Disease suppressiveness to Fusarium wilt of banana in an agroforestry system: Influence of soil characteristics and plant community

Highlights

• Fusarium oxysporum f. sp. cubense race 1 constrains the cultivation of banana cv. Maçã.

• Fusarium wilt was variable on cv. Maçã grown in an agroforestry system in Brazil.

• On the farm, patches with different level of Fusarium wilt suppression were found.

• The suppressive patches had a lower density of the susceptible cv. Maçã.

• A higher diversity of banana cultivars was found in the suppressive patches.

Abstract

One of the most destructive diseases of banana is Fusarium wilt or Panama disease, caused by the soilborne fungus Fusarium oxysporum f. sp. cubense (Foc). Foc is widespread in almost all banana-growing areas and cannot be effectively controlled by chemical or biological measures. Fusarium wilt could potentially be managed by the promotion of soil disease suppressiveness, but little is known how soils attain a higher level of disease suppression and how crop management can impact on this. Banana cultivar (cv.) Maçã, a cultivar highly susceptible to Foc race 1, was grown on a farm managed as agroforestry system in Pedra Dourada, Brazil, where Foc race 1 is present in soil. At some locations on the farm banana plants of cv. Maçã stayed productive, while on others it succumbed rapidly. We hypothesized that the differences in disease severity on the farm could be attributed to different levels of soil disease suppressiveness. In this study, we assessed the level of disease suppression of the different locations and elucidated potential factors that could promote disease suppression in soil. Patches with confirmed presence of Foc race 1 were sampled and tested for Fusarium wilt suppression in greenhouse assays. The plant community composition, soil abiotic properties and soil microbial community of the different locations were compared. Locations with a higher level of disease suppression were characterized by a low density of the susceptible cv. Maçã, a high diversity of other banana varieties, a higher clay content, higher pH and lower soil cover by graminoids. Banana cv. Ouro was only present in the three most suppressive patches. The results of this study suggest that in soils with favorable abiotic properties, a good plant arrangement, in which cv. Maçã is grown in mixed stands with other banana varieties, can help to promote Fusarium wilt suppression.

Introduction

In tropical regions, banana is of high socioeconomic importance, since it is a cash crop in export-oriented plantations, and a food- and cash crop on smallholder farms. Banana is a robust crop with high returns on input, but production of certain cultivars is often restrained by Panama disease (Fusarium wilt), a wilt disease caused by the soil-borne fungus Fusarium oxysporum f.sp. cubense (Foc) (de Oliveira e Silva et al., 2001). Since Foc can produce long-term survival structures, the chlamydospores, or survives as a saprophyte on non-host plant, it is virtually impossible to get rid of the pathogen once the soil is infested. Foc is disseminated via contaminated soil on wheels and shoes, contaminated tools, runoff and irrigation water, latently infected planting material and insects (Meldrum et al., 2013, Ploetz, 2015). Foc levels in soil cannot reliably be monitored as the pathogen is not morphologically distinguishable from non-pathogenic F. oxysporum, and molecular detection methods are still in development (Dita et al., 2010, Peng et al., 2014).

Based on pathogenicity to specific cultivars, Foc has been subdivided into four races, three of which are of economic importance. Cultivars of the groups Gros Michel (AAA) and Silk (AAB) are susceptible to race 1, while cooking bananas, such as Silver Bluggoe (ABB), are susceptible to race 2. Race 4 can affect cultivars of the Cavendish subgroup (AAA) and all cultivars susceptible to race 1 and 2. Race 4 is subdivided in a subtropical (ST4) and tropical (TR4) race 4 depending on the climatic condition in which it can affect Cavendish cultivars. In contrast to Foc race 1, which has been reported in almost all banana growing regions, race 4 is mainly limited to South-East-Asia and Australia, but has recently been observed in Jordan, Pakistan, Lebanon, Mozambique and Oman (Dita et al., 2010, Ordonez et al., 2015, Ploetz, 1990). In export-oriented plantations the problem with Foc race 1, which devastated great areas in the first half of the 20th century, was solved by a shift from the susceptible cultivar Gros Michel to cultivars of the resistant subgroup Cavendish. However, Foc race 1 remains an important challenge in countries such as Brazil, where bananas are mainly grown for local consumption (Borges and da Silva Souza, 2004, Ploetz, 1990).

In Brazil, 96.6% of the total banana production is sold on local markets (Borges and da Silva Souza, 2004), which are dominated by AAB cultivars, which differ widely in their susceptibility to Foc race 1 (Table 1). The area planted with cv. Maçã has decreased due to its high susceptibility to Foc race 1, but this cultivar is very profitable because it is preferred by consumers (Moreira, 1999; personal communication Cândido da Silva). In addition, varieties of the Cavendish subgroup and many cultivars of minor importance, which are in general resistant to Foc race 1, are cultivated (Table 1, Embrapa, 2009).

In susceptible cultivars, Foc is difficult to control since fungicide application is ineffective and uneconomical, and biological control has no proven efficacy in the field (Ploetz, 2015). However, some soils have the potential to suppress Fusarium wilt in spite of the presence of a virulent pathogen (Abadie et al., 1997, Baker and Cook, 1974). Those soils are found worldwide for a number of crops, including banana (Alabouvette, 1986, Alabouvette, 1999, Domínguez et al., 2001, Larkin et al., 1993, Nel et al., 2006, Peng et al., 1999, Scher and Baker, 1980). The capacity of a soil to suppress diseases is ranging along a continuum from highly conducive to suppressive (Amir and Alaboucette, 1993, Janvier et al., 2007). Soil microorganisms play key roles in suppressing soil borne diseases mainly via antagonism or competition. Plants, soil type and microbial interactions are believed to be the main driving forces of the microbial community in soil (Broeckling et al., 2008, Grayston et al., 1998, Wieland et al., 2001) and can thus influence its disease suppressive potential (Garbeva et al., 2004, Janvier et al., 2007, Kinkel et al., 2011).

In Pedra Dourado, Brazil, a farmer observed that banana cv. Maçã (Subgroup Silk, AAB) succumbed to Fusarium wilt on certain locations of his farm, while on others it stayed productive. The farm is managed as an agroforestry system with very diverse plant arrangements. We hypothesized that the variation of disease expression on the farm was due to different degrees of disease suppressiveness in soil. The objective of this study was to assess the disease suppression in the different locations and to identify essential soil and plant community factors that contribute to disease suppressiveness. Knowledge about these factors can lead to optimized crop management strategies that enhance the disease suppressive potential of soils.