas-mediated target mutagenesis of DNA methyltransferase 3.1 (DNMT3.1) that is upregulated in response to caloric restriction in Daphnia magna. The resulting biallelic mutant is viable and did not show any change in growth rate, reproduction, and longevity under nutrient rich conditions. In contrast, under starved conditions, the growth rate of this DNMT3.1 mutant was increased but its reproduction was reciprocally reduced compared to the wild type when the growth and reproduction activities competed during a period from instar 4 to 8. The life span of this mutant was significantly shorter than that of the wild type. We also compared transcriptomes between DNMT3.1 mutant and wild type under nutrient-rich and starved conditions. Consistent with the DNMT3.1 mutant phenotypes, the starved condition led to changes in the transcriptomes of the mutant including differential expression of vitellogenin genes. In addition, we found upregulation of the I am not dead yet (INDY) ortholog, which has been known to shorten the life span in Drosophila, explaining the shorter life span of the DNMT3.1 mutant. These results establish DNMT3.1 as a key regulator for life span and energy allocation between growth and reproduction during caloric restriction. Our findings reveal how energy allocation is implemented by selective expression of a DNMT3 ortholog that is widely distributed among animals. We also infer a previously unidentified adaptation of Daphnia that invests more energy for reproduction than growth under starved conditions.
format	article
author	Nhan Duc Nguyen Tomoaki Matsuura Yasuhiko Kato Hajime Watanabe
author_facet	Nhan Duc Nguyen Tomoaki Matsuura Yasuhiko Kato Hajime Watanabe
author_sort	Nhan Duc Nguyen
title	DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna
title_short	DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna
title_full	DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna
title_fullStr	DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna
title_full_unstemmed	DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna
title_sort	dnmt3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in daphnia magna
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/eedd9464399a4d73801a3c27a3a65d10
work_keys_str_mv	AT nhanducnguyen dnmt31controlstradeoffsbetweengrowthreproductionandlifespanunderstarvedconditionsindaphniamagna AT tomoakimatsuura dnmt31controlstradeoffsbetweengrowthreproductionandlifespanunderstarvedconditionsindaphniamagna AT yasuhikokato dnmt31controlstradeoffsbetweengrowthreproductionandlifespanunderstarvedconditionsindaphniamagna AT hajimewatanabe dnmt31controlstradeoffsbetweengrowthreproductionandlifespanunderstarvedconditionsindaphniamagna
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DNMT3.1 controls trade-offs between growth, reproduction, and life span under starved conditions in Daphnia magna

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