Fusarium Wilt of Banana: Current Knowledge on Epidemiology and Research Needs Toward Sustainable Disease Management

Abstract

Banana production is seriously threatened by Fusarium wilt (FW), a disease caused by the soil-borne fungus Fusarium oxysporum f. sp. cubense (Foc). In the mid-twentieth century FW, also known as "Panama disease", wiped out the Gros Michel banana industry in Central America. The devastation caused by Foc race 1 was mitigated by a shift to resistant Cavendish cultivars, which are currently the source of 99% of banana exports. However, a new strain of Foc, the tropical race 4 (TR4), attacks Cavendish clones and a diverse range of other banana varieties. Foc TR4 has been restricted to East and parts of Southeast Asia for more than 20 years, but since 2010 the disease has spread westward into five additional countries in Southeast and South Asia (Vietnam, Laos, Myanmar, India, and Pakistan) and at the transcontinental level into the Middle East (Oman, Jordan, Lebanon, and Israel) and Africa (Mozambique). The spread of Foc TR4 is of great concern due to the limited knowledge about key aspects of disease epidemiology and the lack of effective management models, including resistant varieties and soil management approaches. In this review we summarize the current knowledge on the epidemiology of FW of banana, highlighting knowledge gaps in pathogen survival and dispersal, factors driving disease intensity, soil and plant microbiome and the dynamics of the disease. Comparisons with FW in other crops were also made to indicate possible differences and commonalities. Our current understanding of the role of main biotic and abiotic factors on disease intensity is reviewed, highlighting research needs and futures directions. Finally, a set of practices and their impact on disease intensity are discussed and proposed as an integrative management approach that could eventually be used by a range of users, including plant protection organizations, researchers, extension workers and growers.

Keywords: Fusarium oxysporum f. sp. cubense; Musa spp; epidemiology; integrated pest management; panama disease.

Figure 1

Global distribution of races of Fusarium oxysporum f. sp. cubense (Foc), causal agent of Fusarium wilt of banana. This map considers producing countries with presence or absence of a given race of Foc and does not represent banana-producing areas by countries. R1: Race 1, R2: Race 2, TR4: Tropical race 4. Races 1 (R1) and 2 (R2) are widely distributed in banana producing countries affecting local varieties (see introduction for more details). Subtropical race 4 was not included as it corresponds to Foc populations present in subtropical producing areas in Australia, Brazil, Canary Islands, China, South Africa and Taiwan, causing intermittent yield losses in Cavendish cultivars. For more information on the distribution of TR4 see http://www.promusa.org/Tropical+race+4+-+TR4#Distribution.

Figure 2

Life cycle of Fusarium oxysporum f. sp. cubense (Foc) in banana. (A) Spores (micro and macro conidia and chlamydospores) rest in the soil or on alternative hosts such as weeds. (B) Chlamydospores germinate stimulated by root exudates and the germ-tubes penetrate banana roots. (C) Foc grows through the cortex to the epidermis and mycelium invades the vascular system. (D) Conidia and chlamydospores are constantly produced in the vascular tissues. Conidia are rapidly distributed through the plant via transpiration system. Mycelium and gum blocks the vascular tissues and first symptoms of yellowing are observed in the older leaves. (E) Foc colonizes and destroys more vascular tissues provoking intense wilting. (F) Infected plant dies and the follower plant (daughter), which was contaminated by the mother plant through vascular connection, shows initial symptoms. Mother plant eventually falls down and disease cycle starts again.

Figure 3

Factors associated to pathogen spreading in Fusarium wilt epidemics in bananas. First incursion (upper left). Vehicles (middle). Planting material (upper right). Animals (upper left). Workers (bottom left). Water (in blue). These factors may operate separately or in association to disperse Fusarium oxysporum f. sp. cubense structures short or long distances.

Figure 4

Diagrammatic representation of four different scenarios of Fusarium wilt occurrence in a banana plantation. (A) The disease is not present. (B) The disease is a quarantine pest and the first incursion was detected. (C) The disease is established, but with a patchy distribution and low levels of incidence. (D) The disease is evenly distributed at high levels of incidence.