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 (C...

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Main Authors: Ahmad Bazli Ramzi, Muhammad Lutfi Che Me, Ummul Syafiqah Ruslan, Syarul Nataqain Baharum, Nor Azlan Nor Muhammad
Format: Article
Language:English
Published: PeerJ Inc. 2019-12-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/8065.pdf
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spelling doaj-6aa2ce2da34a4ee7ab94ac56f460c7ea2020-11-25T01:56:24ZengPeerJ Inc.PeerJ2167-83592019-12-017e806510.7717/peerj.8065Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysisAhmad Bazli Ramzi0Muhammad Lutfi Che Me1Ummul Syafiqah Ruslan2Syarul Nataqain Baharum3Nor Azlan Nor Muhammad4Institute of Systems Biology, Universiti Kebangsaan Malaysia, Bangi, Selangor, MalaysiaInstitute of Systems Biology, Universiti Kebangsaan Malaysia, Bangi, Selangor, MalaysiaInstitute of Systems Biology, Universiti Kebangsaan Malaysia, Bangi, Selangor, MalaysiaInstitute of Systems Biology, Universiti Kebangsaan Malaysia, Bangi, Selangor, MalaysiaInstitute of Systems Biology, Universiti Kebangsaan Malaysia, Bangi, Selangor, MalaysiaBackground 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.https://peerj.com/articles/8065.pdfGanoderma boninenseCell wall degrading enzymeComparative genomicsOil palm pathogenIn silico analysis
collection DOAJ
language English
format Article
sources DOAJ
author Ahmad Bazli Ramzi
Muhammad Lutfi Che Me
Ummul Syafiqah Ruslan
Syarul Nataqain Baharum
Nor Azlan Nor Muhammad
spellingShingle Ahmad Bazli Ramzi
Muhammad Lutfi Che Me
Ummul Syafiqah Ruslan
Syarul Nataqain Baharum
Nor Azlan Nor Muhammad
Insight into plant cell wall degradation and pathogenesis of Ganoderma boninense via comparative genome analysis
PeerJ
Ganoderma boninense
Cell wall degrading enzyme
Comparative genomics
Oil palm pathogen
In silico analysis
author_facet Ahmad Bazli Ramzi
Muhammad Lutfi Che Me
Ummul Syafiqah Ruslan
Syarul Nataqain Baharum
Nor Azlan Nor Muhammad
author_sort Ahmad Bazli Ramzi
title 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_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_sort insight into plant cell wall degradation and pathogenesis of ganoderma boninense via comparative genome analysis
publisher PeerJ Inc.
series PeerJ
issn 2167-8359
publishDate 2019-12-01
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.
topic Ganoderma boninense
Cell wall degrading enzyme
Comparative genomics
Oil palm pathogen
In silico analysis
url https://peerj.com/articles/8065.pdf
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