The Banana and Its Disease

Among fruit in the United States, bananas are top banana. Americans ate an average of 28.22 pounds of bananas in 2018—that's 80 bananas for each person—and a survey found that more people had bought bananas than any other fruit within the prior 12 months. Despite their popularity, the inexpensive snack (prices have remained at an average of $0.57 for the past 48 months) is under attack: a fungal disease is threatening to eliminate our favorite fruit.

This isn't the first time bananas have come under microbial siege. In the 1960s, bananas were under attack from banana wilt disease. That same disease is now threatening the Cavendish variety bananas, just as it did the then-popular Gros Michel banana variety. In that case, the fungus won, essentially eliminating the Gros Michel and forcing banana farmers to switch to a new variety. The Cavendish became the major banana variety when neither scientists nor farmers could halt the spread of or cure Gros Michel banana trees sick with the disease; the Cavendish variety has a natural resistance to the banana wilt disease of the Gros Michel variety. Cavendish now comprise up to 40% of global banana production.

Fusarium wilt disease (also called Banana wilt or Panama disease) is caused by the fungal plant pathogen Fusarium oxysporum f.sp. cubense (FOC). FOC is further divided into different lineages, called races, which are determined by the variety of banana each group can infect; FOC race 1 ravaged the Gros Michel bananas. Cavendish banana plants are resistant to FOC race 1 and for decades were able to thrive in the same soils in which Gros Michel had previously been grown. However, Cavendish bananas are now being threatened by a relative newcomer: FOC tropical race 4.

The FOC tropical race 4 (FOC TR4), a subcategory of FOC race 4, is the most destructive of these groups of fungi by several metrics. It has the widest range of banana variety hosts that it can infect, and it can be found in a wide range of temperatures and climates. Once TR4 emerged in the 1990s, cases quickly sprang up in regions such as southeast Asia, Oceania and the Middle East, demonstrating the ability of the fungus to grow in any conditions that the banana plant can.

Fusarium fungi reside in the soil, where the fungus can access the roots of plants to initiate infection. Like many fungi, it exhibits many cell morphologies, and Fusarium chlamydospores are a dormant form of the fungus that can subsist until the presence of plant root exudates induces germination to a vegetative state. These dormant spores are thought to persist up to 30 years, which can lead to contaminated soils unable to sustain susceptible plant crops for decades.

Within 10 days of planting, a banana tree in infected soil will have its roots colonized with chlamydospores and hyphal cells found among the root hairs. The fungus makes its way through the vascular system, eventually infecting the leaves and causing them to yellow and decay. The entire plant will succumb to its infection within months of disease onset. Due to the spread of FOC TR4, the Cavendish is now in the same danger as its Gros Michel predecessor. The disease threatens bananas that are snack foods in the United States, but are vital sources of nutrients in the regions where they are grown, which consume 85% of the bananas produced.

There are many banana varieties in the world, and you might expect the genetic diversity within the banana species to be an advantage that produces fungal resistance. But few bananas have all the characteristics that allow for worldwide distribution: thick skin to prevent bruising, growth in large numbers within tight bunches, ability to grow in varied climates, a flavor and texture that appeal to people all over the world and the ability to withstand days or weeks of shipping. The Cavendish carries these traits (though it doesn’t ship as well as the Gros Michel), and because of its near-singular perfection, farmers grow it in monoculture.

To grow new trees, the farmer takes the bottom of an old tree, the part known as the rhizome, and cuts it into many smaller pieces. The rhizome is the below-ground plant stem that sends out roots and shoots. When separated from the original tree, pieces of the rhizome will grow into new seedlings that can be harvested and planted in orchards. Each Cavendish tree is therefore derived from its parent and carries the same genetic material, creating a near-clonal population.

In 2017, scientists published that they had successfully created a genetically modified Cavendish variety that is resistant to FOC TR4, and that additional genetic-modification tools may help address plant vulnerability to this problem. No commercially resistant banana strain is yet available, but FOC TR4 is extremely widespread. Previously thought to be confined to southeast Asia and Australia, the first cases in the Middle East were reported in 2013. The first identified case in Colombia in August 2019 means the disease is now in Latin America, the world’s largest banana-producing region, and new countries continue to report infections. Multiple means of fighting infection are the best bet for success. Some scientists think a different approach will address the ability of plants to grow in FOC-infected soils: manipulating the other soil microbes around the fungus.

Rhizospheres and Microbiomes

Like animals, plants have a microbiome, and the composition of this microbiome varies in different parts of the plant: the leaf microbiome has different microbial members than the stem microbiome. The rhizosphere microorganisms (microbes directly surrounding the rhizome) are a part of this plant microbiome. The roots release exudates into the soil directly surrounding them, which encourage microbial growth in the immediate proximity of the plant. These fungi and bacteria play important roles in plant health, such as producing phytohormones that regulate plant metabolism and defense systems, and they occupy space that might otherwise be available to a plant pathogen.

The importance of the rhizosphere in plant health goes back to the early days of microbiology, when agricultural botanist Lorenz Hiltner recognized that Rhizobium inoculants improved nitrogen acquisition in crop legumes. Hiltner focused his research efforts on the rhizosphere and soil microbiology in the early 1900s and went so far as to hypothesize that "the resistance of plants towards pathogenesis is dependent on the composition of the rhizosphere microflora," though he worked most famously on warding off seed phytopathogens. Nevertheless, the idea was planted.

Soil microbiomes are regularly manipulated to benefit healthy growth, but often this involves providing additional nutrients, such as nitrogen. Brazilian microbiologist Johanna Döbereiner spent her life studying nitrogen fixation, and when Brazil ramped up soybean production to become the primary soybean producer in South America, it did so using largely microbial nitrogen sourcing, rather than the chemical fertilizers preferred by farmers in the United States. By discovering new nitrogen-fixing bacteria, Döbereiner's research allowed some sugar cane (Brazil's top export) to obtain 60% of its nitrogen via microbial means. Large-scale soil microbial manipulation for improved plant health is therefore feasible.

Can the Rhizosphere Be Manipulated to Ward off Plant Pathogens?

Many lab-scale experiments show promise when a variety of natural and genetically engineered plant pathogens are tested for this purpose. Microbes use many mechanisms to kill or inhibit other microbes, especially in nutrient-limited environments like soil, and these mechanisms can be hijacked by people to protect crops. The question is always whether these results can be replicated at the necessary scale.

For example, the oomycete Phytophthora infestans is a major pathogen of many plants. The soil bacterium Streptomyces is well-known for secreting antimicrobial compounds, and some of these act against plant pathogens like P. infestans. By isolating and characterizing Streptomyces from many sources, strains that are more potent against crop pathogens can be identified and used by farmers as part of a "green manure"—a mix of microbes that provides nutrients, growth stimulation and prevents disease in place of chemical means. This practice has successfully reduced Phytophthora root rot on alfalfa, among other diseases.

This worked for the oomycete pathogen, but what about antifungal activity that would be necessary to treat FOC TR4 infection?

Banana Microbiome Manipulation

Altering the soil microbiome with a biological agent of control has been a goal of plant pathologists studying plant infectious disease since the 1970s, when the protective role of some microbial species became popularly studied. Biological agents of control act as probiotics to the rhizosphere by promoting plant health through the direct inhibition of plant pathogens. Several microorganisms have moderate success when applied to banana plants in field experiments, including Pseudomonas, Trichoderma, Bacillus and non-pathogenic Fusarium species, which when used aim to titrate out the pathogenic Fusarium by competing directly for the same nutrients and niches.

Pseudomonas species such as P. fluorescens Pf1 have been successfully applied as biocontrol agents against Fusarium wilt of chickpeas and Fusarium wilt of tomatoes, though these diseases are caused by different lineages of F. oxysporum. Several studies have suggested that P. fluorescens Pf1 is one of the strongest inhibitors of FOC TR4, but field studies using a mixture of Pseudomonas strains have been most successful in inhibiting experimental disease.

P. fluorescence is a bacterial endophyte, which are part of the internal microbiota of the plant. All plants have signature bacterial and fungal endophytes, which differ based on plant species, environmental conditions and niche within the plant. Though they exist inside the plant, endophytes access internal structures from the roots, which means the first plant/endophyte interactions occur below ground, the same as initial Fusarium/plant interactions. The presence of P. fluorescens Pf1 within banana plants is enough to double the phenolic content within treated plants, as well as induce expression of plant genes like peroxidase and chitinase that act as antifungal defenses; both have been proposed to explain the protective effect of this strain.

More recently, other bacterial species have been tested in tandem with P. fluorescens Pf1 to better decrease Fusarium infection. Field experiments combining Pf1 with 2 Bacillus subtilis strains decreased disease nearly 80% compared to untreated controls. In their experiments, Kavino and Manoranjitham inoculated the seedlings in a greenhouse to allow establishment of the microbial consortium, before moving the plants to the field. Changes in farming practices, in addition to multipronged beneficial microbial applications, may be necessary to treat infected soils.

Several studies suggest that additional practices, such as crop rotation, could influence the soil microbes present to influence Fusarium growth in local soil. The successive monoculture of banana plants was associated with an increase of Fusarium incidence, which also correlated with a higher fungal richness within the soil. Rotating crops can decrease the soil fungal population: 2-year cycles of pineapples rotated with bananas decreased both FOC TR4 abundance in the soil and disease incidence relative to non-rotated bananas or bananas rotated with maize. Successfully fighting Fusarium wilt may require both microbial treatments and changed behaviors.

Many aphorisms that hold true for human infectious diseases also hold true for plant infectious diseases. A pound of prevention remains worth an ounce of cure: treating the microbiome works best if the beneficial microbes are present before the fungus attacks. But how can the bacteria be added to the plant rhizosphere? There are as many formulations for plant therapeutic deliveries as there are for animal therapeutic deliveries. Though powder and capsule formulations have specific purposes, liquid applications can inoculate beneficial microbes into the rhizome pieces used for propagation and can also be applied to seedlings after planting. Liquid disseminates beneficial microbes, but it can also spread the fungus, so applications must be carefully considered before use.

Many other microorganisms are also under study for use in fighting FOC TR4 infection. These microbial solutions are often multipurpose: some microbes, such as the fungal endophyte Trichoderma, show promise in fighting both Fusarium wilt and Black Sigatoka, another infectious disease of bananas. The ability to fight multiple infectious diseases, plus the ability to promote plant growth through phytohormone production, has created a strong incentive for scientists and banana producers to develop robust and accessible microbial solutions for banana infectious disease problems.

Ecological, economic and societal hurdles remain to be crossed before Fusarium wilt will be reined in, but the scientific and producer communities are galvanized. The Food and Agriculture Organization of the United Nations has convened a Fusarium TR4 Task Force and provides a TR4 Global Network for educational and research resources. Gert Kema, Ph.D., whose lab at Wageningen University in the Netherlands confirmed the Colombian Fusarium isolate, spoke at the 2018 International Congress of Plant Pathology, where he said:

“It is clear that we never should underestimate the threat of Panama disease. By continuously putting it on the agenda, we take our responsibility and realistically call for action. Rather than paper over the cracks and create false hopes, we generate new data and strategies for structural and overall banana improvement.”

Hopefully, the global focus on Fusarium wilt can provide a solution to save the Cavendish-variety banana before it goes the way of the Gros Michel.