Reviews in Agricultural Science
Online ISSN : 2187-090X
Panama Disease of Banana, Identification, Epidemiology and Management: The Indonesian Experience
Arif WibowoAni WidiastutiSiwi IndartiAdy B. PrakosoSiti SubandiyahChristanti Sumardiyono
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2025 Volume 13 Issue 3 Pages 92-104

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Abstract

Bananas are one of the five most important food commodities in the world. In Indonesia, banana production is mostly for domestic consumption, featuring a wide variety of cultivars. In contrast, the global market is dominated by a single cultivar, largely supplied by the world’s biggest banana exporter, Ecuador, followed by Guatemala and Costa Rica. Initially, the global banana market depended on a single cultivar, Gros Michel, for around 60 years, but the first outbreak of Panama disease (race 1 of Fusarium oxysporum f. sp. cubense) led to its destruction. More recently, the Cavendish, which is the global banana clone, was ravaged by the second pandemic of Panama disease caused by Fusarium oxysporum f. sp. cubense Tropical Race 4. This problem severely impacted Indonesia’s banana industries; however, a few national banana industries have survived and have expanded their planting area over the past five years. This review will discuss the identification, ecology, and interaction of the pathogen and the host plant, epidemiology, and management of Panama disease in Indonesia. While Gros Michel, Cavendish, and other banana cultivars are easily found at local markets in Indonesia, the spread of Panama disease of Fusarium oxysporum f. sp. cubense Tropical Race 4 began pandemically 20 years ago, and this section discusses the pandemic epidemiology of the disease. Different identification tools were applied, and diversity of Fusarium oxysporum f. sp. cubense Tropical Race 4 was found in Indonesia. Panama disease management in Indonesia varies based on the local wisdom of the farmer groups or the industry. However, in response to the outbreaks, in 2002, the Indonesian government formed the National Task Force for Banana Wilt Disease Management under the Directorate of Horticultural Plant Protection in the Indonesian Department of Agriculture during the pandemic period of banana wilts, including Fusarium oxysporum f. sp. cubense Tropical Race 4 and banana blood disease.

1. Introduction

Bananas in Indonesia are primarily grown traditionally on smallholder farms with plots of less than 0.5 hectares in backyards, home gardens, or fields, with clusters ranging from a few to hundreds of plants. Some banana industries occupy thousands of hectares in Sumatra and Java. Among fruits, bananas have the highest production, reaching approximately 8.7 million tons in 2021 and increasing annually to around 9.3 million tons in 2023, surpassing tangerines at 2.8 million tons and mangoes at roughly 3.3 million tons that year. Banana production centers in Indonesia with more than 1 million tons per year are in the provinces of East Java, Lampung, and West Java, with production at about 2.2, 1.3, and 1,2 million tons respectively in 2022 [1].

Domestic banana demand is high and the business is highly profitable in Indonesia, resulting in limited banana exports. The economic analysis of smallholder banana farms in Deli Serdang, North Sumatra reported by Simatupang et al. [2] found a Revenue-Cost Ratio (R/C) of 1.1 for the Panama disease-susceptible cultivar Barangan, compared to 2.03 for the more resistant cooking banana cultivar Kepok [3]. A similar report was found on the cultivation of Gros Michel at smallholder farms located about 120 km from the capital of West Java with an R/C value of 1.57 per ha per planting season [4]. In Bireuen District, Aceh province, even though the cultivation of banana cv Barangan is susceptible to Panama disease, the economic value is high, with an R/C value of 5.07 [5].

Indonesia’s local banana markets are diverse, found in traditional village markets, small roadside stores in rural and urban areas, as well as modern markets in business centers. Farmers may sell the bunches of fruits individually directly by the family or through middle merchants who typically visit their farms regularly. Middle merchants may be graded in their business level from small operators in traditional markets to large-scale suppliers for urban banana markets. Some banana industries, on the other hand, produce for modern markets and potentially for export when this is more profitable than domestic sales, typically applying improved cultivation and disease management practices.

Bananas grow easily throughout Indonesia, with many clusters thriving without cultivation in villages, along riverbanks, or in bushes, and often left unattended. These conditions may sustain sources of disease inoculum in the field. Do surviving banana clusters in endemic farms result from good Panama disease management, or do other factors contribute to disease suppression? This review discusses multiple aspects of Panama disease that may be useful to understand pathogen diversity, epidemiology, and disease management.

Panama disease has constrained banana production since its first reported outbreak in Java in 1916. While national economic loss data for banana production are not available, losses were reported during the 1993–1994 banana wilt pandemic. In Lampung, the banana loss was more than 20,000 ha, with a value of 1.2 million USD, and in Riau the value of the loss was 2.5–3 million USD. A major Cavendish industry in Halmahera was also wiped out by the disease and the company’s closure within a few years [6]. Banana exports in Indonesia increased from 1993, reaching the highest volume in 1996 at 100,000 tons, but dropped to about 70,000 tons in 1997–1999 and then collapsed to under 10,000 tons in 2000. Exports recovered slightly until 2013 while still below 5000 tons, and in 2022 went up to 21,000 tons. The problem was due to wilt diseases including Panama disease and Banana Blood Disease (BDB) attacking the global banana cultivar, Cavendish, and Barangan for export [1, 7].

The epidemic of Panama disease in Indonesia started in the early 1990s, but it took years to receive significant attention from the government. The Banana Wilt Disease Management Task Force was established in early 2000 when the disease had spread pandemically throughout the country. The members of the Task Force consisted of scientists, farmer leaders, banana business operators, and government officers. Task Force meetings were held annually, with the meeting location moving from one banana production center to another in different provinces. Focusing on progress reports and technology transfer to support local farmer groups in disease control. While the pandemic appears to be declining, the disease persists sporadically; meanwhile, banana production is improving for several different cultivars including Gros Michel, Mas, Raja Bulu, Kepok, and Cavendish.

2. Pathogen identification

In the smallholder farms, different cultivars of banana are planted in multiple lines or species, contrasting sharply with industrial monoculture plantations. Due to limited intensive cultivated banana industries, the isolates of Fusarium oxysporum f. sp. cubense (Foc) collected in Indonesia are obtained from different local cultivars. Pathogenicity tests on Cavendish or molecular identification using specific primers for TR4 are needed. Six isolates of Foc that originated from banana cv Gros Michel, Kepok (ABB), and Awak (ABB) were virulent to highly virulent on Cavendish, with the rhizome discoloration index (RDI) value ranging from 2.4–3.2 [8]. Foc in Indonesia is quite diverse and distributed throughout the country. Wibowo et al. [9] collected 47 isolates of Foc obtained from different varieties of banana, mostly from Java, with some others from Sumatra, Bangka, and Kalimantan. All of the isolates produced a volatile odor on the rice culture medium, indicating that the isolates were either race 1 or race 4 Foc [10, 11]. Furthermore, by using 20 tester isolates to identify the VCG of the isolates, it was found that three isolates belonged to race 1 with VCG of 0123, 0124 and 0126. One isolate was VCG 0129, and 11 isolates were the VCG of 01213/16. Further analysis of these VCG 1213/16 isolates was positive as FocTR4 using the primer pair of Bently et al. [12]. Two other isolates were matched with the VCG 120, while the other 32 isolates were not matched with any of the 20 tester isolates. Jumjunidang et al. [13] reported that four out of 30 isolates of Foc could not be assigned to the VCGs using available tester isolates. These incompatible isolates may have genetic diversity compared to the reported isolates with established VCGs. The VCG 1213/16 is assumed to be FocTR4, which is virulent on Cavendish. Eight isolates of VCG 1213/16 and two isolates of VCG 120 were all virulent on Cavendish and showed significantly different virulence on the banana cultivars. Furthermore, the study on the production and enzyme activities of the isolates suggested that all VCG 01213/16 produced polygalacturonase related to isoform glycosylated, non-glycosylated endopolygalacturonase with the protein bands of 35 and 37.5 kDa, and exopolygalacturonase of 66 kDa, whereas the VCG 120 isolates produced the other exopolygaracturonase of 74 kDa. The study on the activity of polygalacturonase enzymes related to virulence suggested that the isolates showed diversity in enzyme activity and in virulence level, but the low correlation coefficient between these two parameters suggested that besides polygalaturonase activity there was another factor(s) related to the pathogen virulence [14].

Pratama et al. [15] analyzed 50 Indonesian isolates of Foc; some of the isolates were previously used by Wibowo et al. [9] and collected at the Department of Entomology and Plant Pathology at UGM (Table 1). Using Foc-specific primers, FocEf3 [16], 48 isolates tested positive for Foc, followed by the identification using the specific primers for Foc Race 4 by Lin et al. [17], which resulted in 30 isolates that tested positive as FocR4 and 17 isolates that tested negative as FocR4. Further analysis used three different primer pairs specific for FocTR4: RFLP-specific fragment [12], IGS-specific fragment [18], and SIX1-c [16]. Several isolates testing negative for FocR4 with the primers of Lin et al. [17] showed positive results as FocTR4 with all applied FocTR4-specific primers [12, 16, 18], the isolates of Bnk-12, Bnk-25, and Kgj-2; one isolate (Kp-3) testing positive as FocTR4 by Bently et al. [12] and Dita et al. [18] primers; two isolates of Kdg-1 and Kd-2 testing positive for the primers of Dita et al. [18] and Widinugraheni et al. [16], and five isolates of Cms-1, Grt- 3, U-14, Kbr-1 and Kcr-1 testing positive for only Dita et al. [18] primers. The analysis suggests that the isolates negatively amplified by the specific primers of FocR4 may represent FocR1 or FocR2; however, further analysis revealed that the isolates were positively amplified using the primers of FocTR4, indicating these Foc isolates are potentially considered as a different group containing sequences specific to the three race groups. Some isolates positive for FocR4 primers of Lin et al. [17] were not detected by the primers of FocTR4, potentially considered as FocR4 Subtropic. Conversely, the primers of FocR4 of Lin et al. [17] failed to detect certain FocTR4 isolates, suggesting these may belong to other race groups. Trinitia et al. (2013) demonstrated that the VCG 0124/5 (race 1) isolates, whether alone, combined with VCG 0121 (race 4), or with VCG 01213/6 (TR4), could infect Cavendish, suggesting potential virulence enhancement in race 1 isolates toward Cavendish.

Table 1: Origin of Foc isolates, VCG, race, host cultivar and genotype [15]

No. Locality/provice Code VCG Race Host Cultivar Host Genome
1 Bangka Bnk-12 Nc Ambon AAA
2 Bnk-25 Nc Ambon AAA
3 Bdg-1 Nt Ambon AAA
4 Bdg-1A Nc Ambon AAA
5 Bdg-2 Nt Awak ABB
6 West Java Bjr-1 Nt Kepok ABB
7 Bjr-2 Nc Awak ABB
8 Cms-1 Nt Awak ABB
9 Cjr-1 Nt Ambon AAA
10 Cjr-2 Nt Kepok ABB
11 Grt-1 Nc Ambon AAA
12 Grt-2 Nt Awak ABB
13 Grt-3 Nc Ambon AAA
14 Tsk-1 Nt Awak ABB
15 Tsk-2 Nt Ambon AAA
16 Central Java Bgl-3 01213/16 TR4 Kepok ABB
17 Mnl-1 01213/16 TR4 Kepok kerau ABB
18 Pbn-1 Nt Ambon AAA
19 Prb-1 Nt Ambon AAA
20 Prb-2 Nt Ambon AAA
21 Sdt-1 Nc Ambon AAA
22 Skj-2 Nc Ambon AAA
23 Tmg-4 Nt Awak ABB
24 U-14 Nt Awak ABB
25 Kalimantan Kjg-2 nc Raja AAB
26 East Java Batu-2 Nt Kepok ABB
27 Batu-3 Nc Raja AAB
28 Batu-3B Nc Raja AAB
29 Batu-4 Nc Kepok ABB
30 Kbr-1 Nc Ambon AAA
31 Kdg-1 Nc Kepok ABB
32 Ksp-1 Nt Ambon AAA
33 Pjn-4 0129 R1 Raja AAB
34 Pjn-5 Nc Raja AAB
35 A-13 01213/16 TR4 Ambon AAA
36 Bnt-1 Nc Cavendish AAA
37 Bnt-2 01213/16 TR4 Awak ABB
38 Yogyakarta Btp-1 Nt Ambon AAA
39 Gnk-2 Nc Ambon AAA
40 Kd-2 Nt Awak ABB
41 Kp-1 Nc Ambon AAA
42 Kp-3 Nt Awak ABB
43 Kp-4 Nc Ambon AAA
44 Kp-H Nc Kepok ABB
45 Ktr-1 Nt Awak ABB
46 Slm-1 Nt Ambon AAA
47 Slm-3 Nt Awak ABB
48 Lampung Lmp-1 01213/16 TR4 Raja nangka AAB
49 Lmp-3 Nc Cavendish AAA
50 Lmp-4 Nt Cavendish AAA

Note: Nc: not compatible, Nt: Not tested

From the 50 isolates tested, 35 were grouped into TR4, which were positive against any TR4-specific primers used by Pratama et al. [15]. Figure 1 shows that some isolates were positive for the three different specific primer pairs of FocTR4, some others with two different primer pairs, and the rest were only positive by one pair of primers. These results indicate remarkable genetic diversity within FocTR4, evidenced by the diversity in IGS sequences and the effector gene of SIX1-c, since different isolates were amplified or were not amplified using those specific primers. Since the effector gene of SIX1-c is related to the virulence of FocTR4, those isolates amplified using the specific primer of SIX1-c by Widinugraheni et al. [16] should be harboring the gene related to the aggressiveness of FocTR4; however, some other isolates which were positive as FocTR4 using the IGS primers by Dita et al. [18] were not amplified using the primers of SIX1-c. Further research should investigate the infection performance rate of all of the isolates harboring the related sequence of SIX1-c gene on Cavendish with comparative analysis of negative isolates on the amplification using the primers of FocTR4. Trinita et al. [19] found that the Foc isolates including VCG 01213/16 of Foc TR4, VCG 0121 of Foc R4, and VCG 0124/5 of Foc R1 were able to infect Cavendish with 100% success via single or mixed inoculations, though incubation periods varied significantly according to the isolate inoculated, with the earliest incubation period of 5.95 days for the FocTR4 isolate and the latest incubation period of 17.45 days after the inoculation for FocR1 isolate.

The use of the molecular technique for identifying Indonesian FocTR4 isolates was done in 2010 by Masanto et al. [20] using the primer pair developed by Bently et al. [12]. It was suggested that Foc TR4 was found in Central Java on cv Awak and in East Kalimantan on cv Gros Michel. Rusli et al. [21] found that two Foc lyophilized isolates from UGM collected in mid-1999 from Banyuwangi, East Java were identified as TR4. Furthermore, Dita et al. [18], using their new primers for FocTR4 identification based on IGS region, found that the pathogen was found on cv Manurung. Maryani et al. [22] reported that FocTR4 has spread across the Indonesian islands. Maryani et al. [22] collected 203 Fusarium isolates from wilting bananas of 40 different local varieties across Indonesia, 183 of which were grouped into Fusarium oxysporum species complex (FOSC) based on the sequence of tef1, rpb1, and rpb2 genes which resulted in nine lineages. Among these FOSC isolates, 65% were pathogenic FocTR4 on Cavendish, clustering in lineage 1 and proposed as Fusarium odoratissimum N. Maryani, L. Lombard, Kema & Crous, sp. nov with the type isolate originating from cv Kepok in East Kalimantan. FocR1 was more diverse than FocTR4, and was distributed into several different lineages of 2, 3, 4, 5, 6 and 9.

Figure 1: Identification of FocTR4 Isolates using the primer pairs of Bently et al. [12], Dita et al. [18] and Widinugraheni et al. [16]. The figures in the circles and the intersections performance the isolates with positive results using the related primer pairs.

3. Ecology and epidemiology

Bananas grow throughout Indonesia under various conditions: as cultivated crops, as neglected clusters that were originally planted and then spread to neighboring lands (riverbanks or hillsides) without maintenance, or growing wild in remote areas due to being inedible. These neglected banana clusters are usually low-quality banana varieties, including Pisang Awak, Pisang Sajen, and Pisang Kapas, which are susceptible to Panama disease, especially Foc TR4. When Panama disease infects cultivated bananas, growers typically try to eradicate it or implement disease management. In contrast, infections in neglected or wild bananas often persist, serving as high-risk inoculum sources for other areas through surface runoff and irrigation systems or animals, people, agricultural machinery, or vehicles visiting the infected plants or the endemic land. During the rainy season, new endemic areas often develop when some banana plantations are flooded.

Some smallholder farmers use suckers from endemic areas to plant on other lands, often unaware that these planting materials pose high disease risks. In village smallholder farms, different banana cultivars are usually planted together with other plants or trees. The harvested fruits are transported to the traditional markets or collected by middlemen who cut and collect the fruits from farm to farm. Middlemen’s movement poses a high risk of spreading disease between farms and villages. Once infection occurs, it spreads to the neighboring areas. Nowadays, Panama disease appears sporadically, confirming that the inoculum sources for infection and spreading persist in the field.

In the intensive farms or banana industries, high-value banana cultivars are usually planted, including Cavendish, Gros Michel, Barangan, Rajabulu, and Mas. However, usually monoline or single-cultivar systems are adopted, and susceptible cultivars are planted. Even with implemented disease management, the disease control measures can only delay the spread, as plantations with susceptible cultivars face inevitable destruction within a few years due to the lack of effective control methods beyond resistant cultivars.

Sitepu et al. [23] reported that Foc infection is positively correlated with the infestation by Radopholus similis in North Sumatra. Root parasitic nematode infestation in banana plantations increases the likelihood of root wounds that promote the infection of Foc when the land is Foc endemic. The attack of plant parasitic nematodes on banana roots also increases the incidence of bacterial wilt diseases. Two or more species of plant parasitic nematodes can attack the same plant, thereby causing severely damaged roots to become susceptible to plant diseases [24]. Root damage in banana cv Kepok, including necrotic lesions and burrowings in the cortical tissue of the exoderm and endoderm, was found to be due to Pratylenchus spp. [24]. Pratylenchus spp. also dominated the banana plantations in Yogyakarta province with a population ranging from 348.2–2057.3 per 5 g banana root and 100 g of soil, and other nematodes, including Radopholus, Meloidogyne, and Haplolaimus, were also distributed in Yogyakarta on several banana cultivars.

As a soilborne pathogen, Foc ecology in the soil is affected by the population of other microbial communities that may be suppressing or supporting the development of the pathogen. Sudarma and Suparta [25] reported that the microbial density of soil without Foc is significantly higher than that with Foc, and the density of Foc in the soil without any banana wilt was much lower compared to that with banana wilt of Foc. Wibowo et al. [26] found that Foc-suppressive soil had higher labile carbon content, fluorescein diacetate hydrolysis (FDA), and β-glucosidase levels compared to conducive soil, reflecting greater microbial activity than the conducive soil in surveys conducted in Yogyakarta, Central Java, West Java, and Lampung (Sumatra). The rhizosphere microbial community is affected by the above-ground vegetation, suggesting that intercropping or rotational crops with bananas may engineer the microbial community in the banana rhizosphere. Wibowo et al. [27] found that banana intercropping with Allium spp. increases Foc suppressiveness. Chinese leek and shallot were able to suppress the incidence of Foc up to 40% and 33%, respectively. This suppression effect was also further observed through FDA analysis, revealing significantly reduced total microbial activity in the rhizosphere of banana intercropped with Allium spp. compared to the control treatment without intercropping. Furthermore, the observation of the effect of Allium spp. extracts on Foc showed that the development of the colony and spore germination of Foc in vitro was suppressed by the application of Allium spp. extracts. Pattison et al. [28] found that ground mix vegetation, including broad leaf grasses, green leaf desmodium, and pinto peanut, could suppress Foc development and increase Pisang Awak production through the increase in the activities of free nematode and microbial community. The vegetation effect on Foc development through the involvement of the microbial community is probably also established by the banana cultivar with different resistance against the pathogen. Sun et al. [29] found that the rhizosphere of the Foc-resistant banana cultivar Fj01 maintained a significantly larger bacterial populations and higher urease activity compared to the susceptible Baxi cultivar during growth. Therefore, interaction between ground cover vegetation, banana cultivar selection, and resident microbial communities may contribute significantly to Panama disease development.

4. Management

Foc chlamydospores persist long-term in soil [30], eradication of infected plants. However, the recommendation of glyphosate injection of 10 ml per infected plant was found to be the most effective method to eradicate and kill the fungal pathogen [31]. Eradication and land biosecurity may be applied better in banana industries, but it may be less possible to do in smallholder farm systems due to the complex agricultural social economics involved. Preventing pathogen introduction to disease-free areas may be possible, requiring global quarantine and monitoring.

No effective management exists for Panama disease other than using resistant cultivars. However, given the pathogen’s genetic diversity, the identity of the pathogen used to challenge the cultivar must be carefully selected, and field monitoring of pathogen identity and distribution is essential. The historical development of Gros Michel which was devastated by FocR1, and the success of Cavendish to replace Gros Michel for about a half century before the explosion of FocTR4, demonstrate that resistant cultivars offer the best solution – yet reliance on a single cultivar remains risky for sustainable production. Banana breeding for Foc resistance or genetic manipulation including genome editing needs to be advanced. Furthermore, multiple options of bananas with different performances, tastes, or flavors and functional food contents with different resistance against diseases may also be good for the consumers to choose from and offer better biosafety for production [32, 33].

Anna et al. [34] reported that Gros Michel originated from Jambi has different responses against various VCGs of Foc, resistant to Foc VCG 01219 and VCG 0120, moderately resistant to Foc VCG 0123, susceptible to Foc VCG 0121 and VCG 0124/5, and highly susceptible to Foc VCG 01213/16. On the other hand, using one isolate of FocR1 CPMF0801, Ribeiro et al. [35] found that there was genetic variability against Foc in Brazil. Several cultivated banana accessions and one of wild type banana M. acuminata var malaccensis were tested for resistance against Foc VCG 01213/16. Rejang diploid and tetraploid cultivars were resistant (DSI-RDI of 1), while M. acuminata var. malaccensis and Mas Jambe (AAAA) were moderately susceptible (DSI-RDI of 2). Cavendish and Madu were highly susceptible (DSI-RDI of 5) [36]. Mutation of banana seedlings in in vitro propagation using different concentrations of mutagenic agent was conducted by Saraswati et al. [37]. Different concentrations of EMS (ethyl methane sulfonate), NaN3 (sodium azide), and DES (diethyl sulfate) were applied to banana cv. Rasthali challenged using Foc cultural filtrate and Fusaric acid. The results suggested that three accessions survived the in vivo test using Foc VCG 0124/5 in the greenhouse. The mutation process resulted in three accessions of seedlings surviving against the pathogen inoculation. This technique is still possible to produce somatic or mutagenic variation to resistance against FocTR4.

Sumardiyono et al. [38] studied induced resistance in bananas using fusaric acid. In vitro-propagated Gros Michel plants were challenged on the media containing fusaric acid at the concentration of 1.165–9.32 ppm. Survivors were acclimatized, field-planted in Foc-infested soil, and monitored monthly for five months. Plants cultured in vitro with 1.165 ppm fusaric acid showed resistance to Foc infection with 0% wilting, undetectable salicylic acid, and only 0.23% tylosed xylem. Those treated with 9.32 ppm showed 50% wilting, 2 ppb salicylic acid, and 7.41% tylosed xylem. Untreated controls showed 52.38% wilting, no salicylic acid, and 6.25% tylosed xylem. Induced resistance against, whether through abiotic means or biotic agents, indicates further potential for field protection. However, the existing Foc race/strain in the related field should be well identified.

In Indonesia, the smallholder banana farms and the availability of different banana cultivars for cultivation which are favored by consumers help to sustain the value of bananas in the country. When Gros Michel was destroyed by FocR1, the distribution of the pathogen also spread across the country, but many banana cultivars are still easily found in traditional and modern markets in Indonesia. Smallholder farmers are usually aware of planting multiple cultivars. The global market, however, may require specific fruit performance for transportation, necessitating early selection and development of banana breeding and cultivar improvement.

During the pandemic of banana wilt disease(s) of Foc and blood disease (BDB), the National Task Force of Banana Wilt Management, consisting of farmer leaders, banana agribusinessmen, scientists, and policymakers nationwide, coordinated disease monitoring and documented local management for wider application in other districts or provinces. Most national farmer leaders have undergone Integrated Pest (including Disease) Management Field School, initially focused on rice and staple crops, later expanding to horticultural crops. Biological control using natural enemies and antagonistic microbes (Biological Control Agent or BCA) for managing pests and diseases has been established for farmers to conduct self-production of Trichoderma spp., Pseudomonas fluorescens, Gliocladium sp. produced by the Field Laboratories for Biological Control of Pest and Diseases which were in selected districts in every province. Therefore, the available BCA(s) in any area were recommended to be applied for managing banana wilt diseases.

Djatnika et al. [39] reported that Pseudomonas fluorescens and Gliocladium sp. suppressed Foc by approximately 68% in both greenhouse and field trials in Solok, West Sumatra compared to the control. Soesanto and Rahayuniati [40], using the extract of Foc-antagonistic P. fluorescens P32 and P60, promoted induced resistance of banana cv Rajabulu by postponing the incubation period up to 75–76 days after inoculation, suppressing the infection development in the corm at 26–32 %, and leaf infection development of 20–21%. On the other hand, Syalendra [41] reported that soil solarization and the application of Foc-antagonistic Bacillus in Bogor, West Java with single treatment or in combination could not successfully reduce the incidence of Foc either in the greenhouse or in the field. Sudarma [25] studied the effectiveness of Actinomycetes and it was found that the treatments of three different isolates of Streptomyces could suppress in vitro of Foc colonies from 72–79% andwas able to suppress Foc development on local varieties of bananas in Bali. Suciatmih et al. [42] found that the endophytic fungus Talaromyces sp. 27-4 (M) isolated from Cavendish with a low percentage of Foc infection in Lampung, produced volatile and nonvolatile substances that suppressed Foc development. This fungus may be further studied for biological control of FocTR4.

While BCA application against Foc development has inconsistent results, such as showing successful results only in specific locations, most of the experiments were conducted in a single experimental set. Wibowo et al. [26] found that in Foc-suppressive soil, both silica and manure applications could suppress the disease development; silica improved the host resistance, while the chicken manure increases microbial activity to suppress Foc. Conversely, in conducive soil, the application of silica and manure failed to control the disease development, potentially taking a longer period to overcome established Foc dominance in rhizosphere. Shen et al. [43] reported that consecutive biofertilizer applications over two years were needed to manipulate the rhizosphere for Foc suppression.

The induced resistance of bananas against Foc was studied by using biological agents and abiotic substances. Mycorrhiza inoculated banana seedlings cv Gros Michel show a longer incubation period of two weeks and lower disease intensity of 35–60%, compared to uninoculated seedlings at 80% [44]. Salicylic acid treatment at LC50 improved resistance to moderately resistant levels (LSI-RDI of 1.5–2.25) compared to highly susceptible controls (LSI-RDI of 2.75–4.25) [45]. Chemicals or fungicides may be used for suppressing the pathogen or promoting the host plant resistance. Kristiawati et al. (2014) found that phosphite acid and fosetyl-aluminum on the seedlings of banana cv Cavendish increased the resistance of the host plant against TR4, with the former better than the latter.

In Indonesia, where mostly smallholder farmers cultivate bananas, Panama disease management needs to be well coordinated. The government has established farmer groups (Kelompok Tani) in villages, each with 20–25 farmers and a leader. At the village level, 20 or more groups form a Gapoktan (Gabungan Kelompok Tani), a cooperative with 500+ members. Women’s farmer groups (Kelompok Wanita Tani or KWT) also exist. Networking among farmer groups, Gapoktan, and KWT is strengthened through meetings and IT connections. Agriculture extension officers support technical needs, linking stakeholders from village to national levels. Disease management is coordinated through the Banana Wilt Disease Management Task Force. Technology transfers are conducted via IPM Farmer Field Schools organized by local agricultural institutes (BPTP). In these programs, farmers are trained to produce BCAs and natural pesticides. Recommended technology for integrated management practices include:

  1. 1.   Eradication of infected plants by injecting herbicide into the pseudostem near the corm: 12 ml for mature plants, 2.5 ml for 4–5-month-old plants (~100 cm tall), and 1 ml for smaller plants. Herbicide may be replaced with carnosine (5–10 tbsp/plant). Injection is done 10–40 cm above the corm into the true stem. Burn infected plants and solarize the soil before replanting and BCA application.
  2. 2.   Manage infected soil by digging a canal around the area and filling it with rice husk charcoal.
  3. 3.   Replant infected spots with Foc-resistant cultivars: Rejang, Janten/Ketan, Muli, Tanduk, Raja Kinalun/Pisang Prancis, FHIA-25, and FHIA-17.
  4. 4.   Apply BCAs (Trichoderma, Pseudomonas fluorescens, Gliocladium) to planting holes and immersing the seedlings for a few hours before planting.
  5. 5.   Use suckers from healthy clusters in Foc-free areas; tissue-cultured seedlings are strongly recommended.
  6. 6.   Disinfect tools with sodium hypochlorite before use in each banana cluster.
  7. 7.   Repeat BCA applications with organic fertilizer during cultivation.
  8. 8.   Rotate crops with non-host plants after two to three harvests.

While farmer groups may adapt these recommendations, unmanaged banana farms in neglected areas remain disease-prone and serve as inoculum sources. Thus, even if cultivated bananas recover, disease distribution persists sporadically.

Few large-scale banana industries have operated in Indonesia since the Panama disease pandemic. Nusantara Tropical Farm (NTF) Ltd. in East Lampung survived despite losing 2,000 hectares to FocTR4, reducing its area to 400 ha. Through integrated management crop rotation with cassava, organic fertilizer from cassava waste, and microbial applications the company managed the disease and expanded cultivation. Today, the banana industry is part of Great Giant Food (GGF) Ltd., which rotates bananas and pineapples over 20,000 ha and successfully manages Panama disease for modern markets. In the Philippines, large banana industries blamed smallholder farms for spreading Panama disease. Agricultural socio-economic and political dynamics influence disease control possibilities, sometimes creating unfair conditions and constrained control options [46].

5. Conclusion

Panama disease has spread across the Indonesian archipelago, with the pathogen comprising FocR1, R4, and TR4 during the pandemic period over the past 20 years or more. Pathogen diversity was observed even within the TR4 race, suggesting varying levels of virulence on different banana cultivars. A wide range of banana cultivars and multiple banana lines with varying susceptibility are cultivated by smallholder farms. Integrated disease management, including the application of biological control agents (BCAs) and the empowerment of farmer groups, has helped maintain banana production for domestic consumption. The banana industry has survived by adapting to modern market demands through crop rotation with cassava or pineapple, thereby reducing the incidence and severity of the disease.

Acknowledgment

This article is supported by KNAW-SPIN JR034 Wageningen University and ACIAR HORT 2018/192.

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