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Title: Diatom centromeres suggest a mechanism for nuclear DNA acquisition

Abstract

Centromeres are essential for cell division and growth in all eukaryotes, and knowledge of their sequence and structure guides the development of artificial chromosomes for functional cellular biology studies. Centromeric proteins are conserved among eukaryotes; however, centromeric DNA sequences are highly variable. We combined forward and reverse genetic approaches with chromatin immunoprecipitation to identify centromeres of the model diatom Phaeodactylum tricornutum. We observed 25 unique centromere sequences typically occurring once per chromosome, a finding that helps to resolve nuclear genome organization and indicates monocentric regional centromeres. Diatom centromere sequences contain low-GC content regions but lack repeats or other conserved sequence features. Native and foreign sequences with similar GC content to P. tricornutum centromeres can maintain episomes and recruit the diatom centromeric histone protein CENH3, suggesting nonnative sequences can also function as diatom centromeres. Thus, simple sequence requirements may enable DNA from foreign sources to persist in the nucleus as extrachromosomal episomes, revealing a potential mechanism for organellar and foreign DNA acquisition.

Authors:
 [1];  [2];  [2];  [2];  [1];  [3];  [3];  [2];  [3];  [2];  [2];  [2];  [3];  [1]; ORCiD logo [2]
  1. Univ. of California, San Diego, CA (United States). Integrative Oceanography Division. Scripps Inst. of Oceanography; J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics Group
  2. J. Craig Venter Inst., La Jolla, CA (United States). Synthetic Biology and Bioenergy Group
  3. J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics Group
Publication Date:
Research Org.:
J. Craig Venter Inst., La Jolla, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Gordon and Betty Moore Foundation (United States); National Science Foundation (NSF)
OSTI Identifier:
1367772
Alternate Identifier(s):
OSTI ID: 1423790
Grant/Contract Number:  
SC0008593; GBMF5007; GBMF3828; GBMF5006; MCB-1129303; OCE-1136477
Resource Type:
Journal Article: Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 29; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; diatom; Phaeodactylum tricornutum; episome; centromere; CENH3

Citation Formats

Diner, Rachel E., Noddings, Chari M., Lian, Nathan C., Kang, Anthony K., McQuaid, Jeffrey B., Jablanovic, Jelena, Espinoza, Josh L., Nguyen, Ngocquynh A., Anzelmatti, Miguel A., Jansson, Jakob, Bielinski, Vincent A., Karas, Bogumil J., Dupont, Christopher L., Allen, Andrew E., and Weyman, Philip D. Diatom centromeres suggest a mechanism for nuclear DNA acquisition. United States: N. p., 2017. Web. doi:10.1073/pnas.1700764114.
Diner, Rachel E., Noddings, Chari M., Lian, Nathan C., Kang, Anthony K., McQuaid, Jeffrey B., Jablanovic, Jelena, Espinoza, Josh L., Nguyen, Ngocquynh A., Anzelmatti, Miguel A., Jansson, Jakob, Bielinski, Vincent A., Karas, Bogumil J., Dupont, Christopher L., Allen, Andrew E., & Weyman, Philip D. Diatom centromeres suggest a mechanism for nuclear DNA acquisition. United States. doi:10.1073/pnas.1700764114.
Diner, Rachel E., Noddings, Chari M., Lian, Nathan C., Kang, Anthony K., McQuaid, Jeffrey B., Jablanovic, Jelena, Espinoza, Josh L., Nguyen, Ngocquynh A., Anzelmatti, Miguel A., Jansson, Jakob, Bielinski, Vincent A., Karas, Bogumil J., Dupont, Christopher L., Allen, Andrew E., and Weyman, Philip D. Tue . "Diatom centromeres suggest a mechanism for nuclear DNA acquisition". United States. doi:10.1073/pnas.1700764114.
@article{osti_1367772,
title = {Diatom centromeres suggest a mechanism for nuclear DNA acquisition},
author = {Diner, Rachel E. and Noddings, Chari M. and Lian, Nathan C. and Kang, Anthony K. and McQuaid, Jeffrey B. and Jablanovic, Jelena and Espinoza, Josh L. and Nguyen, Ngocquynh A. and Anzelmatti, Miguel A. and Jansson, Jakob and Bielinski, Vincent A. and Karas, Bogumil J. and Dupont, Christopher L. and Allen, Andrew E. and Weyman, Philip D.},
abstractNote = {Centromeres are essential for cell division and growth in all eukaryotes, and knowledge of their sequence and structure guides the development of artificial chromosomes for functional cellular biology studies. Centromeric proteins are conserved among eukaryotes; however, centromeric DNA sequences are highly variable. We combined forward and reverse genetic approaches with chromatin immunoprecipitation to identify centromeres of the model diatom Phaeodactylum tricornutum. We observed 25 unique centromere sequences typically occurring once per chromosome, a finding that helps to resolve nuclear genome organization and indicates monocentric regional centromeres. Diatom centromere sequences contain low-GC content regions but lack repeats or other conserved sequence features. Native and foreign sequences with similar GC content to P. tricornutum centromeres can maintain episomes and recruit the diatom centromeric histone protein CENH3, suggesting nonnative sequences can also function as diatom centromeres. Thus, simple sequence requirements may enable DNA from foreign sources to persist in the nucleus as extrachromosomal episomes, revealing a potential mechanism for organellar and foreign DNA acquisition.},
doi = {10.1073/pnas.1700764114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 29,
volume = 114,
place = {United States},
year = {Tue Jul 18 00:00:00 EDT 2017},
month = {Tue Jul 18 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1073/pnas.1700764114

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Cited by: 7 works
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Works referenced in this record:

Formation of de novo centromeres and construction of first-generation human artificial microchromosomes
journal, April 1997

  • Harrington, John J.; Bokkelen, Gil Van; Mays, Robert W.
  • Nature Genetics, Vol. 15, Issue 4, p. 345-355
  • DOI: 10.1038/ng0497-345