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Characterization of Streptomyces spp. isolated from the rhizosphere of oil palm and evaluation of their ability to suppress basal stem rot disease in oil palm seedlings when applied as powder formulations in a glasshouse trial

Shariffah-Muzaimah SA, Idris AS, Madihah AZ, Dzolkhifli O, Kamaruzzaman S, Maizatul-Suriza M

World J Microbiol Biotechnol, 2017 Dec 18;34(1):15.
PMID: 29256103 DOI: 10.1007/s11274-017-2396-1

Ganoderma boninense, the main causal agent of oil palm (Elaeis guineensis) basal stem rot (BSR), severely reduces oil palm yields around the world. To reduce reliance on fungicide applications to control BSR, we are investigating the efficacy of alternative control methods, such as the application of biological control agents. In this study, we used four Streptomyces-like actinomycetes (isolates AGA43, AGA48, AGA347 and AGA506) that had been isolated from the oil palm rhizosphere and screened for antagonism towards G. boninense in a previous study. The aim of this study was to characterize these four isolates and then to assess their ability to suppress BSR in oil palm seedlings when applied individually to the soil in a vermiculite powder formulation. Analysis of partial 16S rRNA gene sequences (512 bp) revealed that the isolates exhibited a very high level of sequence similarity (> 98%) with GenBank reference sequences. Isolates AGA347 and AGA506 showed 99% similarity with Streptomyces hygroscopicus subsp. hygroscopicus and Streptomyces ahygroscopicus, respectively. Isolates AGA43 and AGA48 also belonged to the Streptomyces genus. The most effective formulation, AGA347, reduced BSR in seedlings by 73.1%. Formulations using the known antifungal producer Streptomyces noursei, AGA043, AGA048 or AGA506 reduced BSR by 47.4, 30.1, 54.8 and 44.1%, respectively. This glasshouse trial indicates that these Streptomyces spp. show promise as potential biological control agents against Ganoderma in oil palm. Further investigations are needed to determine the mechanism of antagonism and to increase the shelf life of Streptomyces formulations.

Matched MeSH terms: Ganoderma/pathogenicity
An in vitro study of the antifungal activity of Trichoderma virens 7b and a profile of its non-polar antifungal components released against Ganoderma boninense

Angel LP, Yusof MT, Ismail IS, Ping BT, Mohamed Azni IN, Kamarudin NH, et al.

J Microbiol, 2016 Nov;54(11):732-744.
PMID: 27796927

Ganoderma boninense is the causal agent of a devastating disease affecting oil palm in Southeast Asian countries. Basal stem rot (BSR) disease slowly rots the base of palms, which radically reduces productive lifespan of this lucrative crop. Previous reports have indicated the successful use of Trichoderma as biological control agent (BCA) against G. boninense and isolate T. virens 7b was selected based on its initial screening. This study attempts to decipher the mechanisms responsible for the inhibition of G. boninense by identifying and characterizing the chemical compounds as well as the physical mechanisms by T. virens 7b. Hexane extract of the isolate gave 62.60% ± 6.41 inhibition against G. boninense and observation under scanning electron microscope (SEM) detected severe mycelial deformation of the pathogen at the region of inhibition. Similar mycelia deformation of G. boninense was observed with a fungicide treatment, Benlate(®) indicating comparable fungicidal effect by T. virens 7b. Fraction 4 and 5 of hexane active fractions through preparative thin layer chromatography (P-TLC) was identified giving the best inhibition of the pathogen. These fractions comprised of ketones, alcohols, aldehydes, lactones, sesquiterpenes, monoterpenes, sulphides, and free fatty acids profiled through gas chromatography mass spectrometry detector (GC/MSD). A novel antifungal compound discovery of phenylethyl alcohol (PEA) by T. virens 7b is reported through this study. T. virens 7b also proved to be an active siderophore producer through chrome azurol S (CAS) agar assay. The study demonstrated the possible mechanisms involved and responsible in the successful inhibition of G. boninense.

Matched MeSH terms: Ganoderma/drug effects*
Fulltext Growth modulation and metabolic responses of Ganoderma boninense to salicylic acid stress

Ong CE, Ahmad R, Goh YK, Azizan KA, Baharum SN, Goh KJ

PLoS One, 2021;16(12):e0262029.
PMID: 34972183 DOI: 10.1371/journal.pone.0262029

Various phenolic compounds have been screened against Ganoderma boninense, the fungal pathogen causing basal stem rot in oil palms. In this study, we focused on the effects of salicylic acid (SA) on the growth of three G. boninense isolates with different levels of aggressiveness. In addition, study on untargeted metabolite profiling was conducted to investigate the metabolomic responses of G. boninense towards salicylic acid. The inhibitory effects of salicylic acid were both concentration- (P < 0.001) and isolate-dependent (P < 0.001). Also, growth-promoting effect was observed in one of the isolates at low concentrations of salicylic acid where it could have been utilized by G. boninense as a source of carbon and energy. Besides, adaptation towards salicylic acid treatment was evident in this study for all isolates, particularly at high concentrations. In other words, inhibitory effect of salicylic acid treatment on the fungal growth declined over time. In terms of metabolomics response to salicylic acid treatment, G. boninense produced several metabolites such as coumarin and azatyrosine, which suggests that salicylic acid modulates the developmental switch in G. boninense towards the defense mode for its survival. Furthermore, the liquid chromatography time-of-flight mass spectrometry (LC-TOF-MS) analysis showed that the growth of G. boninense on potato dextrose agar involved at least four metabolic pathways: amino acid metabolism, lipid pathway, tryptophan pathway and phenylalanine pathway. Overall, there were 17 metabolites that contributed to treatment separation, each with P<0.005. The release of several antimicrobial metabolites such as eudistomin I may enhance G. boninense's competitiveness against other microorganisms during colonisation. Our findings demonstrated the metabolic versatility of G. boninense towards changes in carbon sources and stress factors. G. boninense was shown to be capable of responding to salicylic acid treatment by switching its developmental stage.

Matched MeSH terms: Ganoderma/metabolism*
Differential expression of oil palm pathology genes during interactions with Ganoderma boninense and Trichoderma harzianum

Alizadeh F, Abdullah SN, Khodavandi A, Abdullah F, Yusuf UK, Chong PP

J Plant Physiol, 2011 Jul 01;168(10):1106-13.
PMID: 21333381 DOI: 10.1016/j.jplph.2010.12.007

The expression profiles of Δ9 stearoyl-acyl carrier protein desaturase (SAD1 and SAD2) and type 3 metallothionein (MT3-A and MT3-B) were investigated in seedlings of oil palm (Elaeis guineensis) artificially inoculated with the pathogenic fungus Ganoderma boninense and the symbiotic fungus Trichoderma harzianum. Expression of SAD1 and MT3-A in roots and SAD2 in leaves were significantly up-regulated in G. boninense inoculated seedlings at 21 d after treatment when physical symptoms had not yet appeared and thereafter decreased to basal levels when symptoms became visible. Our finding demonstrated that the SAD1 expression in leaves was significantly down-regulated to negligible levels at 42 and 63 d after treatment. The transcripts of MT3 genes were synthesized in G. boninense inoculated leaves at 42 d after treatment, and the analyses did not show detectable expression of these genes before 42 d after treatment. In T. harzianum inoculated seedlings, the expression levels of SAD1 and SAD2 increased gradually and were stronger in roots than leaves, while for MT3-A and MT3-B, the expression levels were induced in leaves at 3d after treatment and subsequently maintained at same levels until 63d after treatment. The MT3-A expression was significantly up-regulated in roots at 3d after treatment and thereafter were maintained at this level. Both SAD and MT3 expression were maintained at maximum levels or at levels higher than basal. This study demonstrates that oil palm was able to distinguish between pathogenic and symbiotic fungal interactions, thus resulting in different transcriptional activation profiles of SAD and MT3 genes. Increases in expression levels of SAD and MT3 would lead to enhanced resistance against G. boninense and down-regulation of genes confer potential for invasive growth of the pathogen. Differences in expression profiles of SAD and MT3 relate to plant resistance mechanisms while supporting growth enhancing effects of symbiotic T. harzianum.

Matched MeSH terms: Ganoderma/growth & development*
Cloning of nitric oxide associated 1 (NOA1) transcript from oil palm (Elaeis guineensis) and its expression during Ganoderma infection

Kwan YM, Meon S, Ho CL, Wong MY

J Plant Physiol, 2015 Feb 01;174:131-6.
PMID: 25462975 DOI: 10.1016/j.jplph.2014.10.003

Nitric oxide associated 1 (NOA1) protein is implicated in plant disease resistance and nitric oxide (NO) biosynthesis. A full-length cDNA encoding of NOA1 protein from oil palm (Elaeis guineensis) was isolated and designated as EgNOA1. Sequence analysis suggested that EgNOA1 was a circular permutated GTPase with high similarity to the bacterial YqeH protein of the YawG/YlqF family. The gene expression of EgNOA1 and NO production in oil palm root tissues treated with Ganoderma boninense, the causal agent of basal stem rot (BSR) disease were profiled to investigate the involvement of EgNOA1 during fungal infection and association with NO biosynthesis. Real-time PCR (qPCR) analysis revealed that the transcript abundance of EgNOA1 in root tissues was increased by G. boninense treatment. NO burst in Ganoderma-treated root tissue was detected using Griess reagent, in advance of the up-regulation of the EgNOA1 transcript. This indicates that NO production was independent of EgNOA1. However, the induced expression of EgNOA1 in Ganoderma-treated root tissues implies that it might be involved in plant defense responses against pathogen infection.

Matched MeSH terms: Ganoderma/physiology*
Sequence analysis and gene expression of putative exo- and endo-glucanases from oil palm (Elaeis guineensis) during fungal infection

Yeoh KA, Othman A, Meon S, Abdullah F, Ho CL

J Plant Physiol, 2012 Oct 15;169(15):1565-70.
PMID: 22854183 DOI: 10.1016/j.jplph.2012.07.006

Glucanases are enzymes that hydrolyze a variety β-d-glucosidic linkages. Plant β-1,3-glucanases are able to degrade fungal cell walls; and promote the release of cell-wall derived fungal elicitors. In this study, three full-length cDNA sequences encoding oil palm (Elaeis guineensis) glucanases were analyzed. Sequence analyses of the cDNA sequences suggested that EgGlc1-1 is a putative β-d-glucan exohydolase belonging to glycosyl hydrolase (GH) family 3 while EgGlc5-1 and EgGlc5-2 are putative glucan endo-1,3-β-glucosidases belonging to GH family 17. The transcript abundance of these genes in the roots and leaves of oil palm seedlings treated with Ganoderma boninense and Trichoderma harzianum was profiled to investigate the involvement of these glucanases in oil palm during fungal infection. The gene expression of EgGlc1-1 in the root of oil palm seedlings was increased by T. harzianum but suppressed by G. boninense; while the gene expression of both EgGlc5-1 and EgGlc5-2 in the roots of oil palm seedlings was suppressed by G. boninense or/and T. harzianum.

Matched MeSH terms: Ganoderma/pathogenicity*
Fulltext Transciptome profiling at early infection of Elaeis guineensis by Ganoderma boninense provides novel insights on fungal transition from biotrophic to necrotrophic phase

Bahari MNA, Sakeh NM, Abdullah SNA, Ramli RR, Kadkhodaei S

BMC Plant Biol, 2018 Dec 29;18(1):377.
PMID: 30594134 DOI: 10.1186/s12870-018-1594-9

BACKGROUND: Basal stem rot (BSR) caused by hemibiotroph Ganoderma boninense is a devastating disease resulting in a major loss to the oil palm industry. Since there is no physical symptom in oil palm at the early stage of G. boninense infection, characterisation of molecular defense responses in oil palm during early interaction with the fungus is of the utmost importance. Oil palm (Elaeis guineensis) seedlings were artificially infected with G. boninense inoculums and root samples were obtained following a time-course of 0, 3, 7, and 11 days-post-inoculation (d.p.i) for RNA sequencing (RNA-seq) and identification of differentially expressed genes (DEGs).
RESULTS: The host counter-attack was evidenced based on fungal hyphae and Ganoderma DNA observed at 3 d.p.i which became significantly reduced at 7 and 11 d.p.i. DEGs revealed upregulation of multifaceted defense related genes such as PR-protein (EgPR-1), protease inhibitor (EgBGIA), PRR protein (EgLYK3) chitinase (EgCht) and expansin (EgEXPB18) at 3 d.p.i and 7 d.p.i which dropped at 11 d.p.i. Later stage involved highly expressed transcription factors EgERF113 and EgMYC2 as potential regulators of necrotrophic defense at 11 d.p.i. The reactive oxygen species (ROS) elicitor: peroxidase (EgPER) and NADPH oxidase (EgRBOH) were upregulated and maintained throughout the treatment period. Growth and nutrient distribution were probably compromised through suppression of auxin signalling and iron uptake genes.
CONCLUSIONS: Based on the analysis of oil palm gene expression, it was deduced that the biotrophic phase of Ganoderma had possibly occurred at the early phase (3 until 7 d.p.i) before being challenged by the fungus via switching its lifestyle into the necrotrophic phase at later stage (11 d.p.i) and finally succumbed the host. Together, the findings suggest the dynamic defense process in oil palm and potential candidates that can serve as phase-specific biomarkers at the early stages of oil palm-G. boninense interaction.

Matched MeSH terms: Ganoderma
Dissipation of the fungicide hexaconazole in oil palm plantation

Maznah Z, Halimah M, Ismail S, Idris AS

Environ Sci Pollut Res Int, 2015 Dec;22(24):19648-57.
PMID: 26276276 DOI: 10.1007/s11356-015-5178-z

Hexaconazole is a potential fungicide to be used in the oil palm plantation for controlling the basal stem root (BSR) disease caused by Ganoderma boninense. Therefore, the dissipation rate of hexaconazole in an oil palm agroecosystem under field conditions was studied. Two experimental plots were treated with hexaconazole at the recommended dosage of 4.5 g a.i. palm(-1) (active ingredient) and at double the recommended dosage (9.0 g a.i. palm(-1)), whilst one plot was untreated as control. The residue of hexaconazole was detected in soil samples in the range of 2.74 to 0.78 and 7.13 to 1.66 mg kg(-1) at the recommended and double recommended dosage plots, respectively. An initial relatively rapid dissipation rate of hexaconazole residues occurred but reduced with time. The dissipation of hexaconazole in soil was described using first-order kinetics with the value of coefficient regression (r (2) > 0.8). The results indicated that hexaconazole has moderate persistence in the soil and the half-life was found to be 69.3 and 86.6 days in the recommended and double recommended dosage plot, respectively. The results obtained highlight that downward movement of hexaconazole was led by preferential flow as shown in image analysis. It can be concluded that varying soil conditions, environmental factors, and pesticide chemical properties of hexaconazole has a significant impact on dissipation of hexaconazole in soil under humid conditions.

Matched MeSH terms: Ganoderma
Morphological and transcript changes in the biosynthesis of lignin in oil palm (Elaeis guineensis) during Ganoderma boninense infections in vitro

Goh KM, Dickinson M, Supramaniam CV

Physiol Plant, 2018 Mar;162(3):274-289.
PMID: 28940509 DOI: 10.1111/ppl.12645

Lignification of the plant cell wall could serve as the first line of defense against pathogen attack, but the molecular mechanisms of virulence and disease between oil palm and Ganoderma boninense are poorly understood. This study presents the biochemical, histochemical, enzymology and gene expression evidences of enhanced lignin biosynthesis in young oil palm as a response to G. boninense (GBLS strain). Comparative studies with control (T1), wounded (T2) and infected (T3) oil palm plantlets showed significant accumulation of total lignin content and monolignol derivatives (syringaldehyde and vanillin). These derivatives were deposited on the epidermal cell wall of infected plants. Moreover, substantial differences were detected in the activities of enzyme and relative expressions of genes encoding phenylalanine ammonia lyase (EC 4.3.1.24), cinnamate 4-hydroxylase (EC 1.14.13.11), caffeic acid O-methyltransferase (EC 2.1.1.68) and cinnamyl alcohol dehydrogenase (CAD, EC 1.1.1.195). These enzymes are key intermediates dedicated to the biosynthesis of lignin monomers, the guaicyl (G), syringyl (S) and ρ-hydroxyphenyl (H) subunits. Results confirmed an early, biphasic and transient positive induction of all gene intermediates, except for CAD enzyme activities. These differences were visualized by anatomical and metabolic changes in the profile of lignin in the oil palm plantlets such as low G lignin, indicating a potential mechanism for enhanced susceptibility toward G. boninense infection.

Matched MeSH terms: Ganoderma/physiology
New advances and potentials of fungal immunomodulatory proteins for therapeutic purposes

Ejike UC, Chan CJ, Okechukwu PN, Lim RLH

Crit Rev Biotechnol, 2020 Dec;40(8):1172-1190.
PMID: 32854547 DOI: 10.1080/07388551.2020.1808581

Fungal immunomodulatory proteins (FIPs) are fascinating small and heat-stable bioactive proteins in a distinct protein family due to similarities in their structures and sequences. They are found in fungi, including the fruiting bodies producing fungi comprised of culinary and medicinal mushrooms. Structurally, most FIPs exist as homodimers; each subunit consisting of an N-terminal α-helix dimerization and a C-terminal fibronectin III domain. Increasing numbers of identified FIPs from either different or same fungal species clearly indicates the growing research interests into its medicinal properties which include immunomodulatory, anti-inflammation, anti-allergy, and anticancer. Most FIPs increased IFN-γ production in peripheral blood mononuclear cells, potentially exerting immunomodulatory and anti-inflammatory effects by inhibiting overproduction of T helper-2 (Th2) cytokines common in an allergy reaction. Recently, FIP from Ganoderma microsporum (FIP-gmi) was shown to promote neurite outgrowth for potential therapeutic applications in neuro-disorders. This review discussed FIPs' structural and protein characteristics, their recombinant protein production for functional studies, and the recent advances in their development and applications as pharmaceutics and functional foods.

Matched MeSH terms: Ganoderma

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