Transcriptome analysis of Colletotrichum nymphaeae-Strawberry interaction reveals in planta expressed genes associated with virulence

Colletotrichum nymphaeae, the causal agent of anthracnose fruit rot, is globally recognized as a major pathogen of strawberries due to its economic impact. Fungal pathogens utilize secreted proteins to facilitate infection by acquiring host nutrients and suppressing plant immunity. Understanding the...

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Published in:Frontiers in Plant Science
Main Authors: Egem Ozbudak, Yisel Carrillo-Tarazona, Edinson A. Diaz, Flavia T. Zambon, Lorenzo Rossi, Natalia A. Peres, Sylvain Raffaele, Liliana M. Cano
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1390926/full
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author Egem Ozbudak
Egem Ozbudak
Yisel Carrillo-Tarazona
Edinson A. Diaz
Flavia T. Zambon
Lorenzo Rossi
Natalia A. Peres
Sylvain Raffaele
Liliana M. Cano
author_facet Egem Ozbudak
Egem Ozbudak
Yisel Carrillo-Tarazona
Edinson A. Diaz
Flavia T. Zambon
Lorenzo Rossi
Natalia A. Peres
Sylvain Raffaele
Liliana M. Cano
author_sort Egem Ozbudak
collection DOAJ
container_title Frontiers in Plant Science
description Colletotrichum nymphaeae, the causal agent of anthracnose fruit rot, is globally recognized as a major pathogen of strawberries due to its economic impact. Fungal pathogens utilize secreted proteins to facilitate infection by acquiring host nutrients and suppressing plant immunity. Understanding the transcriptomic responses of C. nymphaeae during infection can provide critical insights into its pathogenic mechanisms. In this study, RNA sequencing (RNA-seq) was performed to profile the transcriptome of C. nymphaeae strain 02-179 during infection of leaf and fruit tissues of the susceptible strawberry (Fragaria x ananassa) cultivar Florida Beauty. Differential gene expression analysis identified fungal genes upregulated during these interactions. Transcriptomic profiling revealed a set of genes encoding secreted effector proteins, including NUDIX hydrolase and LysM domain-containing proteins. Additionally, genes associated with Carbohydrate-Active enzymes (CAZymes), such as multicopper oxidase, pectinesterase, pectate lyase, glycosyl hydrolase family 7, and endochitinase, were significantly upregulated. Notably, two novel tannase genes were identified among the top upregulated genes in strawberry-infected leaves and fruits. Tannase enzymes are hypothesized to degrade tannins, a group of plant secondary metabolites abundant in strawberries, known for their defensive roles against pests and pathogens. The identification of tannase genes and the other genes associated with virulence underscores the complex molecular strategies employed by C. nymphaeae to infect and colonize strawberry tissues. Genes involved in degrading plant cell walls, suppressing host defenses, and potentially overcoming chemical barriers such as tannins play critical roles in the pathogenesis of anthracnose. Further functional characterization of these genes will enhance our understanding of the disease mechanisms and could inform the development of improved management strategies for C. nymphaeae infections in strawberries.
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spelling doaj-art-2da201aa2f03401c824d37f865e8e4542025-08-20T02:48:10ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-01-011510.3389/fpls.2024.13909261390926Transcriptome analysis of Colletotrichum nymphaeae-Strawberry interaction reveals in planta expressed genes associated with virulenceEgem Ozbudak0Egem Ozbudak1Yisel Carrillo-Tarazona2Edinson A. Diaz3Flavia T. Zambon4Lorenzo Rossi5Natalia A. Peres6Sylvain Raffaele7Liliana M. Cano8Indian River Research and Education Center, Department of Plant Pathology, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Fort Pierce, FL, United StatesU.S. Department of Agriculture (USDA), Agricultural Research Service (ARS), U.S. Horticultural Research Laboratory, Fort Pierce, FL, United StatesIndian River Research and Education Center, Department of Plant Pathology, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Fort Pierce, FL, United StatesIndian River Research and Education Center, Department of Plant Pathology, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Fort Pierce, FL, United StatesIndian River Research and Education Center, Department of Horticultural Sciences, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Fort Pierce, FL, United StatesIndian River Research and Education Center, Department of Horticultural Sciences, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Fort Pierce, FL, United StatesGulf Coast Research and Education Center, Department of Plant Pathology, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Wimauma, FL, United StatesLaboratoire des Interactions Plantes Micro-organismes Environnement (LIPME), Centre National de la Recherche Scientifique (CNRS), Institut National de Recherche pour l’agriculture, l’alimentation et l’environnement (INRAE), Université de Toulouse, Castanet-Tolosan, FranceIndian River Research and Education Center, Department of Plant Pathology, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Fort Pierce, FL, United StatesColletotrichum nymphaeae, the causal agent of anthracnose fruit rot, is globally recognized as a major pathogen of strawberries due to its economic impact. Fungal pathogens utilize secreted proteins to facilitate infection by acquiring host nutrients and suppressing plant immunity. Understanding the transcriptomic responses of C. nymphaeae during infection can provide critical insights into its pathogenic mechanisms. In this study, RNA sequencing (RNA-seq) was performed to profile the transcriptome of C. nymphaeae strain 02-179 during infection of leaf and fruit tissues of the susceptible strawberry (Fragaria x ananassa) cultivar Florida Beauty. Differential gene expression analysis identified fungal genes upregulated during these interactions. Transcriptomic profiling revealed a set of genes encoding secreted effector proteins, including NUDIX hydrolase and LysM domain-containing proteins. Additionally, genes associated with Carbohydrate-Active enzymes (CAZymes), such as multicopper oxidase, pectinesterase, pectate lyase, glycosyl hydrolase family 7, and endochitinase, were significantly upregulated. Notably, two novel tannase genes were identified among the top upregulated genes in strawberry-infected leaves and fruits. Tannase enzymes are hypothesized to degrade tannins, a group of plant secondary metabolites abundant in strawberries, known for their defensive roles against pests and pathogens. The identification of tannase genes and the other genes associated with virulence underscores the complex molecular strategies employed by C. nymphaeae to infect and colonize strawberry tissues. Genes involved in degrading plant cell walls, suppressing host defenses, and potentially overcoming chemical barriers such as tannins play critical roles in the pathogenesis of anthracnose. Further functional characterization of these genes will enhance our understanding of the disease mechanisms and could inform the development of improved management strategies for C. nymphaeae infections in strawberries.https://www.frontiersin.org/articles/10.3389/fpls.2024.1390926/fullanthracnoseColletotrichumgene expressionstrawberrytranscriptome
spellingShingle Egem Ozbudak
Egem Ozbudak
Yisel Carrillo-Tarazona
Edinson A. Diaz
Flavia T. Zambon
Lorenzo Rossi
Natalia A. Peres
Sylvain Raffaele
Liliana M. Cano
Transcriptome analysis of Colletotrichum nymphaeae-Strawberry interaction reveals in planta expressed genes associated with virulence
anthracnose
Colletotrichum
gene expression
strawberry
transcriptome
title Transcriptome analysis of Colletotrichum nymphaeae-Strawberry interaction reveals in planta expressed genes associated with virulence
title_full Transcriptome analysis of Colletotrichum nymphaeae-Strawberry interaction reveals in planta expressed genes associated with virulence
title_fullStr Transcriptome analysis of Colletotrichum nymphaeae-Strawberry interaction reveals in planta expressed genes associated with virulence
title_full_unstemmed Transcriptome analysis of Colletotrichum nymphaeae-Strawberry interaction reveals in planta expressed genes associated with virulence
title_short Transcriptome analysis of Colletotrichum nymphaeae-Strawberry interaction reveals in planta expressed genes associated with virulence
title_sort transcriptome analysis of colletotrichum nymphaeae strawberry interaction reveals in planta expressed genes associated with virulence
topic anthracnose
Colletotrichum
gene expression
strawberry
transcriptome
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1390926/full
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