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Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis

BACKGROUND: G. boninense is a hemibiotrophic fungus that infects oil palms (Elaeis guineensis Jacq.) causing basal stem rot (BSR) disease and consequent massive economic losses to the oil palm industry. The pathogenicity of this white-rot fungus has been associated with cell wall degrading enzymes (...

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Autores principales: Ramzi, Ahmad Bazli, Che Me, Muhammad Lutfi, Ruslan, Ummul Syafiqah, Baharum, Syarul Nataqain, Nor Muhammad, Nor Azlan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6927665/
https://www.ncbi.nlm.nih.gov/pubmed/31879570
http://dx.doi.org/10.7717/peerj.8065
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author Ramzi, Ahmad Bazli
Che Me, Muhammad Lutfi
Ruslan, Ummul Syafiqah
Baharum, Syarul Nataqain
Nor Muhammad, Nor Azlan
author_facet Ramzi, Ahmad Bazli
Che Me, Muhammad Lutfi
Ruslan, Ummul Syafiqah
Baharum, Syarul Nataqain
Nor Muhammad, Nor Azlan
author_sort Ramzi, Ahmad Bazli
collection PubMed
description BACKGROUND: G. boninense is a hemibiotrophic fungus that infects oil palms (Elaeis guineensis Jacq.) causing basal stem rot (BSR) disease and consequent massive economic losses to the oil palm industry. The pathogenicity of this white-rot fungus has been associated with cell wall degrading enzymes (CWDEs) released during saprophytic and necrotrophic stage of infection of the oil palm host. However, there is a lack of information available on the essentiality of CWDEs in wood-decaying process and pathogenesis of this oil palm pathogen especially at molecular and genome levels. METHODS: In this study, comparative genome analysis was carried out using the G. boninense NJ3 genome to identify and characterize carbohydrate-active enzyme (CAZymes) including CWDE in the fungal genome. Augustus pipeline was employed for gene identification in G. boninense NJ3 and the produced protein sequences were analyzed via dbCAN pipeline and PhiBase 4.5 database annotation for CAZymes and plant-host interaction (PHI) gene analysis, respectively. Comparison of CAZymes from G. boninense NJ3 was made against G. lucidum, a well-studied model Ganoderma sp. and five selected pathogenic fungi for CAZymes characterization. Functional annotation of PHI genes was carried out using Web Gene Ontology Annotation Plot (WEGO) and was used for selecting candidate PHI genes related to cell wall degradation of G. boninense NJ3. RESULTS: G. boninense was enriched with CAZymes and CWDEs in a similar fashion to G. lucidum that corroborate with the lignocellulolytic abilities of both closely-related fungal strains. The role of polysaccharide and cell wall degrading enzymes in the hemibiotrophic mode of infection of G. boninense was investigated by analyzing the fungal CAZymes with necrotrophic Armillaria solidipes, A. mellea, biotrophic Ustilago maydis, Melampsora larici-populina and hemibiotrophic Moniliophthora perniciosa. Profiles of the selected pathogenic fungi demonstrated that necrotizing pathogens including G. boninense NJ3 exhibited an extensive set of CAZymes as compared to the more CAZymes-limited biotrophic pathogens. Following PHI analysis, several candidate genes including polygalacturonase, endo β-1,3-xylanase, β-glucanase and laccase were identified as potential CWDEs that contribute to the plant host interaction and pathogenesis. DISCUSSION: This study employed bioinformatics tools for providing a greater understanding of the biological mechanisms underlying the production of CAZymes in G. boninense NJ3. Identification and profiling of the fungal polysaccharide- and lignocellulosic-degrading enzymes would further facilitate in elucidating the infection mechanisms through the production of CWDEs by G. boninense. Identification of CAZymes and CWDE-related PHI genes in G. boninense would serve as the basis for functional studies of genes associated with the fungal virulence and pathogenicity using systems biology and genetic engineering approaches.
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spelling pubmed-69276652019-12-26 Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis Ramzi, Ahmad Bazli Che Me, Muhammad Lutfi Ruslan, Ummul Syafiqah Baharum, Syarul Nataqain Nor Muhammad, Nor Azlan PeerJ Agricultural Science BACKGROUND: G. boninense is a hemibiotrophic fungus that infects oil palms (Elaeis guineensis Jacq.) causing basal stem rot (BSR) disease and consequent massive economic losses to the oil palm industry. The pathogenicity of this white-rot fungus has been associated with cell wall degrading enzymes (CWDEs) released during saprophytic and necrotrophic stage of infection of the oil palm host. However, there is a lack of information available on the essentiality of CWDEs in wood-decaying process and pathogenesis of this oil palm pathogen especially at molecular and genome levels. METHODS: In this study, comparative genome analysis was carried out using the G. boninense NJ3 genome to identify and characterize carbohydrate-active enzyme (CAZymes) including CWDE in the fungal genome. Augustus pipeline was employed for gene identification in G. boninense NJ3 and the produced protein sequences were analyzed via dbCAN pipeline and PhiBase 4.5 database annotation for CAZymes and plant-host interaction (PHI) gene analysis, respectively. Comparison of CAZymes from G. boninense NJ3 was made against G. lucidum, a well-studied model Ganoderma sp. and five selected pathogenic fungi for CAZymes characterization. Functional annotation of PHI genes was carried out using Web Gene Ontology Annotation Plot (WEGO) and was used for selecting candidate PHI genes related to cell wall degradation of G. boninense NJ3. RESULTS: G. boninense was enriched with CAZymes and CWDEs in a similar fashion to G. lucidum that corroborate with the lignocellulolytic abilities of both closely-related fungal strains. The role of polysaccharide and cell wall degrading enzymes in the hemibiotrophic mode of infection of G. boninense was investigated by analyzing the fungal CAZymes with necrotrophic Armillaria solidipes, A. mellea, biotrophic Ustilago maydis, Melampsora larici-populina and hemibiotrophic Moniliophthora perniciosa. Profiles of the selected pathogenic fungi demonstrated that necrotizing pathogens including G. boninense NJ3 exhibited an extensive set of CAZymes as compared to the more CAZymes-limited biotrophic pathogens. Following PHI analysis, several candidate genes including polygalacturonase, endo β-1,3-xylanase, β-glucanase and laccase were identified as potential CWDEs that contribute to the plant host interaction and pathogenesis. DISCUSSION: This study employed bioinformatics tools for providing a greater understanding of the biological mechanisms underlying the production of CAZymes in G. boninense NJ3. Identification and profiling of the fungal polysaccharide- and lignocellulosic-degrading enzymes would further facilitate in elucidating the infection mechanisms through the production of CWDEs by G. boninense. Identification of CAZymes and CWDE-related PHI genes in G. boninense would serve as the basis for functional studies of genes associated with the fungal virulence and pathogenicity using systems biology and genetic engineering approaches. PeerJ Inc. 2019-12-18 /pmc/articles/PMC6927665/ /pubmed/31879570 http://dx.doi.org/10.7717/peerj.8065 Text en ©2019 Ramzi et al. https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Agricultural Science
Ramzi, Ahmad Bazli
Che Me, Muhammad Lutfi
Ruslan, Ummul Syafiqah
Baharum, Syarul Nataqain
Nor Muhammad, Nor Azlan
Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis
title Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis
title_full Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis
title_fullStr Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis
title_full_unstemmed Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis
title_short Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis
title_sort insight into plant cell wall degradation and pathogenesis of ganoderma boninense via comparative genome analysis
topic Agricultural Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6927665/
https://www.ncbi.nlm.nih.gov/pubmed/31879570
http://dx.doi.org/10.7717/peerj.8065
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