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Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

Plant cells undergo two types of cell cycles–the mitotic cycle in which DNA replication is coupled to mitosis, and the endocycle in which DNA replication occurs in the absence of cell division. To investigate DNA replication programs in these two types of cell cycles, we pulse labeled intact root ti...

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Autores principales: Wear, Emily E., Song, Jawon, Zynda, Gregory J., Mickelson-Young, Leigh, LeBlanc, Chantal, Lee, Tae-Jin, Deppong, David O., Allen, George C., Martienssen, Robert A., Vaughn, Matthew W., Hanley-Bowdoin, Linda, Thompson, William F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7588055/
https://www.ncbi.nlm.nih.gov/pubmed/33052904
http://dx.doi.org/10.1371/journal.pgen.1008623
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author Wear, Emily E.
Song, Jawon
Zynda, Gregory J.
Mickelson-Young, Leigh
LeBlanc, Chantal
Lee, Tae-Jin
Deppong, David O.
Allen, George C.
Martienssen, Robert A.
Vaughn, Matthew W.
Hanley-Bowdoin, Linda
Thompson, William F.
author_facet Wear, Emily E.
Song, Jawon
Zynda, Gregory J.
Mickelson-Young, Leigh
LeBlanc, Chantal
Lee, Tae-Jin
Deppong, David O.
Allen, George C.
Martienssen, Robert A.
Vaughn, Matthew W.
Hanley-Bowdoin, Linda
Thompson, William F.
author_sort Wear, Emily E.
collection PubMed
description Plant cells undergo two types of cell cycles–the mitotic cycle in which DNA replication is coupled to mitosis, and the endocycle in which DNA replication occurs in the absence of cell division. To investigate DNA replication programs in these two types of cell cycles, we pulse labeled intact root tips of maize (Zea mays) with 5-ethynyl-2’-deoxyuridine (EdU) and used flow sorting of nuclei to examine DNA replication timing (RT) during the transition from a mitotic cycle to an endocycle. Comparison of the sequence-based RT profiles showed that most regions of the maize genome replicate at the same time during S phase in mitotic and endocycling cells, despite the need to replicate twice as much DNA in the endocycle and the fact that endocycling is typically associated with cell differentiation. However, regions collectively corresponding to 2% of the genome displayed significant changes in timing between the two types of cell cycles. The majority of these regions are small with a median size of 135 kb, shift to a later RT in the endocycle, and are enriched for genes expressed in the root tip. We found larger regions that shifted RT in centromeres of seven of the ten maize chromosomes. These regions covered the majority of the previously defined functional centromere, which ranged between 1 and 2 Mb in size in the reference genome. They replicate mainly during mid S phase in mitotic cells but primarily in late S phase of the endocycle. In contrast, the immediately adjacent pericentromere sequences are primarily late replicating in both cell cycles. Analysis of CENH3 enrichment levels in 8C vs 2C nuclei suggested that there is only a partial replacement of CENH3 nucleosomes after endocycle replication is complete. The shift to later replication of centromeres and possible reduction in CENH3 enrichment after endocycle replication is consistent with a hypothesis that centromeres are inactivated when their function is no longer needed.
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spelling pubmed-75880552020-10-30 Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots Wear, Emily E. Song, Jawon Zynda, Gregory J. Mickelson-Young, Leigh LeBlanc, Chantal Lee, Tae-Jin Deppong, David O. Allen, George C. Martienssen, Robert A. Vaughn, Matthew W. Hanley-Bowdoin, Linda Thompson, William F. PLoS Genet Research Article Plant cells undergo two types of cell cycles–the mitotic cycle in which DNA replication is coupled to mitosis, and the endocycle in which DNA replication occurs in the absence of cell division. To investigate DNA replication programs in these two types of cell cycles, we pulse labeled intact root tips of maize (Zea mays) with 5-ethynyl-2’-deoxyuridine (EdU) and used flow sorting of nuclei to examine DNA replication timing (RT) during the transition from a mitotic cycle to an endocycle. Comparison of the sequence-based RT profiles showed that most regions of the maize genome replicate at the same time during S phase in mitotic and endocycling cells, despite the need to replicate twice as much DNA in the endocycle and the fact that endocycling is typically associated with cell differentiation. However, regions collectively corresponding to 2% of the genome displayed significant changes in timing between the two types of cell cycles. The majority of these regions are small with a median size of 135 kb, shift to a later RT in the endocycle, and are enriched for genes expressed in the root tip. We found larger regions that shifted RT in centromeres of seven of the ten maize chromosomes. These regions covered the majority of the previously defined functional centromere, which ranged between 1 and 2 Mb in size in the reference genome. They replicate mainly during mid S phase in mitotic cells but primarily in late S phase of the endocycle. In contrast, the immediately adjacent pericentromere sequences are primarily late replicating in both cell cycles. Analysis of CENH3 enrichment levels in 8C vs 2C nuclei suggested that there is only a partial replacement of CENH3 nucleosomes after endocycle replication is complete. The shift to later replication of centromeres and possible reduction in CENH3 enrichment after endocycle replication is consistent with a hypothesis that centromeres are inactivated when their function is no longer needed. Public Library of Science 2020-10-14 /pmc/articles/PMC7588055/ /pubmed/33052904 http://dx.doi.org/10.1371/journal.pgen.1008623 Text en © 2020 Wear et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wear, Emily E.
Song, Jawon
Zynda, Gregory J.
Mickelson-Young, Leigh
LeBlanc, Chantal
Lee, Tae-Jin
Deppong, David O.
Allen, George C.
Martienssen, Robert A.
Vaughn, Matthew W.
Hanley-Bowdoin, Linda
Thompson, William F.
Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots
title Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots
title_full Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots
title_fullStr Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots
title_full_unstemmed Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots
title_short Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots
title_sort comparing dna replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7588055/
https://www.ncbi.nlm.nih.gov/pubmed/33052904
http://dx.doi.org/10.1371/journal.pgen.1008623
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