Postharvest Diseases Management of Fruits and Vegetables: History
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Contributor:
Farid Moradinezhad
,
Azam Ranjbar

Sustainable agriculture requires factors to directly stimulate plant growth and induce the plant’s innate immune system to protect against stresses. Protection of plants is one of the main approaches to the supply of food resource. Furthermore, improved techniques for plant disease management must be environmentally sustainable, reliable, acceptable by society, and chemical-free to ensure sustainable food security. Although it is not possible to accurately determine postharvest losses due to diseases and physiological disorders, the use of proper harvesting and transportation methods that minimize damage to the product, along with optimal storage conditions that prevent the development of diseases, will be effective in reducing these postharvest losses. Since handling and storage conditions are potential threats for postharvest spoilage, it is necessary to identify environmentally friendly approaches and their precision mechanisms for postharvest disease management. Biological control, non-chemical, and eco-friendly techniques have been investigated for this purpose.

  • biological control
  • biosensors
  • combined treatments
  • edible coatings
  • nanotechnology

1. Introduction

Plant diseases are a major threat to various ecosystems and crops, so researchers develop new strategies to prevent pathogen growth and increase produce quality. The use of resistant species and cultivars produced by gene transfer [1] is eco-friendly and affordable in inhibiting losses caused by pathogens [2][3]. As well, the selection of somaclonal variation and mutation induction provides an essential strategy for disease management [4]. The importance of genes such as smutin and peroxidase that contain antifungal compounds for inducing resistance to pathogens has been proved [5]. Down-regulation of terpenes in transgenic oranges induces defense reactions against Penicillium digitatum [6][7]. In addition, it has been noted that myrcene stimulates the spore germination of P. digitatum through the upregulation of central carbon and energy metabolism [8], and terpene limonene causes citrus green mold through the regulation of reactive oxygen species (ROS) homeostasis in P. digitatum spores [9]. Additionally, appropriate agricultural practices [10], including lack of planting pathogen-host plants near fruit trees, removing sources of inoculation such as diseased branches or fruits, and using windbreaks to reduce spore dispersal will be effective [11].
The factors limiting the shelf life such as postharvest diseases are among the biological limitations that cause more economic losses than occur during cultivation [12][13]. Most postharvest pathogens are necrotrophic fungi that destroy cells using cell-wall-degrading enzymes (CWDEs) or mycotoxins (toxic secondary metabolites of fungi). Fungal species from the genera Alternaria, Aspergillus, Botrytis, Colletotrichum, Fusarium, Geotrichum, Gloeosporium, Monilinia, Mucor, Penicillium, and Rhizopus are known to produce mycotoxins and postharvest diseases [14][15]. Mycotoxins are low molecular weight compounds able to elicit a toxic response in humans through exposure at very low levels [16]. Postharvest disease development is influenced by pathogen biology, growth stage, and handling. Infection of pathogens could be delayed by using resistant cultivars [17]. On the other hand, the production of mycotoxins depends on physical, biological, and environmental factors [18]. The most important environmental factors are temperature, relative humidity, carbon dioxide levels, nutrient availability, and physical damage [19]. Due to the increase in world population, prevention of postharvest losses has become more critical. Generally, good agricultural practices and controlled storage conditions are essential to minimize pathogen contamination. In recent years, physical methods such as thermal treatments (hot water, steam heat, and hot air) to control plant pathogens have been effective [20][21][22]. The thermal process disrupts normal metabolism (ripening or senescence) by creating moderate and reversible stress [23]. Proteomic analysis showed that up-regulated proteins by heat treatment were related to defense response and redox metabolism. Therefore, the loss reduction is due to the expression of proteins related to carbohydrate and energy metabolism [24]. Investigating the effect of thermal processing on the microbiome of apple fruit indicates a decrease in fungal–bacterial diversity [25]. However, heat treatment has undesirable effects on nutritional quality among vitamin reduction, protein denaturation, and sensory properties [26]. In order to reduce the adverse effects, non-thermal food processing techniques such as ionizing radiation, cold plasma, and high-pressure processing pulse electric field radiation were used [27].

2. Postharvest Diseases Management

2.1. Biological Control

The primary benefit of a fruit-based diet is the modification of nutrients, including enrichment with fiber, phenolic compounds, and complex sugars that maintain a healthy microbiota in the human gut [28][29]. One of the most effective methods to prevent disease is the application of biological control agents (BCAs) [30]; through competition for nutrients, the production of secondary metabolites such as volatile organic compounds (VOCs), lytic enzymes, and the activation of the plant defense system, they function as antagonists of fungal diseases [31][32][33] (Figure 1). Microbial antagonists significantly modulate the fruit microbiome and improve fruit health by inhibiting pathogenic aerobic microbial species and promoting beneficial microorganisms [34]. The role of endophytic microorganisms in increasing resistance to stresses, availability to nutrients, and promoting growth has been proven [35]. Endophytes Debaryomyces hansenii, Galactomyces geotrichum, Pichia kudriavzevii, Rhodotorula glutinis, and Schwanniomyces vanrijae isolated from apple fruit [36], Proteobacteria, Actinobacteria, and Bacilli isolated from banana, guava, mango, papaya fruits [37], Metschnikowia, Hanseniaspora, Acinetobacter, Gluconobacter isolated from grape berries [38] and Lactobacillus plantarum CM-3 in strawberries [39] as microbial antagonists through the synthesis of phytohormones and VOCs inhibit fruit pathogens [40]. VOCs are low molecular weight compounds that are composed of alcohols, aldehydes, esters, aromatic and aliphatic hydrocarbons, terpenes, nitrides, and sulfides with strong antimicrobial effect [41].
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Figure 1. Proposed mechanisms of action biological control agents against plant pathogens.
Acceptance of bacteria as BCAs in the control of fungal diseases can be attributed to their strong inhibitory capacity, rapid colonization, and low nutritional requirements [31][42]. Probiotic bacteria’s secondary metabolism enables them to synthesize and release secondary metabolites with antimicrobial capacity, such as non-volatile organic compounds and VOCs with a broad range of biological functions [43][44]. Bacterial antagonists belong to the group of plant growth-promoting bacteria (PGPB) [45]. PGPB are a group of non-pathogenic beneficial bacteria that live autonomously in the soil or rhizosphere, the phyllosphere (epiphytes), and plant tissues (endophytes) [46]. Plant growth-promoting rhizobacteria (PGPR) reduce the level of ethylene under stress and pathogen attack [47], suppress the activity of pathogens through competition for nutrients, production of lytic enzymes, inhibition of the synthesis of toxins [48], and stimulation of plant growth and survival [47]. PGPR both rhizospheric and endophytic bacterial strains inhibited Panama disease in field and greenhouse by inducing resistance to Fusarium wilt in banana [49], and compounds produced by PGPR such as antibiotics with pathogen control are related [50]. Antibiotics are a heterogeneous group of low molecular weight organic compounds [51] which inhibit the growth of phytopathogenic fungi such as Aspergillus flavus, Alternaria solani, Fusarium oxysporum, Colletotrichum gloeosporioides by disrupting the structure of the cell wall or the function of the membrane of microorganisms, disrupting the synthesis of proteins and the function of respiratory enzymes [52]. Iturin, pyrrolnitrin, and syringeomycin are the most important antibiotics for postharvest diseases [53]. PGPR known as NJN-6 of Bacillus amyloliquefaciens produces various secondary metabolites for inhibiting soil-borne pathogens. Therefore, the NJN-6 strain reduced the severity of Panama disease and improved the growth of banana seedlings [30]. 
Bacteria indirectly activate local and systemic responses in plants [13]. Studies have shown that genes related to L-phenylalanine metabolism, amino acid biosynthesis, plant hormone signal transduction, and programmed cell death (PCD) regulation are induced by antagonistic microorganisms [54]. Bacterial antagonist B. siamensis decreased the expression of catalase (CAT); however, the expression of superoxide dismutase (SOD) was increased. Increasing SOD activity can enhance defense against pathogens [55]. In grapes, P. fluorescent and B. amyloliquefaciens reduce the incidence of B. cinerea by increasing the enzyme activity of CAT, peroxidase (POD), polyphenol oxidase (PPO), phenylalanine ammonia-lyase (PAL), and chalcone isomerase (CHI) [56][57]. It has been reported that Bacillus halotolerans and B. subtilis induce activities of POD, PPO, PAL, and CHI enzymes in strawberries and blueberries for resistance to B. cinerea [58][59]. The responses induced by Bacillus licheniformis and Bacillus sonorensis against the pathogen P. digitatum in Indian gooseberries and grapes are considered a type of plant defense response [60][61]. The application of Aureobasidium pullulans cell suspension maintained chitinase and 1,3-glucanase levels of avocado fruit [62], and Serratia sp. bacterial extracts showed high potential to control postharvest rot caused by C. gloeosporioides in avocados [63]. Likewise, the extracts of B. subtilis, Pseudomonas brenneri, and Pseudomona koreensis significantly inhibited germination and hyphae growth of B. cinerea and A. alternata in blueberries by producing metabolites like arthrofactins [64].

2.2. Biosensors

Disease development is closely related to physiological stages, host tissue characteristics, and environmental conditions. Biosensors transform biological responses into detectable electrical signals [65]. Biosensors such as antibodies, antimicrobial peptides, cells, organelles, microorganisms, enzymes, and nucleic acid [65] have the capacity to monitor the microbial flora of fruits and vegetables. Antibodies and antimicrobial peptide-based biosensor design to detect bacteria due to their superior properties such as stability, multiple site for bacteria capture and high specificity were considered [66]. Nucleic acids are molecules with high affinity and specificity to interact with a target [67] and enzymatic sensors measure target components by utilizing the catalytic reaction of enzymes with sugars, amino acids, proteins, and lipids as substrates [67]. The development of sensors based on phytochemicals or ripening genes is effective in controlling spoilage. Recently, a sensor composed of a metal catalyst and carbon nanotubes has been developed to monitor ethylene to determine the time of spoilage of fruits and vegetables [68]. Based on the luminescent responses of the bacteria to changes in VOCs following contamination, whole-cell bacterial biosensors can detect P. digitatum in oranges [69]. In this way, a colorimetric sensor containing AuNPs modified with the Aspergillus niger spore-binding peptide was developed to detect A. niger spores [70]. Addition of nanoparticles to electrochemical biosensors was used for rapid monitoring of Penicillium through immobilization of penicillinase enzyme using N-5-azido-2-nitrobenzoemideyl [71].

2.3. Nanotechnology

Nanotechnology use is efficient for antimicrobial agents in fresh products. Nanomaterials offer advantages such as bioavailability, controlled release, bio preservatives, and performance improvement. Nanoparticles are variable in size and amorphous or crystalline and are able to link with biological molecules like nucleic acids, peptides, and proteins [72][73]. A wide range of metals and their oxide-based single- and multi-walled carbon nanotubes and nanocomposites have been used. Gold, silver, zinc, cerium, titanium dioxide (TiO2), silica, silica–silver, alumina–silicate, and chitosan are nanoparticles used to control plant pathogens [74][75].
The fungicidal activity of TiO2 nanoparticles has been proven against fungal pathogens Venturia inaequalis and Fusarium solani [76] and likewise manganese oxide (MnO2) nanoparticles against the pathogens causing wilt diseases in watermelon, eggplant, and tomatoes [77]. The inhibition of pathogens B. cinerea and P. expansum by using nanoparticles of zinc oxide is due to the induction of reactive oxygen species [78]. A honeycomb-like structure of silica nanoparticles is used in the targeted delivery of DNA and chemicals into plants [79]. Similarly, growth suppression of B. cinerea, C. gloeosporioides, Magnaporthe grisea, and Pythium ultimum was shown in solution of silica–silver [80]. Mycotoxin determination of pathogens has been conducted using nanocarbon materials like carbon nanowires and nanotubes [81]. Spray drying, precipitation, ionic gelation, emulsion cross-linking, sieving, and reverse micellar are used to produce chitosan-based agro-nanochemicals [82]. Chitosan-based nanoparticles have been used to reduce postharvest decay [83][84] through an inhibitory effect against Aspergillus sp., Fusarium sp., and Alternaria sp. [85]. Nanomaterials with chitosan coating films can control mesophilic aerobic, yeast, and mold contaminations by modulating the ripening index and increasing enzyme activities [86]. The chitosan-AgNPs based-composite showed remarkably higher antifungal activity against C. gloeosporioides [87]. Nanocomposites of selenium and chitosan nanoparticles synthesized using pomegranate peel extracts and Fenneropenaeus indicus shells stimulated the deformation of P. digitatum hyphae [88]. Thyme oil in an edible coating based on chitosan nanoparticles showed complete inhibition of C. gloeosporioides of avocado [89].

2.4. Plant Growth Regulators (PGRs)

PGRs are factors affecting gene expression and related biological activities. As a short- to medium-term strategy, plant-derived natural compounds, such as plant hormones, associated with defense systems have been considered [90]. Melatonin (MT), as a signaling molecule and antioxidant [91], is vital in physiological processes [92], response to stresses [93], and resistance to pathogens [94]. Exogenous application of MT significantly increased disease resistance in strawberries [95], kiwi [96], plums [97], bananas [95], and grapes [98] and reduced decay. The effects of synergism MT with NO and ROS induce disease resistance [99][100]. Induction of resistance by MT is associated with the expression of defense genes/proteins, such as POD, lipid transfer proteins (LTPs), chitinases, β-1,3-glucanases, and pathogenesis-related (PR) proteins [98][101]. MT and NO induce phytohormones such as SA, JA, and MAPK signaling pathways [102][103]. Exogenous melatonin stimulated endogenous melatonin production in the mesocarp and exocarp of plum, and total phenol and anthocyanin increased in the mesocarp [104]. A rise in JA and its precursor (oxo-phytodienoic acid (OPDA)) was detected in mesocarp by hormonal analysis [104]. Therefore, melatonin induces the JA signaling pathway to increase total phenol and anthocyanins. JA is involved in promoting the biosynthesis of phenylpropanoid compounds such as anthocyanins [105] by regulating the WD-repeat/bHLH/MYB complexes [106]. MeJA activates defense responses against stresses [107].
Artificial inoculation of table grapes immersed in MT showed that MT did not significantly inhibit hyphae growth and spore germination but reduced the severity of gray mold disease [108]. MT reduces the MDA content and prevents the increase in cell membrane permeability by synthesizing and accumulating phenols and flavonoids. Simultaneously, the activity of defense enzymes such as SOD, POD, CAT, PAL, PPO, chitinase, and β-1,3 glucanase significantly increases [109].
SA and MeJA are critical in plant interactions to induce systemic defense against pathogenic microorganisms [110]. The activity of PPO and POD, increased proportionally to the content of SA and JA in citrus treated and infected with P. italicum and P. digitatum, resulted in inhibiting both molds [111]. Pan et al. (2020) reported that MeJA significantly reduced the diameter of the lesions caused by B. dothidea on kiwifruit [112]. MeJA significantly increased the activity of defense-related enzymes such as CAT, POD, SOD, PPO, chitinase, and β-1,3-glucanase. It also increased the accumulation of total phenolic compounds, while lipid oxidation decreased [112]. MeJA increased the activity of PAL and 4-coumarate-CoA ligase (4CL), total phenol, total flavonoid, lignin, individual phenols such as chlorogenic acid, neochlorogenic acid, and epicatechin in peach [113].

2.5. Edible Coatings

Natural films and coatings include polysaccharides (pectin, cellulose, starch, gums), lipids (fatty acids, acetylated glycerides, surfactants, waxes), proteins (fatty acids, collagen, gelatin, waxes, resins, whey), and composite polymers. The principal components for producing biodegradable films are film-forming biopolymers which include carbohydrates, proteins, solubilizing medium, and plasticizers [114]. The majority of the edible coating components are polysaccharides such as chitosan, alginate, cellulose, carrageenan, pectin, starch, and proteins such as whey and casein [115]. In addition to maintaining structural integrity due to the arrangement of hydrogen bonds, polysaccharide-based films have good barrier properties [116]. Protein-based coatings have lower moisture barrier properties than polysaccharide-based films [117]. Lipid-based coatings have very high moisture barrier properties due to the greater polarity difference [118]. Polysaccharides and proteins due to their hydrophilic nature are used for transport active components such as antioxidant and antimicrobial agents [119]. Starch and alginate are considered for bio-packaging due to their gelatinization properties [120] and the ability to form hydrogels and encapsulation barriers, respectively [121]. Chitosan has attracted attention due to its properties as a gelling agent and the ability to form hydrogen bonds and hydrophobic interactions [122]. Low gaseous permeability is an important property of edible coating in order to slow down the respiration and transpiration processes, thereby delaying ripening and senescence. Among other features is the control of the migration of oxygen, carbon dioxide, and moisture from the outside environment into the products, the inertness of coating substances, nature transparent, non-toxic, non-sticky, low viscous, economical and possessing a quick drying nature, digestible, and no change in sensory characteristics (taste, smell or color) of products [123]. Reduced water loss, microbial decay inhibition, protection against chilling damage, and appearance enhancement are among the benefits of coatings in food preservation [124]. The mechanical properties of edible films and coatings are highly influenced by the types of biopolymers, and also the addition of plasticizers and surfactants [125]. Chitosan is one of the principal edible coatings in postharvest disease management of fresh products [126].
Some natural components have been used to formulate edible coatings. Natural gums can induce defense reactions and reduce plant diseases. Gum arabic increased PPO activity in strawberries [127], and peach gum increased PPO, POD, PAL, and chitinase activity in blueberries [128]. Propolis extract significantly reduced the postharvest microbial decay of blueberries [129]. The application of propolis extract in an edible gelatin coating on raspberries had an inhibitory effect on B. cinerea and P. digitatum strains [130]. The tragacanth gum coating preserves the sensory and quality properties of apple fruit by reducing the microbial load [131]. Corn starch with papaya leaf extract significantly extended the shelf life and decreased the fruit spoilage percentage [132]. The incorporation of antioxidant, antifungal, and antimicrobial additives in bioactive bio-packaging is common [133]. Chitosan–polylactic acid films containing Melaleuca alternifolia essential oil improved the flexibility and elongation at break of the film and controlled postharvest diseases in mango [134]. Increasing the concentration of cinnamaldehyde in chitosan-graph-based edible films, in addition to improving the mechanical properties of elastic modulus, tensile strength, and elongation at break, had antifungal properties against P. italicum and Rhizopus stolonifera [135]. The hydroxyl group in the EO chain replaces the internal hydrogen bonds between the polymers by forming hydrogen bonds and leads to an increase in the free spaces between the molecules, thus reducing the stiffness and increasing the flexibility of the film [136]. The reaction between essential oil compounds and the cell membrane of microorganisms results in antimicrobial properties [137]. The bioactive film based on chitosan and gum arabic with the addition of cinnamon essential oil created an entangled structure and the water barrier properties increased in addition to the antioxidant potential [138]. Pectin beeswax coating containing eugenol is a viable method to maintain the quality of citrus [139]. Although essential oils enhance antimicrobial properties, they may lead to low water-solubility and offensive odors from the edible coatings [140]. Therefore, the effectiveness of edible coatings was studied as a biological control strategy [141], and simultaneous use of edible coatings and probiotics was investigated for their antifungal activity [142].

2.6. Essential Oils (EOs)

Applying EOs is an eco-friendly and sustainable method for postharvest disease management [143]. The function of EOS against postharvest fungi happens at the level of the cell membrane (disruption of the cell membrane integrity) or at the level of cell metabolism (dysfunction of mitochondria, vacuole, and inhibition of efflux pumps) [144] EOs often have a complex composition containing terpenes (monoterpenes, sesquiterpenes, diterpenes, norterpenes), phenylpropanoids, and sulfur and nitrogen compounds [145]. The synergistic effects of the constituents of EOs [146] reduce the possibility of pathogen survival or resistance [147]. It seems the presence of monoterpenes (hydrocarbon and oxygenated monoterpene) and sesquiterpenes (hydrocarbon, oxygenated sesquiterpenes) in EOs, is thought to produce antioxidant and antibacterial properties [148]. In fact, molecules with a phenolic structure, for example, thymol and carvacrol, or aldehydes, such as p-anisaldehyde and ketones, significantly inhibit pathogen growth [149]. Pomegranate peel phenolic extracts stimulate expression of PAL, chitinase, chalcone synthase (CHS), and mitogen-activated protein kinase kinase (MAPKK), which contribute to the activation of plant defenses for response to reactive oxygen species (ROS) [150] and therefore inhibits the germination of P. italicum and P. digitatum conidia [150]. Applying EOs to manage mango anthracnose showed that clove and thyme oils inhibited conidia germination and mycelia growth [151]. An assay growth inhibition of fungal strains and Escherichia coli showed that the inhibitory activity of cinnamon and clove oils was due to the bioactive compounds of cinnamaldehyde and eugenol, respectively [152]. Thymol fumigation reduced anthracnose in avocados [153]. Thymol fumigation increased the activity of chitinase and β-1,3-glucanase, which can hydrolyze fungal cell wall polymers and activate plant defense systems [154]. Thymol inhibited citrus blue mold [155] and in addition to direct antifungal effects, it caused a rapid accumulation of hydrogen peroxide, leading to increased activity of defense enzymes such as β-1,3-glucanase, chitinase, PAL, POD, PPO, and LOX [155]. Thymol inhibits pomegranate fruit rot by disrupting the function of cell-wall-degrading enzyme fungi such as cellulase and pectinase [156].

This entry is adapted from the peer-reviewed paper 10.3390/horticulturae9101099

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