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The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters

View ORCID ProfileJelly H.M. Soffers, View ORCID ProfileSergio Garcia-Moreno Alcantara, Xuanying Li, View ORCID ProfileWanqing Shao, Christopher W. Seidel, Hua Li, Julia Zeitlinger, Susan M. Abmayr, Jerry L. Workman
doi: https://doi.org/10.1101/2021.06.18.448946
Jelly H.M. Soffers
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
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  • ORCID record for Jelly H.M. Soffers
Sergio Garcia-Moreno Alcantara
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
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Xuanying Li
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
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Wanqing Shao
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
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Christopher W. Seidel
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
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Hua Li
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
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Julia Zeitlinger
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
2Department of Pathology and Laboratory Medicine, University of Kansas School of Medicine, Kansas City, Kansas, 66160, USA
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Susan M. Abmayr
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
3Department of Anatomy and Cell Biology, University of Kansas School of Medicine, Kansas City, Kansas, 66160, USA
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Jerry L. Workman
1Stowers Institute for Medical Research, Kansas City, Missouri, 64110, USA
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  • For correspondence: jlw@stowers.org
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Abstract

The Spt/Ada-Gcn5 Acetyltransferase (SAGA) coactivator complex has multiple modules with different enzymatic and non-enzymatic functions. How each module contributes to gene activation in specific biological contexts is not well understood. Here we analyzed the role of the non-enzymatic core module during Drosophila oogenesis. We show that depletion of several SAGA-specific subunits belonging to the core module blocked egg chamber development during mid-oogenesis stages, resulting in stronger phenotypes than those obtained after depletion of SAGA’s histone acetyltransferase module or deubiquitination module. These results, as well as additional genetic analyses pointing to an interaction with TBP, suggested a differential role of SAGA modules at different promoter types. However, SAGA subunits co-occupied all promoter types of active genes in ChIP-seq and ChIP-nexus experiments. Thus, the SAGA complex appears to occupy promoters in its entirety, consistent with the strong biochemical integrity of the complex. The high-resolution genomic binding profiles are congruent with SAGA recruitment by activators upstream of the start site, and retention on chromatin by interactions with modified histones downstream of the start site. The stronger genetic requirement of the core module during oogenesis may therefore be explained through its interaction with TBP or its role in recruiting the enzymatic modules to the promoter. We propose the handyman principle, which posits that a distinct genetic requirement for specific components may conceal the fact that the entire complex is physically present.

Author Summary Embryonic development critically relies on the differential expression of genes in different tissues. This involves the dynamic interplay between DNA, sequence-specific transcription factors, coactivators and chromatin remodelers which guide the transcription machinery to the appropriate promoters for productive transcription. To understand how this happens at the molecular level, we need to understand when and how coactivator complexes such as SAGA function. SAGA consists of multiple modules with well characterized enzymatic functions. This study shows that the non-enzymatic core module of SAGA is required for Drosophila oogenesis, while the enzymatic functions are largely dispensable. Despite this differential requirement, SAGA subunits appear to be broadly recruited to all promoter types, consistent with the biochemical integrity of the complex. These results suggest that genetic requirements and physical organization do not always go hand in hand.

Competing Interest Statement

This work was supported by funding from the Stowers Institute for Medical Research and a grant from the National Institute of General Medical Sciences (R35GM118068) to Jerry L Workman. I have read the journal's policy and the authors of this manuscript have the following competing interests: J. Zeitlinger owns a patent on ChIP-nexus.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted June 18, 2021.
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The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters
Jelly H.M. Soffers, Sergio Garcia-Moreno Alcantara, Xuanying Li, Wanqing Shao, Christopher W. Seidel, Hua Li, Julia Zeitlinger, Susan M. Abmayr, Jerry L. Workman
bioRxiv 2021.06.18.448946; doi: https://doi.org/10.1101/2021.06.18.448946
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The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters
Jelly H.M. Soffers, Sergio Garcia-Moreno Alcantara, Xuanying Li, Wanqing Shao, Christopher W. Seidel, Hua Li, Julia Zeitlinger, Susan M. Abmayr, Jerry L. Workman
bioRxiv 2021.06.18.448946; doi: https://doi.org/10.1101/2021.06.18.448946

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