The Small Ras Superfamily GTPase Rho4 of the Maize Anthracnose Fungus <i>Colletotrichum graminicola</i> Is Required for β-1,3-glucan Synthesis, Cell Wall Integrity, and Full Virulence

Small Ras superfamily GTPases are highly conserved regulatory factors of fungal cell wall biosynthesis and morphogenesis. Previous experiments have shown that the Rho4-like protein of the maize anthracnose fungus <i>Colletotrichum graminicola</i>, formerly erroneously annotated as a Rho1...

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Main Authors: Ely Oliveira-Garcia, Lala Aliyeva-Schnorr, Alan De Oliveira Silva, Seif El Din Ghanem, Kathrin Thor, Edgar Peiter, Holger B. Deising
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/8/10/997
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author Ely Oliveira-Garcia
Lala Aliyeva-Schnorr
Alan De Oliveira Silva
Seif El Din Ghanem
Kathrin Thor
Edgar Peiter
Holger B. Deising
author_facet Ely Oliveira-Garcia
Lala Aliyeva-Schnorr
Alan De Oliveira Silva
Seif El Din Ghanem
Kathrin Thor
Edgar Peiter
Holger B. Deising
author_sort Ely Oliveira-Garcia
collection DOAJ
description Small Ras superfamily GTPases are highly conserved regulatory factors of fungal cell wall biosynthesis and morphogenesis. Previous experiments have shown that the Rho4-like protein of the maize anthracnose fungus <i>Colletotrichum graminicola</i>, formerly erroneously annotated as a Rho1 protein, physically interacts with the β-1,3-glucan synthase Gls1 (Lange et al., 2014; Curr. Genet. 60:343–350). Here, we show that Rho4 is required for β-1,3-glucan synthesis. Accordingly, Δ<i>rho4</i> strains formed distorted vegetative hyphae with swellings, and exhibited strongly reduced rates of hyphal growth and defects in asexual sporulation. Moreover, on host cuticles, conidia of Δ<i>rho4</i> strains formed long hyphae with hyphopodia, rather than short germ tubes with appressoria. Hyphopodia of Δ<i>rho4</i> strains exhibited penetration defects and often germinated laterally, indicative of cell wall weaknesses. In planta differentiated infection hyphae of Δ<i>rho4</i> strains were fringy, and anthracnose disease symptoms caused by these strains on intact and wounded maize leaf segments were significantly weaker than those caused by the WT strain. A retarded disease symptom development was confirmed by qPCR analyses. Collectively, we identified the Ras GTPase Rho4 as a new virulence factor of <i>C. graminicola</i>.
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spelling doaj.art-b707ef52ec484d33b9868d8c8d6b7b632023-11-24T00:46:25ZengMDPI AGJournal of Fungi2309-608X2022-09-0181099710.3390/jof8100997The Small Ras Superfamily GTPase Rho4 of the Maize Anthracnose Fungus <i>Colletotrichum graminicola</i> Is Required for β-1,3-glucan Synthesis, Cell Wall Integrity, and Full VirulenceEly Oliveira-Garcia0Lala Aliyeva-Schnorr1Alan De Oliveira Silva2Seif El Din Ghanem3Kathrin Thor4Edgar Peiter5Holger B. Deising6Institute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin Luther University Halle-Wittenberg, Betty-Heimann-Str. 3, D-06120 Halle, Saale, GermanyInstitute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin Luther University Halle-Wittenberg, Betty-Heimann-Str. 3, D-06120 Halle, Saale, GermanyInstitute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin Luther University Halle-Wittenberg, Betty-Heimann-Str. 3, D-06120 Halle, Saale, GermanyInstitute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin Luther University Halle-Wittenberg, Betty-Heimann-Str. 3, D-06120 Halle, Saale, GermanyInstitute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin Luther University Halle-Wittenberg, Betty-Heimann-Str. 3, D-06120 Halle, Saale, GermanyInstitute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin Luther University Halle-Wittenberg, Betty-Heimann-Str. 3, D-06120 Halle, Saale, GermanyInstitute of Agricultural and Nutritional Sciences, Faculty of Natural Sciences III, Martin Luther University Halle-Wittenberg, Betty-Heimann-Str. 3, D-06120 Halle, Saale, GermanySmall Ras superfamily GTPases are highly conserved regulatory factors of fungal cell wall biosynthesis and morphogenesis. Previous experiments have shown that the Rho4-like protein of the maize anthracnose fungus <i>Colletotrichum graminicola</i>, formerly erroneously annotated as a Rho1 protein, physically interacts with the β-1,3-glucan synthase Gls1 (Lange et al., 2014; Curr. Genet. 60:343–350). Here, we show that Rho4 is required for β-1,3-glucan synthesis. Accordingly, Δ<i>rho4</i> strains formed distorted vegetative hyphae with swellings, and exhibited strongly reduced rates of hyphal growth and defects in asexual sporulation. Moreover, on host cuticles, conidia of Δ<i>rho4</i> strains formed long hyphae with hyphopodia, rather than short germ tubes with appressoria. Hyphopodia of Δ<i>rho4</i> strains exhibited penetration defects and often germinated laterally, indicative of cell wall weaknesses. In planta differentiated infection hyphae of Δ<i>rho4</i> strains were fringy, and anthracnose disease symptoms caused by these strains on intact and wounded maize leaf segments were significantly weaker than those caused by the WT strain. A retarded disease symptom development was confirmed by qPCR analyses. Collectively, we identified the Ras GTPase Rho4 as a new virulence factor of <i>C. graminicola</i>.https://www.mdpi.com/2309-608X/8/10/997appressoriaβ-1,3-glucan synthesis<i>Colletotrichum graminicola</i>fungal cell wallshyphopodiapenetration defect
spellingShingle Ely Oliveira-Garcia
Lala Aliyeva-Schnorr
Alan De Oliveira Silva
Seif El Din Ghanem
Kathrin Thor
Edgar Peiter
Holger B. Deising
The Small Ras Superfamily GTPase Rho4 of the Maize Anthracnose Fungus <i>Colletotrichum graminicola</i> Is Required for β-1,3-glucan Synthesis, Cell Wall Integrity, and Full Virulence
Journal of Fungi
appressoria
β-1,3-glucan synthesis
<i>Colletotrichum graminicola</i>
fungal cell walls
hyphopodia
penetration defect
title The Small Ras Superfamily GTPase Rho4 of the Maize Anthracnose Fungus <i>Colletotrichum graminicola</i> Is Required for β-1,3-glucan Synthesis, Cell Wall Integrity, and Full Virulence
title_full The Small Ras Superfamily GTPase Rho4 of the Maize Anthracnose Fungus <i>Colletotrichum graminicola</i> Is Required for β-1,3-glucan Synthesis, Cell Wall Integrity, and Full Virulence
title_fullStr The Small Ras Superfamily GTPase Rho4 of the Maize Anthracnose Fungus <i>Colletotrichum graminicola</i> Is Required for β-1,3-glucan Synthesis, Cell Wall Integrity, and Full Virulence
title_full_unstemmed The Small Ras Superfamily GTPase Rho4 of the Maize Anthracnose Fungus <i>Colletotrichum graminicola</i> Is Required for β-1,3-glucan Synthesis, Cell Wall Integrity, and Full Virulence
title_short The Small Ras Superfamily GTPase Rho4 of the Maize Anthracnose Fungus <i>Colletotrichum graminicola</i> Is Required for β-1,3-glucan Synthesis, Cell Wall Integrity, and Full Virulence
title_sort small ras superfamily gtpase rho4 of the maize anthracnose fungus i colletotrichum graminicola i is required for β 1 3 glucan synthesis cell wall integrity and full virulence
topic appressoria
β-1,3-glucan synthesis
<i>Colletotrichum graminicola</i>
fungal cell walls
hyphopodia
penetration defect
url https://www.mdpi.com/2309-608X/8/10/997
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