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PreprintCited by 4Developmental Biology and Gene RegulationDiptera species taxonomy and behaviorChromosomal and Genetic Variations

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Twenty-seven ZAD-ZNF genes of Drosophila melanogaster are orthologous to the embryo polarity determining mosquito gene cucoid

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Li, Muzi, Kasan, Koray, Saha, Zinnia, Yoon, Yoseop, Schmidt-Ott, Urs·2022·PLoS ONE
DOI 10.1101/2022.09.04.506554PMC PMC9810180

Preprint — published as 10.1371/journal.pone.0274716 · Paper page

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Abstract

The C2H2 zinc finger gene cucoid establishes anterior-posterior (AP) polarity in the early embryo of culicine mosquitoes. This gene is unrelated to genes that establish embryo polarity in other fly species (Diptera), such as the homeobox gene bicoid , which serves this function in the traditional model organism Drosophila melanogaster . The cucoid gene is a conserved single copy gene across lower dipterans but nothing is known about its function in other species, and its evolution in higher dipterans, including Drosophila, is unresolved. We found that cucoid is a member of the ZAD-containing C2H2 zinc finger (ZAD-ZNF) gene family and is orthologous to 27 of the 91 members of this family in D. melanogaster , including M1BP, ranshi, ouib, nom, zaf1, odj, Nnk, trem, Zif , and eighteen uncharacterized genes. Available knowledge of the functions of cucoid orthologs in Drosophila melanogaster suggest that the progenitor of this lineage specific expansion may played a role in regulating chromatin. We also describe many aspects of the gene duplication history of cucoid in the brachyceran lineage of D. melanogaster , thereby providing a framework for predicting potential redundancies among these genes in D. melanogaster .

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Fig 1 Predicted structure of Cucoid. Structure of a Cucoid homodimer (maternal isoform from C. quinquefasciatus, GenBank: QFQ59549.1) as predicted by AlphaFold2 (AlphaFold identifier for Cucoid structure: A0A5P8HWN4) is shown with the two chains colored in red and blue above a simplified sketch of full-length Cucoid protein with the N-terminal end to the left and the C-terminal end to the right, and ZAD and ZNFs marked by colored rectangles.
Fig 1 Predicted structure of Cucoid. Structure of a Cucoid homodimer (maternal isoform from C. quinquefasciatus, GenBank: QFQ59549.1) as predicted by AlphaFold2 (AlphaFold identifier for Cucoid structure: A0A5P8HWN4) is shown with the two chains colored in red and blue above a simplified sketch of full-length Cucoid protein with the N-terminal end to the left and the C-terminal end to the right, and ZAD and ZNFs marked by colored rectangles.CC BY · PubMed Central
Fig 2 Manually rooted maximum likelihood protein tree of ZAD-ZNF family members in D. melanogaster. Orthologs that were identified based on reciprocal protein BLAST (see Table 1) are marked by red arrow heads. Colored lines correspond to chromosomal gene clusters (see Fig 3).
Fig 2 Manually rooted maximum likelihood protein tree of ZAD-ZNF family members in D. melanogaster. Orthologs that were identified based on reciprocal protein BLAST (see Table 1) are marked by red arrow heads. Colored lines correspond to chromosomal gene clusters (see Fig 3).CC BY · PubMed Central
Fig 3 Synteny of genes in the Cucoid clade. Genes of the Cucoid clade are distributed in clusters on the right arm of chromosome 3, except CG9215 (not shown) which is located on the X chromosome. M1BP cluster (orange), CG14711 cluster (green), CG4424 cluster (blue), Odj cluster (light blue), CG31441 cluster (purple), Zif (black), other dispersed genes (outlined).
Fig 3 Synteny of genes in the Cucoid clade. Genes of the Cucoid clade are distributed in clusters on the right arm of chromosome 3, except CG9215 (not shown) which is located on the X chromosome. M1BP cluster (orange), CG14711 cluster (green), CG4424 cluster (blue), Odj cluster (light blue), CG31441 cluster (purple), Zif (black), other dispersed genes (outlined).CC BY · PubMed Central
Fig 4 Conservation of Cucoid introns. Multiple sequence alignment of Cucoid orthologs from lower dipterans and Cucoid clade members of D. melanogaster. Conserved intron positions are boxed, and the red zigzags represent the splicing points. Similarity of aligned amino acids was assessed using the Blosum62 matrix with black representing 100% similarity, dark grey 80–100% similarity, light grey 60–80% similarity, and white less than 60% similarity.
Fig 4 Conservation of Cucoid introns. Multiple sequence alignment of Cucoid orthologs from lower dipterans and Cucoid clade members of D. melanogaster. Conserved intron positions are boxed, and the red zigzags represent the splicing points. Similarity of aligned amino acids was assessed using the Blosum62 matrix with black representing 100% similarity, dark grey 80–100% similarity, light grey 60–80% similarity, and white less than 60% similarity.CC BY · PubMed Central
Fig 5 Cucoid clade protein tree is consistent with gene synteny in D. virilis. (A) Synteny of cucoid orthologs in D. virilis. Genes are color coded to indicate their relationship to gene clusters in D. melanogaster (see Fig 3). (B) Manually rooted maximum likelihood protein tree of Cucoid orthologs from D. melanogaster and D. virilis. Note that D. virilis has two CG17801 orthologs.
Fig 5 Cucoid clade protein tree is consistent with gene synteny in D. virilis. (A) Synteny of cucoid orthologs in D. virilis. Genes are color coded to indicate their relationship to gene clusters in D. melanogaster (see Fig 3). (B) Manually rooted maximum likelihood protein tree of Cucoid orthologs from D. melanogaster and D. virilis. Note that D. virilis has two CG17801 orthologs.CC BY · PubMed Central
Fig 6 Syntenies of cucoid orthologs in Lucilia, Bactrocera, and Hermetia. Genes are color coded to indicate their relationship to gene clusters in D. melanogaster. (A) Synteny of cucoid orthologs in Lucilia cuprina. (B) Synteny of cucoid orthologs in Bactrocera dorsalis. (C) Synteny of cucoid orthologs in Hermetia illucens.
Fig 6 Syntenies of cucoid orthologs in Lucilia, Bactrocera, and Hermetia. Genes are color coded to indicate their relationship to gene clusters in D. melanogaster. (A) Synteny of cucoid orthologs in Lucilia cuprina. (B) Synteny of cucoid orthologs in Bactrocera dorsalis. (C) Synteny of cucoid orthologs in Hermetia illucens.CC BY · PubMed Central
Fig 7 Evolution of the Cucoid clade family in higher flies. Inferred gene duplications in the Cucoid clade based on data in this study and D. melanogaster gene ages reported elsewhere [55]. For details see text. Gene clusters (hexagons) and gene loci (triangles) are indicated. For color code see Fig 2.
Fig 7 Evolution of the Cucoid clade family in higher flies. Inferred gene duplications in the Cucoid clade based on data in this study and D. melanogaster gene ages reported elsewhere [55]. For details see text. Gene clusters (hexagons) and gene loci (triangles) are indicated. For color code see Fig 2.CC BY · PubMed Central

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Metadata

Authors
Li, M., Kasan, K., Saha, Z., Yoon, Y., & Schmidt-Ott, U.
Affiliations
  • University of Chicago (US)
  • University of California, Irvine (US)
ORCID
Venue
PLoS ONE
Publisher
openRxiv
Published
2022-09-05
Volume
18
Issue
1
Pages
e0274716-e0274716
ISSN
1932-6203 (ISSN-L)
DOI
10.1101/2022.09.04.506554
PMC
PMC9810180
OpenAlex
W4313461042
Cited by
4
References
1
Citations by year
2025: 4
FWCI
0.36
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Knowledge@UChicago (University of Chicago) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • University of Chicago (cc-by)
Funders
  • University of Chicago
  • Peking University
  • National Institutes of Health
  • Directorate for Biological Sciences
  • National Institute of General Medical Sciences (R01GM127366)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Diptera species taxonomy and behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
Keywords
embryonic polarity, anterior-posterior axis, Drosophila melanogaster, chromatin regulation, Bicoid, gene family evolution
MeSH terms
Animals, Drosophila, Drosophila melanogaster, Culicidae, Transcription Factors, Zinc Fingers, Drosophila Proteins

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