Innovation of heterochromatin functions drives rapid evolution of essential ZAD-ZNF genes in Drosophila

Kasinathan, Bhavatharini; Colmenares, Serafin U.; McConnell, Hannah; Young, Janet M.; Karpen, Gary H.; Malik, Harmit S.

doi:10.7554/eLife.63368

Innovation of heterochromatin functions drives rapid evolution of essential ZAD-ZNF genes in Drosophila

Journal Article · Tue Nov 10 00:00:00 EST 2020 · eLife

DOI:https://doi.org/10.7554/eLife.63368· OSTI ID:1816074

^[1]; ^[2]; McConnell, Hannah ^[3]; ^[3]; ^[2]; ^[4]

Univ. of Washington, Seattle, WA (United States). School of Medicine. Medical Scientist Training Program; Univ. of Washington, Seattle, WA (United States). Molecular and Cellular Biology Graduate program; Fred Hutchinson Cancer Research Center, Seattle, WA (United States). Division of Basic Sciences; OSTI
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Innovative Genomics Inst., Berkeley, CA (United States)
Fred Hutchinson Cancer Research Center, Seattle, WA (United States). Division of Basic Sciences
Fred Hutchinson Cancer Research Center, Seattle, WA (United States). Division of Basic Sciences. Howard Hughes Medical Inst.

Contrary to dogma, evolutionarily young and dynamic genes can encode essential functions. We find that evolutionarily dynamic ZAD-ZNF genes, which encode the most abundant class of insect transcription factors, are more likely to encode essential functions in Drosophila melanogaster than ancient, conserved ZAD-ZNF genes. We focus on the Nicknack ZAD-ZNF gene, which is evolutionarily young, poorly retained in Drosophila species, and evolves under strong positive selection. Yet we find that it is necessary for larval development in D. melanogaster. We show that Nicknack encodes a heterochromatin-localizing protein like its paralog Oddjob, also an evolutionarily dynamic yet essential ZAD-ZNF gene. We find that the divergent D. simulans Nicknack protein can still localize to D. melanogaster heterochromatin and rescue viability of female but not male Nicknack-null D. melanogaster. Our findings suggest that innovation for rapidly changing heterochromatin functions might generally explain the essentiality of many evolutionarily dynamic ZAD-ZNF genes in insects.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1816074

Journal Information:: eLife, Journal Name: eLife Vol. 9; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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