Application of plant natural products for the management of postharvest diseases in fruits

The genus name Penicillium is located in the Ascomycota division of fungi (CABI, 2021a). Blue and green moulds, which are caused by the P. italicum and P. digitatum, respectively, have been considered as the most important pathogens which cause the highest economic postharvest losses in citrus fruits. These are wound pathogens, which can infect the fruits that are at the preharvest stage in the field and/or at the postharvest stage during handling, packaging or storage in cold rooms. P. digitatum is the first of the Penicillium species whose complete genome was entirely sequenced (Palou, 2014). Both of the species were reported to be a problem in many countries in the continents of Africa, Asia, Europe, North America, South America and Oceania (CABI, 2021a, 2021b).

Both of the fungi may enter into the fruits from the mechanical damages during harvest or handling and can spread from fruit to fruit. On the other hand, the stem end of the fruits is an important entry point for all Penicillium species (Ladeniya, 2008). The optimum temperatures are between 20 °C and 25 °C, where the growth of the fungi significantly slows below 5 °C or above 30 °C (El-Otmani et al., 2011). Besides their decay damages, both of these fungi produce quite an amount of ethylene and may cause rapid senescence of nearby fruits. P. italicum is more problematic for fruits since it can spread in the package. This fungus is a nesting-type; it produces enzymes and softens the nearby fruit. On the contrary, P. digitatum is not a nesting-type and it is difficult for it to infect adjacent fruits. Since it may infect the fruits during preharvest or postharvest, both orchard and pack house sanitation are significantly important. Benomyl, imazalil, propiconazole and thiabendazole are among the most used fungicides against Penicillium rots in citrus fruits (Ladeniya, 2008; Abo-Elyousr et al., 2021).

This is a necrotrophic (kills host cells and uses the nutrients for its own growth) and airborne fungus which is reported to affect many plant species, mostly pome fruits, stone fruits, grapes and berries, and attacking more than 200 crops (Williamson et al., 2007). It can cause soft rotting not only on the fruits, but also on the aerial plant parts, including vegetables. It mostly causes damage on the mature tissues of plants, but its entry into the host takes place during the early states when the tissues are young. Thus, the main damages caused by B. cinerea occur after harvest during storage (Abdel-Rahim and Abo-Elyousr, 2017). Besides, massive losses may occur in the fields, especially in greenhouse crops before harvest (Staats et al., 2007). The fungus has a diverse mode of attack and survival ability as conidia or mycelia. Because of these characteristics, a single measure alone cannot be effective in controlling this fungus. The symptoms of the fungus can vary widely, where soft rots together with collapse and water-soaked parenchyma tissues occur. This is generally followed by grey masses of conidia as the most common symptom (Williamson et al., 2007). These symptoms adversely impact the marketability of the products. Some of the active ingredients of the fungicides against B. cinereae are thiram, mancozeb and captan. However, recent studies suggest that there are some resistant genotypes against captan or others. Studies also suggest that dicarboximides are effective against B. cinerea while its target sites are both conidia and mycelium (Leroux, 2004). A broad-spectrum fungicide, strobilurin, has also been reported to be effective by inhibiting cytochrome b, while the other biosynthesis-inhibiting fungicide, fenhexamid, has also been reported to be effective. However, due to the problems of resistance, none of them could provide optimal efficacy (De Waard et al., 2006). Besides the chemical control, as for all other diseases, control of the environmental conditions could help to manage B. cinerea. It is well known that this fungus prefers high humidity, moderate temperature and reduced light. Therefore, management of these environmental conditions would help to improve crops’ and/or products’ resistance against the fungi. Several studies recommend that there are some other alternatives to fungicides, i.e. salts against B. cinerea (Youssef et al., 2019, 2020).

Alternaria spp. is a broad genus of fungi that includes several major plant pathogenic species. They are also known to grow indoors and cause some allergens on human beings. The spores of Alternaria spp. are airborne and have been commonly found on plant wastes, soil and water. The Alternaria spp. colonies can be in very different colours, including grey, green and black. According to Nowicki et al. (2012), Alternaria spp. is responsible for approximately 20% of the spoilage in horticultural crops, which may reach up to 80% in some conditions. However, it is also known that some of the Alternaria spp. are beneficial, while they can be used as biocontrol agents against some invasive weeds (Aschehoug et al., 2012). One of the most common species of Alternaria is the Alternaria alternata, which can asexually propagate from its spores, named conidia (Timmer et al., 2003). A. alternata is the main cause of black spots on harvested fruits, which develop during storage (under favourable conditions) and damage the marketability of the products. It is also the main cause of black rot in cherry tomatoes, fruit spot on apples, brown spot on mandarins, fruit rot on capsicum, black heart on pomegranate, stem-end rot on mango and late blight on pistachios (Troncoso-Rojas and Tiznado-Hernández, 2014; Kahramanoğlu et al., 2018). Besides the chemical treatments, heat treatment and natural plant-based products can be used (Troncoso-Rojas and Tiznado-Hernández, 2014). It can grow in extreme conditions, but prefers free moisture and a temperature of around 20–25 °C (Timmer et al., 2003).

Colletotrichum spp. is among the most important phytopathogens. It is reported to include more than 200 species in its genera (Marin-Felix et al., 2017). Some species of Colletotrichum spp. cause anthracnose and damage many tropical and subtropical fruits (Shivas et al., 2016). Anthracnose significantly reduces the marketability of stored fruits. It damages anthracnose, and so the symptoms may appear on fruits, and also on the flowers, leaves and branches of several horticultural crops. Its symptoms begin as tiny rounded leaf spots with yellow halos on the leaves and become chlorotic, which may lead to premature defoliation. On the other hand, symptoms on the fruits commonly appear as brown lesions, which results in microbial decay in the fruits. The spores may appear in grey to orange colours, and these turn into lesions in mature fruits (Thomidis, 2014). The spores of the fungus may easily grow and develop on crops and disperse with water splashes to other plant parts, causing a secondary inoculum. High moisture (varying from 62% to 95%) with a temperature of 20–30 °C favours the dispersal of the conidia (Cannon et al., 2012). Some of the major fruits affected by anthracnose are avocado, strawberry, banana, peach, apple, grape, mango, citrus, pomegranate and guava. It may cause premature fall in citrus fruits, especially during the rainy seasons and during bloom (Silva and Michereff, 2013; Xavier et al., 2019).

Another important fungal pathogen which causes brown rot, especially in the stone fruits, is Monilinia spp. belonging to the Helotiales order. According to Martini and Mari (2014), the estimated economic loss around the world is approximately 1.7 M€ · year⁻¹. The three main species of this genus are Monilinia fructicola, Monilinia fructigena and Monilinia laxa. The phytopathogens are known to begin infections on the above-ground plant parts with several different types of symptoms, including cankers on elder tissues, blighting of blossoms and, most importantly for us, the fruit rots. Some pre- and postharvest fungicides were reported to be effective for the regular control of brown rot, but as described before, the consumer preferences have led to demand for alternatives in management of the disease (Uysal-Morca and Kinay-Teksür, 2019). The brown rot fungus is ascomycetes and can produce sexual spores (ascospores). The wet season favours its growth and development. Besides, warm climates also stimulate the growth and development of brown rot. The damage mainly starts at the tree, as the formation of blights in blossoms and/or twigs is accompanied with soft decay in fruits, most commonly peaches, plums and cherries and rarely on apples and pears. Increase in the sugar content of the fruits, just before harvest, increases the susceptibility of the fruits to brown rot. Therefore, the unripe, green fruits are more tolerant to brown rot. Therefore, starting from the site selection (orchard location), continuing with the cultural practices and pre- and postharvest treatments, we infer that these are all together important for the management of brown rot. Alternatives to chemical treatments are undergoing research, where the antagonistic isolates of Bacillus and Pseudomonas spp. were noted to provide success in controlling brown rot after harvest (Ritchie, 2000).

Proteins are biomaterials formed by amino acids. In total, 20 amino acids have been identified till today, and numerous of them are attached to each other in long chains and form as proteins. Hydrolysis (cleavage of a covalent bond) can be used to release amino acids from the proteins. Proteins have been used to produce EF or EC to preserve fruits and vegetables (Baldwin et al., 2011).

Lipids are biomolecules that include hydrocarbons and make up the building blocks of the structure and function of living cells. They include hydrophobic (water-repellent) compounds which are insoluble in water and soluble in non-polar solvents. Fats, oils, waxes and some vitamins (i.e. A, D, E and K) are some examples of lipids (Baldwin et al., 2011). The fragile characteristic of the lipids makes it necessary for them to be commonly incorporated with other compounds, such as polysaccharides (Donhowe, 1994). Oils and waxes are the most important lipids used in food preservation. Besides, dispersion of oils or waxes in water or other hydrophilic solutions is also known as emulsion coating (Baldwin et al., 2011).

Polysaccharides obtained from animals (chitin and chitosan) or plants (cellulose, pectin, gum polymers, starch, Aloe vera etc.) are available in large quantities in nature, and these are complex carbohydrates with glycosidic bonds (Thakur and Thakur, 2016; Khalil Bagy et al., 2020). Polysaccharides have the ability to produce biodegradable films, which have advantages in food storage since they are capable of controlling gaseous composition, respiration and transpiration of the fresh produce (Freitas et al., 2014). Polysaccharide-based materials, EF/EC, provide good barrier against oxygen and carbon dioxide, but have a low ability to control water vapour, because of their hydrophilic characteristics (Rhim et al., 2013).

Besides the above-described primary products (metabolites) of plants, numerous studies have suggested that phytochemicals (secondary metabolites) isolated from plants can be used to control many phytopathogens, including thymol (Pérez-Alfonso et al., 2012), pinocembrin (Chen et al., 2020), citral (Wei et al., 2021) and alkaloids (Musto et al., 2014) isolated from plant sources, extracts or essential oils (Moraes Bazioli et al., 2019). In a very recent study, Yang et al. (2021) noted that the cinnamaldehyde, eugenol and carvacrol nanoemulsion have a high ability to reduce the decay of citrus fruits caused by P. digitatum. In another study, Annona muricata fruit extracts were reported to have the ability to alternatively control Alternaria spp. spots in tomato fruit. The in vitro assays with 6% of methanol extracts of the seeds were found to have approximately 90% inhibition of radial mycelial growth of A. alternata, whereas the in vivo studies resulted in 84% disease inhibition (Rizwana et al., 2021). Besides, canola and mustard extracts were reported to have a significant influence on the prevention of the development of P. digitatum in oranges. It was suggested that this efficacy is a result of the volatile compounds of the extracts (Koltz et al., 2020). EC and EF incorporated with plant extracts (Fantasia japonica) can be used to control P. italicum disease in citrus fruits (Liu et al., 2017).