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Centromere-mediated chromosome break drives karyotype evolution in closely related Malassezia species

Sundar Ram Sankaranarayanan, Giuseppe Ianiri, Md. Hashim Reza, Bhagya C. Thimmappa, Promit Ganguly, Marco A. Coelho, Sheng Sun, Rahul Siddharthan, Christian Tellgren-Roth, Thomas L Dawson Jr., Joseph Heitman, View ORCID ProfileKaustuv Sanyal
doi: https://doi.org/10.1101/533794
Sundar Ram Sankaranarayanan
1Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Center for Advanced Scientific Research, Jakkur P.O, Bengaluru-560064.
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Giuseppe Ianiri
2Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710, USA
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Md. Hashim Reza
1Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Center for Advanced Scientific Research, Jakkur P.O, Bengaluru-560064.
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Bhagya C. Thimmappa
1Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Center for Advanced Scientific Research, Jakkur P.O, Bengaluru-560064.
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Promit Ganguly
1Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Center for Advanced Scientific Research, Jakkur P.O, Bengaluru-560064.
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Marco A. Coelho
2Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710, USA
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Sheng Sun
2Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710, USA
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Rahul Siddharthan
3The Institute of Mathematical Sciences/HBNI, Taramani, Chennai 600 113, India
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Christian Tellgren-Roth
4National Genomics Infrastructure, Science for Life Laboratory, Department of Immunology, Genetics and Pathology, Uppsala University, 75108 Uppsala, Sweden
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Thomas L Dawson Jr.
5Skin Research Institute Singapore, Agency for Science, Technology and Research (A*STAR), 138648, Singapore
6Medical University of South Carolina, School of Pharmacy, Department of Drug Discovery, 29425, USA
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Joseph Heitman
2Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710, USA
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  • For correspondence: heitm001@duke.edu sanyal@jncasr.ac.in
Kaustuv Sanyal
1Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Center for Advanced Scientific Research, Jakkur P.O, Bengaluru-560064.
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  • ORCID record for Kaustuv Sanyal
  • For correspondence: heitm001@duke.edu sanyal@jncasr.ac.in
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Abstract

Intra-chromosomal or inter-chromosomal genomic rearrangements often lead to speciation (1). Loss or gain of a centromere leads to alterations in chromosome number in closely related species. Thus, centromeres can enable tracing the path of evolution from the ancestral to a derived state (2). The Malassezia species complex of the phylum Basiodiomycota shows remarkable diversity in chromosome number ranging between six and nine chromosomes (3–5). To understand these transitions, we experimentally identified all eight centromeres as binding sites of an evolutionarily conserved outer kinetochore protein Mis12/Mtw1 in M. sympodialis. The 3 to 5 kb centromere regions share an AT-rich, poorly transcribed core region enriched with a 12 bp consensus motif. We also mapped nine such AT-rich centromeres in M. globosa and the related species Malassezia restricta and Malassezia slooffiae. While eight predicted centromeres were found within conserved synteny blocks between these species and M. sympodialis, the remaining centromere in M. globosa (MgCEN2) or its orthologous centromere in M. slooffiae (MslCEN4) and M. restricta (MreCEN8) mapped to a synteny breakpoint compared with M. sympodialis. Taken together, we provide evidence that breakage and loss of a centromere (CEN2) in an ancestral Malassezia species possessing nine chromosomes resulted in fewer chromosomes in M. sympodialis. Strikingly, the predicted centromeres of all closely related Malassezia species map to an AT-rich core on each chromosome that also shows enrichment of the 12 bp sequence motif. We propose that centromeres are fragile AT-rich sites driving karyotype diversity through breakage and inactivation in these and other species.

Significance statement The number of chromosomes can vary between closely related species. Centromere loss destabilizes chromosomes and results in reduced number of chromosomes to drive speciation. A series of evidence from studies on various cancers suggest that an imbalance in kinetochore-microtubule attachments results in breaks at the centromeres. To understand if such events can cause chromosome number changes in nature, we studied six species of Malassezia, of which three possess eight chromosomes and others have nine chromosomes each. We find signatures of chromosome breakage at the centromeres in organisms having nine chromosomes. We propose that the break at the centromere followed by fusions of acentric chromosomes to other chromosomes could be a plausible mechanism shaping the karyotype of Malassezia and related organisms.

Classification Biological sciences, Genetics

Footnotes

  • E-mail address of authors SRS (sundar_ram{at}jncasr.ac.in), GI (giuseppe.ianiri{at}duke.edu), MHR (hashimreza{at}jncasr.ac.in), BCT (bhagyathimmappa{at}gmail.com), PG (promitganguly1{at}gmail.com), MAC (marco.dias.coelho{at}duke.edu), SS (sheng.sun{at}duke.edu), RS (rsidd{at}imsc.res.in), CTR (christian.tellgren{at}igp.uu.se), TLD (thomas_dawson{at}sris.a-star.edu.sg)

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Posted January 29, 2019.
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Centromere-mediated chromosome break drives karyotype evolution in closely related Malassezia species
Sundar Ram Sankaranarayanan, Giuseppe Ianiri, Md. Hashim Reza, Bhagya C. Thimmappa, Promit Ganguly, Marco A. Coelho, Sheng Sun, Rahul Siddharthan, Christian Tellgren-Roth, Thomas L Dawson Jr., Joseph Heitman, Kaustuv Sanyal
bioRxiv 533794; doi: https://doi.org/10.1101/533794
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Centromere-mediated chromosome break drives karyotype evolution in closely related Malassezia species
Sundar Ram Sankaranarayanan, Giuseppe Ianiri, Md. Hashim Reza, Bhagya C. Thimmappa, Promit Ganguly, Marco A. Coelho, Sheng Sun, Rahul Siddharthan, Christian Tellgren-Roth, Thomas L Dawson Jr., Joseph Heitman, Kaustuv Sanyal
bioRxiv 533794; doi: https://doi.org/10.1101/533794

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