Nonrandom segregation of sister chromosomes by Escherichia coli MukBEF

Structural maintenance of chromosomes (SMC) complexes contribute to chromosome organization in all domains of life. In Escherichia coli, MukBEF, the functional SMC homolog, promotes spatiotemporal chromosome organization and faithful chromosome segregation. Here, we address the relative contribution...

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Main Authors: Mäkelä, J, Uphoff, S, Sherratt, DJ
Format: Journal article
Language:English
Published: National Academy of Sciences 2021
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author Mäkelä, J
Uphoff, S
Sherratt, DJ
author_facet Mäkelä, J
Uphoff, S
Sherratt, DJ
author_sort Mäkelä, J
collection OXFORD
description Structural maintenance of chromosomes (SMC) complexes contribute to chromosome organization in all domains of life. In Escherichia coli, MukBEF, the functional SMC homolog, promotes spatiotemporal chromosome organization and faithful chromosome segregation. Here, we address the relative contributions of MukBEF and the replication terminus (ter) binding protein, MatP, to chromosome organization–segregation. We show that MukBEF, but not MatP, is required for the normal localization of the origin of replication to midcell and for the establishment of translational symmetry between newly replicated sister chromosomes. Overall, chromosome orientation is normally maintained through division from one generation to the next. Analysis of loci flanking the replication termination region (ter), which demark the ends of the linearly organized portion of the nucleoid, demonstrates that MatP is required for maintenance of chromosome orientation. We show that DNA-bound β2-processivity clamps, which mark the lagging strands at DNA replication forks, localize to the cell center, independent of replisome location but dependent on MukBEF action, and consistent with translational symmetry of sister chromosomes. Finally, we directly show that the older (“immortal”) template DNA strand, propagated from previous generations, is preferentially inherited by the cell forming at the old pole, dependent on MukBEF and MatP. The work further implicates MukBEF and MatP as central players in chromosome organization, segregation, and nonrandom inheritance of genetic material and suggests a general framework for understanding how chromosome conformation and dynamics shape subcellular organization.
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spelling oxford-uuid:44d13bbe-f37e-47fa-a016-f28100ffc1522022-03-26T15:03:58ZNonrandom segregation of sister chromosomes by Escherichia coli MukBEFJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:44d13bbe-f37e-47fa-a016-f28100ffc152EnglishSymplectic ElementsNational Academy of Sciences2021Mäkelä, JUphoff, SSherratt, DJStructural maintenance of chromosomes (SMC) complexes contribute to chromosome organization in all domains of life. In Escherichia coli, MukBEF, the functional SMC homolog, promotes spatiotemporal chromosome organization and faithful chromosome segregation. Here, we address the relative contributions of MukBEF and the replication terminus (ter) binding protein, MatP, to chromosome organization–segregation. We show that MukBEF, but not MatP, is required for the normal localization of the origin of replication to midcell and for the establishment of translational symmetry between newly replicated sister chromosomes. Overall, chromosome orientation is normally maintained through division from one generation to the next. Analysis of loci flanking the replication termination region (ter), which demark the ends of the linearly organized portion of the nucleoid, demonstrates that MatP is required for maintenance of chromosome orientation. We show that DNA-bound β2-processivity clamps, which mark the lagging strands at DNA replication forks, localize to the cell center, independent of replisome location but dependent on MukBEF action, and consistent with translational symmetry of sister chromosomes. Finally, we directly show that the older (“immortal”) template DNA strand, propagated from previous generations, is preferentially inherited by the cell forming at the old pole, dependent on MukBEF and MatP. The work further implicates MukBEF and MatP as central players in chromosome organization, segregation, and nonrandom inheritance of genetic material and suggests a general framework for understanding how chromosome conformation and dynamics shape subcellular organization.
spellingShingle Mäkelä, J
Uphoff, S
Sherratt, DJ
Nonrandom segregation of sister chromosomes by Escherichia coli MukBEF
title Nonrandom segregation of sister chromosomes by Escherichia coli MukBEF
title_full Nonrandom segregation of sister chromosomes by Escherichia coli MukBEF
title_fullStr Nonrandom segregation of sister chromosomes by Escherichia coli MukBEF
title_full_unstemmed Nonrandom segregation of sister chromosomes by Escherichia coli MukBEF
title_short Nonrandom segregation of sister chromosomes by Escherichia coli MukBEF
title_sort nonrandom segregation of sister chromosomes by escherichia coli mukbef
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