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:	Emily E Wear, Jawon Song, Gregory J Zynda, Leigh Mickelson-Young, Chantal LeBlanc, Tae-Jin Lee, David O Deppong, George C Allen, Robert A Martienssen, Matthew W Vaughn, Linda Hanley-Bowdoin, William F Thompson
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2020
Materias:	Genetics QH426-470
Acceso en línea:	https://doaj.org/article/d95231f4b73940138ebe1343c36485a7
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spelling	oai:doaj.org-article:d95231f4b73940138ebe1343c36485a72021-12-02T20:03:26ZComparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots.1553-73901553-740410.1371/journal.pgen.1008623https://doaj.org/article/d95231f4b73940138ebe1343c36485a72020-10-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1008623https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Plant 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.Emily E WearJawon SongGregory J ZyndaLeigh Mickelson-YoungChantal LeBlancTae-Jin LeeDavid O DeppongGeorge C AllenRobert A MartienssenMatthew W VaughnLinda Hanley-BowdoinWilliam F ThompsonPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 16, Iss 10, p e1008623 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Genetics QH426-470
spellingShingle	Genetics QH426-470 Emily E Wear Jawon Song Gregory J Zynda Leigh Mickelson-Young Chantal LeBlanc Tae-Jin Lee David O Deppong George C Allen Robert A Martienssen Matthew W Vaughn Linda Hanley-Bowdoin William F Thompson Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots.
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.
format	article
author	Emily E Wear Jawon Song Gregory J Zynda Leigh Mickelson-Young Chantal LeBlanc Tae-Jin Lee David O Deppong George C Allen Robert A Martienssen Matthew W Vaughn Linda Hanley-Bowdoin William F Thompson
author_facet	Emily E Wear Jawon Song Gregory J Zynda Leigh Mickelson-Young Chantal LeBlanc Tae-Jin Lee David O Deppong George C Allen Robert A Martienssen Matthew W Vaughn Linda Hanley-Bowdoin William F Thompson
author_sort	Emily E Wear
title	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_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_sort	comparing dna replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots.
publisher	Public Library of Science (PLoS)
publishDate	2020
url	https://doaj.org/article/d95231f4b73940138ebe1343c36485a7
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Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots.

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