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Control of Ganoderma boninense: A Causal Agent of Basal Stem Rot Disease in Oil Palm with Endophyte Bacteria In Vitro.

Byline: M. RAHAMATH BIVI, M. SITI NOOR FARHANA, A. KHAIRULMAZMI1 AND A. IDRIS - E-mail kcik@hotmail.com

ABSTRACT

The objective of this study was to screen the potential endophytic bacteria to be used as a biological control for Ganoderma boninense, the major causal pathogen of Basal Stem Rot (BSR) disease in oil palm. Twenty endophytic bacteria were isolated from symptomless oil palm roots but only seven isolates showed inhibitory effect by suppressing the mycelial growth of G. boninense.

The isolated bacteria were screened in vitro by dual culture assay and culture filtrate test for their antagonistic properties towards G. boninense. Four bacterial endophytes (EB2, EB4, EB5 and EB6) were established to have potential as biocontrol agents based on their percentage inhibition of radial growth (PIRG) more than 50%. There was significantly difference in inhibitory effect (pless than0.05) for dual culture test and these endophytic bacteria inhibited the fungal growth by an average of 52.78, 83.33, 67.59 and 93.52%, respectively on NA medium.

Culture filtrate test likewise was showed a significant different for percentage of mycelia rowth (pless than0.05). Endophytic bacteria EB2, EB4, EB5 and EB6 suppressed the fungal growth by an average of 56.65, 91.45, 69.48 and 97.95%, respectively. Interestingly, out of four potential endophytic bacterial isolates, two, isolates namely EB4 and EB6, produced significantly (pless than0.05) higher inhibitory effect than two more isolates of EB2 and EB5. Changes of hyphae occurred in prsence of both bacteria of EB4 and EB6. Deformity and shrinkage of hyphae in EB6 was more apparent than in EB4 through mycelial growth test. Identification of species for these two bacteria was done using Biolog(r) System where EB6 was successfully identified as Pseudomonas aeruginosa but EB4 could not be unidentified. Therefore, in vitro activities of EB4 and P. aeruginosa against G. boninense in these studies suggested that these endophytic bacteria can be used as an effective biological control agent.

(c) 2010 Friends Science Publishers

Key Words: Basal stem rot disease; Dual culture assay test; Culture filtrate test; Mycelia test; Pseudomonas aeruginosa

INTRODUCTION

Elaeis guineensis Jacq., which is commonly known as the oil palm is the most crucial species in the genus Elaeis which belongs to the family Palmae. Oil palm is truly "a golden crop of Malaysia" since it generates profitable export earnings for the country and truly nature's gifts for alleviating poverty in Malaysia (Basiron, 2007). Malaysia is currently the world's largest producer and exporter of oil palm. Areas of oil palm have increased from 54,000 hectares in 1960 to 4.05 million hectares in 2005, reflecting a compound annual growth of 10.06%. Production increased from 94,000 tones in 1960 to 15 million tones in 2005, or almost 160 times within 45 years.

This represents a compound annual growth of 11.93% per year (Basiron, 2007). In Malaysia, the oil palm is blessed by being largely disease free, but suffering from one major disease, Basal Stem Rot (BSR) caused by Ganoderma species. BSR was first recorded in the country in 1928 (Sharples, 1928). With no known remedy at present, it is the major disease of oil palm and, therefore, of great economic importance to the Malaysian oil palm industry. BSR infects palms as young as 12-24 months after planting and is serious on palms of 4-5 years age, particularly in replanted areas (Singh, 1990).

In new oil palm planted from jungle or rubber, BSR incidence of 25% has been recorded after 25 years while in that planted from coconut, an incidence of 60% occurred after 16 years (Singh, 1991) whereas oil palm to oil palm under planting has resulted in 33% infection after 15 years. BSR infection resulted in crop loss, in severe cases turning a loss up to 45% of the yield (Singh, 1991). Oil palm has an economic life span of 25-30 years. Basal stem rot can kill more than 80% of stands by the time they are half-way through normal economic life (Abdul Razak et al., 2004).

Field controls of BSR by contact chemicals have not been very successful even in vitro efficacy of fungicides have not been reported against the fungus (Soepena et al., 2000). This may be due to the fact that both visibly infected and subclinical palms may already have the disease established by the time treatment is applied.

Control by physical methods such as clean clearing and tree surgery has had but transient effects, although there is tstify that BSR can be To cite this paper: Bivi, M.R., M.S.N. Farhana, A. Khairulmazmi and A. Idris, 2010. Control of Ganoderma boninense: a causal agent of basal stem rot disease in oil palm with endophyte bacteria In Vitro. Int. J. Agric. Biol., 12: 833-839 dealt if all the disease inoculum is removed before planting or replanting the crop. The idea therefore is to avoid infection, instead to cure the infected palms.

Thus, management of BSR in new or young oil palm areas should include: (1) using a potting mix with clean soil for growing the seedlings in polybags, (2) eradicating all disease inoculums in the field before planting or replanting and (3) applying chemical or biological control agent (Soepena et al., 2000).

Astute observations of the low incidence of disease due to pathogenic Ganoderma species in some natural stands, suggest that the disease is most likely kept under control by some biological means. Due to these observations, recent control measures to overcome the Ganoderma problem are now focused on the use of biological control agents. For example, saprophytes can be used to compete against Ganoderma to reduce its opportunity for colonizing oil palm roots. Several promising antagonists such as Trichoderma (Shukla and Uniyal, 1989; Wijesekera et al., 1996; Sariah, 2003) and Penicillium (Dharmaputra et al., 1989) have shown in vitro antagonistic activity against G. boninense. Some of endophytic microorganisms such as Serratia spp., Burkholderia spp.,

Pseudomonas spp., Bacillus spp. and Fusarium spp. have been found to induce systemic resistance in plants and shown biological traits like antibiotic activity and lysis (Kloepper et al., 1992: Dorworth and Callan, 1996). They have been isolated from a wide range of hosts including wild and cultivated crops, such as woody plants (Bills, 1996), banana (Pan et al., 1997) and grass (Clay, 1998). Endophytic microorganisms are therefore a relatively new field of study in biological disease control. Endophytic bacteria live in the plant tissues without doing substantive harm or gaining benefit other than residency (Kobayashi and Palumbo, 2000; Zaiton et al., 2008).

Introducing endophytic bacteria to the roots to control plant disease is to manipulate the indigenous bacterial communities of the roots in a manner, which leads to enhanced suppression of soil-borne pathogens. The use of endophytic bacteria should thus be preferred to other biological control agents as they are internal colonizers, with better ability to compete within the vascular systems, limiting Ganoderma for both nutrients and space during its proliferation. This study was therefore, undertaken with following objectives; to isolate endophytic bacteria from symptomless oil palm roots and to screen the potential endophytic bacteria against G. boninense in vitro and identify the most potential bacteria using Biolog(r) System.

MATERIALS AND METHODS

Root sampling: Oil palm roots were obtained from University Putra Malaysia, Bintulu Sarawak Campus. Healthy palms were randomly selected and sampled with the roots taken about 0.2 m from their bases at 20 cm depth. Each palm was sampled at three points around its bases and both primary and secondary roots were collected.

All the roots from each palm were bulked and stored in refrigerator at 4oC before isolation of microbial organisms.

Ganoderma boninense culture: G. boninense pure culture plates were taken from Malaysian Palm Oil Board (MPOB) at Bangi, Selangor. The pure culture was initially isolated from infested oil palm plantation situated in Miri and Bintulu Division, Sarawak. The plates of G. boninense culture were then sub-cultured to mass multiply a pure culture of the pathogen for this study (Fig. 1).

Isolation of endophyte bacteria: Endophyte bacteria were isolated from the oil palm roots and cultured on nutrient agar (NA) medium. Root samples from each palm 10 cm long were taken and rinsed under tap water for 5 min to remove any adhering soil from their surface. Then 0.5 cm from both ends was discarded and the remaining root divided into three sections of three cm in length. The sections were surface sterilized by dipping in 10% Clorox for two minutes, then in 50, 70, 90 and 100% ethanol for 30 s each (Schena et al., 2003).

They were then rinsed three times with sterilized distilled water to remove all the chemicals and allowed to dry on a sterilized filter paper. One cm from the ends of each section was discarded. The cuticle from the middle section was removed and it was cut into two sections of 0.5 cm each. Then, the root sections placed in sterilized distilled water of 250 mL conical flasks and allowed to agitate for one day at 150 rpm. Afterwards, one mL of the original sample was taken out and addd to 9 mL of sterilized distilled water to give 10-1 dilution of original sample. Similarly, serial dilution of 10-2, 10-3, 10-4, 10-5 and 10-6 were prepared. Later on, 10 uL of 10-6 dilution was placed in each Petri dishes and hockey stick was used to flatten out the suspension on NA media for bacteria. Then, Petri dishes were incubated at 30oC. Endophyte bacterial colonies were then further isolated by sub culturing single bacterial colony on NA media plates. Pure cultures were maintained in refrigerator at 4oC for further study

Bacterial gram staining: One droplet of distilled water was dropped onto a slide and smeared with bacterium. The bacterial smear was air dried and heated. The slide was then stained with crystal violet for one to two minutes. The slide was flooded with iodine for one to two minutes after stained with distilled water to remove the acetone alcohol. The slide was then washed thoroughly with distilled water to remove the acetone alcohol. Safranin was flooded onto the slide for two minutes followed by distilled water to remove safranin colour. The excess water was blotted and dried over Bunsen flame. The slide was then examined under compound microscope to identify the cell morphology and group of the bacteria.

In vitro screening of endophyte bacteria against G. boninense: The bacterial isolates were screened for their antagonistic activity against G. boninense in vitro by the dual culture and culture filtrate tests, based on the percentage inhibition of radial growth (PIRG) (Jinantana and Sariah, 1997).

Dual culture assay test: To evaluate the antagonistic activity of the endophytic bacteria isolates, a five mm diameter agar disc was taken from the five day-old PDA culture of G. boninense and plugged centrally in nutrient agar plate and then colonies of endophytic bacteria was streaked three cm away from G. boninense plug. The PIRG was obtained after seven days incubation and the most promising bacteria with more 50% PIRG kept for further study.

All the test antagonistic pairings were incubated at 28+-2oC. The ability of the endophyte bacteria to inhibit the growth of G. boninense was assessed after seven days incubation by measuring the radius of the G. boninense colony in the direction towards the antagonist colony (R2). The data were later transformed into percentage inhibition of radial growth (PIRG) in relation to the radial growth of G. boninense in the control plate (R1) using the formula:

R1 [?] R 2

PIRG = ---------------- x 100%

R1

Culture filtrate test: The endophytic bacteria that gave good results in the dual culture test were inoculated in 250 mL nutrient broth and maintained at 28+-2oC in the dark for seven days. The culture was then centrifuged at 10000 rpm for five min, supernatant collected and pellet discarded. The supernatant was filtered through a 0.25 um membrane filter in sterile conditions. The filtrate was incorporated into sterilized double strength PDA in ratio 2:1, 20 mL of the amended agar was poured into each Petri plate and allowed to solidify. A G. boninense mycelial plug was centrally inoculated in each of the plate. Non-amended PDA was used as the control. The diameter of the mycelial growth of G. boninense was measured over seven days. The antagonistic activity was expressed as PIRG in relation to the mycelia growth of G. boninense in the control plate.

Preparation of bacterial suspension: Twenty five mL of NB was prepared for each 150 mL conical flask. NB in the conical flasks was then autoclaved and cooled. One loop of each bacterium screened from the pure culture and was transferred into each conical flask and shaken for 24 h at 160 rpm.

Mycelia growth test: A mycelial plug was taken from the edge of six day old culture of G. boninense and dipped into selected bacterial suspension for 30 min and air dried in the laminar airflow chamber. Treated mycelia plugs were placed on Petri dishes containing PDA medium. Fungal plugs dipped in sterile distilled water served as a control. The PDA plates were then incubated at 28+-2degC for seven days. Hyphal strands at the end of the fungal colony were removed and examined under a compound microscope for abnormalities, if any.

Identification of endophyte bacteria: Potential endophytic bacterial isolates were identified by Biolog(r) identification system which followed the Biolog procedures. The procedures for identification utilized 96 wells of microplate containing 95 different dried carbon sources plus control.

Bacterial isolates were initially determined for gram reaction, and oxidase test for categorizing into enteric or non-enteric bacteria. Enteric bacteria are gram negative and negative oxidase. Non-enteric bacteria are gram negative and oxidase positive. Bacteria were then cultured onto biolog universal growth (BUG) medium for 24 h at 26+-2degC to promote growth and retention of its metabolic activity. Bacterial suspension was prepared in the inoculants solution (0.1 g Gellan Gum, 4 g NaCl, 0.3 g Pluronic F-68 and 1 L distilled water) with concentration for non-enteric bacteria at 52%, enteric bacteria at 63% and positive gram bacteria at 25-28% transmission using biolog's spectrophotometer.

Bacterial suspension was inoculated into GN or GP micro plates depending on gram reaction cluster, 145 uL per well using the 8 channel repeating pipette. Microplate was covered with its lid and incubated at 28 to 30degC for 24 h to allow the utilization of carbon sources. Reading result was directly done after inserting the incuated microplate into the Biologs reader apparatus for identifying the bacteria up to species level.

Statistical analysis: The experiments in dual culture and culture filtrate test were conducted in Completely Randomized Design (CRD) with four replicates. Recorded data were analyzed with SAS(r) Software. The significant data was determined using Duncan's Multiple Range Test at 5% probability level. The percentage data were transformed into Arcsine transformation before subjected to ANOVA.

RESULTS

Isolation of endophytic bacteria: Twenty endophytic bacteria groups were successfully isolated from the symptomless oil palm roots. The separation of bacterial endophytic was carried out on the basis of morphological characteristics such as colony colour, elevation, the margin of colony and colony surface. The pure culture of each isolates was maintained for screening test against G. boninense. Gram staining was carried out for each endophytic bacterial to determine whether it is in Gram-positive or negative group. All the bacteria were gram negative (Table I). From the statistical analysis EB4 and EB6 had the maximum inhibitory effect against G. boninense and both bacteria were Gram-negative and rod-shaped.

In vitro Screening of Microbial Bacteria against G. boninense

Dual culture assay test: The dual culture test is an established method used to distinguish isolates with antagonistic potential from large populations. All the microbial endophytes tested gave different degrees of inhibition toward the mycelial growth of G. boninense. The bacterial isolates had a significantly higher antagonism than the fungal isolates with the exception of Trichoderma. However, as Trichoderma are aerobic fungi with their endophytic nature yet to be established, they were not further evaluated. Furthermore, in these studies the focus

Table I: The graming and shape of isolated bacteria from symptomless oil palm roots

Bacterial

isolate###Gram###Shape

EB1###Negative###Rod

EB2###Negative###Rod

EB3###Negative###Rod

EB4###Negative###Rod

EB5###Negative###Rod

EB6###Negative###Curved rod

EB7###Negative###Rod

EB8###Negative###Rod

EB9###Negative###Rod

EB10###Negative###Rod

EB11###Negative###Rod

EB12###Negative###Rod

EB13###Negative###Rod

EB14###Negative###Rod

EB15###Negative###Rod

EB16###Negative###Rod

EB17###Negative###Rod

EB18###Negative###Rod

EB19###Negative###Rod

EB20###Negative###Rod

Table II: Antagonistic potential of endophytic bacteria in dual culture test against G. boninense in vitro

Isolates###Inhibitory effect (PIRG)*

EB1###48.15de

EB2###52.78d

EB3###35.19ef

EB4###83.33b

EB5###67.59c

EB6###93.52a

EB7###21.30f

Table III: Antagonistic potential of endophytic bacteria in culture filtrate test against G. boninense in vitro

Isolates###Inhibitory effect (PIRG)*

EB2###56.65d

EB4###91.45b

EB5###69.48c

EB6###96.95a

Means in the same column with different alphabet(s) are significantly different (p less than 0.05) according to DMRT

*Percentage inhibition of radial growth of G.boninense after seven days of incubation was only on endophytic bacteria rather than endophytic fungi. Isolated bacteria with inhibitory characteristics were selected and screened by means of dual culture assay test. Out of 20 endophytic bacteria, only seven showed inhibitory effect by suppressing the mycelia growth of G. boninense on NA media subsequently after seven days of incubation at 28+-2degC. From the seven potential endophytic bacteria, only four isolates gave PIRG greater than 50%, while the other three bacterial isolates EB1, EB3 and EB7 gave PIRG less than 50%. Interestingly, these four isolates namely EB2, EB4, EB5 and EB6 (P. aeruginosa) produced significantly (pless than0.05) higher inhibitory effect 52.78, 83.33, 67.78 and 93.33%, respectively than the other isolates (Table II), with respect to the control after seven days of incubation (Fig. 2).

Therefore, four isolates from this category were selected for further screening test based on culture filtrate test. and EB6 (P. aeruginosa) were observed under 400 magnifications. Malformation of hyphae occurred in the presence of EB6 (P. aeruginosa) (B) compared with hyphae in the control plate. Hyphae of G. boninense treated with EB4 were shrunk as observed in (Fig. 4C). Moreover, the treated fungus also showed the reduction in the coverage of spore produced.

Bacterial identification using biolog(r) system: From Biolog system endophytic bacteria EB6 was successfully identified to species level; it was Pseudomonas aeruginosa but EB4 species could not be identified or unidentified due to limitation of the method used.

DISCUSSION

The abundance of red stained Gram-negative endophytic bacteria in the oil palm roots was supported by the frequency of their isolation. In other plants (cereals, vegetables and woody plants), the bacteria isolated from the xylem tissues are mainly (about 78 to 84% of the population) Gram-negative (Gardner et al., 1982; Bell et al., 1995). In this case, 100% (20 out of 20) of isolates were Gram-negative. Some of the bacterial endophytes from the genera Pseudomonas, Burkholderia and Serratia might have the potential to control G. boninense, as they were mostly found in healthy roots from symptomless palms. They also occur mostly in the vascular systems adjacent to the phloem and xylem vessels and are uniform throughout the cortex, which suggests that they may play a role in inhibiting penetration by Ganoderma and their movement to the vascular systems.

The role of endophytes in protecting plants against pathogens has been mentioned by several authors. For instance, Clay (1998) speculated that the interaction between a host plant and its endophytic microorganisms is one of the mechanisms of disease resistance. Some studies have shown that functioning communities of endophytes in plants contribute to their resistance to pathogens e.g., microbial endophytes in potato controlling bacterial soft rot (Sturz et al., 1999). Furthermore, Reiter et al. (2002), studying the response of endophytic bacterial communities in potato, suggested that disease may be inhibited by a diverse endophyte community maintaining the pathogen population below the threshold for expression of pathogenicity.

In this study, 20 endophytic bacteria were isolated from symptomless oil palm roots and isolation of bacterial endophytic were carried out based on morphological characteristics such as colony colour, colony surface, elevation, margin of colony and colony surface. These isolated bacteria were known as EB1, EB2, EB3, EB4, EB5, EB6, EB7, EB8, EB9, EB10, EB11, EB12, EB13, EB14, EB15, EB16, EB17, EB18, EB19, EB20. Out of 20 endophytic bacteria isolated, only seven of them (EB1, EB2, EB3, EB4, EB5, EB6 and EB7) showed inhibitory effect against the mycelia of G. boninense. From these seven potential endophytic bacteria, only four isolates (EB2, EB4, EB5 and EB6) gave PIRG greater than 50% on dual culture assay test.

These four isolates produced higher inhibitory effect than the other isolates. According to the culture filtrate test, out of these four potential endophytic bacteria only two bacteria (EB4 and EB6) produced very high PIRG value. Moreover, the effect of the inhibition of potential endophytic bacteria against G. boninense was investigated using compound microscope.

The changes of hyphal tips of G. boninense happened once treated with Pseudomonas aeruginosa and EB4 were observed under 400 magnifications. A great malformation of hyphae occurred in the presence of P. aeruginosa as compared with hyphae in the control plate. Hyphae of G. boninense treated with EB4 were shrunk compared with control. These bacteria were screened to determine the best candidate to control Basal Stem Rot disease in oil palm. Result of this study showed that there are potential endophytic bacteria to control BSR disease caused by G. boninense.

The most efficacious biocontrol agents identified in this study were EB4 and EB6. These endophytic bacteria were identified using the Biolog(r) system and one of the isolates (EB6) has been successfully identified to the species level to be Pseudomonas aeruginosa and one more bacterium (EB4) could not be identified. This might be a new species and no data concerning this species (EB4) were in the list of Biolog data base.

The results of the in vitro screening supported this speculation as the bacterium with the maximum PIRG value in the dual culture tests with 93.52 and 83.33% meanwhile for culture filtrate tests with 96.95 and 91.45% were Pseudomonas aeruginosa and EB4, respectively. Pseudomonas is known as growth-promoting bacteria and inducer of systemic resistance against fungal, bacterial and viral diseases (Liu et al., 1995; Chen et al., 2000) by producing metabolites with antimicrobial activity against pathogens (Dikin et al., 2005). They are also known to produce siderophores that restrict pathogen growth by limiting iron availability in the soil.

This obligate aerobic is also an opportunistic pathogen causing harm to human and animals (Ndip et al., 2005). Oil palm roots support large and more diverse taxa of endophytes including those with antagonistic properties against G. boninense. Since Ganoderma infection is often initiated at the roots, an endophyte isolated at the 'target' site would have lesser problem in adating and colonizing the host plant, leading to a more efficient disease control.

It has been demonstrated that the isolated endophytic bacteria are antagonistic to the pathogen in vitro (Dikin et al., 2005) but their ability to colonise the plant is important to test. To improve this study, in vivo or field study should be performed to confirm their efficacy. This is supported by Jubina and Girija (1998), on already established nursery plants of black pepper where one of the Bacilli isolates showing poor inhibition of the fungal pathogen in the dual culture, exhibited the maximum disease suppression in the in vivo biological control assay.

In conclusion, BSR caused by G. boninense is the most destructive disease of oil palm in Malaysia. The use of conventional contact fungicides has not given much control, as the disease is systemic. Thus, hygienic cultural practices with biological control are being explored to control the disease. The control of soil-borne pathogens is particularly complex, because the diseases occur in the dynamic environment at the interface of the roots with the soil. Although endophytic bacteria, especially P. aeruginosa showed biological control potential against BSR, further studies must be conducted to verify their effectiveness in the field. The population density of the endophytes to be applied must also be determined, as well as the best method of application. The effects of agrochemicals on the bacteria have also to be evaluated so as not to compromise their effectiveness against BSR disease.

Acknowledgement: This research was supported by Universiti Putra Malaysia (UPM). Special appreciation is extended to Mrs. Siti Fatimah for her assistant and technical support. Last but not the least we thank staff of UPMKB and MPOB for their support and assistant during research activities.

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(Received 15 July 2010; Accepted 01 September 2010)

Department of Crop Science, Faculty of Agriculture and Food Sciences, UPM Bintulu Campus, Sarawak, Malaysia

Division of Biology, Malaysian Palm Oil Board (MPOB), Bangi, Selangor, Malaysia
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