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Cell type specific polyploidization in the royal fat body of termite queens

Tissue-specific endopolyploidy is widespread among plants and animals and its role in organ development and function has long been investigated. In insects, the fat body cells of sexually mature females produce substantial amounts of egg yolk precursor proteins (vitellogenins) and exhibit high polyp...

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Autores principales: Nozaki, Tomonari, Tasaki, Eisuke, Matsuura, Kenji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10566149/
https://www.ncbi.nlm.nih.gov/pubmed/37821917
http://dx.doi.org/10.1186/s40851-023-00217-6
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author Nozaki, Tomonari
Tasaki, Eisuke
Matsuura, Kenji
author_facet Nozaki, Tomonari
Tasaki, Eisuke
Matsuura, Kenji
author_sort Nozaki, Tomonari
collection PubMed
description Tissue-specific endopolyploidy is widespread among plants and animals and its role in organ development and function has long been investigated. In insects, the fat body cells of sexually mature females produce substantial amounts of egg yolk precursor proteins (vitellogenins) and exhibit high polyploid levels, which is considered crucial for boosting egg production. Termites are social insects with a reproductive division of labor, and the fat bodies of mature termite queens exhibit higher ploidy levels than those of other females. The fat bodies of mature termite queens are known to be histologically and cytologically specialized in protein synthesis. However, the relationship between such modifications and polyploidization remains unknown. In this study, we investigated the relationship among cell type, queen maturation, and ploidy levels in the fat body of the termite Reticulitermes speratus. We first confirmed that the termite fat body consists of two types of cells, that is, adipocytes, metabolically active cells, and urocytes, urate-storing cells. Our ploidy analysis using flow cytometry has shown that the fat bodies of actively reproducing queens had more polyploid cells than those of newly emerged and pre-reproductive queens, regardless of the queen phenotype (adult or neotenic type). Using image-based analysis, we found that not urocytes, but adipocytes became polyploid during queen differentiation and subsequent sexual maturation. These results suggest that polyploidization in the termite queen fat body is associated with sexual maturation and is regulated in a cell type-specific manner. Our study findings have provided novel insights into the development of insect fat bodies and provide a basis for future studies to understand the functional importance of polyploidy in the fat bodies of termite queens. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40851-023-00217-6.
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spelling pubmed-105661492023-10-12 Cell type specific polyploidization in the royal fat body of termite queens Nozaki, Tomonari Tasaki, Eisuke Matsuura, Kenji Zoological Lett Research Article Tissue-specific endopolyploidy is widespread among plants and animals and its role in organ development and function has long been investigated. In insects, the fat body cells of sexually mature females produce substantial amounts of egg yolk precursor proteins (vitellogenins) and exhibit high polyploid levels, which is considered crucial for boosting egg production. Termites are social insects with a reproductive division of labor, and the fat bodies of mature termite queens exhibit higher ploidy levels than those of other females. The fat bodies of mature termite queens are known to be histologically and cytologically specialized in protein synthesis. However, the relationship between such modifications and polyploidization remains unknown. In this study, we investigated the relationship among cell type, queen maturation, and ploidy levels in the fat body of the termite Reticulitermes speratus. We first confirmed that the termite fat body consists of two types of cells, that is, adipocytes, metabolically active cells, and urocytes, urate-storing cells. Our ploidy analysis using flow cytometry has shown that the fat bodies of actively reproducing queens had more polyploid cells than those of newly emerged and pre-reproductive queens, regardless of the queen phenotype (adult or neotenic type). Using image-based analysis, we found that not urocytes, but adipocytes became polyploid during queen differentiation and subsequent sexual maturation. These results suggest that polyploidization in the termite queen fat body is associated with sexual maturation and is regulated in a cell type-specific manner. Our study findings have provided novel insights into the development of insect fat bodies and provide a basis for future studies to understand the functional importance of polyploidy in the fat bodies of termite queens. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40851-023-00217-6. BioMed Central 2023-10-11 /pmc/articles/PMC10566149/ /pubmed/37821917 http://dx.doi.org/10.1186/s40851-023-00217-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Nozaki, Tomonari
Tasaki, Eisuke
Matsuura, Kenji
Cell type specific polyploidization in the royal fat body of termite queens
title Cell type specific polyploidization in the royal fat body of termite queens
title_full Cell type specific polyploidization in the royal fat body of termite queens
title_fullStr Cell type specific polyploidization in the royal fat body of termite queens
title_full_unstemmed Cell type specific polyploidization in the royal fat body of termite queens
title_short Cell type specific polyploidization in the royal fat body of termite queens
title_sort cell type specific polyploidization in the royal fat body of termite queens
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10566149/
https://www.ncbi.nlm.nih.gov/pubmed/37821917
http://dx.doi.org/10.1186/s40851-023-00217-6
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