Mechanistic basis of branch-site selection in filamentous bacteria.

Many filamentous organisms, such as fungi, grow by tip-extension and by forming new branches behind the tips. A similar growth mode occurs in filamentous bacteria, including the genus Streptomyces, although here our mechanistic understanding has been very limited. The Streptomyces protein DivIVA is...

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Main Authors: David M Richards, Antje M Hempel, Klas Flärdh, Mark J Buttner, Martin Howard
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Computational Biology
Online Access:https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002423&type=printable
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author David M Richards
Antje M Hempel
Klas Flärdh
Mark J Buttner
Martin Howard
author_facet David M Richards
Antje M Hempel
Klas Flärdh
Mark J Buttner
Martin Howard
author_sort David M Richards
collection DOAJ
description Many filamentous organisms, such as fungi, grow by tip-extension and by forming new branches behind the tips. A similar growth mode occurs in filamentous bacteria, including the genus Streptomyces, although here our mechanistic understanding has been very limited. The Streptomyces protein DivIVA is a critical determinant of hyphal growth and localizes in foci at hyphal tips and sites of future branch development. However, how such foci form was previously unknown. Here, we show experimentally that DivIVA focus-formation involves a novel mechanism in which new DivIVA foci break off from existing tip-foci, bypassing the need for initial nucleation or de novo branch-site selection. We develop a mathematical model for DivIVA-dependent growth and branching, involving DivIVA focus-formation by tip-focus splitting, focus growth, and the initiation of new branches at a critical focus size. We quantitatively fit our model to the experimentally-measured tip-to-branch and branch-to-branch length distributions. The model predicts a particular bimodal tip-to-branch distribution results from tip-focus splitting, a prediction we confirm experimentally. Our work provides mechanistic understanding of a novel mode of hyphal growth regulation that may be widely employed.
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publishDate 2012-01-01
publisher Public Library of Science (PLoS)
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spelling doaj-art-f355d39b753545708fef2d1debdd11562025-08-20T03:10:02ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582012-01-0183e100242310.1371/journal.pcbi.1002423Mechanistic basis of branch-site selection in filamentous bacteria.David M RichardsAntje M HempelKlas FlärdhMark J ButtnerMartin HowardMany filamentous organisms, such as fungi, grow by tip-extension and by forming new branches behind the tips. A similar growth mode occurs in filamentous bacteria, including the genus Streptomyces, although here our mechanistic understanding has been very limited. The Streptomyces protein DivIVA is a critical determinant of hyphal growth and localizes in foci at hyphal tips and sites of future branch development. However, how such foci form was previously unknown. Here, we show experimentally that DivIVA focus-formation involves a novel mechanism in which new DivIVA foci break off from existing tip-foci, bypassing the need for initial nucleation or de novo branch-site selection. We develop a mathematical model for DivIVA-dependent growth and branching, involving DivIVA focus-formation by tip-focus splitting, focus growth, and the initiation of new branches at a critical focus size. We quantitatively fit our model to the experimentally-measured tip-to-branch and branch-to-branch length distributions. The model predicts a particular bimodal tip-to-branch distribution results from tip-focus splitting, a prediction we confirm experimentally. Our work provides mechanistic understanding of a novel mode of hyphal growth regulation that may be widely employed.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002423&type=printable
spellingShingle David M Richards
Antje M Hempel
Klas Flärdh
Mark J Buttner
Martin Howard
Mechanistic basis of branch-site selection in filamentous bacteria.
PLoS Computational Biology
title Mechanistic basis of branch-site selection in filamentous bacteria.
title_full Mechanistic basis of branch-site selection in filamentous bacteria.
title_fullStr Mechanistic basis of branch-site selection in filamentous bacteria.
title_full_unstemmed Mechanistic basis of branch-site selection in filamentous bacteria.
title_short Mechanistic basis of branch-site selection in filamentous bacteria.
title_sort mechanistic basis of branch site selection in filamentous bacteria
url https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002423&type=printable
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AT markjbuttner mechanisticbasisofbranchsiteselectioninfilamentousbacteria
AT martinhoward mechanisticbasisofbranchsiteselectioninfilamentousbacteria