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

Centromeres of Candida albicans form on unique and different DNA sequences but a closely related species, Candida tropicalis, possesses homogenized inverted repeat (HIR)-associated centromeres. To investigate the mechanism of centromere type transition, we improved the fragmented genome assembly and...

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Main Authors: Guin, Krishnendu, Chen, Yao, Mishra, Radha, Siti Rawaidah B. M. Muzaki, Thimmappa, Bhagya C., O'Brien, Caoimhe E., Butler, Geraldine, Sanyal, Amartya, Sanyal, Kaustuv
Other Authors: School of Biological Sciences
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Language:English
Published: 2020
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Online Access:https://hdl.handle.net/10356/145247
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spelling sg-ntu-dr.10356-1452472023-02-28T17:08:10Z Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres Guin, Krishnendu Chen, Yao Mishra, Radha Siti Rawaidah B. M. Muzaki Thimmappa, Bhagya C. O'Brien, Caoimhe E. Butler, Geraldine Sanyal, Amartya Sanyal, Kaustuv School of Biological Sciences Science::Biological sciences 3D Genome Chromosomal Rearrangements Centromeres of Candida albicans form on unique and different DNA sequences but a closely related species, Candida tropicalis, possesses homogenized inverted repeat (HIR)-associated centromeres. To investigate the mechanism of centromere type transition, we improved the fragmented genome assembly and constructed a chromosome-level genome assembly of C. tropicalis by employing PacBio sequencing, chromosome conformation capture sequencing (3C-seq), chromoblot, and genetic analysis of engineered aneuploid strains. Further, we analyzed the 3D genome organization using 3C-seq data, which revealed spatial proximity among the centromeres as well as telomeres of seven chromosomes in C. tropicalis. Intriguingly, we observed evidence of inter-centromeric translocations in the common ancestor of C. albicans and C. tropicalis. Identification of putative centromeres in closely related Candida sojae, Candida viswanathii and Candida parapsilosis indicates loss of ancestral HIR-associated centromeres and establishment of evolutionary new centromeres (ENCs) in C. albicans. We propose that spatial proximity of the homologous centromere DNA sequences facilitated karyotype rearrangements and centromere type transitions in human pathogenic yeasts of the CUG-Ser1 clade. Ministry of Education (MOE) Nanyang Technological University Published version We thank all the members of KS laboratory and AS laboratory for stimulating discussions and critical reading of the manuscript. We acknowledge S Sun and J Heitman for helping with SMRT-seq of C. tropicalis at the PacBio sequencing facility at Duke University. We also thank AIS Khalil for helping with CNAtra software for CNV analysis. Illumina sequencing experiments for the C. sojae genome were performed at Clevergene Biocorp, Bangalore, India. We also thank B Suma for confocal microscopy, JNCASR. KG acknowledges Shyama Prasad Mukherjee Fellowship from Council of Scientific and Industrial Research (CSIR), Govt. of India [07/733 (0181)/2013-EMR-I] and financial assistance from JNCASR. This project is supported by a grant (BT/PR27490/Med/29/1323/2018) from the Department of Biotechnology (DBT), Govt. of India to KS. KS acknowledges TATA innovation fellowship (BT/HRD/35/01/03/2017) and Department of Biotechnology grant in Life Science Research, Education and Training at JNCASR (BT/INF/22/SP27679/2018). Intramural funding from JNCASR is acknowledged. This work is also supported by Nanyang Technological University’s Nanyang Assistant Professorship grant and Singapore Ministry of Education Academic Research Fund Tier 1 grant [RG39/18] to AS. 2020-12-15T08:41:55Z 2020-12-15T08:41:55Z 2020 Journal Article Guin, K., Chen, Y., Mishra, R., Siti Rawaidah B. M. Muzaki, Thimmappa, B. C., O'brien, C. E., . . . Sanyal, K. (2020). Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres. eLife, 9, e58556-. doi:10.7554/eLife.58556 2050-084X https://hdl.handle.net/10356/145247 10.7554/eLife.58556 32469306 9 en RG39/18 eLife © 2020 Guin et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
3D Genome
Chromosomal Rearrangements
spellingShingle Science::Biological sciences
3D Genome
Chromosomal Rearrangements
Guin, Krishnendu
Chen, Yao
Mishra, Radha
Siti Rawaidah B. M. Muzaki
Thimmappa, Bhagya C.
O'Brien, Caoimhe E.
Butler, Geraldine
Sanyal, Amartya
Sanyal, Kaustuv
Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
description Centromeres of Candida albicans form on unique and different DNA sequences but a closely related species, Candida tropicalis, possesses homogenized inverted repeat (HIR)-associated centromeres. To investigate the mechanism of centromere type transition, we improved the fragmented genome assembly and constructed a chromosome-level genome assembly of C. tropicalis by employing PacBio sequencing, chromosome conformation capture sequencing (3C-seq), chromoblot, and genetic analysis of engineered aneuploid strains. Further, we analyzed the 3D genome organization using 3C-seq data, which revealed spatial proximity among the centromeres as well as telomeres of seven chromosomes in C. tropicalis. Intriguingly, we observed evidence of inter-centromeric translocations in the common ancestor of C. albicans and C. tropicalis. Identification of putative centromeres in closely related Candida sojae, Candida viswanathii and Candida parapsilosis indicates loss of ancestral HIR-associated centromeres and establishment of evolutionary new centromeres (ENCs) in C. albicans. We propose that spatial proximity of the homologous centromere DNA sequences facilitated karyotype rearrangements and centromere type transitions in human pathogenic yeasts of the CUG-Ser1 clade.
author2 School of Biological Sciences
author_facet School of Biological Sciences
Guin, Krishnendu
Chen, Yao
Mishra, Radha
Siti Rawaidah B. M. Muzaki
Thimmappa, Bhagya C.
O'Brien, Caoimhe E.
Butler, Geraldine
Sanyal, Amartya
Sanyal, Kaustuv
format Article
author Guin, Krishnendu
Chen, Yao
Mishra, Radha
Siti Rawaidah B. M. Muzaki
Thimmappa, Bhagya C.
O'Brien, Caoimhe E.
Butler, Geraldine
Sanyal, Amartya
Sanyal, Kaustuv
author_sort Guin, Krishnendu
title Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
title_short Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
title_full Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
title_fullStr Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
title_full_unstemmed Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
title_sort spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
publishDate 2020
url https://hdl.handle.net/10356/145247
_version_ 1759857873102307328