Repression precedes independent evolutionary gains of a highly specific gene expression pattern

Jian Pu; Zinan Wang; Haosu Cong; Jacqueline S.R. Chin; Jessa Justen; Cédric Finet; Joanne Y. Yew; Henry Chung

doi:10.1016/j.celrep.2021.109896

Repression precedes independent evolutionary gains of a highly specific gene expression pattern

Jian Pu, Zinan Wang, Haosu Cong, Jacqueline S.R. Chin, Jessa Justen, Cédric Finet, Joanne Y. Yew, Henry Chung

Entomology

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3 Scopus citations

Abstract

Highly specific expression patterns can be caused by the overlapping activities of activator and repressor sequences in enhancers. However, few studies illuminate how these sequences evolve in the origin of new enhancers. Here, we show that expression of the bond gene in the semicircular wall epithelium (swe) of the Drosophila melanogaster male ejaculatory bulb (EB) is controlled by an enhancer consisting of an activator region that requires Abdominal-B driving expression in the entire EB and a repressor region that restricts this expression to the EB swe. Although this expression pattern is independently gained in the distantly related Scaptodrosophila lebanonensis and does not require Abdominal-B, we show that functionally similar repressor sequences are present in Scaptodrosophila and also in species that do not express bond in the EB. We suggest that during enhancer evolution, repressor sequences can precede the evolution of activator sequences and may lead to similar but independently evolved expression patterns.

Original language	English
Article number	109896
Journal	Cell Reports
Volume	37
Issue number	4
DOIs	https://doi.org/10.1016/j.celrep.2021.109896
State	Published - Oct 26 2021

Bibliographical note

Publisher Copyright:
© 2021 The Author(s)

Funding

We thank Caitlin Peffers, Mei Luo, Ian Paulsen, and Cole Richards for technical assistance and the Bloomington Drosophila Stock Center for fly stocks and reagents. We acknowledge critical comments to the manuscript by Dr. David Arnosti (Michigan State University) and Dr. Sean B. Carroll (University of Maryland, College Park, MD). J.Y.Y. and J.S.R.C. were supported by the Singapore National Research Foundation (NRF-RF2010-06). J.Y.Y. was also supported by the National Institutes of Health (Grant No. 1P20GM125508). H. Chung was supported by USDA NIFA via Michigan State University AgBioresearch (Umbrella project MICL02522). J.P. and H. Chung designed research; J.P. Z.W. H. Cong, J.S.R.C. J.J. C.F. J.Y.Y. and H. Chung performed research; J.P. Z.W. C.F. J.Y.Y. and H. Chung analyzed data; and J.P. and H. Chung wrote the paper with input from other authors. The authors declare no competing interests. We thank Caitlin Peffers, Mei Luo, Ian Paulsen, and Cole Richards for technical assistance and the Bloomington Drosophila Stock Center for fly stocks and reagents. We acknowledge critical comments to the manuscript by Dr. David Arnosti (Michigan State University) and Dr. Sean B. Carroll (University of Maryland, College Park, MD). J.Y.Y. and J.S.R.C. were supported by the Singapore National Research Foundation ( NRF-RF2010-06 ). J.Y.Y. was also supported by the National Institutes of Health (Grant No. 1P20GM125508 ). H. Chung was supported by USDA NIFA via Michigan State University AgBioresearch (Umbrella project MICL02522 ).

Funders	Funder number
Michigan State University
National Institutes of Health (NIH)
USDA NIFA
Michigan State University AgBioResearch	MICL02522
National Research Foundation Singapore	NRF-RF2010-06
National Institute of General Medical Sciences DP2GM119177 Sophie Dumont National Institute of General Medical Sciences	P20GM125508

Keywords

Abd-B
activator
cis-regulatory evolution
enhancer
fatty acyl-CoA elongase
repressor

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2021.109896

Cite this

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title = "Repression precedes independent evolutionary gains of a highly specific gene expression pattern",

abstract = "Highly specific expression patterns can be caused by the overlapping activities of activator and repressor sequences in enhancers. However, few studies illuminate how these sequences evolve in the origin of new enhancers. Here, we show that expression of the bond gene in the semicircular wall epithelium (swe) of the Drosophila melanogaster male ejaculatory bulb (EB) is controlled by an enhancer consisting of an activator region that requires Abdominal-B driving expression in the entire EB and a repressor region that restricts this expression to the EB swe. Although this expression pattern is independently gained in the distantly related Scaptodrosophila lebanonensis and does not require Abdominal-B, we show that functionally similar repressor sequences are present in Scaptodrosophila and also in species that do not express bond in the EB. We suggest that during enhancer evolution, repressor sequences can precede the evolution of activator sequences and may lead to similar but independently evolved expression patterns.",

keywords = "Abd-B, activator, cis-regulatory evolution, enhancer, fatty acyl-CoA elongase, repressor",

author = "Jian Pu and Zinan Wang and Haosu Cong and Chin, \{Jacqueline S.R.\} and Jessa Justen and C{\'e}dric Finet and Yew, \{Joanne Y.\} and Henry Chung",

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doi = "10.1016/j.celrep.2021.109896",

language = "English",

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AU - Chin, Jacqueline S.R.

AU - Justen, Jessa

AU - Finet, Cédric

AU - Yew, Joanne Y.

AU - Chung, Henry

PY - 2021/10/26

Y1 - 2021/10/26

N2 - Highly specific expression patterns can be caused by the overlapping activities of activator and repressor sequences in enhancers. However, few studies illuminate how these sequences evolve in the origin of new enhancers. Here, we show that expression of the bond gene in the semicircular wall epithelium (swe) of the Drosophila melanogaster male ejaculatory bulb (EB) is controlled by an enhancer consisting of an activator region that requires Abdominal-B driving expression in the entire EB and a repressor region that restricts this expression to the EB swe. Although this expression pattern is independently gained in the distantly related Scaptodrosophila lebanonensis and does not require Abdominal-B, we show that functionally similar repressor sequences are present in Scaptodrosophila and also in species that do not express bond in the EB. We suggest that during enhancer evolution, repressor sequences can precede the evolution of activator sequences and may lead to similar but independently evolved expression patterns.

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Repression precedes independent evolutionary gains of a highly specific gene expression pattern

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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