Abstract: Background and Objective: Ganoderma spp., have been reported as invasive tree pathogen and mostly reported in oil palm, however, information about the degradation in different land-use are limited. The rot disease caused by Ganoderma in the rainforest and agro plantation was investigated. In addition, this study was aimed to analyze the pathogenicity of Ganoderma infected forest and rubber trees to oil palm tree. Materials and Methods: Rot disease incidence and severity were measured in the rainforest, oil palm plantation and rubber plantation in two landscapes in Indonesia. The basidiocarps on infected trees were collected and the growth rate of Ganoderma on potato dextrose agar was measured. Selected Ganoderma from the forest, oil palm plantation and rubber plantation were tested for their virulence on oil palm seedling. Results: Ganoderma was a generalist tree pathogen since trees in different land-uses were infected. Interestingly, forest trees are more severe than mono plantations. Each Ganoderma has significantly different growth ability. When the virulence of Ganoderma tested in the oil palm seedling, only Ganoderma collected from oil palm plantation infected the oil palm seedlings with almost 100% in 10 weeks. Ganoderma from rubber plantation infected the oil palm seedlings very slow while the forest’s Ganoderma did not infect the oil palm. Conclusion: Ganoderma is a wide range pathogen that potentially degraded woody trees in different land-uses. Although the mycelial of Ganoderma showed vary differ rapid growth, which may have related to the virulence, Ganoderma from forest and rubber trees performed less virulence to oil palm seedlings.
INTRODUCTION
Forest conversion into managed plantations of oil palm and rubber has been reported to decrease the diversity of root-associated fungi and fungal community structures were changed with pronounced increases of plant pathogens1,2. Ganoderma, as a soil-borne pathogen3, is one of the plant pathogen enriched in the forest compared to monospecific plantations1. For the last decade, there have been limited reports in Indonesia evaluating the root rot disease severity due to land-use change at the scale of the landscapes in Indonesia. Most presented about the management of the disease, for instance, the use of biological agents in controlling Ganoderma, bio fungicides and chemicals4-8.
Ganoderma is the most distributed genus of pathogenic fungi in oil palm9-11 and rubber plantations12,13. Distribution of Ganoderma is an essential feature to understand the epidemic spread of the pathogen better. Infections of Ganoderma to a plant initiated by the contact of healthy plant roots with infected roots. Subsequently, penetration and degradation of root tissue will continue because Ganoderma produces degradation enzymes for lignin and suberin10,14. Currently, there is still no effective control for Ganoderma infections in an existing stand15,16. There is also still a lack of information on the spatial as well as temporal pattern or distribution of the disease, especially under natural field epidemic condition. Distribution maps of plant diseases as an authoritative source for accurate data on the worldwide distribution of plant diseases of economic or quarantine importance are urgently needed.
Since the evolution of Ganoderma in Indonesia not studied much, it is crucial to know the extent of disease incidence and severity caused by this pathogen. This study was aimed to provide baseline data on the disease incidence and severity of rot disease in the forests and plantations of oil palm and rubber. Besides, the study was also conducted to show the virulence of Ganoderma from different land-uses to oil palm seedlings.
MATERIALS AND METHODS
The study was located in Jambi, Sumatra, Indonesia. Survey and sampling were started from March, 2018. The plots consisted of forest, oil palm plantation and rubber plantation in two landscapes of Bukit Duabelas and Harapan. The study sites have been described in the previous studies by Brinkmann et al.1, Sahner et al.2 and Schulz et al.17.
| Table 1: | Class of disease scale assessed |
There were 4 plots per land-use. Each plot was extended to 250 m2 to have more tree vegetation out of existing plot. Trees assessed as dead or alive with rot disease symptoms and with or without a fruiting body of Ganoderma. Each Ganoderma found was collected and transported to the laboratory of Plant Pathology Tadulako University.
Rot disease incidence and severity in different land-uses: The diagnosis of the disease incidence and severity classes4 in Table 1 and calculated with the equations18.
Mycelial growth of Ganoderma and the disease incidence in oil palm seedling: Ganoderma collected were grown on potato dextrose agar (PDA) at 25°C and repeated 3 times. The fastest growth of Ganoderma from each land-use was selected and inoculated in rubber-wood block (12×6×6 cm: Length×width×height). Once the rubber-wood covered by the mycelia, it is then added into the pot filled with soil and incubated for a week19. The pot planted with three months of oil palm seedling and repeated 15 times for each Ganoderma tested. The disease incidence caused by Ganoderma in oil palm seedling was calculated.
Statistic analyses: The data of Ganoderma growth were compared and calculated with ANOVA one way. Significant results then continued with the Tukey’s honestly significant difference test. Since the data of the disease incidence in oil palm seedling did not meet the normal distribution for ANOVA, the statistics were performed with the Kruskal-Wallis test (p = 0.05). All the data analysis20 were done in R 3.5.1.
RESULTS
Ganoderma rot disease symptom, incidence and severity in different land-use systems: The observation of the rot disease showed that forest, oil palm and rubber trees potentially infected by Ganoderma. Forest trees infected by Ganoderma showed more severe than oil palm and rubber trees (Table 2). Bukit Duabelas and Harapan rainforests had 86.95 and 83% disease incidence, respectively. However, Harapan rainforest had the highest disease severity (64.26%) than Bukit Duabelas (46.07%). During the survey, it was noted that the tree decay was not only a basal stem rot but also upper stem rot, which is the most diagnostic sign of rot disease caused by Ganoderma in the forest, rubber and oil palm trees as presented in Fig. 1-3. Not only basal stem rot, upper stem rot was also found, for instance in the forest (Fig. 1a) where the basidiocarp of Ganoderma was found as a specific sign at the basal stem (Fig. 1b). Infected oil palm trees showed symptoms with spear ±3 leaves that were not open. The old leaves were necrosis and hang on the tree (Fig. 2a), with some basidiocarps at the bottom of the stem (Fig 2b). Also, upper stem rot was recorded in oil palm tree (Fig. 2c). The rubber tree showed necrosis leaves and die with the basidiocarp of Ganoderma at the basal stem (Fig. 3a, b).
Growth of Ganoderma: A total of 10 Ganoderma collected from the forest, 8 from oil palm and ten from rubber plantations were inoculated on PDA. Ganoderma BF1, HF1, HF5 and HF7 were significantly growing faster compared to other Ganoderma collected from Bukit Duabelas and harapan rainforests (Fig. 4a). The mycelial growth of Ganoderma BO1, BO2, HO2 from oil palm was the fastest colonizer compared to other Ganoderma collected from oil palm plantations (Fig. 4b). Ganoderma BR1 and BR4 grew significantly faster compared to other Ganoderma from rubber plantations (Fig. 4c). In the seventh day after inoculation on PDA, the fast growing Ganoderma covered 7-9 cm diameter of the media.
Disease incidence in oil palm seedling: Of all the Ganoderma tested, the disease development was only clearly appeared in oil palm seedling infected by Ganoderma collected from oil palm plantations. Figure 5 shows the disease incidence caused by Ganoderma BO1 developed from time to time. Until the 10th week, the oil palm seedlings mostly infected with all necrosis leaves. Ganoderma collected from rubber tree (BR1) infected the oil palm slower, about 20% incidences until 10 weeks. In contrast, Ganoderma from the forest (BF1) did not infect and produce any symptom in oil palm seedlings.
| Fig. 1(a-b): | Basal stem rot disease of (a) Forest tree and (b) With Ganoderma’s basidiocarp |
| Table 2: | Rot disease incidence and severity of forest, oil palm and rubber trees in Bukit Duabelas and Harapan rainforest |
The basidiocarp of Ganoderma on the basal stem of the oil palm seedling was appeared as infected by Ganoderma BO1 with all necrotic leaves at the 10th week (Fig. 6). Kruskal-Wallis test indicated that Ganoderma from oil palm trees differs in producing disease incidence compared to Ganoderma from the forest and rubber trees (p = 0.05).
| Fig. 2(a-c): | Symptoms of basal stem rot disease in oil palm, (a) Old leaves were necrosis and hang on the tree, (b) Basidiocarp of Ganoderma at the basal stem and (c) Upper stem rot symptom |
| Fig. 3(a-b): | Rubber tree attacked by, (a) Basal stem rot disease and (b) With fungal basidiocarp at the basal stem |
| Fig. 4(a-c): | Mycelial growth of Ganoderma spp., on the 7th day after inoculated on PDA. The Ganoderma collected from, (a) Forest trees in Bukit Duabelas (BF) and Harapan (HF), (b) Oil palm trees in Bukit Duabelas (BO) and Harapan (HO) and (c) Rubber trees in Bukit Duabelas (BR) and Harapan (HR) |
| Data show Mean±SD (n = 3), alphabets represented that they are statistically significant then each other | |
| Fig. 5: | Rot disease incidence caused by Ganoderma in oil palm seedlings |
| Three Ganoderma used to virulence tests were representing the origin plot (Ganoderma BF1 from the forest, BO1 from oil palm and BR1 from the rubber trees), mean (n = 15) | |
| Fig. 6: | Rot disease in oil palm infected by Ganoderma |
| The basidiocarp of Ganoderma appeared on the soil after the oil palm seedling dead | |
DISCUSSION
Ganoderma, a fungal genus belonging to the Ganodermataceae family and Polyporales order, is a plant-pathogenic species in this genus that can cause severe diseases (stem, butt and root rots). As plant pathogens, Ganoderma spp., have been studied since it kills trees and other woody species valued for their products (wood, seeds, gum, fragrances, bioactive compounds) and their ecological importance21,22. The plant infected by Ganoderma through roots in the soil by vegetative spread15 and enters the plant cells by spores23.
A mass high throughput sequencing has been done1 and Ganoderma was detected enriched in rain forest compared to a monospecific plantation of oil palm and rubber. At the same study sites, it was found higher disease rot incidence and severity caused by Ganoderma in the forest. Ganoderma has a broad host range as a generalist woody plant pathogen24. The spread of the rot disease explained traditionally by a root contact between infected tree root to surround oil palm25. This fact tends to be a possible way of the spread of the disease in the current study. Tropical rain forests are grown with dense vegetation and shrubs in between. The humidity that is maintained throughout the year is suitable for Ganoderma to have a long-term host. The airborne dispersal by spores might also be the case since wind, rain and insect are potential vectors26,27. Unlike forests, oil palm and rubber plantations very common fertilized and fungicide by the farmers in Sumatra. It could be the reason the low incidence of rot disease on those sites compared to forests.
The mycelial growth of Ganoderma on PDA showed not similar rate. The previous study reported that the growth rate Ganoderma on various substrates. The growth of Ganoderma on media has been tested different culture conditions and found optimum temperature, carbon and nitrogen sources for the growth of Ganoderma28. Different carbon-nitrogen sources for the substrate of Ganoderma also has been observed29. Dextrin, galactose and fructose were favorable carbon. Ammonium acetate, glycine, arginine and calcium nitrate were the most preferred nitrogen for Ganoderma growth. This study, however, did not assess substrate content since PDA in the same condition was used. Therefore, the different growth of Ganoderma hypothetically affected by different fungal ability in utilizing the same substrate.
Interestingly, Ganoderma collected from forest did not infect the oil palm seedlings until ten weeks after inoculation, while Ganoderma from rubber plantation infected the seedling very slow. Ganoderma boninense has been reported as the most invasive Ganoderma against oil palm in East Asian countries30. Other Ganoderma spp., were harmful to many woody plants. Ganoderma is a degrading wood fungus with its ability to lignify31. Plantation areas or other tree ecosystems are susceptible to this fungus. This study shows a fundamental data about woody plant damage in different land-uses caused by Ganoderma. This result can be essential information to stakeholders to develop recommendations for controlling the rot disease.
CONCLUSION
Overall, this study showed that Ganoderma is a wide range pathogen that potentially degraded woody trees in different land-uses. Although the mycelial of Ganoderma showed differ rapid growth, which may have related to the virulence, Ganoderma from forest and rubber trees performs less virulence to oil palm trees.
SIGNIFICANCE STATEMENT
From the results of this study it was discovered that rot disease by Ganoderma spread in different land-uses of forest, oil palm plantation and rubber plantation. The growth rate of Ganoderma collected was determined. Interestingly, Ganoderma from forest and rubber trees were not harmful as Ganoderma from oil palm when tested in oil palm seedlings. The results of this study contributes to design disease control strategies. On that basis, this study has provided accurate
baseline data on the distribution of rot disease by the land use change. Currently, these data are not available by the relevant authorities in Jambi where the study conducted. These data will also be a national reference to estimate yield losses of palm oil and rubber production caused by Ganoderma. In addition, it also improving the register of Ganoderma in National databases related varying virulence, which is important for practical management advice in the long term.
ACKNOWLEDGMENT
We thank the Minister of Research and the Higher Education Republic of Indonesia (Contract Number: 097/SP2H/LT/DPRM/2018) to provide funding for this study. We also thank the Access Benefit Sharing (ABS) program of CRC 990 subproject B07 to partially funded this study.