Pathogen Interaction: Towards Understanding and...

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ABSTRACT

Ganoderma boninense has been identified as a ‘white rot’ pathogen that causes basal stem rot (BSR) disease in oil palm. In spite of numerous reports on the severity of BSR and its effect on the oil palm industry, no single treatment has effectively tackled the problem. Most control measures have to date continued to give variable and inconsistent results. The current major drawback in combating BSR in oil palm is the lack of sufficient information on the defining mode of action of the fungus and its relationship with oil palm. To gain a deeper insight into the Ganoderma-oil palm interaction, we review here some of the current knowledge in both the physical infection process and the molecular consequences, with reference to general interactions of other pathogenic species towards their host plants.

ABSTRAK

Ganoderma boninense telah dikenal pasti sebagai patogen ‘reput putih’ yang menyebabkan penyakit reput pangkal batang (RPB) sawit. Walaupun banyak laporan mengenai kemudaratan RPB dan kesannya pada industri sawit, namun tiada rawatan tunggal yang berkesan boleh menangani masalah tersebut. Kebanyakan langkah kawalan yang telah dilaksanakan kini tidak memberi keputusan yang konsisten. Kelemahan utama dalam memerangi RPB ialah kekurangan maklumat lengkap mengenai proses interaksi antara kulat patogen tersebut dan sawit. Untuk mendapatkan gambaran yang lebih menyeluruh, artikel ini mengupas secara terperinci proses fizikal dan molekular yang berlaku semasa infeksi, disulam dengan rujukan terhadap interaksi spesis patogenik yang lain.

Pathogen Interaction: Towards Understanding and Controlling Basal Stem Rot in Oil Palm

Noor Azmi Shaharuddin* and Mohamad Arif Abd Manaf**

Keywords: basal stem rot, pathogen-host interaction, Ganoderma boninense.

* Faculty of Biotechnology & Biomolecular Sciences, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia.

** Malaysian Palm Oil Board, P. O. Box 10620, 50720 Kuala Lumpur, Malaysia.

AN OVERVIEW OF PLANT DEFENSE RESPONSES

The battle between host and pathogen has constantly been the interest of scientific research since the dawn of civilization. Pathogens, having the advantage of larger numbers, have always seemed to end up ahead. This is partly due to the fact that pathogenic microorganisms whose generation time is measured in minutes rather than years, can adapt much faster than their hosts. Unlike animals, plants are immobile and therefore seem passive in the face of an attack by their adversaries. However, given the diversity and persistency of the attacks, plants have through evolution improved their combat strategy, which includes the development of highly complicated defense systems. It is, therefore, not surprising when a particular plant is resistant to most of the attacking pathogens.

Generally, to resist pathogen invasion, plants manifest passive and active layers of defense which take the form of physical and chemical barriers. In the passive form of defense, the outer structures of plants such as lipophilic cuticula, thorns, spikes and trichomes reduce the chances of successful penetration by pathogens. These structures prevent the attackers from reaching the soft plant tissues. They also help in reducing the wettability of the plant surface that would otherwise accommodate a higher number of harmful pathogens. The presence of lignin also provides a barrier against pathogen attack by protecting the energy-rich cellulose and hemicelluloses of the plants (Pedersena et al., 2005). Lignin is a water-impermeable seal that gives strength, especially to the cell walls of xylem tissue.

Besides physical barriers, plants also produce a diverse assortment of secondary metabolites that display anti-microbial and anti-fungal activities (Dixon, 2001). One example is avenacin A-1, a saponin, which is produced in the roots of oat plants (Carter et al., 1999). Gaeumannomyces graminis, a major destructive fungal pathogen of wheat and barley, is extremely sensitive to avenacin A-1, and oat plants deficient in saponin biosynthesis are susceptible to G. graminis infection (Papadopoulou et al., 1999). Glucosinolates, another example of

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secondary metabolites, are precursors to bioactive toxic compounds such as isothiocynate, nitrile and thiocynate that display antifungal activities.

Should the pathogens overcome these first bar-riers, the plants will engage their second stage of defense strategy. This involves an induction of a multitude of cell genetic reprogramming, such as hypersensitive response (HR), up-regulation of de-fense-related genes, accumulation of pathogenesis-related (PR) proteins, and production of an oxida-tive burst. HR is a genetically-encoded inducible mechanism elicited by pathogen-specific avirulence determinants that causes necrosis and cell death to restrict the growth of a pathogen. It is an active process that results in the death of individual cells, tissues or whole organs. Phytoalexin, a specific an-ti-microbial substance of low molecular weight, has also been shown to accumulate rapidly at the sites of pathogen infection. Its production is induced by microbial challenge, chemical or physical agents, and it is host-specific rather than pathogen-specific (Tsuji et al., 1992). Phytoalexin accumulates earlier in incompatible than in compatible host-pathogen interactions. Fungal strains which degrade phyto-alexins are more virulent than strains without the ability to detoxify these compounds (Naoumkina et al., 2007).

Accumulation of PR proteins is another active form of plant defense. Plant PR proteins have been identified and classified into 17 families (Mitsu-hara et al., 2008). They accumulate after pathogen infection or related situations in many plant spe-cies. PR proteins such as β-1,3-glucanase and chi-tinase are relatively small molecules, acidic and stable. They accumulate either in the apoplast or vacuoles of plant cells and are directly involved in slowing down fungal growth (Egea et al., 1996). They are also indirectly responsible for releasing breakdown products from fungal cell walls which could act as signal molecules to activate the plant defense response (White, 1979; Uknes et al., 1992). Interestingly, some plants produce cyanide to de-fend themselves, especially against herbivores. Cy-anide is produced as cyanogenic glycosides which are stored in the vacuole of the cell (Selmar et al., 1988; Park et al., 2004) to protect the cell from auto-toxicity.

STUDIES ON MODEL PLANTS

A large amount of information on plant-pathogen interactions has been obtained from studies on the fungal infection of the model plant Arabidopsis and economically important crops such as maize and rice. In defending themselves against the attacking pathogens, plants would stand a much better chance if they activate a combination of their

defense responses. Passive mechanisms, coupled with active induced mechanisms, would generally confer a long-lasting resistance to the plants. In fact, the success of plant’s defense responses is even greater if infective interaction of the pathogen is recognised at an early stage of infection. Many gene products are required for pathogenesis to enable an organism to colonise a host and cause disease.

The specificity of the plant-pathogen interaction is very much dependent on the ability of both plant and pathogen to continually produce or detect spe-cific cues secreted into their establishments. Most of the plant pathogenic microbes secrete effector proteins, known as Avr-effector (avirulence) pro-teins, and some of these proteins are recognised by corresponding R (resistance) proteins in the plant cells. A matching R-gene product in a vegetal cell recognises elicitor proteins, the Avr-effector, of each infective pathogen. This concept of plant disease resistance was first developed by Dr H H Flor more than 50 years ago based on his analysis of the dif-ferential reactions of flax to the rust fungus Melamp-sora lini (Halterman and Martin, 1997). According to his hypothesis – now termed the ‘gene-for-gene’ model – for every resistance gene in a plant cell there is a specific and related gene for virulence in the pathogen to which it is susceptible (Flor, 1960). Flor (1960) further stated that resistance would not occur unless a resistance allele (R gene) is present in the host along with a corresponding avirulence gene (Avr gene) in the pathogen. Halterman and Martin (1997) summarised the essence of Flor’s hy-pothesis in a statement as illustrated in Figure 1.

The critical feature of the ‘gene-for-gene’ hy-pothesis is that two sets of proteins are required: one from the pathogen and one from the host. The protein comes only from a dominant gene or allele, and not from a corresponding recessive allele. As shown in Figure 1, incompatibility (I) between plant and pathogen results only from specific combina-tions of the resistance allele, R, with the avirulence allele, avr, whereas compatibility (C) results from any of the other three combinations r/avr, R/no avr and r/no avr. Alleles R and avr are the dominant genes. The proteins encoded by avr and R genes are postulated to interact with each other, either direct-ly or indirectly, to activate signaling cascades lead-ing to resistance. Most R genes encode proteins that contain a nucleotide-binding site and leucine-rich repeats (Ameline-Torregrosa et al., 2008).

Pathogen-Arabidopsis Interaction

In the Arabidopsis-Phytophthora sojae interaction, a phenomenon known as cytoplasmic aggregation was observed in the Arabidopsis epidermal cells

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(Takemoto et al., 2003). P. sojae is the causal agent of stem and root rots of soyabean. Cytoplasmic ag-gregation involves a rapid translocation of the cy-toplasm and subcellular components to the site of pathogen penetration of the cell, where polymerisa-tion of actin, inhibition of cell death, callose depo-sition and pathogenesis-related protein expression occur. This phenomenon is common in an early re-sponse reaction of plant cells to fungal pathogens. It is induced by the pressure generated by the pen-etrating hyphae.

During P. sojae infection, actin microfilaments

are re-arranged to form large bundles, focusing on the penetration site. In other phytosystems, the microfilament cables are observed to accumulate more frequently around the infection site in the susceptible host than in the resistant host (Cutler and Somerville, 2005). Deposition of these materi-als at the infection sites is believed to generate the physical, as well as chemical, barriers to fungal en-trance through the plant cell wall. The hypothesis is strengthened by the observation that de-poly-merisation of actin cytoskeleton inhibits the forma-tion of the cytoplasmic aggregate and reduces the plant’s ability to inhibit pathogen attack (Yao and Allen, 2007). It has also been observed that the cy-toplasmic aggregation events are induced even before P. sojae penetration begins, indicating an in-volvement of a chemical elicitor released by the at-tacking pathogen.

Pathogen-secreted hydrolytic enzymes that de-grade cell wall polymers are also able to induce

defense responses in plants. The most extensively studied cell wall-degrading enzymes are endopo-lygalacturonases (PG). PG are important virulence factors for necrotrophic soft rot-causing pathogens such as the fungus Bottrytis cinerea. However, PG itself does not directly induce the plant defense re-sponse but rather causes the release from the plant cell wall of the true elicitors, namely oligogalactu-ronides (OG). Recently, Ferrari et al., showed that Arabidopsis OG increase resistance to Bottrytis ci-nerea independently of well-characterised defense-related jasmonic acid (JA) and salicylic acid (SA)-mediated signaling (Ferrari et al., 2007). They also proposed that genes that are involved in the bio-synthesis of secondary metabolites, such as PAD3, play a major role in determining the enhanced re-sistance against B. cinerea observed in OG-treated plants. SA is required for systemic acquired resist-ance against many viruses, bacteria and fungi (Ri-naldi et al., 2007).

It has been shown that inoculation of Arabidopsis with incompatible strains of the fungus Alternaria brassicicola results in a systemic response leading to the sustained induction of genes such as PR1 and PDF1.2, respective markers for the salicylate and jasmonate defense-signaling pathways. A grow-ing body of evidence has also indicated that basal resistance to this pathogen requires a functional jasmonate/ethylene pathway (Brown et al., 2003; Huffaker and Ryan, 2007). PR1 genes have been fre-quently used as marker genes for systemic acquired resistance in many plant species. In Arabidopsis, 22 genes are listed as predicted PR1 genes but only one PR1 gene (At2g14610), which encodes a basic protein, is confirmed to be pathogen-responsive (van Loon et al., 2006). In rice, however, Agrawal et al. (2001) reported the successful induction of two PR1 genes, OsPR1a and 1b, by blast fungus infec-tion. These genes have been found to encode pu-tative acidic and basic proteins, respectively, and have also shown responses to environmental stress-es and treatments with some chemicals. A total of 32 predicted PR1 genes has been proposed to be present in the rice genome (van Loon et al., 2006).

Pathogen-maize Interaction

Besides Arabidopsis, pathosystem studies on maize and rice are also of great interest to crop dis-ease researchers. Maize harbours a diverse commu-nity of non-mycorrhizal fungal endophytes such as several species in the fungal genus Fusarium. Fusar-ium verticillioides for example causes seedling blight and stem-, seed-, root-, and ear-rots. F. verticillioides has a wide host range, including sorghum, millet and sugar-cane, but it is most frequently isolated from maize.

Source: adapted from Halterman and Martin (1997).

Figure 1. Model of gene-for-gene interactions between plants and pathogens. Plants may contain a dominant resistance allele (R) or a recessive allele (r) that does not confer resistance. Pathogens may express a corresponding avirulence (avr) gene or they may lack such a gene. An incompatible interaction (I), resulting in disease resistance, occurs only when the plant and pathogen contain corresponding R and avr genes, respectively. All other reactions are compatible (C) and lead to disease symptoms.


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Maize displays several protein-based mecha-nisms of resistance to microbial invasion. It pro-duces benzoxazinoid, a toxic secondary metabo-lite. The primary benzoxazinoids found in maize are 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3-one (DIMBOA) and its desmethoxy derivative, 2,4-dihydroxy-2H-1,4-benzoxazin-3-one (DIBOA) (Saunders and Kohn, 2008). DIMBOA and DIBOA are also highly synthesised in young seedlings of several species within the Poaceae family, which in-cludes wheat, rye, maize, teosinte and some wild barley species. They provide a constitutive defense against herbivory, as well as fungal and bacterial infections. F. verticillioides, however, has a high tol-erance towards these compounds due to its ability to detoxify them. This characteristic has been sug-gested to increase the ecological fitness of Fusarium in maize fields (Macías et al., 2006).

Sindhu et al. (2008) reported that the maize Hm1 gene provides protection against the fungus Cochliobolus carbonum by directly inactivating the Helminthosporium carbonum (HC) toxin, an epoxide-containing cyclic tetrapeptide, which is produced by the pathogen as a key virulence factor for colo-nising maize. C. carbonum causes devastating dam-age in almost every part of the maize plant: blight-ing of the leaves, rotting of the roots and the stalk, and molding of the ear. The Hm1 gene encodes an NADPH-dependent reductase (Johal and Briggs, 1992). The gene or its homologs are conserved in monocots such as rice and barley (Han et al., 1997). Whether the interaction between this protein and its attacking pathogen is a common defense system in monocot plants remains unknown.

Pathogen-rice Interaction

Rice blast, the most serious disease of cultivated rice (Oryza sativa), is caused by the hemi-biotrophic ascomyceteous fungus Magnaporthe oryzae. The dis-ease provides an excellent model system to study plant-fungal interactions mainly due to the public availability of the host and pathogen genome se-quences (http://www.mgosdb.org). Magnaporthe oryzae was the first filamentous fungal pathogen to have a complete genome sequence made publicly available (Dean et al., 2005).

During infection, Magnaporthe oryzae mechanically breaches the outer plant surface using an appressorium, a dome-shaped cell that produces a specialised hypha which pierces the plant surface. This dome-shaped cell generates enormous turgor pressure and physical force, allowing the fungus to breach the host cuticle and invade plant tissue. Turgor is generated by the accumulation of compatible solutes, including glycerol, which is

synthesised in large quantities in the appressorium (Skamnioti and Gurr, 2007). Melanin deposition in the cell wall of the appressorium is essential for maintaining turgor pressure. Upon reaching the epidermal cell lumen, the appressorium expands to form a narrow filamentous primary hypha. The filamentous hypha then becomes a conduit for moving the nucleus and cytoplasmic contents from the appressorium into the growing primary hypha. In a compatible interaction, primary hyphae differentiate into thicker, bulbous invasive hyphae that fill the first-invaded cells and then move into neighbouring cells.

Recently, the M. oryzae invasion event was visu-ally detailed by Kankanala et al. (2007). By applying live-cell imaging and FM4-64 dye-loading experi-ments, they characterised the spatial and temporal development of the invasive hyphae inside the in-vaded rice cells (Figure 2). They reported three dis-tinct types of hyphae that play a role in biotrophic invasion: (1) filamentous primary hyphae in the first-invaded plant cell; (2) bulbous invasive hy-phae in first-invaded and in subsequently invaded plant cells; and (3) filamentous invasive hyphae that initially grow in successively invaded cells. Primary hyphae grow in the lumens of the first-in-vaded cells after pressure-based appressorial pene-tration. Filamentous invasive hyphae are produced in the lumens of successively invaded rice cells af-ter the occurrence of an internal wall penetration event that does not require high pressures. Both primary hyphae and invasive hyphae differentiate into bulbous invasive hyphae, and both are coated in plant membrane featuring distinctive membrane caps. It was also observed that the primary hyphae often lose viability after the invasive hyphae are established inside the host cell. Filamentous and bulbous invasive hyphae however remain viable as the fungus spreads to new rice cells in the develop-ing lesion.

Nevertheless, the molecular processes regulat-ing appressorium formation are still incompletely understood. Work by Oh et al. (2008) provides some insights into the role of protein degradation and amino acid metabolism in appressorium forma-tion and function. Oh et al. performed microarray studies to identify the wide fluctuations in gene expression of the rice genome during germination, appressorium induction and maturation. During appressorium formation, several proteases includ-ing the putative vacuolar subtilisin-like protease SPM1, which is required for penetration and in planta growth, are up-regulated. The data also re-veal that genes involved in targeting proteins for degradation, as well as the machinery involved in protein degradation, are also up-regulated. Several


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proteases with export signals are found to be up-regulated, suggesting that they may be secreted and act as virulence factors.

Somewhat surprisingly, some genes that are well-documented for appressorium development appear to be down-regulated. Hydrophobin, for instance, is more highly expressed in spores ger-minating on a hydrophilic surface than in incipient appressoria, suggesting that the gene products are required initially and perhaps transiently for subse-quent morphological changes, and this is consistent with a role in surface sensing and attachment. Once the environmental cue is detected and the intracel-lular signal pathways are activated, these proteins may no longer be needed for appressorium forma-tion to proceed.

Insect-plant Interaction

Besides model plants, the current understanding of plant defense responses has also been achieved

through the study of insect-induced biotic stress. Insects damage crops either by depleting photo-assimilates, manipulating growth and nutrient par-titioning, or in some cases injecting toxins into the plant. Studies that compare insect-responsive gene expression in resistant and susceptible plants have identified a subset of genes that is related to innate resistance, including transcripts involved in oxida-tive stress, signaling, cell wall modification, water transport, metal homeostasis, vitamin biosynthesis, carbon assimilation and nitrogen mobilisation (Pat-rick et al., 2002; Divol et al., 2005). Among them, cell wall-modifying enzymes, xyloglucan endotrans-glycosylase and pectin methyl esterases, are the most readily detected in infested plants. Park et al. (2006) has reported the up-regulation of cell wall-related genes in response to greenbugs feeding on resistant sorghum. Divol et al. (2005) also found a strong systemic up-regulation of genes encoding cellulose synthase and expansin in celery petiole phloem in response to green peach aphids feeding on the leaves.

When insects feed on plants, the plasma mem-brane is depolarised in the vicinity of the bite zone followed by a transient increase in the cytosolic cal-cium ion (Ca2+) in the same region (Maischak et al., 2007). Insect salivary secretions are found to signifi-cantly contribute to the increased Ca2+. The Ca2+ is recognised as a secondary messenger in numerous plant signaling pathways. Insect salivary glands produce a potential source of many avirulence fac-tors as they contain complex mixtures of lipopro-teins, phospholipids and carbohydrates, as well as numerous proteolytic, hydrolytic, oxidative and cell wall-degrading enzymes. These components of salivary secretions generate local and systemic pro-duction of reactive oxygen species (ROS), mostly hydrogen peroxide (H2O2) – a strong depolarising molecule.

The generation of ROS is a common plant re-sponse to pathogen invasion as ROS potentiates a hypersensitive response at the infection site. In re-sponse to herbivores, H2O2 levels increase as long as the attack persists as the insect actively intro-duces considerable amounts of H2O2 into the dam-aged tissues. Furthermore, the presence of H2O2 in the plant in response to herbivory could be advan-tageous in preventing secondary microbial infec-tion of the wound site. Caterpillar oral secretions containing volicitin and other fatty acid conjugates have been found to trigger the release of plant vola-tiles that attract the natural enemies of insect herbi-vores (Major and Constabel, 2006).

Herbivory also stimulates the production of JA, its precursor 12-oxophytodienoic acid, and ethylene, whereas the levels of abscisic acid and

Source: adapted from Kankanala et al. (2007).

Figure 2. Live-cell imaging of M. oryzae invasive hyphae (IH) and rice cell membranes. (A) and (B) Differential staining patterns with RB and FM4-64 in rice sheath epidermal cells invaded by EYFP-labelled fungal strain KV1 (green). Arrows indicate sites where appressoria had penetrated into host cells. (A) RB dye (purple) stained the endoplasmic reticulum inside rice cells and fungal IH at 36 hpi. Bar = 10 μm. (B) Plant membrane and endocytotic membranes in rice cells were stained to saturation with FM4-64 (red). Narrow primary hyphae (P) extending from the penetration site differentiated into bulbous IH inside two invaded rice cells at 27 hpi. (C) Invasive-like hyphae formed in vitro on dialysis membrane internalise FM4-64. (D) The membrane encasing the IH had an FM4-64–stained connection (arrow) to rice membrane at the cell periphery.

A B

C D


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indole acetic acid are often decreased (Adie et al., 2007; Chung et al., 2008). There is evidence of a to-bacco mitogen-activated protein kinase, such as a wound-induced protein kinase (WIPK), playing a role in the signaling of abiotic and biotic stresses, pathogens and plant hormones (Maffei et al., 2007). WIPK is essential for JA formation by eliciting the transcription of FAD7, which catalyses the conver-sion of linoleic acid to linolenic acid, a precursor of JA. Enhanced ethylene production is another early and active response of plants to biotic stresses (van Loon et al., 2006). Insect infestation has also been shown to modulate SA production (Campbell et al., 2002).

BASAL STEM ROT IN OIL PALM

Ganoderma boninense has been identified as a ‘white rot’ pathogen (Paterson, 2007) that causes basal stem rot (BSR) disease in oil palm. The disease has long been reported in Ghana, Zaire (now Republic of Congo), Nigeria, Cameroon, Angola, Sán Tomé and Principe, Tanzania and Rhodesia (Turner, 1981). In Malaysia and Indonesia, the world’s two largest palm oil exporters, BSR is regarded as one of the most commercially devastating diseases of oil palm. Recent reports indicate that the incidence of BSR appears to occur increasingly earlier from one planting cycle to the next (Breton et al., 2006). BSR incidence increases with replanting, especially in areas with a bad history of Ganoderma infection as well as in areas that were previously planted with coconut. The disease symptoms include rotting of the basal stem, the presence of bracket-shaped fungal fruiting bodies and the yellowing of the crown. Ganoderma often weakens trunks or roots so that chances of mechanical failure are exponentially increased. Most of the time, the infected palms need to be felled and excavated. If the palms remain standing, the infected trunks may become hollow, making them susceptible to wind damage.

Detection and Control Strategy

BSR epidemiology and its route of infection are still being disputed. The current assumption is that disease spread is by contact of living palm roots with colonised debris within the soil, or by contact with infected roots (Idris et al., 2004a). However, re-cent studies suggest a different perspective. Based on an interfertility study, Pilotti et al. (2003) have suggested the involvement of basidiospores as the main mode of dispersal of G. boninense. A recent field study conducted by the Malaysian Palm Oil Board (MPOB) at two locations, namely FELCRA Seberang Perak, Batu Gajah and MPOB Research Station, Teluk Intan, also points to the same possi-bility. It was found that the beetle Episcapha 4-macu-

lata can carry basidiospores of Ganoderma and has the potential to infect oil palm (unpublished data). With the increasing number of upper stem rot in-cidents, in which the appearance of the fruiting bodies is no longer confined to the basal stem, the role of insects in disseminating Ganoderma basidio-spores to different parts of the palm cannot be over-looked. Extensive research towards characterising the relationship between the insect and its host plant is appropriate and urgent.

Molecular techniques, such as PCR, repetitive DNA polymorphism analysis and amplification of rDNA spacers, have been employed for the early detection of the disease. Other methods that have been developed for early detection of BSR incidence include a method known as Canopy Temperature Difference (CTD) (Haniff and Roslan, 2006). The method exploits the fact that BSR-infected palms have a reduced transpiration rate due to their water-stressed condition, which subsequently leads to an increase in oil palm leaf temperature. The infected palms can also be detected by Picus® sonic tomography, initially developed for detecting Douglas fir, beech, oak and sycamore trees artificially infected with Ganoderma resinaceum, G. adspersum and G. applanatum (Deflorio et al., 2008). Earlier, Mazliham et al. (2007) reported on an improved version of the tomography method for detecting infected palms. They produced better tomography images and hence a better assessment of the disease stage.

In spite of numerous reports on the severity of BSR and its effect on the oil palm industry, no sin-gle treatment has effectively tackled the problem. Most control measures to date have continued to give variable and inconsistent results. One of the control strategies currently being employed in oil palm plantations is by adopting correct techniques of land preparation, such as soil tilling, prior to re-planting, and the eradication of diseased palms (Id-ris et al., 2004a; 2005) at the time of oil palm replant-ing. The application of this sanitation technique for controlling Ganoderma reduces BSR incidence in re-planted oil palm. The technique has been adopted by industry, as exemplified by FELDA, Johor (50 ha), FELCRA, Perak (1000 ha) and Borneo Sam-udra, Sabah (450 ha).

Flooding the infected areas has been suggested to help control the fungi, based on the inability of G. boninense and G. australe mycelia to survive in conditions of high soil moisture content (Chang, 2003). Unlike some other species of Ganoderma, G. boninense and G. australe do not produce asexual structures such as chlamydospores (Pilotti et al., 2002) that provide resistance to severe environmental stresses such as soil waterlogging.


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The application of wide-spectrum fungicides such as hexaconazole and bromoconazole has been shown to limit the spread of Ganoderma within infected palms (Idris et al., 2004b).

The introduction of antagonistic soil microbes such as arbuscular mycorrhizal fungi (AMF) as a biocontrol agent holds a promising solution to the problem as it has been shown to reduce the num-ber of G. boninense-infected oil palm seedlings (Hashim, 2003; Nor Sarashimatun and Tey, 2009). Increased uptake of nutrients (especially phospho-rous), higher production of secondary and tertiary roots, and increased production of secondary me-tabolites such as flavanoids, β-1,3 glucanases and peroxidase have been postulated to contribute to this outcome.

Trichoderma species combat BSR by competitive-ly displacing Ganoderma for nutrients and space in a particular environment (Sariah, 2003). They coil around the hyphae of the Ganoderma in a lectin-me-diated reaction and degrade the cell walls, limiting the growth and activity of Ganoderma. Sariah also reported a positive correlation between the popu-lation of Trichoderma and the age of the palms, i.e. the Trichoderma species are significantly more abun-dant in mature fields than in younger plantings. A larger population of this antagonistic fungus in in-land and jungle soils than in coastal soils has also been recorded (Sariah, 2003). Nagappan et al. (2009) investigated the use of T. harzianum as the main antagonist in combination with other Trichoderma species, namely T. longibrachiatum and T. virens, to inhibit G. boninense in oil palm seedlings. They con-cluded that a single treatment of T. harzianum is the best compared with the mixed species application. They also observed that once Ganoderma infection has established, Trichoderma is no longer able to control the infection and save the plants.

Currently, Trichoderma species are the active in-gredients in a variety of commercial biofungicides used to control a range of economically important aerial and soil-borne fungal plant pathogens (Lu et al., 2004). Wide-scale use of these biocontrol agents is expected to delay, if not prevent, the infection of palms replanted in fields previously devastated by Ganoderma. Great care, however, needs to be taken to ensure that they do not contaminate the final product of oil palm as Trichoderma species produce toxic secondary metabolites (Paterson, 2006). Re-cently, a nursery evaluation of endophytic bacteria such as Agrobacterium radiobacter, Burkholderia cepa-cia and Pseudomonas syringae in controlling G. bonin-ense infection in oil palm was conducted (Maizatul and Idris, 2009). After six months of treatment, A. radiobacter was found to be the most effective in suppressing the disease as BSR incidence was

greatly reduced by up to 74%.

Genetic improvement, based on a search for durable genotype resistance in oil palm, is one of the definite ways of slowing down the spread of the disease as this approach is inexpensive and does not require investment in new machinery. MPOB has identified several oil palm progenies that are partially resistant to G. boninense (Idris et al., 2004c). The most tolerant progeny is PK4195 (Zaire D × Cameroon P). The tolerant progeny is expressed by showing low severity of foliar symptoms and slow progress in Ganoderma infection in the root and stem tissues. There is also interest at MPOB in generating oil palm varieties with reduced levels of Ganoderma susceptibility using existing genetic materials. Development of transgenic oil palm carrying PR genes for glucanase and chitinase for fungal resistance has also been carried out. Glucanase and chitinase are known to be capable of hydrolysing the two main carbohydrate components of most fungal cell walls, viz., chitin and b-1,3-glucan.

G. boninense-Oil Palm Interaction

Identifying underlying molecular mechanisms necessary for pathogenesis in a wide range of path-ogenic species is a major and common goal of any pathosystem research. Although significant efforts have gone into the identification of pathogenicity determinants, only a small number of genetically tractable pathogenic fungi have been validated. This is generally due to the limitation in generating a mutant fungal strain with a non-functioning ver-sion of the gene. There are also severe restrictions to studying pathogenicity by mutating only one gene at a time as many virulence-associated processes, such as the development of infection structures and haustoria, are likely to involve a large number of gene products. The current major drawback in combating BSR in oil palm is the lack of sufficient information on the defining mode of action of the fungus and its relationship with oil palm. To gain a deeper insight into the Ganoderma-oil palm interac-tion, it is therefore imperative to understand both the physical infection process and the molecular consequences.

BSR is a vascular disease. Darus et al. (1991) ob-served profuse hyphal growth within Ganoderma-infected phloem and xylem vessels of naturally diseased palms. Earlier, the same research group had investigated the formation of chlamydospore-like structures, manifested as a black line in the ves-sels of infected palms (Darus et al., 1989). However, since then not many studies have been carried out to investigate further the Ganoderma-oil palm in-teraction. Detailed information, especially during


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the infection event at a molecular level is still very much lacking.

Consequently, since 2002 MPOB has started studies on the gene expression profile and bio-chemical events of Ganoderma-infected palms. Sam-ples of roots, basal stems and leaves of infected palms up to 12 months of age have been collected and subjected to various molecular and proteomics analyses. These studies are conducted with the aim of enhancing the understanding of the molecular response to infection, and ultimately of developing a diagnostic tool for early detection of Ganoderma infection and Ganoderma tolerance. By using MAL-DI-TOF analysis, Syahanim et al. (2009) have man-aged to identify eight unique protein spots from the infected roots of the oil palms. Interestingly, 19 dif-ferentially expressed genes that showed sequence similarity to the pathogenesis-related and defense- and stress-related genes identified from the same samples (Fazliza et al., 2009).

Other research institutions and universities have also embarked upon this initiative. Tee et al. (2009) have reported the first global analysis of transcription changes in oil palms infected with G. boninense. They profiled transcripts in oil palm roots infected with G. boninense using cDNA microarray and revealed that 173 genes were differentially regulated as compared with the control. Genes that are related to stress and defense formed the largest functional category (13%). A genotypic screening approach known as nucleotide binding site-profil-ing (NBS-profiling) has been employed to identify G. boninense resistance genes in oil palm (Tan et al., 2009). NBS-profiling has been used extensively to identify and map resistance gene analogues.

Information Sharing and Deposition

Due to the intense interest in comparative genomics in this field, a number of specialised pathogen-host interaction (PHI) databases have been set up. PHI-base (http://www.phi-base.org), for example, is a free web-accessible database that catalogues experimentally verified pathogenicity, virulence and effector genes from bacterial, fun-gal and oomycete pathogens, which infect human, animal, plant, insect, fish and fungal hosts (Win-nenburg et al., 2008). PHI-base is sponsored by Rothamsted Research and The Biotechnology and Biological Sciences Research Council (BBSRC, UK), and is being developed and maintained by scien-tists at Rothamsted Research.

PHIDIAS (Pathogen-Host Interaction Data In-tegration and Analysis System) (http://www.phidias.us) is yet another comprehensive public

resource of a PHI database that permits integra-tion and analysis of genome sequences, curated lit-erature data for general PHI information and PHI networks, and PHI-related gene expression data (Xiang et al., 2007). PHIDIAS is unique in that it in-tegrates information from other existing PHI data-bases such as PathoPlant (http://www.pathoplant.de) that deals with plant-pathogen interactions, signal transduction reactions and microarray gene expression data from Arabidopsis thaliana (Bülow et al., 2007), and e-Fungi (http://www.e-fungi.org.uk), an online resource for comparative genomic analy-sis of the fungi (Cornell et al., 2007; Hedeler et al., 2007). Unfortunately, at the moment not much data on Ganoderma fungus can be found in these data-bases.

Recently, MPOB initiated an Oil Palm Genome Programme with the ultimate aim of completely sequencing and exploiting oil palm genome infor-mation. Once the programme is fully matured, it is expected to generate a huge amount of data con-taining valuable information. This will include in-formation on important agricultural traits such as yield components, height increment, oil quality and value-added products, tissue culture amenity and abnormality, and also disease resistance. All this information will be stored in and can be retrieved from soon-to-be established databases and will be made available in public domains. Data mining of this database and cross-referencing with the exist-ing data in the other public-accessible databases would definitely hasten the process of eliminating the problems that are now faced by the oil palm in-dustry.

ACKNOWLEDGEMENT

The authors wish to acknowledge the Director-General of MPOB for permission to publish this article. They are also grateful for the critical review of this article by Dr Omar Rasid, Ms Nurniwalis Abdul Wahab, Dr Abrizah Othman and Dr Ravigadevi Sambanthamurthi of the Advanced Biotechnology and Breeding Centre, MPOB.

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