The dynamic landscape of gene regulation during Bombyx mori oogenesis
Abstract 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 expressio...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2017-09-01
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| Series: | BMC Genomics |
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| Online Access: | http://link.springer.com/article/10.1186/s12864-017-4123-6 |
| _version_ | 1819110618335019008 |
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| author | Qiang Zhang Wei Sun Bang-Yong Sun Yang Xiao Ze Zhang |
| author_facet | Qiang Zhang Wei Sun Bang-Yong Sun Yang Xiao Ze Zhang |
| author_sort | Qiang Zhang |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-22T03:44:35Z |
| format | Article |
| id | doaj.art-bc5e48276e6d4109955136f0d0c321e7 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-22T03:44:35Z |
| publishDate | 2017-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-bc5e48276e6d4109955136f0d0c321e72022-12-21T18:40:10ZengBMCBMC Genomics1471-21642017-09-0118111310.1186/s12864-017-4123-6The dynamic landscape of gene regulation during Bombyx mori oogenesisQiang Zhang0Wei Sun1Bang-Yong Sun2Yang Xiao3Ze Zhang4Laboratory of Evolutionary and Functional Genomics, School of Life Sciences, Chongqing UniversityLaboratory of Evolutionary and Functional Genomics, School of Life Sciences, Chongqing UniversityLaboratory of Evolutionary and Functional Genomics, School of Life Sciences, Chongqing UniversitySericulture & Agri-food Research Institute, Guangdong Academy of Agriculture ScienceLaboratory of Evolutionary and Functional Genomics, School of Life Sciences, Chongqing UniversityAbstract 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.http://link.springer.com/article/10.1186/s12864-017-4123-6Bombyx moriOogenesisGene regulationEcdysteroid biosynthesisCo-expression networkTranscription factors |
| spellingShingle | Qiang Zhang Wei Sun Bang-Yong Sun Yang Xiao Ze Zhang The dynamic landscape of gene regulation during Bombyx mori oogenesis BMC Genomics Bombyx mori Oogenesis Gene regulation Ecdysteroid biosynthesis Co-expression network Transcription factors |
| 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 | Bombyx mori Oogenesis Gene regulation Ecdysteroid biosynthesis Co-expression network Transcription factors |
| url | http://link.springer.com/article/10.1186/s12864-017-4123-6 |
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