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Early Diverging Fungus Mucor circinelloides Lacks Centromeric Histone CENP-A and Displays a Mosaic of Point and Regional Centromeres

58 Pages Posted: 6 Aug 2019 Sneak Peek Status: Review Complete

See all articles by María I. Navarro-Mendoza

María I. Navarro-Mendoza

University of Murcia - Department of Genetics and Microbiology

Carlos Pérez-Arques

University of Murcia - Department of Genetics and Microbiology

Shweta Panchal

Jawaharlal Nehru Centre for Advanced Scientific Research - Molecular Biology and Genetics Unit

Francisco E. Nicolás

University of Murcia - Department of Genetics and Microbiology

Stephen J. Mondo

US Department of Energy Joint Genome Institute

Promit Ganguly

Jawaharlal Nehru Centre for Advanced Scientific Research - Molecular Biology and Genetics Unit

Jasmyn Pangilinan

US Department of Energy Joint Genome Institute

Igor V. Grigoriev

US Department of Energy Joint Genome Institute

Joseph Heitman

Duke University - Department of Molecular Genetics & Microbiology

Kaustuv Sanyal

Jawaharlal Nehru Centre for Advanced Scientific Research - Molecular Biology and Genetics Unit

Victoriano Garre

University of Murcia; University of Murcia - Department of Genetics and Microbiology

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Abstract

Centromeres are rapidly evolving across eukaryotes, despite performing a conserved function to ensure high fidelity chromosome segregation. CENP-A chromatin is a hallmark of a functional centromere in most organisms. Due to its critical role in kinetochore architecture, the loss of CENP-A is tolerated in only a few organisms, many of which possess holocentric chromosomes. Here, we characterize the consequence of the loss of CENP-A in the fungal kingdom. Mucor circinelloides, an opportunistic human pathogen, lacks CENP-A along with the evolutionarily conserved CENP-C, but assembles a monocentric chromosome with a localized kinetochore complex throughout the cell cycle. Mis12 and Dsn1, two conserved kinetochore proteins were found to bind nine short overlapping regions, each comprising an ~200-bp AT-rich sequence followed by a centromere-specific conserved motif that echoes the structure of budding yeast point centromeres. Resembling fungal regional centromeres, these core centromere regions are embedded in large genomic expanses devoid of genes yet marked by Grem-LINE1s, a novel retrotransposable element silenced by the Dicer-dependent RNAi pathway. Our results suggest that these hybrid features of point and regional centromeres arose from the absence of CENP-A, thus defining novel mosaic centromeres in this early-diverging fungus.

Keywords: Centromere, Kinetochore, Histone variant, CENP-A, Mis12, DNS1, CENP-T, Mitosis, Mucoromycotina, early-diverging fungi, ChIP

Suggested Citation

Navarro-Mendoza, María I. and Pérez-Arques, Carlos and Panchal, Shweta and Nicolás, Francisco E. and Mondo, Stephen J. and Ganguly, Promit and Pangilinan, Jasmyn and Grigoriev, Igor V. and Heitman, Joseph and Sanyal, Kaustuv and Garre, Victoriano, Early Diverging Fungus Mucor circinelloides Lacks Centromeric Histone CENP-A and Displays a Mosaic of Point and Regional Centromeres (August 3, 2019). Available at SSRN: https://ssrn.com/abstract=3431419 or http://dx.doi.org/10.2139/ssrn.3431419
This is a paper under consideration at Cell Press and has not been peer-reviewed.

María I. Navarro-Mendoza

University of Murcia - Department of Genetics and Microbiology ( email )

Spain

Carlos Pérez-Arques

University of Murcia - Department of Genetics and Microbiology ( email )

Spain

Shweta Panchal

Jawaharlal Nehru Centre for Advanced Scientific Research - Molecular Biology and Genetics Unit ( email )

Jakkur, Bangalore
India

Francisco E. Nicolás

University of Murcia - Department of Genetics and Microbiology ( email )

Spain

Stephen J. Mondo

US Department of Energy Joint Genome Institute ( email )

Walnut Creek, CA
United States

Promit Ganguly

Jawaharlal Nehru Centre for Advanced Scientific Research - Molecular Biology and Genetics Unit ( email )

Jakkur, Bangalore
India

Jasmyn Pangilinan

US Department of Energy Joint Genome Institute ( email )

Walnut Creek, CA
United States

Igor V. Grigoriev

US Department of Energy Joint Genome Institute ( email )

Walnut Creek, CA
United States

Joseph Heitman

Duke University - Department of Molecular Genetics & Microbiology ( email )

100 Fuqua Drive
Durham, NC 27708-0204
United States

Kaustuv Sanyal

Jawaharlal Nehru Centre for Advanced Scientific Research - Molecular Biology and Genetics Unit ( email )

Jakkur, Bangalore
India

Victoriano Garre (Contact Author)

University of Murcia

Avda Teniente Flomesta, 5
Murcia, Murcia 30100
Spain

University of Murcia - Department of Genetics and Microbiology ( email )

Spain

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