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The dynamic landscape of gene regulation during Bombyx mori oogenesis

BACKGROUND: Oogenesis in the domestic silkworm (Bombyx mori) is a complex process involving previtellogenesis, vitellogenesis and choriogenesis. During this process, follicles show drastic morphological and physiological changes. However, the genome-wide regulatory profiles of gene expression during...

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Autores principales: Zhang, Qiang, Sun, Wei, Sun, Bang-Yong, Xiao, Yang, Zhang, Ze
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5594438/
https://www.ncbi.nlm.nih.gov/pubmed/28893182
http://dx.doi.org/10.1186/s12864-017-4123-6
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author Zhang, Qiang
Sun, Wei
Sun, Bang-Yong
Xiao, Yang
Zhang, Ze
author_facet Zhang, Qiang
Sun, Wei
Sun, Bang-Yong
Xiao, Yang
Zhang, Ze
author_sort Zhang, Qiang
collection PubMed
description BACKGROUND: Oogenesis in the domestic silkworm (Bombyx mori) is a complex process involving previtellogenesis, vitellogenesis and choriogenesis. During this process, follicles show drastic morphological and physiological changes. However, the genome-wide regulatory profiles of gene expression during oogenesis remain to be determined. RESULTS: In this study, we obtained time-series transcriptome data and used these data to reveal the dynamic landscape of gene regulation during oogenesis. A total of 1932 genes were identified to be differentially expressed among different stages, most of which occurred during the transition from late vitellogenesis to early choriogenesis. Using weighted gene co-expression network analysis, we identified six stage-specific gene modules that correspond to multiple regulatory pathways. Strikingly, the biosynthesis pathway of the molting hormone 20-hydroxyecdysone (20E) was enriched in one of the modules. Further analysis showed that the ecdysteroid 20-hydroxylase gene (CYP314A1) of steroidgenesis genes was mainly expressed in previtellogenesis and early vitellogenesis. However, the 20E–inactivated genes, particularly the ecdysteroid 26-hydroxylase encoding gene (Cyp18a1), were highly expressed in late vitellogenesis. These distinct expression patterns between 20E synthesis and catabolism-related genes might ensure the rapid decline of the hormone titer at the transition point from vitellogenesis to choriogenesis. In addition, we compared landscapes of gene regulation between silkworm (Lepidoptera) and fruit fly (Diptera) oogeneses. Our results show that there is some consensus in the modules of gene co-expression during oogenesis in these insects. CONCLUSIONS: The data presented in this study provide new insights into the regulatory mechanisms underlying oogenesis in insects with polytrophic meroistic ovaries. The results also provide clues for further investigating the roles of epigenetic reconfiguration and circadian rhythm in insect oogenesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4123-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-55944382017-09-14 The dynamic landscape of gene regulation during Bombyx mori oogenesis Zhang, Qiang Sun, Wei Sun, Bang-Yong Xiao, Yang Zhang, Ze BMC Genomics Research Article BACKGROUND: Oogenesis in the domestic silkworm (Bombyx mori) is a complex process involving previtellogenesis, vitellogenesis and choriogenesis. During this process, follicles show drastic morphological and physiological changes. However, the genome-wide regulatory profiles of gene expression during oogenesis remain to be determined. RESULTS: In this study, we obtained time-series transcriptome data and used these data to reveal the dynamic landscape of gene regulation during oogenesis. A total of 1932 genes were identified to be differentially expressed among different stages, most of which occurred during the transition from late vitellogenesis to early choriogenesis. Using weighted gene co-expression network analysis, we identified six stage-specific gene modules that correspond to multiple regulatory pathways. Strikingly, the biosynthesis pathway of the molting hormone 20-hydroxyecdysone (20E) was enriched in one of the modules. Further analysis showed that the ecdysteroid 20-hydroxylase gene (CYP314A1) of steroidgenesis genes was mainly expressed in previtellogenesis and early vitellogenesis. However, the 20E–inactivated genes, particularly the ecdysteroid 26-hydroxylase encoding gene (Cyp18a1), were highly expressed in late vitellogenesis. These distinct expression patterns between 20E synthesis and catabolism-related genes might ensure the rapid decline of the hormone titer at the transition point from vitellogenesis to choriogenesis. In addition, we compared landscapes of gene regulation between silkworm (Lepidoptera) and fruit fly (Diptera) oogeneses. Our results show that there is some consensus in the modules of gene co-expression during oogenesis in these insects. CONCLUSIONS: The data presented in this study provide new insights into the regulatory mechanisms underlying oogenesis in insects with polytrophic meroistic ovaries. The results also provide clues for further investigating the roles of epigenetic reconfiguration and circadian rhythm in insect oogenesis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4123-6) contains supplementary material, which is available to authorized users. BioMed Central 2017-09-11 /pmc/articles/PMC5594438/ /pubmed/28893182 http://dx.doi.org/10.1186/s12864-017-4123-6 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Zhang, Qiang
Sun, Wei
Sun, Bang-Yong
Xiao, Yang
Zhang, Ze
The dynamic landscape of gene regulation during Bombyx mori oogenesis
title The dynamic landscape of gene regulation during Bombyx mori oogenesis
title_full The dynamic landscape of gene regulation during Bombyx mori oogenesis
title_fullStr The dynamic landscape of gene regulation during Bombyx mori oogenesis
title_full_unstemmed The dynamic landscape of gene regulation during Bombyx mori oogenesis
title_short The dynamic landscape of gene regulation during Bombyx mori oogenesis
title_sort dynamic landscape of gene regulation during bombyx mori oogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5594438/
https://www.ncbi.nlm.nih.gov/pubmed/28893182
http://dx.doi.org/10.1186/s12864-017-4123-6
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