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Comparative Genomic Analysis of Dactylonectria torresensis Strains from Grapevine, Soil and Weed Highlights Potential Mechanisms in Pathogenicity and Endophytic Lifestyle

The soil-borne fungus Dactylonectria torresensis is the most common causal agent of black-foot disease in Europe. However, there is a lack of understanding on how this fungus can provoke plant symptoms. In this study, we sequenced, annotated and analyzed the genomes of three isolates of D. torresens...

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Autores principales: Gramaje, David, Berlanas, Carmen, Martínez-Diz, María del Pilar, Diaz-Losada, Emilia, Antonielli, Livio, Beier, Sabrina, Gorfer, Markus, Schmoll, Monika, Compant, Stéphane
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7712071/
https://www.ncbi.nlm.nih.gov/pubmed/33138048
http://dx.doi.org/10.3390/jof6040255
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author Gramaje, David
Berlanas, Carmen
Martínez-Diz, María del Pilar
Diaz-Losada, Emilia
Antonielli, Livio
Beier, Sabrina
Gorfer, Markus
Schmoll, Monika
Compant, Stéphane
author_facet Gramaje, David
Berlanas, Carmen
Martínez-Diz, María del Pilar
Diaz-Losada, Emilia
Antonielli, Livio
Beier, Sabrina
Gorfer, Markus
Schmoll, Monika
Compant, Stéphane
author_sort Gramaje, David
collection PubMed
description The soil-borne fungus Dactylonectria torresensis is the most common causal agent of black-foot disease in Europe. However, there is a lack of understanding on how this fungus can provoke plant symptoms. In this study, we sequenced, annotated and analyzed the genomes of three isolates of D. torresensis collected from asymptomatic vine, weed and soil. Sequenced genomes were further compared to those of 27 fungal species including root and aerial pathogens, white rot degraders, indoor biodeterioration agents, saprotrophs, dark septate endophytes and mycorrhiza. Strains of D. torresensis present genomes with between 64 and 65 Mbp and with up to 18,548 predicted genes for each strain. Average Nucleotide Identity (ANI) shows that strains are different according to genome contents. Clusters of orthologous groups were compared, and clusters of genes related to necroses were particularly detected in all strains of D. torresensis (necrosis inducing peptides and proteins, and ethylene inducing peptides) as well as several genes involved in resistance against fungicides frequently used in viticulture such as copper. Interestingly, an expanded high number of genes related to carbohydrate-active enzymes were detected in each Dactylonectria strain, especially those related to glycoside hydrolases that could be involved in penetration of plant tissues or pathogenicity. An increased number of candidate genes for CAZyme classes AA9 and AA3-1 supports the ability of strains to efficiently degrade plant material. High numbers of genes of D. torresensis related to secretome and small secreted proteins were further characterized. Moreover, the presence of several gene clusters such as fujikurin-like genes was detected and were normally found in Fusarium fujikuroi, that have been linked to fungal pathogenicity. The phenotypes of the three strains investigated showed further difference in light response. We found that Dactylonectria strains have an increased number of photoreceptor encoding genes and we showed sequence alterations. Altogether, the results highlight several gene clusters present in D. torresensis strains that could be linked to endophytic lifestyle, pathogenicity, plant maceration and degradation of plant tissues as well as adaptation to soil contaminated with metals and metalloids and light response.
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spelling pubmed-77120712020-12-04 Comparative Genomic Analysis of Dactylonectria torresensis Strains from Grapevine, Soil and Weed Highlights Potential Mechanisms in Pathogenicity and Endophytic Lifestyle Gramaje, David Berlanas, Carmen Martínez-Diz, María del Pilar Diaz-Losada, Emilia Antonielli, Livio Beier, Sabrina Gorfer, Markus Schmoll, Monika Compant, Stéphane J Fungi (Basel) Article The soil-borne fungus Dactylonectria torresensis is the most common causal agent of black-foot disease in Europe. However, there is a lack of understanding on how this fungus can provoke plant symptoms. In this study, we sequenced, annotated and analyzed the genomes of three isolates of D. torresensis collected from asymptomatic vine, weed and soil. Sequenced genomes were further compared to those of 27 fungal species including root and aerial pathogens, white rot degraders, indoor biodeterioration agents, saprotrophs, dark septate endophytes and mycorrhiza. Strains of D. torresensis present genomes with between 64 and 65 Mbp and with up to 18,548 predicted genes for each strain. Average Nucleotide Identity (ANI) shows that strains are different according to genome contents. Clusters of orthologous groups were compared, and clusters of genes related to necroses were particularly detected in all strains of D. torresensis (necrosis inducing peptides and proteins, and ethylene inducing peptides) as well as several genes involved in resistance against fungicides frequently used in viticulture such as copper. Interestingly, an expanded high number of genes related to carbohydrate-active enzymes were detected in each Dactylonectria strain, especially those related to glycoside hydrolases that could be involved in penetration of plant tissues or pathogenicity. An increased number of candidate genes for CAZyme classes AA9 and AA3-1 supports the ability of strains to efficiently degrade plant material. High numbers of genes of D. torresensis related to secretome and small secreted proteins were further characterized. Moreover, the presence of several gene clusters such as fujikurin-like genes was detected and were normally found in Fusarium fujikuroi, that have been linked to fungal pathogenicity. The phenotypes of the three strains investigated showed further difference in light response. We found that Dactylonectria strains have an increased number of photoreceptor encoding genes and we showed sequence alterations. Altogether, the results highlight several gene clusters present in D. torresensis strains that could be linked to endophytic lifestyle, pathogenicity, plant maceration and degradation of plant tissues as well as adaptation to soil contaminated with metals and metalloids and light response. MDPI 2020-10-29 /pmc/articles/PMC7712071/ /pubmed/33138048 http://dx.doi.org/10.3390/jof6040255 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Gramaje, David
Berlanas, Carmen
Martínez-Diz, María del Pilar
Diaz-Losada, Emilia
Antonielli, Livio
Beier, Sabrina
Gorfer, Markus
Schmoll, Monika
Compant, Stéphane
Comparative Genomic Analysis of Dactylonectria torresensis Strains from Grapevine, Soil and Weed Highlights Potential Mechanisms in Pathogenicity and Endophytic Lifestyle
title Comparative Genomic Analysis of Dactylonectria torresensis Strains from Grapevine, Soil and Weed Highlights Potential Mechanisms in Pathogenicity and Endophytic Lifestyle
title_full Comparative Genomic Analysis of Dactylonectria torresensis Strains from Grapevine, Soil and Weed Highlights Potential Mechanisms in Pathogenicity and Endophytic Lifestyle
title_fullStr Comparative Genomic Analysis of Dactylonectria torresensis Strains from Grapevine, Soil and Weed Highlights Potential Mechanisms in Pathogenicity and Endophytic Lifestyle
title_full_unstemmed Comparative Genomic Analysis of Dactylonectria torresensis Strains from Grapevine, Soil and Weed Highlights Potential Mechanisms in Pathogenicity and Endophytic Lifestyle
title_short Comparative Genomic Analysis of Dactylonectria torresensis Strains from Grapevine, Soil and Weed Highlights Potential Mechanisms in Pathogenicity and Endophytic Lifestyle
title_sort comparative genomic analysis of dactylonectria torresensis strains from grapevine, soil and weed highlights potential mechanisms in pathogenicity and endophytic lifestyle
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7712071/
https://www.ncbi.nlm.nih.gov/pubmed/33138048
http://dx.doi.org/10.3390/jof6040255
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