Transciptome profiling at early infection of Elaeis guineensis by Ganoderma boninense provides novel insights on fungal transition from biotrophic to necrotrophic phase

Bahari, Mohammad Nazri Abdul; Sakeh, Nurshafika Mohd; Abdullah, Siti Nor Akmar; Ramli, Redzyque Ramza; Kadkhodaei, Saeid

doi:10.1186/s12870-018-1594-9

Cited by 44 publications

(64 citation statements)

References 104 publications

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“…Intriguingly, oil palm EgJUB1 was found to co-express with two SA-dependent genes of EgTGA1 and EgNPR1. Our results were more in line with the SAdependent master regulator of NPR1, a cofactor of TGA1 reported by [55], which induces Pathogenesis related (PR) genes [56] during biotrophic phase.…”

Section: Discussionsupporting

confidence: 90%

EgJUB1 and EgERF113 transcription factors as master regulators of defense response in Elaeis guineensis against the hemibiotrophic Ganoderma boninense

Sakeh

Abdullah

Bahari

et al. 2020

Preprint

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Background Hemibiotrophic pathogen such as the fungal pathogen Ganoderma boninense that is destructive to oil palm, manipulates host defense mechanism by strategically switching from biotrophic to necrotrophic phase. Our previous study revealed two distinguishable expression profiles of oil palm genes that formed the basis in deducing biotrophic phase at early interaction which switched to necrotrophic phase at later stage of infection. Results The present report is a continuing study from our previous published transcriptomic profiling of oil palm seedlings against G. boninense. We focused on identifying differentially expressed genes (DEGs) encoding transcription factors (TFs) from the same RNA-seq data resulting in 106 upregulated and 108 downregulated TFs being identified. DEGs involved in four established defense-related pathways are presented which are responsible in cell wall modification, reactive oxygen species (ROS)-mediated signaling, programmed cell death (PCD) and plant innate immunity. We discovered upregulation of JUNGBRUNNEN 1 (EgJUB1) during fungal biotrophic phase while Ethylene Responsive Factor 113 (EgERF113) demonstrated prominent upregulation when the palm switches to defense against necrotrophic phase. EgJUB1 was shown to have binding activity to a 19 bp palindromic SNBE1 element, WNNYBTNNNNNNNAMGNHW found in the promoter region of co-expressing EgHSFC-2b. Further in silico analysis of promoter regions revealed co-expression of EgJUB1 with TFs containing SNBE1 element with single nucleotide change at either the 5th or 18th position. Meanwhile, EgERF113 binds to both GCC and DRE/CRT elements promoting plasticity in upregulating the downstream defense-related genes. Both TFs were proven to be nuclear localized based on subcellular localization experiment using onion epidermal cells. Conclusion Our findings demonstrated unprecedented transcriptional reprogramming of specific TFs potentially to enable regulation of specific set of genes during different infection phases of this hemibiotrophic fungal pathogen. The results propose EgJUB1 and EgERF113 as key TFs in orchestrating the defense mechanisms during biotrophic and during the subsequent transition to necrotrophic phase, respectively. Identification of these phase-specific oil palm TFs is important in designing strategies to tackle or attenuate the progress of infection.

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Section: Discussionsupporting

confidence: 90%

EgJUB1 and EgERF113 transcription factors as master regulators of defense response in Elaeis guineensis against the hemibiotrophic Ganoderma boninense

Sakeh

Abdullah

Bahari

et al. 2020

Preprint

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“…Higher expression of cell wall degrading enzymes (GH, PL, GT) were observed in necrotrophic Leptosphaeria biglobosa as compared to hemibiotrophic counterpart, L. maculans which accumulated higher CBM during early stage of plant infection (Lowe et al, 2014). Similar CAZymes interplays were suggested in the early infection of G. boninense that aimed at overcoming the oil palm host defense response mechanisms including hypersensitive response (HR) leading to the switch from biotrophic stage to the more aggressive necrotrophic attacks culminating in host cell death and successful invasion (Bahari et al, 2018). A closer look of the CAZymes in the selected pathogenic fungi would therefore enable genome-wide profiling of carbohydrate-active enzymes that are distinct and correlated with the fungal mode of infection.…”

Section: Resultsmentioning

confidence: 76%

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

Ramzi

Ruslan

et al. 2019

PeerJ

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BackgroundG. 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.MethodsIn 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.ResultsG. 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.DiscussionThis 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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“…Half of the basal stem would have been destroyed by the fungus, compromising intake of water and nutrients, before the first symptom is observed [ 2 , 3 ]. The fungus, G. boninense is recognized as a hemibiotroph, which established an intermediate lifestyle of biotroph before switching to necrotroph [ 4 , 5 ]. The biotrophic phase involves colonization of host plant tissues and extraction of nutrients for survival by the pathogen while keeping the host cells intact [ 3 ].…”

Section: Introductionmentioning

confidence: 99%

EgJUB1 and EgERF113 transcription factors as potential master regulators of defense response in Elaeis guineensis against the hemibiotrophic Ganoderma boninense

et al. 2021

Self Cite

View full text Add to dashboard Cite

Background Hemibiotrophic pathogen such as the fungal pathogen Ganoderma boninense that is destructive to oil palm, manipulates host defense mechanism by strategically switching from biotrophic to necrotrophic phase. Our previous study revealed two distinguishable expression profiles of oil palm genes that formed the basis in deducing biotrophic phase at early interaction which switched to necrotrophic phase at a later stage of infection. Results The present report is a continuing study from our previous published transcriptomic profiling of oil palm seedlings against G. boninense. We focused on identifying differentially expressed genes (DEGs) encoding transcription factors (TFs) from the same RNA-seq data; resulting in 106 upregulated and 108 downregulated TFs being identified. The DEGs are involved in four established defense-related pathways responsible for cell wall modification, reactive oxygen species (ROS)-mediated signaling, programmed cell death (PCD) and plant innate immunity. We discovered upregulation of JUNGBRUNNEN 1 (EgJUB1) during the fungal biotrophic phase while Ethylene Responsive Factor 113 (EgERF113) demonstrated prominent upregulation when the palm switches to defense against necrotrophic phase. EgJUB1 was shown to have a binding activity to a 19 bp palindromic SNBE1 element, WNNYBTNNNNNNNAMGNHW found in the promoter region of co-expressing EgHSFC-2b. Further in silico analysis of promoter regions revealed co-expression of EgJUB1 with TFs containing SNBE1 element with single nucleotide change at either the 5th or 18th position. Meanwhile, EgERF113 binds to both GCC and DRE/CRT elements promoting plasticity in upregulating the downstream defense-related genes. Both TFs were proven to be nuclear-localized based on subcellular localization experiment using onion epidermal cells. Conclusion Our findings demonstrated unprecedented transcriptional reprogramming of specific TFs potentially to enable regulation of a specific set of genes during different infection phases of this hemibiotrophic fungal pathogen. The results propose the intricacy of oil palm defense response in orchestrating EgJUB1 during biotrophic and EgERF113 during the subsequent transition to the necrotrophic phase. Binding of EgJUB1 to SNBE motif instead of NACBS while EgERF113 to GCC-box and DRE/CRT motifs is unconventional and not normally associated with pathogen infection. Identification of these phase-specific oil palm TFs is important in designing strategies to tackle or attenuate the progress of infection.

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Transciptome profiling at early infection of Elaeis guineensis by Ganoderma boninense provides novel insights on fungal transition from biotrophic to necrotrophic phase

Cited by 44 publications

References 104 publications

EgJUB1 and EgERF113 transcription factors as master regulators of defense response in Elaeis guineensis against the hemibiotrophic Ganoderma boninense

EgJUB1 and EgERF113 transcription factors as master regulators of defense response in Elaeis guineensis against the hemibiotrophic Ganoderma boninense

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

EgJUB1 and EgERF113 transcription factors as potential master regulators of defense response in Elaeis guineensis against the hemibiotrophic Ganoderma boninense

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