Internal fruit rot (Fusarium spp.) in bell pepper: An integrated approach for a complex disease

In our current society, peppers (Capsicum spp.) play an important role in food, medical, ornamental and many other uses. Consumption is increasing, new uses are being discovered, and the interest of the general public for this crop seems insatiable. Belgian greenhouse pepper production is mainly focused on export and peppers are traded under the high-quality label of ‘Flandria’. From the beginning of this century the well-recognized high-quality is challenged by a common disease known as internal fruit rot (IFR), which is mainly caused by members of the Fusarium lactis species complex (FLASC) and to a lesser extent by F. oxysporum and F. proliferatum. Infection start via the flower but symptoms appear only at maturation and harvest. External symptoms such as sunken lesions, only appear at later stages, when the fruits already progressed through the supply chain towards the consumers resulting in rejection of entire lots of bell peppers by retailers. Due to this problem, the confidence in bell pepper growers is diminishing, and losing retail channels and buyers becomes a real threat with its financial consequences for growers.

Although IFR is a major threat for bell pepper production worldwide, only limited research has been conducted on the pathogen and how to control infection in a sustainable way. To regain retailers’ trust and reduce yield losses, a full comprehension of the plant-pathogen-environment interaction is inevitable in order to be able to develop sustainable control measures. Instead of focussing on a particular aspect of the disease, this PhD study explores a multidisciplinary approach to tackle an important detrimental disease.

As germination kinetics revealed that FLASC dominance could not be attributed to a faster germination time, the understanding the impact of environmental factors on the growth and sporulation of the pathogens (FLASC, F. oxysporum, F. proliferatum) should provide an integrated understanding of the respective ecological niches of these pathogens. All three pathogens share common growth and sporulation optima at 25 °C, 0.96 aw and normal atmosphere conditions. FLASC distinguishes itself by is tolerance of low acidic environments, showing significantly more growth and sporulation at pH 3 than F. oxysporum and F. proliferatum which favour pH levels of 4 and 5 respectively. Bell peppers are generally characterized by an acidic pH and acidity in peppers increases from about pH 5.5 to a 4.5 during ripening which is suitable for all three pathogens to grow. But as sucrose levels increase significantly during ripening of bell pepper and Fusarium spp. acidifies its ambient environment under high sucrose levels, it is possible that acidity further increases to levels whereby only FLASC could grow sufficient to cause the majority of IFR symptoms.

   Cultivar specificity of bell peppers towards IFR has been observed in both florescence and harvest stages in experimental and greenhouse conditions. This difference in IFR sensitivity could not be linked with flower morphology, such as coarser flowers, dehiscence stand of flower organs or fruit load. A bio-assay to quickly assess cultivars’ sensitivity towards IFR was used and relays on pin-inoculation of fruits with FLASC mycelium. Sensitive cultivars developed larger lesions in the mature, coloured stage then less-sensitive cultivars; which proved to be consistent with the observed results of the greenhouse trials. Although IFR was rarely observed in green, immature fruits; the bio-assay showed that these fruits are highly resistible towards mycelial growth of FLASC. During fruit ripening, a plethora of significant changes of sugars, organic acids, amino acids and phenols occur. Hence, an in vitro microplate assay was developed to assess the influence of changing concentrations of metabolites on FLASC germination and growth during ripening of fruits. Based on the microplate assay data, it can be postulated suppression of FLASC growth by high concentrations of the flavonoid quercetin (40 - 400 µg g-1 fwt), which is abundantly present in green fruits but diminishes during ripening, can also underlie the resistance of green bell peppers towards IFR. Moreover, the unsuitable ambient pH and potential unavailability of nutrients (e.g. amino acids, sugars,…) can state the high resistibility of green bell pepper fruits towards IFR.  

In order to obtain an integrated, sustainable approach, this PhD study also focussed on both pre- and post-harvest measures to tackle IFR infection. In vitro selection and greenhouse trials provided two potential biocontrol agents of the genus Gliocladium roseum which effectively reduced IFR infections with 30 % after flower application. To reduce losses due to fungal deterioration caused by the latent infections of internal fruit rot even after pre-harvest measures, equilibrium modified atmosphere packaging (EMAP) was tested to suppress the pathogen. Besides positive effects on fruit quality parameters such as weight loss, fruit firmness, colour, vitamin C content, total titrable acidity and brix values; EMAP stored fruits showed significantly lesser fruits with severe symptoms of IFR than fruits stored under atmospheric conditions.

Finally, recommendations are presented ,encompassing the whole bell pepper production chain from breeders toward retailers, to tackle the internal fruit rot problem in an integrated, sustainable way.