Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres

  1. Krishnendu Guin
  2. Yao Chen
  3. Radha Mishra
  4. Siti Rawaidah BM Muzaki
  5. Bhagya C Thimmappa
  6. Caoimhe E O'Brien
  7. Geraldine Butler
  8. Amartya Sanyal  Is a corresponding author
  9. Kaustuv Sanyal  Is a corresponding author
  1. Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, India
  2. School of Biological Sciences, Nanyang Technological University, Singapore
  3. School Of Biomolecular & Biomed Science, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Ireland
5 figures and 12 additional files

Figures

Figure 1 with 6 supplements
Construction of the gapless assembly of C. tropicalis type strain MYA-3404 in seven chromosomes.

(A) Schematic showing the stepwise construction of the gapless chromosome-level assembly (Assembly2020) of C. tropicalis (also see Figure 1—figure supplement 1 and Figure 1—figure supplement 2). (B) …

Figure 1—figure supplement 1
Schematic of the strategies used for construction of the gapless chromosome-level assembly of C. tropicalis.

(A - D) The outline of the steps followed for the construction of the genome assembly. (A) Major steps followed for 3C-sequencing in this study were (I) crosslinking, (II) restriction digestion, and …

Figure 1—figure supplement 2
Orphan contigs are alleles in the diploid genome of C. tropicalis.

(A) IGV track images showing the coverage of 3C-seq data on the y-axis (number of reads mapped per bin for each million of the total reads) over the orphan contigs and a control locus from Chr1. (B) …

Figure 1—figure supplement 3
Schematic outline of the strategy followed for N-gap filling and scaffolding of sub-telomeres.

(A - B) Strategy-I and strategy-II (Materials and methods) for filling N-gaps without flanking repeats or with flanking repeats, respectively. Repeats are presented as black arrows. (C) Schematic …

Figure 1—figure supplement 4
Identification of CNVs in the C. tropicalis strain MYA-3404.

(A) EtBr stained gel images and phosphorimages obtained from Southern hybridization experiments using a centromere-proximal (Probe A) and a centromere-distal probe (Probe B) from Chr4 (Supplementary …

Figure 1—figure supplement 5
Chromoblot, sequence coverage analysis, and haplotyping for validation of the chromosome-level genome assembly of C. tropicalis.

(A) Schematic of the balanced heterozygous translocation between Chr1B and Chr4B. The DUP4 locus is highlighted with the black striped box. The junction between Chr1 and Chr4 on Chr1B and Chr4B are …

Figure 1—figure supplement 6
Partial conservation of a LOH block in each of the C. albicans, C. tropicalis and C. sojae genome.

The circos tracks represent the SNP density, positions of the centromeres, Indel density, Illumina sequence coverage (the sequence coverage at the rDNA loci is clipped for clearer representation and …

Figure 2 with 1 supplement
Spatial genome organization reveals centromere-centromere and telomere-telomere contacts in C. tropicalis.

(A) A representative field image of C. tropicalis (strain CtKS102) cells expressing Protein-A tagged CENP-ACse4. CENP-A signals (red) were obtained using anti-Protein A antibodies by indirect …

Figure 2—figure supplement 1
Analysis of 3C-seq data reveals interchromosomal and intrachromosomal telomeric contacts in C. tropicalis genome.

(A) Histogram of all interchromosomal interactions (excluding zero values; gray) was plotted from the 3C-seq contact probability matrix (bin size = 2 kb) of C. tropicalis. The mean value of all …

Figure 3 with 1 supplement
Genome-wide mapping of interchromosomal synteny breakpoints in C. tropicalis identifies a spatial cue for karyotype evolution.

(A) Scaled representation of the color-coded orthoblocks (relative to C. albicans chromosomes) and ICSBs (white lines) in C. tropicalis (Materials and methods). Orthoblocks are defined as stretches …

Figure 3—figure supplement 1
Genome-wide synteny analysis between C. albicans and C. tropicalis suggests evidence of inter-centromere translocations in the last common ancestor.

(A) Synteny maps of C. tropicalis chromosomes (the lowermost line of each panel, marked by filled black circles numbered from 1 to R), with respect to C. albicans chromosomes (lines above the C. …

Figure 4 with 2 supplements
Genome-wide analysis of centromere DNA sequences across the CUG-Ser1 clade reveals the emergence of unique centromeres from an ancestral homogenized inverted repeat-associated centromere type.

(A) A dot-plot matrix representing the sequence and structural homology among species of the CUG-Ser1 clade was generated using Gepard (Materials and methods). (B) A logo plot showing the 12-bp-long …

Figure 4—figure supplement 1
Identification of HIR-associated centromeres in the CUG-Ser1 clade.

(A) Schematic of the method used for the identification of putative centromeres in C. sojae, C. viswanathii, and C. parapsilosis. Putative centromeric loci in these species were tested for gene …

Figure 4—figure supplement 2
Inter-species conservation of centromere DNA sequences of closely related Candida species.

(A) Bean plots showing the distribution of the percent sequence identity among the centromeric left repeat (LR), the central core (CC), and right repeat (RR) elements in C. tropicalis (Ct), C. sojae

The spatial genome organization remained conserved in the CUG-Ser1 clade despite centromere type diversity.

(A) A maximum likelihood-based phylogenetic tree of closely related CUG-Ser1 species analyzed in this study. The centromere structure of each species is shown and drawn to scale. (B) A model showing …

Additional files

Source data 1

Source_data_combined.

https://cdn.elifesciences.org/articles/58556/elife-58556-data1-v3.xlsx
Supplementary file 1

Assembly C with 12 contigs.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp1-v3.pptx
Supplementary file 2

Assembly of sub-telomeres and filling up N-gaps in the genome assembly of C. tropicalis using de contigs.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp2-v3.pptx
Supplementary file 3

Statistics for different versions of genome the assembly of C. tropicalis (MYA-3404) generated in this study.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp3-v3.pptx
Supplementary file 4

A comparative analysis of Assembly A and the improved Assembly2020 of C. tropicalis.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp4-v3.pptx
Supplementary file 5

Features of centromere DNA elements in C. sojae.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp5-v3.pptx
Supplementary file 6

Features of centromere DNA elements in C. viswanathii.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp6-v3.pptx
Supplementary file 7

Centromere coordinates used for identifying conserved DNA sequence motifs in Candida species.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp7-v3.pptx
Supplementary file 8

List of strains used in this study.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp8-v3.pptx
Supplementary file 9

List of primers used in this study.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp9-v3.pptx
Supplementary file 10

List of plasmids used in this study.

https://cdn.elifesciences.org/articles/58556/elife-58556-supp10-v3.pptx
Transparent reporting form
https://cdn.elifesciences.org/articles/58556/elife-58556-transrepform-v3.docx

Download links