Coevolution of the CDCA7-HELLS ICF-related nucleosome remodeling complex and DNA methyltransferases

  1. Hironori Funabiki  Is a corresponding author
  2. Isabel E Wassing
  3. Qingyuan Jia
  4. Ji-Dung Luo
  5. Thomas Carroll
  1. Laboratory of Chromosome and Cell Biology, The Rockefeller University, United States
  2. Bioinformatics Resource Center, The Rockefeller University, United States
7 figures, 1 table and 1 additional file

Figures

CDCA7 is absent from model organisms with undetectable genomic 5mC.

Filled squares and open squares indicate presence and absence of an orthologous protein(s), respectively. CDCA7 homologs are absent from model organisms where DNMT1, DNMT3 and 5mC on genomic are …

Figure 1—source data 1

Lists of proteins and species used in this study.

Tab1, Full list. The list contains species names, their taxonomies, Genbank accession numbers of proteins, PMID of references supporting the 5mC status, and genome sequence assembly statistics. ND; not detected. DNMT5 proteins shown in red lack the Snf2-like ATPase domain. UHRF1 proteins shown in red lack the Ring-finger E3 ubiquitin-ligase domain. CDCA7 proteins shown in red indicate ambiguous annotation as described in the main text. CDCA7 orthologs that contain additional conserved domains found by NCBI CD-search were shown in light blue. Tab2, Full list 2. The list is used to make presence (1) or absence (0) list. Tab3 Ecdysozoa CoPAP. List of presence/absence annotations for Ecdysozoa species used for CO-PAP analysis. Tab4 Full CoPAP1. List of presence/absence data annotations for the panel of all 180 species used for CO-PAP analysis. Fungal CDCA7F proteins with class II zf-4CXXC_R1 are included in CDCA7. Tab5 Full CoPAP2. List of presence/absence data annotations for the panel of all 180 species used for CO-PAP analysis. Fungal CDCA7F proteins are included in class II zf-4CXXC_R1. Tab6 Full clustering. Table used for clustering analysis. Tab7 Metazoan invertebrates. Table used for clustering analysis for metazoan invertebrates. Tab7 No 5mC list. List of species where absence of genomic 5mC has been experimentally shown.

https://cdn.elifesciences.org/articles/86721/elife-86721-fig1-data1-v1.xlsx
Figure 2 with 1 supplement
CDCA7 paralogs in vertebrates.

(A) Schematics of vertebrate CDCA7 primary sequence composition, based on NP_114148. Yellow lines and light blue lines indicate positions of evolutionary conserved cysteine residues and residues …

Figure 2—source data 1

Multiple sequence alignment of zf-4CXXC_R1 domains.

The zf-4CXXC_R1 domains were aligned by MUSCLE v5.

https://cdn.elifesciences.org/articles/86721/elife-86721-fig2-data1-v1.zip
Figure 2—source data 2

An IQ-TREE result of the consensus phylogenetic tree generation of zf-4CXXC_R1 containing proteins.

Figure 2—source data 2 was used for the analysis by IQ-TREE.

https://cdn.elifesciences.org/articles/86721/elife-86721-fig2-data2-v1.txt
Figure 2—figure supplement 1
Evolutionary conservation of CDCA7-family proteins and other zf-4CXXC_R1-containig proteins.

Amino acid sequences of zf-4CXXC_R1 domain from indicated species were aligned with CLUSTALW. A phylogenetic tree of this alignment is shown. Genbank accession numbers of analyzed sequences are …

Figure 3 with 1 supplement
CDCA7 homologs and other zf-4CXXC_R1-containing proteins in Arabidopsis.

Top; alignments of the zf-4CXXC_R1 domain found in Arabidopsis thaliana. Bottom; domain structure of the three classes of zf-4CXXC_R1-containing proteins in Arabidopsis.

Figure 3—figure supplement 1
Sequence alignment and classification of zf-4CXXC_R1 domains across eukaryotes.

CDCA7 orthologs are characterized by the class I zf-4CXXC_R1 domain, where eleven cysteine residues and three residues mutated in ICF patients are conserved. Class II zf-4CXXC_R1 domain is similar …

Evolutionary conservation of CDCA7F, HELLS and DNMTs in fungi.

(A) Sequence alignment of fungi-specific CDCA7F with class II zf-4CXXC_R1 sequences. (B) Domain architectures of zf-4CXXC_R1-containg proteins in fungi. The class II zf-4CXXC_R1 domain is indicated …

Figure 5 with 4 supplements
Evolutionary conservation of CDCA7, HELLS, and DNMTs.

The phylogenetic tree was generated based on Timetree 5 (Kumar et al., 2022). Filled squares and open squares indicate presence and absence of an orthologous protein(s), respectively. Squares with …

Figure 5—source data 1

Multiple sequence alignment of the SNF2 ATPase domains of HELLS homologs and other SNF2-family proteins.

The SNF2 ATPase domains of HELLS and other SNF2-family proteins after removing the variable linker regions were aligned by MUSCLE v5.

https://cdn.elifesciences.org/articles/86721/elife-86721-fig5-data1-v1.zip
Figure 5—source data 2

An IQ-TREE result of the consensus phylogenetic tree generation of HELLS homologs and other SNF2-family proteins.

Figure 5—source data 1 was used for the analysis by IQ-TREE.

https://cdn.elifesciences.org/articles/86721/elife-86721-fig5-data2-v1.txt
Figure 5—figure supplement 1
Evolutionary conservation of CDCA7, HELLS, and DNMTs.

Presence and absence of each annotated proteins in the panel of 180 eukaryote species is marked as filled and blank boxes. The phylogenetic tree was generated by iTOL, based on NCBI taxonomy by …

Figure 5—figure supplement 2
Phylogenetic tree of HELLS and other SNF2 family proteins.

Amino acid sequences of full-length HELLS proteins from the panel of 180 eukaryote species listed in Figure 1—source data 1 were aligned with full length sequences of other SNF2 family proteins with …

Figure 5—figure supplement 3
Phylogenetic tree of the SNF2-domain.

Amino acid sequences of SNF2-doman without variable insertions from representative HELLS and DDM1-like proteins from Figure 3 were aligned with the corresponding domain of other SNF2 family proteins …

Figure 5—figure supplement 4
Phylogenetic tree of DNMT proteins.

DNA methyltransferase domain of DNMT proteins across eukaryotes (Figure 1—source data 1, excluding majority of those from Metazoa), the Escherichia coli DNA methylases DCM and Dam, and Homo sapiens

Figure 5—figure supplement 4—source data 1

Multiple sequence alignment of DNA methyltransferase domains for Figure 5—figure supplement 4.

DNMT domains from various DNMTs were aligned by MUSCLE v5.

https://cdn.elifesciences.org/articles/86721/elife-86721-fig5-figsupp4-data1-v1.zip
Figure 5—figure supplement 4—source data 2

An IQ-TREE result of the consensus phylogenetic tree generation of DNMTs for Figure 5—figure supplement 4.

Figure 5—figure supplement 4—source data 1 was used for the analysis by IQ-TREE.

https://cdn.elifesciences.org/articles/86721/elife-86721-fig5-figsupp4-data2-v1.txt
Figure 6 with 1 supplement
Coevolution of CDCA7, HELLS, UHRF1, and DNMT1 in Ecdysozoa.

(A) Presence (filled squares) /absence (open squares) patterns of indicated proteins and genomic 5mC in selected Ecdysozoa species. Squares with dotted lines imply preliminary-level genome …

Figure 6—figure supplement 1
CoPAP analysis of CDCA7, HELLS, and DNMTs in eukaryotes.

CoPAP analysis of 180 eukaryote species. Presence and absence patterns of indicated proteins during evolution were analyzed. List of species are shown in Figure 1—source data 1 (A, Tab4. Full CoPAP1;…

Synteny of Hymenoptera genomes adjacent to CDCA7 genes.

Genome compositions around CDCA7 genes in Hymenoptera insects are shown. For genome with annotated chromosomes, chromosome numbers (Chr) or linkage group numbers (LG) are indicated at each gene …

Tables

Key resources table
Reagent type(species) or resourceDesignationSource or referenceIdentifiersAdditional information
Software, algorithmMacVectorMacVector, IncVersion 16–18
Software, algorithmMusclehttps://www.drive5.com/muscle/Muscle5.1
Software, algorithmIQ-TREEhttp://www.iqtree.org/Version 2.0.3 and 2.2.2.6
Software, algorithmTimetreehttp://www.timetree.org/Version 5
Software, algorithmphyloThttps://phylot.biobyte.de/Version 2
Software, algorithmiTOLhttps://itol.embl.de/Version 6
Software, algorithmCoPAPhttp://copap.tau.ac.il/source.php
Software, algorithmETE Toolkithttp://etetoolkit.org/
Software, algorithmJalviewhttps://www.jalview.org/Version 2.22.2.7

Additional files

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