Gianfranco Romanazzi
Erica Feliziani
Dharini Sivakumar2- 1Department of Agricultural, Food and Environmental Sciences, Marche Polytechnic University, Ancona, Italy
- 2Department of Crop Sciences, Postharvest Technology Group, Tshwane University of Technology, Pretoria, South Africa
Chitosan is a natural biopolymer from crab shells that is known for its biocompatibility, biodegradability, and bioactivity. In human medicine, chitosan is used as a stabilizer for active ingredients in tablets, and is popular in slimming diets. Due to its low toxicity, it was the first basic substance approved by the European Union for plant protection (Reg. EU 2014/563), for both organic agriculture and integrated pest management. When applied to plants, chitosan shows triple activity: (i) elicitation of host defenses; (ii) antimicrobial activity; and (iii) film formation on the treated surface. The eliciting activity of chitosan has been studied since the 1990’s, which started with monitoring of enzyme activities linked to defense mechanisms (e.g., chitinase, β-1,3 glucanase, phenylalanine ammonia-lyase) in different fruit (e.g., strawberry, other berries, citrus fruit, table grapes). This continued with investigations with qRT-PCR (Quantitative Real-Time Polymerase Chain Reaction), and more recently, with RNA-Seq. The antimicrobial activity of chitosan against a wide range of plant pathogens has been confirmed through many in-vitro and in-vivo studies. Once applied to a plant surface (e.g., dipping, spraying), chitosan forms an edible coating, the properties of which (e.g., thickness, viscosity, gas and water permeability) depend on the acid in which it is dissolved. Based on data in literature, we propose that overall, the eliciting represents 30 to 40% of the chitosan activity, its antimicrobial activity 35 to 45%, and its film-forming activity 20 to 30%, in terms of its effectiveness in the control of postharvest decay of fresh fruit. As well as being used alone, chitosan can be applied together with many other alternatives to synthetic fungicides, to boost its eliciting, antimicrobial and film-forming properties, with additive, and at times synergistic, interactions. Several commercial chitosan formulations are available as biopesticides, with their effectiveness due to the integrated combination of these three mechanisms of action of chitosan.
Introduction
Chitosan is the linear polysaccharide of glucosamine and N-acetylglucosamine units joined by β-1,4-glycosidic links and it is obtained by deacetilation of chitin through exposure to NaOH solutions or to the enzyme chitinase. Chitosan and chitin are naturally occurring polymers. For their biocompatibility and biosafety, their applications are widespread in many industries, such as cosmetology, food, biotechnology, pharmacology, medicine, and agriculture (Ding et al., 2013; Lei et al., 2014). In particular, chitosan has increasing interest in plant protection as a natural fungicide and plant defense booster, and meets the interest of many researchers, that used it to prolong the storage of an array of fruit and vegetables worldwide. Chitosan was the first compound in the list of basic substances approved in the European Union for plant protection purposes (Reg. EU 66 2014/563), for both organic agriculture and integrated pest management. A comprehensive review on the available data on the effectiveness of chitosan was published recently, for its preservation of fruit and vegetables, both alone and in combination with other treatments, and its mechanisms of action (Romanazzi et al., 2017). However, the increasing knowledge of this biopolymer (Figure 1) and the fast advances in basic and applied research in this field require a more focused and schematic update based on the last 5 years of investigations (2013–2018). The reader can then focus on specific aspects from the long list of other reviews that have appeared on the subject, among which some have focused on the applications of chitosan to fruit and vegetables (Bautista-Baňos et al., 2006; Bautista-Baòos et al., 2016; Zhang et al., 2011). When applied to plants, chitosan shows triple activity: (i) elicitation of host defenses; (ii) antimicrobial activity; and (iii) film formation on the treated surface. We will cover the recent information on these issues in the following sections, which is also listed comprehensively in the Tables, with examples of these applications.
FIGURE 1. Number of documents available on Scopus through searches with keywords ‘chitosan’ and ‘postharvest’ in ‘Article title, Abstract, and Keywords’ or in ‘All fields’ published over the last 30 years (accessed on 6 November 2018).
Effectiveness of Chitosan in the Control of Postharvest Decay of Fruit
The potential effectiveness of chitosan as a coating for fresh fruit was first proposed by Muzzarelli (1986). The first in-vivo application of chitosan on fruit was in the Josep Arul Laboratory, by Ahmed El Ghaouth, who produced a list of papers through the last decade of the last century. These included El Ghaouth et al. (1992), where they applied chitosan to strawberries and other fruit, both alone and in combinations with other potential biocontrol agents, which then contributed to the develop of some commercial formulations. Following these promising investigations, and with the growing need for alternatives to the use of synthetic fungicides, chitosan use became popular, and it was proposed to be part of a new class of plant protectants (Bautista-Baňos et al., 2006). Chitosan coatings have now been applied to numerous temperate and subtropical fruit, both alone and in combination with other treatments (Tables 1–3), with generally additive, and in some cases synergistic, effectiveness (Romanazzi et al., 2012).
TABLE 1. Postharvest chitosan treatments with other applications for storage decay of temperate fruit.
TABLE 2. Postharvest chitosan treatments with other applications for storage decay of subtropical fruit.
TABLE 3. Preharvest chitosan treatments with other applications for storage decay of temperate fruit.
Chitosan Eliciting Activity
Chitosan is known to elicit plant defences against several classes of pathogens, including fungi, viruses, bacteria and phytoplasma (El Hadrami et al., 2010). Moreover, in some studies, its eliciting activity was reported to be effective on pests (Badawy and Rabea, 2016). Based on our experience, the eliciting activity of chitosan accounts for 30 to 40% of its effectiveness in the control of postharvest decay of fresh fruit (Figure 2). The extent of this eliciting activity depends on the reactivity of the fruit tissues, and it is well known that fruit responses to stress decline with ripening (Romanazzi et al., 2016). This eliciting activity of chitosan has been studied since the 1990’s, which started with monitoring of the activities of enzymes linked to the defense mechanisms (e.g., chitinase) in different fruit (e.g., strawberries) (El Ghaouth et al., 1992). This was followed by investigations on other berries, citrus fruit and table grapes, among others. More recently, tools such as qRT-PCR and in recent years RNA-Seq (RNA-Sequencing) have allowed important information to be gained, first at the level of single gene expression, and then later at the level of global gene expression (Xoca-Orozco et al., 2017). This has provided good understanding of the multiple actions of chitosan applications and how they affect a number of physiological changes in fruit. As an example, the application of chitosan to strawberries at different times before harvest can affect the expression of a thousand or more genes (Landi et al., 2017). Some examples that have become available in the literature over the last 5 years are listed in Table 4, which deal with the physiological changes that can occur in chitosan-treated fruit, both when the biopolymer is applied alone, and when it is combined with other treatments. The eliciting activity of chitosan is particularly effective toward latent infections, as a more reactive fruit can stop the infection process, through a balance that resembles quorum sensing, which is well known for bacterial infections (Papenfort and Bassler, 2016).
FIGURE 2. Proportion of antimicrobial, eliciting, and film-forming properties of chitosan.
TABLE 4. Physiological changes that can occur in fresh fruit after chitosan treatment, alone or in combination with other applications.
Chitosan Antimicrobial Activity
Numerous studies on chitosan inhibitory activities toward numerous microrganisms have been carried out since the first report of almost half a century ago (Allan and Hadwiger, 1979). The antimicrobial activities of chitosan against a wide range of plant pathogens have been confirmed by any of in-vitro and in-vivo studies. The antimicrobial activity of chitosan is one of its main properties, and this depends on the concentration at which it is applied. In the control of postharvest decay of fresh fruit, the antimicrobial activity can account for 35–45% of its effectiveness, as an antifungal barrier on a fruit inhibits the germination of fungal spores and slows down the rate of decay-causing fungi of already infected fruit, both latently and actively (Figure 2). A standard application rate of chitosan to provide a significant control of postharvest decay of fruit and vegetables can be considered 1%, except for the control of Penicillia, where higher concentrations may be needed to provide a good effectiveness. The degree of deacetylation and the molecular weight of chitosan characterize its properties, such as the number of positively charges of amino groups and therefore, its electrostatic interactions with different substrate and organisms at different pH. Chitosan with a higher degree of deacetylation, which has greater numbers of positive charges, would also be expected to have stronger antibacterial activities. On the other hand, numerous studies have generated different results relating to correlations between the chitosan bactericidal activities and its molecular weight (Romanazzi et al., 2017). In addition, there are many differences between the chitosan antifungal and antibacterial activities and several mechanisms relating to these remain still unclear and further researches are needed (Romanazzi et al., 2017).
Chitosan Film-Forming Properties
Once applied to a plant surface by dipping or spraying, chitosan can form an edible coating, the properties of which (e.g., thickness, viscosity, gas, and water permeability) greatly depend on the acid in which the biopolymer is dissolved. The film-forming properties of chitosan account for 20–30% of the chitosan effectiveness in the control of postharvest decay of fruit and vegetables (Figure 2). Coating produces a barrier for gas exchanges and reduced respiration, and slows down fruit ripening. Of note, a less ripe fruit is less sensitive to postharvest decay.
Toward Large-Scale Commercial Applications
When first used in experimental trials, chitosan needed to be dissolved in an acid (e.g., hydrochloric acid, acetic acid, which were among the most effective ones; see Romanazzi et al., 2009), and then taken to the optimal pH (∼5.6) This approach can even take 1–2 days, and it is impractical for use by growers. More recently, several commercial chitosan formulations that can be dissolved in water have become available on the market to be used as a biopesticides (Table 5). Some of these are formulated as powders, and then the cost of shipping is lower (although still higher compared to most of the commercially available synthetic fungicides), although the chitosan needs to be dissolved in water, in some cases a few hours before its application. This makes chitosan more difficult to use, as the grower wants to use an alternative to synthetic fungicides in the same way as a commercial compound, such that it should have the same effectiveness. This objective can be achieved with liquid formulations, which have concentrations of 2–15%. In this case, the cost of shipping is higher, as the volumes are larger due to the amounts of water that travel with the chitosan. In tests of three different commercial products, even when used at the same concentration, differential effectiveness was seen (Feliziani et al., 2013a). The higher cost of chitosan treatment compared to standard applications might also induce companies toward the use of low doses (e.g., even well below 0.1%), Based on data in literature, the optimal dose is around 1%, while decreasing the concentration, the effectiveness declines. Furthermore, when the concentration of chitosan is decreased, its effectiveness also declines. However, applications to the plant canopy also need to take in account possible phytotoxic effects, mainly if repeated applications occur. This has been shown for grapevines (Romanazzi et al., 2016a), such that for these purposes a good concentration might be 0.5%. However, under some particular conditions, even low concentrations of chitosan (e.g., 0.02%) in a commercial formulation can be beneficial, such as for the improved storage of litchi (Jiang et al., 2018).
TABLE 5. Some chitosan-based commercial products that are available for control of postharvest diseases of fruit and vegetables.
Concluding Remarks
The effectiveness of chitosan application arises from the integrated combination of its three mechanisms of action. There are increasing consumer requests for fruit and vegetables to be free from residues of synthetic pesticides, such that the rules defined by the public administration have become more limiting in terms of the active ingredients allowed and the maximum residue limits. Also, large stores compete with each other to further reduce these limits, compared to the legal thresholds (Romanazzi et al., 2016b). These trends make the concept of the application of alternatives to synthetic fungicides more popular, and among these the main one that is already used in human medicine is chitosan, which is particularly welcomed by public opinion. These aspects have promoted further studies based on the multiple actions of chitosan on fruit and vegetables. Therefore, further increases in our knowledge are expected following the widespread practical application of chitosan due to the regulation of its use in agriculture and the interest of companies to promote chitosan-based products, with potential benefits for the growers, the consumers and the environment.
Author Contributions
GR proposed the review, collected data on chitosan popularity over time and on commercial products, coordinated the authors, and wrote the article. EF collected papers on effectiveness of chitosan on temperate fruit and on the mechanisms of action in the tables, and helped with the writing. DS collected papers on effectiveness of chitosan on tropical fruit and on the mechanisms of action in the tables, and helped with the writing.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Keywords: antimicrobial activity, biopolymer, coating, induced resistance, natural fungicide
Citation: Romanazzi G, Feliziani E and Sivakumar D (2018) Chitosan, a Biopolymer With Triple Action on Postharvest Decay of Fruit and Vegetables: Eliciting, Antimicrobial and Film-Forming Properties. Front. Microbiol. 9:2745. doi: 10.3389/fmicb.2018.02745
Received: 04 July 2018; Accepted: 26 October 2018;
Published: 04 December 2018.
Edited by:
Boqiang Li, Institute of Botany (CAS), ChinaReviewed by:
Xianghong Meng, Ocean University of China, ChinaHongbing Deng, Wuhan University, China
Copyright © 2018 Romanazzi, Feliziani and Sivakumar. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Gianfranco Romanazzi, Zy5yb21hbmF6emlAdW5pdnBtLml0