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      Woronin body-based sealing of septal pores

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Highlights

          • Upon wounding, Woronin bodies seal hyphal septa in filamentous ascomycetes.

          • Little is known about the mechanism underpinning Woronin body translocation.

          • Passive bulk flow of cytoplasm may move Woronin bodies into the septal pore.

          • Mechanisms that involve Lah proteins are likely to support Woronin body based sealing.

          • ATP is required to prevent Woronin bodies from closing pores in healthy cells.

          Abstract

          In ascomycete fungi, hyphal cells are separated by perforate septa, which allow cell-to-cell communication. To protect against extensive wound-induced damage, septal pores are sealed by peroxisome-derived Woronin bodies (WBs). The mechanism underpinning WB movement is unknown, but cytoplasmic bulk flow may “flush” WBs into the pore. However, some studies suggest a controlled and active mechanism of WB movement. Indeed, in the wheat pathogen Zymoseptoria tritici cellular ATP prevents WBs from pore sealing in unwounded cells. Thus, cells appear to exert active control over WB closure. Here, we summarize our current understanding of WB-based pore sealing in ascomycete fungi.

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          Most cited references16

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          Mechanoenzymatics of titin kinase.

          Biological responses to mechanical stress require strain-sensing molecules, whose mechanically induced conformational changes are relayed to signaling cascades mediating changes in cell and tissue properties. In vertebrate muscle, the giant elastic protein titin is involved in strain sensing via its C-terminal kinase domain (TK) at the sarcomeric M-band and contributes to the adaptation of muscle in response to changes in mechanical strain. TK is regulated in a unique dual autoinhibition mechanism by a C-terminal regulatory tail, blocking the ATP binding site, and tyrosine autoinhibition of the catalytic base. For access to the ATP binding site and phosphorylation of the autoinhibitory tyrosine, the C-terminal autoinhibitory tail needs to be removed. Here, we use AFM-based single-molecule force spectroscopy, molecular dynamics simulations, and enzymatics to study the conformational changes during strain-induced activation of human TK. We show that mechanical strain activates ATP binding before unfolding of the structural titin domains, and that TK can thus act as a biological force sensor. Furthermore, we identify the steps in which the autoinhibition of TK is mechanically relieved at low forces, leading to binding of the cosubstrate ATP and priming the enzyme for subsequent autophosphorylation and substrate turnover.
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            A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane.

            G Jedd, N Chua (2000)
            The Woronin body is a membrane-bound organelle that has been observed in over 50 species of filamentous fungi. However, neither the composition nor the precise function of the Woronin body has yet been determined. Here we purify the Woronin body from Neurospora crassa and isolate Hex1, a new protein containing a consensus sequence known as peroxisome-targeting signal-1 (PTS1). We show that Hex1 is localized to the matrix of the Woronin body by immunoelectron microscopy, and that a green fluorescent protein- (GFP-)Hex1 fusion protein is targeted to yeast peroxisomes in a PTS1- and peroxin-dependent manner. The expression of the HEX1 gene in yeast generates hexagonal vesicles that are morphologically similar to the native Woronin body, implying a Hex1-encoded mechanism of Woronin-body assembly. Deletion of HEX1 in N. crassa eliminates Woronin bodies from the cytoplasm and results in hyphae that exhibit a cytoplasmic-bleeding phenotype in response to cell lysis. Our results show that the Woronin body represents a new category of peroxisome with a function in the maintenance of cellular integrity.
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              Hex-1, a gene unique to filamentous fungi, encodes the major protein of the Woronin body and functions as a plug for septal pores.

              We have identified a gene, named hex-1, that encodes the major protein in the hexagonal crystals, or Woronin bodies, of Neurospora crassa. Analysis of a strain with a null mutation in the hex-1 gene showed that the septal pores in this organism were not plugged when hyphae were damaged, leading to extensive loss of cytoplasm. When grown on agar plates containing sorbose, the hex-1(-) strain showed extensive lysis of hyphal tips. The HEX-1 protein was predicted to be 19,125 Da. Analysis of the N-terminus of the purified protein indicated that 16 residues are cleaved, yielding a protein of 17,377 Da. A polyclonal antibody raised to the HEX-1 protein recognized multiple forms of the protein, apparently dimers and tetramers that were resistant to solubilization by sodium dodecyl sulfate and reducing reagents. Treatment of the protein with phosphatase caused dissociation of these oligomers. Preparations enriched in Woronin bodies contained catalase activity, which was not detected in comparable fractions from the hex-1(-) mutant strain. These results support the hypothesis that the Woronin body is a specialized peroxisome that functions as a plug for septal pores. Copyright 2000 Academic Press.
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                Author and article information

                Contributors
                Journal
                Fungal Genet Biol
                Fungal Genet. Biol
                Fungal Genetics and Biology
                Academic Press
                1087-1845
                1096-0937
                1 December 2017
                December 2017
                : 109
                : 53-55
                Affiliations
                [a ]School of Biosciences, University of Exeter, Stocker Road, Exeter EX4 4QD, United Kingdom
                [b ]Donder’s Chair, University of Utrecht, Department of Biology, Padualaan 8, 3584 CH Utrecht, The Netherlands
                Author notes
                [* ]Corresponding author at: School of Biosciences, University of Exeter, Stocker Road, Exeter EX4 4QD, United Kingdom.School of BiosciencesUniversity of ExeterStocker RoadExeterEX4 4QDUnited Kingdom g.steinberg@ 123456exeter.ac.uk
                Article
                S1087-1845(17)30151-2
                10.1016/j.fgb.2017.10.006
                5745230
                29107012
                602a8f29-6546-46c7-b4c6-ca1efc741ddf
                © 2017 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 June 2017
                : 3 October 2017
                : 22 October 2017
                Categories
                Article

                Plant science & Botany
                woronin bodes,zymoseptoria tritici,septal pore,wb, woronin body
                Plant science & Botany
                woronin bodes, zymoseptoria tritici, septal pore, wb, woronin body

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