Next Article in Journal
Effects of Irrigation on N2O Emissions in a Maize Crop Grown on Different Soil Types in Two Contrasting Seasons
Next Article in Special Issue
Influence of Iron-Enriched Biochar on Cd Sorption, Its Ionic Concentration and Redox Regulation of Radish under Cadmium Toxicity
Previous Article in Journal
Epistasis and Quantitative Resistance to Pyricularia oryzae Revealed by GWAS in Advanced Rice Breeding Populations
Previous Article in Special Issue
Development of Microwave Slow-Wave Comb Applicators for Soil Treatment at Frequencies 2.45 and 0.922 GHz (Theory, Design, and Experimental Study)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 10
Issue 12
10.3390/agriculture10120624
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Mechanism of Plant Growth Promotion and Disease Suppression by Chitosan Biopolymer

by
Moutoshi Chakraborty
1,
Mirza Hasanuzzaman
2,*,
Mahfuzur Rahman
3,
Md. Arifur Rahman Khan
4,
Pankaj Bhowmik
5,
Nur Uddin Mahmud
1,
Mohsin Tanveer
6 and
Tofazzal Islam
1,*
1
Institute of Biotechnology and Genetic Engineering (IBGE), Bangabandhu Sheikh Mujibur Rahman Agricultural University, BSMRAU Road, Gazipur 1706, Bangladesh
2
Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka 1207, Bangladesh
3
Agriculture & Natural Resources, Extension Service, West Virginia University, Morgantown, WV 26506, USA
4
Department of Agronomy, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh
5
National Research Council of Canada, Saskatoon, SK S7N 0W9, Canada
6
Tasmanian Institute of Agriculture, University of Tasmania Australia, Hobart 7005, Australia
*
Authors to whom correspondence should be addressed.
Agriculture 2020, 10(12), 624; https://doi.org/10.3390/agriculture10120624
Submission received: 30 October 2020 / Revised: 3 December 2020 / Accepted: 9 December 2020 / Published: 11 December 2020
(This article belongs to the Special Issue Recent Advances in Technological and Agronomic Practices for Sustainable Agriculture)
Browse Figures
Versions Notes

Abstract

:
The chitosan (CHT) biopolymer is a de-acetylated chitin derivative that exists in the outer shell of shrimp, shellfish, lobster or crabs, as well as fungal cell walls. Because of its biodegradability, environmental non-toxicity, and biocompatibility, it is an ideal resource for sustainable agriculture. The CHT emerged as a promising agent used as a plant growth promoter and also as an antimicrobial agent. It induces plant growth by influencing plant physiological processes like nutrient uptake, cell division, cell elongation, enzymatic activation and synthesis of protein that can eventually lead to increased yield. It also acts as a catalyst to inhibit the growth of plant pathogens, and alter plant defense responses by triggering multiple useful metabolic pathways. This review emphasizes the role and mechanisms of CHT as a plant growth promoter and disease suppressor, and its future implications in agriculture.

1. Introduction

Chitosan (CHT) is a poly (1,4)-2-amino-2-deoxy-β-D glucose, a de-acetylation derivative of chitin, found in arthropod exoskeletons, which includes crustaceans like lobsters, shrimps and crabs, insects, mollusc radulae, beaks of cephalopod and fish, and lissamphibian scales [1]. The discovery of Chitosan (pronounced as Kite-O-San) dates back to 1811, when a French Professor Henri Braconnot of Natural History first found “chitin” from which it is derived. He found a mushroom extract which would not dissolve in sulphuric acid, and he called it ‘fungine’ [2,3]. In 1823, it was named ‘chitin’ after another scientist Auguste Odier extracted it from cuticles of beetle and called it ‘chiton’. Chitin was the first man-identified polysaccharide, about 30 years prior to cellulose. The concept was further recognized when the existence of nitrogen in the chitin was demonstrated by Lassaigne in 1843. Professor C. Rouget undertook the alkaline treatment of chitin in 1859, resulting in an acid dissoluble substance, unlike chitin itself. Hoppe-Seiler gave the name “chitosan” to de-acetylated chitin [4]. Although chitin has long been an unused natural component, interest in this biopolymer and its derivatives like CHT has grown significantly in recent years due to its diversified biological properties.
The biopolymer CHT is safe, cheap and its chemical structure can easily be converted to develop relevant polymers for specified applications. These features make CHT a molecule of great significance in a wide range of potential users, from health care and biotechnological industries to farmers [5,6]. It is biodegradable, environment friendly for agriculture, and not toxic to humans or other organisms [7]. It has shown efficacy in reducing disease incidence and increasing crop growth, yield, and quality. The CHT has been documented as an elicitor of plants’ natural defense response, and has been utilized as a natural product to combat pathogenic diseases before and after harvest [8]. It functions as an antifungal [9], antibacterial [10], antiviral [11], and bionematicidal agent [12]. Chitosan has been widely utilized as a coating agent of different nuts, cereals, fruits, and vegetables to protect from post-harvest losses, and increase the duration of storage and preservation [13,14]. A wide range of studies showed that foliar application of CHT improves plant growth, yield and induces synthesis of secondary metabolites like polyphenolics, flavonoids, lignin, and phytoalexins in plants [15,16]. It influences seed plasma membrane permeability, enhances sugar and proline concentration, boosts peroxidase (POD), phenylalanine ammonia-lyase (PAL), tyrosine ammonialyase (TAL) and catalase (CAT) activities [17]. This article will focus on the effects and mechanisms of CHT as a plant growth promoter and disease suppressor, as well as its future implications in agriculture.

2. Chitosan and Its Structural Diversity

Chitosan is a linear biopolymer comprising two sub-units, i.e., D-glucosamine and N-acetyl-D-glucosamine, connected by 1,4-glycosidic bonds to each other [18,19]. There are three rings in the structure of the CHT molecule. CHT displays three functional groups, primary and secondary groups of hydroxyls and amine. CHT also contains beta-1, 4 glycosidic bonds. The oxygen atoms (O1 and O2) are bound to the atoms of C6–C7 and C10–C13 [20]. These functional groups allow them to undergo chemical modifications easily. Chemical derivatives of CHT have gained increasing emphasis over the last decade owing to their biological, chemical and functional benefits over unmodified CHT in terms of solubility, gelling properties, nature of amphiphilic hydrophobic variants, and ability to manipulate chemical conjugates and self-assembling nanostructures, and enhanced biocompatibility [21]. Modification can be achieved through physical or chemical techniques such as cross-linking, grafting, incorporation of substituents or composites. Chitosan possesses many reactive amino side groups that improve CHT’s applicability and provide the possibility of developing a broad range of CHT derivatives.
Oligochitosan is one of the important water-soluble CHT derivatives. Along with other polysaccharides, CHT can also be hydrolyzed by biodegrading agents owing to its unstable glycosidic linkages. Oligochitosan can be developed by various methods like hydrolysis of acids [22], oxidative degradation [23], enzymatic hydrolysis [24], and ultrasonic degradation [25]. The amphiphilic properties of CHT derivatives have significantly enhanced their solubility and capacity to be self-assembled by intra- and intermolecular interaction of hydrophobic moieties as aggregates and micelles. It acts as an outstanding model for drug delivery and improves gene therapy transfection [26]. Hydroxyalkyl CHTs are formed when CHT reacts with epoxide. Self-assembled glycol CHT-based nanoparticles were prepared as a drug carrier [27]. Another cationic water-soluble derivative of CHT is the trimethylchitosan ammonium. It is formed due to the quaternization of CHT, i.e., by reacting with methyl iodide and sodium hydroxide to lower CHT acetyl content. Trimethylchitosan ammonium exhibits flocculating qualities such as dispersions of kaolin, making it essential in paper processing [28]. CHT’s mucoadhesive characteristics have been enhanced through the thiol group immobilization on polymer. Thiolated CHT improves permeation and shows excellent coherent properties for extended, regulated delivery of embedded therapeutic substances [29].
N-carboxymethyl CHT is a water-soluble CHT derivative with a broad range of uses in the food, medical, and gene therapy sectors [30]. It can be produced by glyoxylic acid treatment of CHT. It is required to build various protein drug delivery systems, like super porous hydrogels, cross-linked hydrogels, and pH-sensitive hydrogels [31]. N-methylene phosphonic CHT (NMPC) is an anionic derivative that exhibits amphoteric characteristics. NMPC has cation-binding efficacy, like Ca2+ and several transition metals (Cd2+, Cu2+, Zn2+) [32]. N-arylated CHT has a hydrophobic nature as well as hydrophilic and nucleophilic properties at the atom of nitrogen [33].
CHT sulfates, besides their antisclerotic, antibacterial, antiviral, antioxidant, and enzyme inhibition functions, have been shown to have anticoagulant and heamagglutination action owing to a structural resemblance to heparin. They also have excellent adsorption capabilities and are used for the recovery of metal ions. Compounds of sulfur are grafted onto CHT for mercury recovery and precious metal uptake. Sulphonic CHTs are fine metallic oxide flocculants [34]. Another functional by-product of CHT, lactic-glycolic acid-chitosan hydrogels, show greater interactions between water and CHT chains. These may be generated without any catalyst by direct grafting of D, L-lactic, or glycolic acid on CHT. This has significant usage for drug delivery systems and wound dressings in the biomedical sector [35]. CHT bonded with sugar has unique receptor-binding characteristics and is being studied for its antiviral impacts [36]. A CHT-containing cyclodextrin pendant has been produced to improve the drug delivery systems, cosmetics, and textile effluent decontamination [37].
Modifications of CHT with phosphorylcholine substances offer anticoagulant properties. Enzymatic grafting of phenolic substances onto CHT has been documented utilizing tyrosinase to impart water solubility under specific conditions [38]. DNA delivery is performed using grafted CHTs such as PEG–CHT, galactosylated CHT, etc. [39]. Most of the hydrogels grafted with polyacryl show stimulus-sensitive behavior such as pH or temperature, or both [40]. CHT salts such as formate, lactate, acetate, malate, citrate, glyoxylate, tartarate, pyruvate, malonate, ascorbate, and glycolate are soluble in water. CHT is most desired for its charges and diverse functional groups that make it possible to exploit into several variants with applications in different areas [41].

3. Effect of Chitosan Biopolymer on Plant Growth

Chitosan functions as a plant growth promoter in various crops such as beans, potato, radish, gerbera, soybean, cabbage, and other crops. As a result of plant growth promotion, it also enhances yield. Chitosan has a major influence on the growth rates of shoots, roots, flowering, and the number of flowers. As chitosan molecules are extremely hydrophilic, they reduce stress damage in plant cells by decreasing water content and accelerating several biological macromolecules’ activities. Three trials were conducted on orchids to determine the effect of CHT on organogenesis; the results showed that CHT could produce positive results at a very low concentration [42,43,44]. The results also suggested that CHT was working as a consequence of other metabolic processes rather than merely enhancing nitrogen nutritional quality or as a source of energy for the production of carbohydrates. Both Pornpeanpakdee et al. [43] and Nahar et al. [44] found that orchid growth (Dendrobium and Cymbidium) was stimulated by the supply of CHT to micropropagated plants that grow under sterile conditions. This is corroborated by other findings showing increased growth in aseptic conditions like tissue cultured grapes [45] and the growth of Phyla dulcis in liquid bioreactors [46].
Significant growth improvements have been found by several studies in daikon radishes [47], cabbage [48], soybean sprouts [49], sweet basil [50], and also in ornamental crops, including Gerbera [51] and Dendrobium orchids [42] by various modes of application such as in vitro, in vivo, soil application, pot application and biofertilization. To increase maize yield, a mixture of CHT and plant-growth-promoting rhizobacteria can be utilized as biofertilizers [52]. It is utilized in potted freesia cultivation as a biostimulator [53]. Vasudevan et al. [54] reported that the use of CHT formulation could accelerate the length of root and shoot and yield of rice grain. It also promotes the growth of plants such as pepper, cucumber and tomato raised in the nursery. Therefore, we have enlisted some important agricultural crops that showed improved plant growth and development due to the application of CHT (Table 1).

4. Suppression of Plant Disease by Chitosan

Chitosan has gained popularity in recent years as an environmentally friendly approach to controlling crop diseases [82]. Among the most documented properties of CHT is its effective antimicrobial activity against a wide range of micro-organisms, including fungi, bacteria, viruses, and nematodes. An antimicrobial component is classified as a component that kills micro-organisms or suppresses their growth [83].

4.1. Antifungal Activity of CHT

Since Allan and Hadwiger [84] documented CHT as a bio-fungicide in 1979, it has gained considerable interest in terms of plant protection research. Fungicidal efficacy of CHT against different species of fungi and Oomycetes has been reported [85,86]. It prevents the growth of several pathogenic fungi in vitro, such as Alternaria alternata, Botrytis cinerea, Penicillium digitatum, Colletotrichum gleosporoides, Rhizopus stolonifera, etc. The suppression was found in different stages of pathogen development, including hyphal growth, spore formation, spore viability, germination, and fungal virulence factor production [87]. El Ghaouth et al. [88] found that CHT has been effective in completely suppressing the mycelial development of Pythium aphanidermatum. In the study on Phytophthora capsici in peppers by Xu et al. [89], it was observed that the major impact detected in the pathogen was the disturbance of the endomembrane system, particularly the vacuoles’ integrity. It controlled damping-off [90], Alternaria blight in tomato [10], and inhibited the growth of Fusarium oxysporum f. sp. tracheiphilum [91]. CHT successfully prevents the radial hyphal growth, spore formation, germination of spore, and elongation of Fusarium spp. [90,92], Rhizopus spp. [93,94], Penicillium spp. [95], Phytophthora spp. [96,97], Botrytis spp. [98] and Alternaria spp. [10]. The major advantage of CHT use is that it can be formulated and utilized to improve its antifungal activity as a natural antifungal agent in nanoparticles and many other forms. Ing et al. [99] documented an improved inhibitory effect of CHT nanoparticles against Candida albicans and Fusarium solani compared with the regular form of CHT. Chitosan silver nanoparticles suppressed Colletotrichum gloeosporioides conidia germination more efficiently than CHT alone [100].
CHT also has potential in controlling fungal diseases like root rot (Bipolaris sorokiniana) of wheat [87], kernel rot (Aspergillus flavus) of pre-harvest maize [101], disease of pear caused by Physalospora piricola and Alternaria kikuchiana [102], brown rot (Monilinia fructicola) of peach fruit [103], post-harvest pathogenic fungi (Rhizopus stolonifer, Aspergillus niger) of grapes [93], anthracnose (Plasmopara viticola) and downy mildew (Elsinoe ampelina) of grapevines [104], and downy mildew (Sclerospora graminicola) of pearl millet [105].
Furthermore, the antifungal activity of CHT was also documented in vivo in several plant–pathogen systems like in rice against Rhizoctonia solani [106], in potato against Phytophthora infestans [107], in tomato against Fusarium oxysporum [108], in pepper against Phytophthora capsici [89], in tobacco against Phytophthora parasitica [96], in strawberry and in grapevine against Botrytis cinerea [109,110], and in dragon fruit against Colletotrichum gloeosporoides [111]. It also controls Penicillium spp. [95], Puccinia spp. [112], and Colletotrichum spp. [113], which causes diseases in a wide variety of crops. These studies have demonstrated that CHT is fungistatic against necrotrophic and biotrophic pathogens. Therefore, we enlisted the antifungal efficacy of CHT obtained from numerous studies on different crops, fruits and vegetables in Table 2.

4.2. Antibacterial Activity of CHT

Like fungi, bacteria are also extremely sensitive to CHT and its derivatives. Most antibacterial CHT reports relate to human bacterial diseases caused by Staphylococcus aureus, Escherichia coli and other Bacillus species. While CHT shows bactericidal activities toward a range of human diseases caused by bacteria, it might be anticipated that CHT can protect plants from bacterial infections. Some researchers recently found that CHT has strong in vitro and in vivo antibacterial activities towards different plant pathogenic bacteria, like Xanthomonas spp. [149,150], Pseudomonas spp. [151,152], Streptomyces scabies [153], Burkholderia seminalis [154], Acidovorax spp. [155,156]; Ralstonia solanacearum [157], and Staphylococcus aureus [152].
Foliar application of a commercial CHT formulation (Armour-Zen®) was capable of reducing the occurrence of Xanthomonas vesicatoria in vitro and in vivo growing tomato plants [150]. Li et al. [149] also reported significant antibacterial activity towards leaf streak (Xanthomonas oryzae pv. oryzicola) and leaf blight (Xanthomonas oryzae pv. oryzae) of rice. CHT solutions have considerably decreased disease incidence and lesion length of broccoli that were inoculated with Pseudomonas fluorescens [151]. A commercial formulation of CHT known as Elexa strongly protected cucumber from bacterial angular leaf spot damage caused by Pseudomonas lachrymans [158]. The inhibitory activity of CHT against bacteria varied with concentration of CHT used [155], molecular weight [159], bacterial type (Gram-positive and Gram-negative) [160], bacterial surface and cell wall composition structure [161], solvent type [162]; period of incubation and abiotic factors [163]. From these findings, it is apparent that CHT can be utilized as a potential control agent for plant diseases caused by bacteria. Bacterial plant pathogens that are inhibited by CHT are enlisted in Table 3.

4.3. Antiviral Activity of CHT

Chitosan has been demonstrated to suppress a few plant viral diseases. Nevertheless, it has yet to be proven that CHT inactivates viruses directly, which in itself would seem impossible, as viruses do not have chitin or associated polysaccharides. It has been proved that CHT inhibits the systemic proliferation of viroids and viruses across the plant and enhances the host’s hypersensitive reactions to infection [87]. CHT’s ability to inhibit viral plant infections is not dependent on type of virus, as CHT impacts the plant itself by triggering resistance to viral diseases [168]. Chirkov et al. [169] observed that CHT application on potato plants inoculated with potato virus X (PVX) displayed resistance to PVX virus. In addition, CHT-treated tomato plants displayed resistance to tomato mosaic virus, and also improved their vegetative growth [170]. Moreover, the formulation of CHT with plant growth-promoting rhizobacteria exerted leaf curl virus resistance in tomato plants [171]. CHT has also been found to be efficient towards the suppression of squash mosaic virus (SMV) [172]. CHT protected different plant species from systemic and local infection [169] when virus particles were applied on plant leaves either by inoculating or spraying. The effects of CHT on various phyto-pathogenic viruses are listed in Table 4.

4.4. Nematicidal Activity of CHT

A range of studies has suggested, from the 1980s onward, that CHT is useful in controlling the population of plant pathogenic nematode [177]. Application of CHT in soil promotes the multiplication of chitinolytic microorganisms that degrade chitin containing the organ of plant parasitic nematodes, and reduces egg hatching and the viability of larvae and adults belonging to Meloidogyne javanica [178], Meloidogyne arenaria [177], and Heterodera schachtii [179]. Due to the high nitrogen content in CHT, higher emissions of ammonia can also create toxicity to nematodes [180]. CHT showed elicitor activity by activating mechanisms of systemic and local resistance of tomato plants toward the root-knot nematode Meloidogyne incognita. CHT with low molecular weight controls M. Incognita in a better way [180]. Pinewood nematode (Bursaphelen chusxylophilus), a stem nematode, is managed by CHT–based nanoparticles of avermectin [181]. CHT improves the parasitism of Meloidogyne javanica eggs by Pochonia chlamydosporia, and also increases the differentiation of appressorium in Pochonia chlamydosporia [178]. In addition, Westerdahl et al. [179] reported that chitosan’s control level of nematodes on walnuts and potatoes was higher compared to synthetic nematicide 1,3-dichloropropene. The effects of CHT on various plant pathogenic nematodes are summarized in Table 5.

5. Mechanism of Actions of Chitosan Biopolymer

5.1. CHT as a Plant Growth Promoter

Numerous findings have been documented on various crops regarding the application of CHT as in vitro, in vivo, soil application, pot application and biofertilization to promote plant growth (Figure 1). CHT facilitates plant growth by increasing the uptake and availability of water and important nutrients by adjusting osmotic pressure in the cells [17]. For the past decade, signaling mechanisms of CHT and its derivatives were studied to control plant growth and development processes. Initial findings revealed that CHT helped activate the hydrolytic enzymes needed to degrade and mobilize reserve food materials including starch and protein [188]. CHT can promote the division of root cells by activating plant hormones including auxin and cytokinin that further lead to increased nutrient intake [189,190]. Other potential contributions are higher seed germination, enhanced seedling growth and development, and activation of antioxidant enzymes to prevent the potential damage by the reactive oxygen species (ROS) at the time of seed germination [62,74,188].
Amin et al. [191] reported that plant-growth-enhancing activities of CHT can be directly linked to impacts on plant physiological mechanisms, including nutrient absorption, cell division, cell elongation, enzymatic activation and synthesis of protein. According to Batool and Asghar [70], Carum copticum seeds primed with varied concentrations of CHT led to an increase in percentage of germination, rate of germination, vigor index of seedling, hypocotyl, and dry weight and radical length compared to control. Shao et al. [58] observed that maize seeds soaked with CHT significantly enhanced the percentage of germination. Seed priming with CHT Nanoparticles (NPs) stimulated seed germination percentage and the vigor index of maize, tomato, and chickpea, leading to the early establishment of healthy seedlings [59,62,74].
Zeng and Luo [192] stated that CHT has an excellent property of forming a semi-permeable film on the seed surface that can retain the moisture of the seed and absorb additional moisture from the soil, thereby promoting seed germination. Treatment of maize seed with Cu-chitosan NPs controlled the synthesis of hydrolytic enzymes like protease and α-amylase, and strengthened their activities. Increased activity of protease and α-amylase led to the rapid mobilization and degradation of preserved food, which resulted in increased germination and SVI of maize [59]. CHT NPs also significantly enhanced the biophysical properties, such as the nutrient intake and net rate of photosynthesis, which contributed to coffee seedling growth promotion. Positively charged nano-sized CHT can easily penetrate into plant cells or adhere to plant surfaces and enhance seed germination and biophysical properties. CHT also increased crop yield substantially by improving the index of photosynthesis by enhancing stomatal function and chlorophyll content. The polycationic CHT raises stomatal cells’ osmotic pressure, resulting in increased stomatal opening and CO2 integration. In addition, CHT also enhances the biomass content of the leaf area and nitrogen fixation nodules of soybean [193].

5.2. CHT as Plant Disease Suppressor

From the discovery of chitosan’s broad-spectrum antimicrobial properties, considerable interest in this polymer and its derivatives has arisen in recent years. Several research findings have undoubtedly proven their potential application in controlling plant diseases in agriculture (Figure 2). Research related to unraveling the mechanism involved with the antimicrobial activity of microbiocides is an essential step in the developmental process. Nonetheless, the actual mechanisms of the antimicrobial activities of CHT and similar natural products are still unclear, which somehow restricts their use. Over the past decades, multiple modes of action have been suggested to explain CHT’s antimicrobial activity. Based on the findings from current studies, some concrete evidence regarding CHT’s antimicrobial mechanism and its potential to induce plant defense responses is now available. These growing proofs confirm that the CHT and CHT-derived products have dual modes of action, i.e., they suppress pathogen growth and alter the plant defense responses [194,195,196].
There are numerous reactive amino groups present in the structure of polycationic CHT polymer, which can be protonated, so the polymer can bear a net positive charge. The existence of reactive amino groups and positive charge is hypothesized to be the basis of CHT’s direct antimicrobial actions. The electrostatic interaction of negatively charged cell membranes of microbes with positively charged CHT and its derivatives leads to agglutination, destruction, and alteration of the cell membrane’s intracellular ultrastructure, which induces death of the organism [197,198]. The Gram-positive bacterial cell wall comprises a thick teichoic acid-rich peptidoglycan layer that is negatively charged due to the existence of phosphate groups within the structure, as lipopolysaccharides convey a highly negative charge to the bacterial surface in Gram-negative bacteria. In addition, the fungal cell membrane and viral envelope contain similar negatively charged substances (proteins, and glycoproteins). Recently, Lopez-Moya et al. [114] reported that CHT induces plasma membrane permeabilization of Magnaporthe oryzae fungus of rice, and influences NADPH oxidase-dependent synthesis of ROS, important for fungal pathogenicity.
CHT can also affect the cell membrane structure by interfering with proteins in bacterial cell membrane (Figure 2) [199]. Therefore, it is assumed that membrane proteins may be the target molecules for the action of CHT on cell surfaces. The potassium ion efflux has been reported as an early cell response to the presence of certain cationic molecules. A rapid potassium efflux was reported, which was dependent on the concentration of CHT. Moreover, CHT has a strong inhibitory effect on H+-ATPase activity in the Rhizopus stolonifer plasma membrane. Decreased activity of H+-ATPase may result in proton accumulation within the cell, leading to the inhibition of chemical transport driven for the exchange of H+/K+ [200]. The positively charged CHT molecules thus associate with negatively charged pathogenic surfaces, which damage the structure of the cell. This damage causes significant modifications to the surface of the cell and improves the membrane permeability, resulting in intracellular molecules’ leakage and eventually impairing vital activities of the pathogen [201,202,203].
An essential role of the cell wall and cell membrane is to protect the internal substances so that they do not spill outside of the cell [204]. Chung and Chen [205] stated that CHT responded to both the cell wall and cell membrane, and inhibited the bacterial growth through a two-step synchronous mechanism: the initial cell wall separation from its cell membrane, accompanied by cell membrane destruction. The function of the pathogen genetic material may be interfered with by CHT. The nucleic acid (DNA or RNA) contains negatively charged phosphate groups in the primary chain. The CHT can penetrate the cell wall and attach to the negatively charged DNA, thus blocking the mRNA and the essential pathogenic proteins’ synthesis [198,206].
It is believed that CHT with lower molecular weight can move through the cell wall of bacteria [207,208], degrade intracellular materials from the colloidal phase to degeneration and flocculation, interfere with normal physiological and metabolic activities of bacteria or interact with genetic materials directly [209,210], and then suppress the bacterial reproduction, which leads to micro-organisms’ death. It is assumed that CHT may bind with DNA and inhibit messenger RNA (mRNA) synthesis via penetration to the microorganism nuclei and interfere with mRNA and protein synthesis [201,207].
The mechanism of action of CHT could also be linked to its capacity to chelate certain necessary nutrients, trace elements, and metal ions required for bacterial and fungal growth [201,211]. Another potential mode of CHT’s antibacterial effect is depositing on pathogen surface and forming a thick layer of polymer. This thick polymer film inhibits the process of nutrient flow and microbial metabolism that are important to their survival [194]. Plants also defend themselves against pathogens by creating a remarkable array of structural, chemical and protein-based safeguards designed to identify and arrest invasive pathogens before they can cause significant damage [212].
However, CHT only displays its antibacterial effect in an acidic medium, due to its low solubility beyond pH 6.5. CHT’s water-soluble derivatives can also be strong candidates, like polycationic biocide, which are soluble in both basic and acidic physiological conditions [213].
The impacts of CHT on the plant–fungal interaction of Botrytis cinerea in tomatoes and strawberries have been linked with aflatoxin reduction, phenolic, and phytoalexin precursors elicitation, increased production of chitinases and other plant defense factors [195,214]. In addition to producing phytoalexin, CHT also blocks the production of toxin by Alternaria alternata and macerating enzymes by Erwinia [215,216]. The direct interaction of Aspergillus flavus with CHT has been documented as generation of hyphal swelling and weakening [93]. The fungistatic properties of CHT against Rhizopus stolonifer were linked to its ability to cause morphological modifications in the cell wall [217].
CHT’s antiviral activity was found to rely on average polymerization frequency, degree of N-deacetylation, quality of positive charge, and character of the molecule’s chemical modifications. CHT is hypothesized to suppress viral infection by triggering a hypersensitive response, reducing the phage bacterial cells’ viability, neutralizing phage particle infectivity, and preventing the replication of virulent phage [168]. Phage particle silencing and disruption of bacteriophage replication at the cellular level are the key factors in preventing phage infections by CHT. By its potential to trigger resistance to viral diseases in plants, CHT exhibits an antiviral effect to inhibit the replication of bacteriophages in contaminated microorganism cultures. Imitating the plant’s interaction with a phytopathogen, CHT triggers a broad array of protective responses in the plant, which restrict the systemic spread of viroids and viruses throughout the plant, resulting in systemic acquired resistance development [168].
Some studies show that CHT and its derivatives are powerful elicitors and inducers of systemically acquired resistance of plants against a wide array of pathogens. CHT and oligochitosan induce hosts to generate protein, enzymes, and secondary metabolites linked to the protection from pathogens [194,206,218]. CHT and its derivatives enhance glucanase levels and activity in rice, wheat, tobacco, etc. [219,220,221]. CHT and its derivatives are also reported to enhance the activity of chitinase, peroxidase, phenylalanine ammonia-lyase, polyphenol oxidase, superoxide dismutase and catalase in wheat, cucumber, tomato, sweet cherries, table grapes, pears, orange, strawberries, Zanthoxylum bungeanum and ginseng [194,196,222,223,224,225]. The pathogen is inhibited directly or indirectly by all the stated proteins and enzymes. Generally, genes which functionally produce disease resistance are known as pathogenesis-associated genes. Several findings revealed that CHT uses several modes to improve the function of pathogenesis-associated genes. According to Hoat et al. [226], CHT and chitin significantly triggered the pathogenesis-associated gene expression in oat leaves. It is well known that in the plant defense system, secondary metabolites, including phytoalexins, suberization, lignin and phenolic compounds, perform a major role. The role of CHT in defense-associated secondary metabolites accumulation in plant tissue was reported in the 1980s, since Hadwiger and Beckman [227] noticed that CHT could trigger the accumulation of phytoalexin in soybean pod at a concentration of 0.9 μg mLG1 in 24 h.
Resistant plants possess the ability to identify plant pathogens quickly to activate the defense mechanism rapidly and fruitfully. Activation of the defensive mechanism is expressed through hypersensitive response (HR) in the infection site and activation of defense in the unaffected part of the plant [228]. The elicitation of HR and systemic acquired resistance (SAR) are regulated by the host and pathogen’s genetic background and depends on a complex signal exchange that occurs under the given environmental conditions. Signal transduction mechanisms consist of stimulation of the target receptor on the cell membrane or intracellular site, followed by signal propagation to the target cell by one or more second messengers and the formation of physiological response sequences. Lectin and kinase 1 (CERK1) are two cell membrane receptors that are able to bind CHT and its oligomers [229,230]. CHT also affects the DNA conformation of the plant. Because of the high affinity of DNA backbone to negatively charged phosphates, CHT can modify chromatin by competing with specific nuclear proteins for the DNA binding sites, which in turn block gene transcription [206,226]. It has been reported that ROS, Ca2+, nitric oxide (NO), ethylene (ET), jasmonic acid (JA), abscisic acid (ABA) and salicylic acid (SA) all participate in the CHT-mediated signaling pathway [6,194].
From the above-mentioned body of literature, it may be concluded that CHT and its derivatives are capable of directly destroying the pathogen and activating the immune (defense response) system of plants via various signaling processes or through regulatory molecules engaged in signal transduction [231]. The mode of action of CHT in preventing plant infections has not been clearly understood, despite extensive study. Some of the proposed modes of action of CHT against various pathogens are enlisted in Table 6.

6. Concluding Remarks and Future Perspectives

Chitosan, a chitin derivative, is the second most widely distributed abundant natural polymer. Over the last decade, the number of uses of CHT and its derivatives has significantly increased. The availability of information on biocompatible and biological characteristics of CHT makes it a potential bioactive substance for agriculture. CHT is a versatile nontoxic compound with multiple modes of action to positively impact plant health. Its application can mitigate the broad use of chemical pesticides, at least in part. To date, there is ample evidence to suggest that plants may achieve improved tolerance to a broad range of pathogenic micro-organisms, and promote growth and development after the application of CHT, suggesting that the utilization of natural elicitors like CHT may be an essential component of sustainable agriculture.
While a lot of work has been done, several issues still remain unclear pertaining to the mechanisms of pathogens’ growth inhibition by CHT, inducing plant immunity, accelerating plant growth and development. In that regard, research and development should pay attention to discovering new derivatives of CHT, as their effective chemical alteration might significantly boost its antimicrobial efficacy, improve its chemical and physical characteristics, and enhance its field applicability by ensuring low mammalian toxicity. CHT and its derivatives apparently rely on their molecular weight for the majority of physiological activity and functionality. In addition, further study is needed to confirm whether biopolymers like CHT have the ability to influence physiological processes or metabolism in microbes. Future studies may aim at explaining the real target molecule on the cell membrane, or even other intracellular targets in case of an antimicrobial mechanism of action. Moreover, further investigations are also required for pathogen resistance mechanisms against this polymer.
Therefore, future studies should also concentrate on understanding the details at the molecular levels, which can offer an insight into the unknown biochemical mechanisms of CHT. It may provide significant benefits if gene mutant strains of microbes can be developed to study the antimicrobial mechanisms of CHT. Combined proteome and transcriptome study of known proteins and genes would enhance our knowledge of the complex CHT-mediated signal pathway and allow for improving biotechnological approaches in plant infection control and growth promotion. A better understanding of CHT’s mode of action in plants and pathogens would improve the possibility of its effective application. Furthermore, the collaboration and participation of research organizations, government regulatory authorities and industries will be the primary key to the success of CHT use by unraveling its antimicrobial characteristics, innate immunity-induced activities, growth enhancement in plants and biotechnological prospects for sustainable agriculture.

Author Contributions

Conceptualization, T.I.; funding acquisition, T.I.; writing—original draft preparation, M.C.; writing—review and editing, T.I., M.H., M.R., M.A.R.K., P.B., N.U.M., M.T.; preparation of tables and figures, M.C., M.H., M.T.; supervision, T.I. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Krishi Gobeshona Foundation (KGF), Bangladesh through a coordinated project No. KGF TF 50-C/17 to T.I. of the Institute of Biotechnology and Genetic Engineering of BSMRAU, Bangladesh.

Acknowledgments

The authors are thankful to the Krishi Gobeshona Foundation (KGF), Bangladesh (KGF-TF 50-C/17) for funding this work. The funders had no role in study design, data collection and decision to publish, or preparation of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kurita, K. Chitin and chitosan: Functional biopolymers from marine crustaceans. Mar. Biotechnol. 2006, 8, 203–226. [Google Scholar] [CrossRef]
  2. Braconnot, H. Sur la nature des champignons. Annu. Chem. 1811, 79, 265–304. [Google Scholar]
  3. Labrude, P.; Becq, C. Pharmacist and chemist Henri BraconnotLe pharmacien et chimiste Henri Braconnot. Rev. Hist. Pharm. 2003, 51, 61–78. [Google Scholar] [CrossRef]
  4. Hoppe-Seiler, F. Ueber chitosan und zellulose. Ber. Dtsch. Chem. Ges. 1894, 27, 3329–3331. [Google Scholar] [CrossRef]
  5. Anitha, A.; Sowmya, S.; Kumar, P.T.S.; Deepthi, S.; Chennazhi, K.P.; Ehrlich, H.; Tsurkan, M.; Jayakumar, R. Chitin and chitosan in selected biomedical applications. Prog. Polym. Sci. 2014, 39, 1644–1667. [Google Scholar] [CrossRef]
  6. Malerba, M.; Cerana, R. Chitosan effects on plant systems-A review. Int. J. Mol. Sci. 2016, 17, 996. [Google Scholar] [CrossRef] [PubMed]
  7. Park, Y.; Kim, M.H.; Park, S.C.; Cheong, H.; Jang, M.K.; Nah, J.W.; Hahm, K.S. Investigation of the antifungal activity and mechanism of action of LMWS-chitosan. J. Microbiol. Biotechnol. 2008, 18, 1729–1734. [Google Scholar]
  8. Wang, B.; Zhang, S.; Wang, X.; Yang, S.; Jiang, Q.; Xu, Y.; Xia, W. Transcriptome analysis of the effects of chitosan on the hyperlipidemia and oxidative stress in high-fat diet fed mice. Int. J. Biol. Macromol. 2017, 102, 104–110. [Google Scholar] [CrossRef]
  9. Sathiyabama, M.; Charles, R.E. Fungal cell wall polymer based nanoparticles in protection of tomato plants from wilt disease caused by Fusarium oxysporum f. sp. lycopersici. Carbohydr. Polym. 2015, 133, 400–407. [Google Scholar] [CrossRef]
  10. Sathiyabama, M.G.; Akila, R.; Einstein, C. Chitosan-induced defence responses in tomato plants against early blight disease caused by Alternaria solani (Ellis and Martin) Sorauer. Arch. Phytopathol. Plant Prot. 2014, 47, 1777–1787. [Google Scholar] [CrossRef]
  11. Kulikov, S.N.; Chirkov, S.N.; Ilina, A.V.; Lopatin, S.A.; Varlamov, V.P. Effect of the molecular weight of chitosan on its antiviral activity in plants. Appl. Biochem. Microbiol. 2006, 42, 200–203. [Google Scholar] [CrossRef]
  12. Silva, M.; Nunes, D.; Cardoso1, A.R.; Ferreiral, D.; Britol, M.; Pintadol, M.E.; Vasconcelos, M.W. Chitosan as a biocontrol agent against the pinewood nematode (Bursaphelenchus xylophilus). For. Pathol. 2014, 44, 420–423. [Google Scholar] [CrossRef]
  13. Sun, D.; Liang, G.; Xie, J.; Lei, X.; Mo, Y. Improved preservation effects of litchi fruit by combining chitosan coating with ascorbic acid treatment during postharvest storage. Afr. J. Biotechnol. 2010, 9, 3272–3279. [Google Scholar]
  14. Rahman, M.; Mukta, J.A.; Sabir, A.A.; Gupta, D.R.; Mohi-ud-din, M.; Hasanuzzaman, M.; Miah, M.G.; Rahman, M.; Islam, M.T. Chitosan biopolymer promotes yield and stimulates accumulation of antioxidants in strawberry fruit. PLoS ONE 2018, 13, e0203769. [Google Scholar] [CrossRef] [PubMed]
  15. Emami Bistgani, Z.; Siadat, S.A.; Bakhshandeh, A.; Ghasemi Pirbalouti, A.; Hashemi, M. Interactive effects of drought stress and chitosan application on physiological characteristics and essential oil yield of Thymus daenensis Celak. Crop J. 2017, 5, 407–415. [Google Scholar] [CrossRef]
  16. Xoca-Orozco, L.-Á.; Cuellar-Torres, E.A.; González-Morales, S.; Gutiérrez-Martínez, P.; López-García, U.; Herrera-Estrella, L.; Vega-Arreguín, J.; Chacón-López, A. Transcriptomic analysis of avocado hass (Persea americana Mill) in the interaction system fruit-chitosan-Colletotrichum. Front. Plant Sci. 2017, 8, 956. [Google Scholar] [CrossRef] [Green Version]
  17. Guan, Y.; Hu, J.; Wang, X.; Shao, C. Seed priming with chitosan improves maize germination and seedling growth in relation to physiological changes under low temperature stress. J. Zhejiang Univ. Sci. B 2009, 10, 427–433. [Google Scholar] [CrossRef] [Green Version]
  18. Muzzarelli, R.A. Natural Chelating Polymers; Alginic Acid, Chitin and Chitosan. In Natural Chelating Polymers; Alginic Acid, Chitin and Chitosan; Pergamon Press: Oxford, UK, 1973. [Google Scholar]
  19. Rinaudo, M. Chitin and chitosan: Properties and applications. Prog. Polym. Sci. 2006, 31, 603–632. [Google Scholar] [CrossRef]
  20. Shahidi, F.; Abuzaytoun, R. Chitin, chitosan, and co-products: Chemistry, production, applications, and health effects. Adv. Food Nutr. Res. 2005, 49, 93–135. [Google Scholar]
  21. Sarmento, B.; Francisco, M.; Goycoolea, F.M.; Sosnik, A.; das Neves, J. Chitosan and chitosan derivatives for biological applications: Chemistry and functionalization. Int. J. Carbohy. Chem. 2011, 802693. [Google Scholar] [CrossRef] [Green Version]
  22. Aljbour, N.D.; Beg, M.D.H.; Gimbun, J. Acid hydrolysis of chitosan to oligomers using hydrochloric acid. Chem. Eng. Technol. 2019, 42, 1741–1746. [Google Scholar] [CrossRef]
  23. Ma, Z.; Wang, W.; Wu, Y.; He, Y.; Wu, T. Oxidative degradation of chitosan to the low molecular water-soluble chitosan over peroxotungstate as chemical scissors. PLoS ONE 2014, 9, e100743. [Google Scholar] [CrossRef] [PubMed]
  24. Kaczmarek, M.B.; Struszczyk-Swita, K.; Li, X.; Szczęsna-Antczak, M.; Daroch, M. Enzymatic modifications of chitin, chitosan, and chitooligosaccharides. Front. Bioeng. Biotechnol. 2019, 7, 243. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Kasaai, M.R.; Arul, J.; Charlet, G. Fragmentation of chitosan by ultrasonic irradiation. Ultrason. Sonochem. 2008, 15, 1001–1008. [Google Scholar] [CrossRef] [PubMed]
  26. Dowling, M.B.; Kumar, R.; Keibler, M.A.; Hess, J.R.; Bochicchio, G.V.; Raghavan, S.R. A self-assembling hydrophobically modified chitosan capable of reversible hemostatic action. Biomaterials 2011, 32, 3351–3357. [Google Scholar] [CrossRef] [PubMed]
  27. Park, J.H.; Kwon, S.; Lee, M.; Chung, H.; Kim, J.H.; Kim, Y.S.; Park, R.W.; Kim, I.S.; Seo, S.B.; Kwon, I.C.; et al. Self-assembled nanoparticles based on glycol chitosan bearing hydrophobic moieties as carriers for doxorubicin: In vivo biodistribution and antitumor activity. Biomaterials 2006, 27, 119–126. [Google Scholar] [CrossRef] [PubMed]
  28. Zargar, V.; Asghari, M.; Dashti, A. A review on chitin and chitosan polymers: Structure, chemistry, solubility, derivatives, and applications. ChemBioEng Rev. 2015, 2, 204–226. [Google Scholar] [CrossRef]
  29. Kafedjiiski, K.; Krauland, A.H.; Hoffer, M.H.A. Bernkop-Schnurch, synthesis and in vitro evaluation of a novel thiolated chitosan. Biomaterials 2005, 26, 819–826. [Google Scholar] [CrossRef]
  30. Khanjari, A.; Karabagias, I.; Kontominas, M. Combined effect of N, O-carboxymethyl chitosan and oregano essential oil to extend shelf life and control Listeria monocytogenes in raw chicken meat fillets. LWT Food Sci. Technol. 2013, 53, 94–99. [Google Scholar] [CrossRef]
  31. Yin, L.; Fei, L.; Cui, F.; Tang, C.; Yin, C. Superporous hydrogels containing poly (acrylic acidco-acrylamide)/O-carboxymethyl chitosan interpenetrating polymer networks. Biomaterials 2007, 28, 1258–1266. [Google Scholar] [CrossRef]
  32. Xiao, B.; Wan, Y.; Wang, X.; Zha, Q.; Liu, H.; Qiu, Z.; Zhang, S. Synthesis and characterization of N-(2-hydroxy)propyl-3-trimethyl ammonium chitosan chloride for potential application in gene delivery. Colloids Surf. B Biointerfaces 2012, 91, 168–174. [Google Scholar] [CrossRef] [PubMed]
  33. Sajomsang, W. Synthetic methods and applications of chitosan containing pyridylmethyl moiety and its quaternized derivatives: A review. Carbohydr. Polym. 2010, 80, 631–647. [Google Scholar] [CrossRef]
  34. Xing, R.; Yu, H.; Liu, S.; Zhang, W.; Zhang, Q.; Li, Z.; Li, P. Antioxidant activity of differently regioselective chitosan sulfates in vitro. Bioorg. Med. Chem. 2005, 13, 1387–1392. [Google Scholar] [CrossRef] [PubMed]
  35. Abd-Alla, M.; Wafaa, M. New safe methods for controlling anthracnose disease of mango (Mangifera indica L.) fruits caused by Colletotrichum gloeosporioides (Penz.). J. Am. Sci. 2010, 8, 361–367. [Google Scholar]
  36. Morimoto, M.; Saimoto, H.; Usui, H.; Okamoto, Y.; Minami, S.; Shigemasa, Y. Biological activities of carbohydrate-branched chitosan derivatives. Biomacromolecules 2001, 2, 1133–1136. [Google Scholar] [CrossRef]
  37. Prabaharan, M.; Mano, J.F. Chitosan derivatives bearing cyclodextrin cavities as novel adsorbent matrices. Carbohydr. Polym. 2006, 63, 153–166. [Google Scholar] [CrossRef]
  38. Kumar, G.; Smith, P.J.; Payne, G.F. Enzymatic grafting of a natural product onto chitosan to confer water solubility under basic conditions. Biotechnol. Bioeng. 1999, 63, 154–165. [Google Scholar] [CrossRef]
  39. Park, I.K.; Park, Y.H.; Shin, B.A.; Choi, E.S.; Kim, Y.R.; Akaike, T.; Cho, C.S. Galactosylated chitosan-graft-dextran as hepatocyte-targeting DNA carrier. J. Control. Release 2000, 69, 97–108. [Google Scholar] [CrossRef]
  40. Mahdavinia, G.R.; Pourjavadi, A.; Hosseinzadeh, H.; Zohuriaan, M.J. Modified chitosan 4. Superabsorbent hydrogels from poly (acrylic acid-co-acrylamide) grafted chitosan with salt-and pH-responsiveness properties. Eur. Polym. J. 2004, 40, 1399–1407. [Google Scholar] [CrossRef]
  41. Prashanth, K.V.H.; Tharanathan, R.N. Chitin/chitosan: Modifications and their unlimited application potential – An overview. Trends. Food Sci. Technol. 2007, 18, 117–131. [Google Scholar] [CrossRef]
  42. Chandrkrachang, S. The applications of chitin in agriculture in Thailand. Adv. Chitin Sci. 2002, 5, 458–462. [Google Scholar]
  43. Pornpeanpakdee, P.; Pichyangkura, R.; Chadchawan, S.; Limpanavech, P. Chitosan effects on Dendrobium ‘Eiskul’ Protocorm-like body production. In Proceedings of the 31st Congress on Science and Technology of Thailand, Nakornrachaseema, Thailand, 18–20 October 2005; pp. 1–3. [Google Scholar]
  44. Nahar, S.J.; Kazuhiko, S.; Haque, S.M. Effect of Polysaccharides Including Elicitors on Organogenesis in Protocorm-like Body (PLB) of Cymbidium insigne in vitro. J. Agric. Sci. Technol. 2012, 2, 1029–1033. [Google Scholar]
  45. Barka, E.A.; Eullaffroy, P.; Clément, C.; Vernet, G. Chitosan improves development, and protects Vitis vinifera L. against Botrytis cinerea. Plant Cell Rep. 2004, 22, 608–614. [Google Scholar] [CrossRef] [PubMed]
  46. Sauerwein, M.; Flores, H.M.; Yamazaki, T.; Shimomura, K. Lippia dulcis shoot cultures as a source of the sweet sesquiterpene hernandulcin. Plant Cell Rep. 1991, 9, 663–666. [Google Scholar] [CrossRef] [PubMed]
  47. Tsugita, T.; Takahashi, K.; Muraoka, T.; Fukui, H. The application of chitin/chitosan for agriculture (in Japanese). In Proceedings of the Special Session of the 7th Symposium on Chitin and Chitosan, Fukui, Japan, 6 March 1993; Japanese Society for Chitin and Chitosan: Fukui, Japan, 1993; pp. 21–22. [Google Scholar]
  48. Spiegel, Y.; Kafkafi, U.; Pressman, E. Evaluation of a protein-chitin derivative of crustacean shells as a slow-release nitrogen fertilizer on Chinese cabbage. J. Hortic. Sci. 1988, 63, 621–628. [Google Scholar] [CrossRef]
  49. Lee, Y.S.; Kim, Y.H.; Kim, S.B. Changes in the respiration, growth, and vitamin C content of soybean sprouts in response to chitosan of different molecular weights. Hortic. Sci. 2005, 40, 1333–1335. [Google Scholar] [CrossRef] [Green Version]
  50. Pirbalouti, A.G.; Malekpoor, F.; Salimi, A.; Golparvar, A. Exogenous application of chitosan on biochemical and physiological characteristics, phenolic content and antioxidant activity of two species of basil (Ocimum ciliatum and Ocimum basilicum) under reduced irrigation. Sci. Hortic. 2017, 217, 114–122. [Google Scholar] [CrossRef]
  51. Wanichpongpan, P.; Suriyachan, K.; Chandrkrachang, S. Effects of Chitosan on the growth of Gerbera flower plant (Gerbera jamesonii). In Chitin and Chitosan in Life Science, Proceedings of the Eighth International Chitin and Chitosan Conference and Fourth Asia Pacific Chitin and Chitosan Symposium, Yamaguchi, Japan, 21–23 September 2000; Uragami, T., Kurita, K., Fukamizo, T., Eds.; Kodansha Scientific: Tokyo, Japan, 2001; pp. 198–201. [Google Scholar]
  52. Choudhary, R.C.; Kumaraswamy, R.V.; Kumari, S.; Sharma, S.S.; Pal, A.; Raliya, R.; Biswas, P.; Saharan, V. Cu-chitosan nanoparticle boost defense responses and plant growth in maize (Zea mays L.). Sci. Rep. 2017, 7, 9754–9765. [Google Scholar] [CrossRef]
  53. Salachna, P.; Zawadzinska, A. Effect of chitosan on plant growth, flowering and corms yield of potted freesia. J. Ecol. Eng. 2014, 15, 93–102. [Google Scholar]
  54. Vasudevan, P.; Reddy, M.S.; Kavitha, S.; Velusamy, P.; Paul Raj, R.S.D.; Priyadarisini, V.B.; Bharathkumar, S.; Kloepper, J.W.; Gnanamanickam, S.S. Role of biological preparations in enhancement of rice seedling growth and seed yield. Curr. Sci. 2002, 83, 1140–1143. [Google Scholar]
  55. Phothi, R.; Theerakarunwong, C.D. Effect of chitosan on physiology, photosynthesis and biomass of rice (Oryza sativa L.) under elevated ozone. Aust. J. Crop Sci. 2017, 11, 624–630. [Google Scholar] [CrossRef]
  56. Chibu, H.; Shibayama, H.; Arima, S. Effects of chitosan application on the shoot growth of rice and soybean. Jpn. J. Crop Sci. 2002, 71, 206–211. [Google Scholar] [CrossRef] [Green Version]
  57. Zong, H.; Liu, S.; Xing, R.; Chen, X.; Li, P. Protective effect of chitosan on photosynthesis and antioxidative defense system in edible rape (Brassica rapa L.) in the presence of cadmium. Ecotoxicol. Environ. Saf. 2017, 138, 271–278. [Google Scholar] [CrossRef]
  58. Shao, C.X.; Hu, J.; Song, W.J.; Hu, W.M. Effects of seed priming with chitosan solutions of different acidity on seed germination and physiological characteristics of maize seedling. Agric. Life Sci. 2005, 31, 705–708. [Google Scholar]
  59. Saharan, V.; Kumaraswamy, R.; Choudhary, R.C.; Kumari, S.; Pal, A.; Raliya, R.; Biswas, P.J. Cu-Chitosan nanoparticle mediated sustainable approach to enhance seedling growth in maize by mobilizing reserved food. Agric. Food Chem. 2016, 64, 6148–6155. [Google Scholar] [CrossRef] [PubMed]
  60. Falcón-Rodríguez, A.B.; Costales, D.; Gónzalez-Peña, D.; Morales, D.; Mederos, Y.; Jerez, E.; Cabrera, J.C. Chitosans of different molecular weight enhance potato (Solanum tuberosum L.) yield in a field trial. Span. J. Agric. Res. 2017, 15, e0902. [Google Scholar]
  61. Kowalski, B.; Jimenez Terry, F.; Herrera, L.; Agramonte Peñalver, D. Application of soluble chitosan in vitro and in the greenhouse to increase yield and seed quality of potato minitubers. Potato Res. 2006, 49, 167–176. [Google Scholar] [CrossRef]
  62. Saharan, V.; Sharma, G.; Yadav, M.; Choudhary, M.K.; Sharma, S.; Pal, A.; Raliya, R.; Biswas, P. Synthesis and in vitro antifungal efficacy of Cu–chitosan nanoparticles against pathogenic fungi of tomato. Int. J. Biol. Macromol. 2015, 75, 346–353. [Google Scholar] [CrossRef]
  63. Mondal, M.M.A.; Malek, M.A.; Puteh, A.B.; Ismail, M.R.; Ashrafuzzaman, M.; Naher, L. Effect of foliar application of chitosan on growth and yield in okra. Aust. J. Crop Sci. 2012, 6, 918–921. [Google Scholar]
  64. Sultana, S.; Islam, M.; Khatun, M.A.; Hassain, M.A.; Huque, R. Effect of Foliar Application of Oligo-chitosan on growth, yield and quality of tomato and eggplant. Asian J. Agric. Res. 2017, 11, 36–42. [Google Scholar]
  65. Pereira, A.E.S.; Silva, P.M.; Oliveira, J.L.; Oliveira, H.C.; Fraceto, L.F. Chitosan nanoparticles as carrier systems for the plant growth hormone gibberellic acid. Colloids Surf. B Biointerfaces 2017, 150, 141–152. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Akter, J.; Jannat, R.; Hossain, M.M.; Ahmed, J.U.; Rubayet, M.T. Chitosan for plant growth promotion and disease suppression against anthracnose in chilli. Int. J. Agric. Environ. Biotechnol. 2018, 3, 806–817. [Google Scholar] [CrossRef] [Green Version]
  67. Chookhongkha, N.; Miyagawa, S.; Jirakiattikul, Y.; Photchanachai, S. Chili growth and seed productivity as affected by chitosan. In Proceedings of the International Conference on Agriculture Technology and Food Sciences (ICATFS’2012), Manila, Philippines, 17–18 November 2012; pp. 17–18. [Google Scholar]
  68. Mahmood, N.; Abbasi, N.A.; Hafiz, I.A.; Ali, I.; Zakia, S. Effect of biostimulants on growth, yield and quality of bell pepper cv. Yolo wonder. Pak. J. Agric. Sci. 2017, 54, 311–317. [Google Scholar]
  69. Anusuya, S.; Sathiyabama, M. Effect of chitosan on growth, yield and curcumin content in turmeric under field condition. Biocatal. Agric. Biotechnol. 2016, 6, 102–106. [Google Scholar] [CrossRef]
  70. Batool, M.; Asghar, R. Seed priming with chitosan improves the germination and growth performance of ajowan (Carum copticum) under salt stress. Eurasia J. Biosci. 2013, 7, 69–76. [Google Scholar]
  71. Ziani, K.; Ursúa, B.; Maté, J.I. Application of bioactive coatings based on chitosan for artichoke seed protection. Crop Prot. 2010, 29, 853–859. [Google Scholar] [CrossRef]
  72. Shehata, S.; Fawzy, Z.; El-Ramady, H. Response of cucumber plants to foliar application of chitosan and yeast under greenhouse conditions. Aust. J. Basic Appl. Sci. 2012, 6, 63–71. [Google Scholar]
  73. Mahdavi, B.; Safari, H. Effect of chitosan on growth and some physiological characteristics of chickpea under salinity stress condition. J. Plant Process Funct. 2015, 4, 117–127. [Google Scholar]
  74. Anusuya, S.; Nibiya Banu, K. Silver-chitosan nanoparticles induced biochemical variations of chickpea (Cicer arietinum L.). Biocatal. Agric. Biotechnol. 2016, 8, 39–44. [Google Scholar] [CrossRef]
  75. Van, S.N.; Minh, H.D.; Anh, D.N. Study on chitosan nanoparticles on biophysical characteristics and growth of Robusta coffee in green house. Biocatal. Agric. Biotechnol. 2013, 2, 289–294. [Google Scholar]
  76. Mutka, J.A.; Rahman, M.; Sabir, A.A.; Gupta, D.R.; Surovy, M.Z.; Rahman, M.; Islam, M.T. Chitosan and plant probiotics application enhance growth and yield of strawberry. Biocatal. Agric. Biotechnol. 2017, 11, 9–18. [Google Scholar]
  77. González Gómez, H.; Ramírez Godina, F.; Ortega Ortiz, H.; Benavides Mendoza, A.; Robledo Torres, V.; Cabrera De la Fuente, M. Use of chitosan-PVA hydrogels with copper nanoparticles to improve the growth of grafted watermelon. Molecules 2017, 22, 1031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Zagzog, O.A.; Gad, M.M.; Hafez, N.K. Effect of nano-chitosan on vegetative growth, fruiting and resistance of malformation of mango. Trends Hortic. Res. 2017, 6, 673–681. [Google Scholar]
  79. Sauerwein, M.; Yamazaki, T.; Shimomura, K. Hernandulcin in hairy root cultures of Lippia dulcis. Plant Cell Rep. 1991, 9, 579–581. [Google Scholar] [CrossRef]
  80. Irawati, E.B.; Sasmita, E.R.; Suryawati, A. Application of chitosan for vegetative growth of kemiri sunan plant in marginal land. IOP Conf. Ser. Earth Environ. Sci. 2019, 250, 012089. [Google Scholar] [CrossRef]
  81. Trzcinska, A.; Bogusiewic, A.; Szkop, M.; Drozdowski, S. Effect of chitosan on disease control and growth of scots pine (Pinus sylvestris L.) in a forest nursery. Forest 2015, 6, 3165–3176. [Google Scholar] [CrossRef] [Green Version]
  82. Orzali, L.; Corsi, B.; Forni, C.; Riccioni, L. Chitosan in agriculture: A new challenge for managing plant disease. In Biological Activities and Application of Marine Polysaccharides; Shalaby, E.A., Ed.; IntechOpen: London, UK, 2017. [Google Scholar]
  83. Andrews, J.M. Determination of minimum inhibitory concentrations. J. Antimicr. Chemoth. 2001, 48, 5. [Google Scholar] [CrossRef] [Green Version]
  84. Allan, C.R.; Hadwiger, L.A. The fungicidal effect of chitosan on fungi of varying cell wall composition. Exp. Mycol. 1979, 3, 285–287. [Google Scholar] [CrossRef]
  85. Muzzarelli, R.A.A.; Tarsi, R.; Filippini, O.; Giovanetti, E.; Biagini, G.; Varaldo, P.E. Antimicrobial properties of N-carboxybutyl chitosan. Antimicrob. Agents Chemother. 1990, 34, 2019–2023. [Google Scholar] [CrossRef] [Green Version]
  86. Vasyukova, N.I.; Chalenko, G.I.; Gerasimova, N.G.; Perekhod, E.A.; Ozeretskovskaya, O.L.; Irina, A.V.; Varlamov, V.P.; Albulov, A.I. Chitin and chitosan derivatives as elicitors of potato resistance to late blight. Appl. Biochem. Microbiol. 2005, 36, 372–376. [Google Scholar] [CrossRef]
  87. Badawy, M.E.I.; Rabea, E.I. A biopolymer chitosan and its derivatives as promising antimicrobial agents against plant pathogens and their applications in crop protection. Int. J. Carbohydr. Chem. 2011, 2011, 460381. [Google Scholar] [CrossRef]
  88. El Ghaouth, A.; Arul, J.; Wilson, C.; Benhamou, N. Ultrastructural and cytochemical aspects of the effect of chitosan on decay of bell pepper fruit. Physiol. Mol. Plant Pathol. 1994, 44, 417–432. [Google Scholar] [CrossRef]
  89. Xu, J.; Zhao, X.; Han, X.; Du, Y. Antifungal activity of oligochitosan against Phytophthora capsici and other plant pathogenic fungi in vitro. Pestic. Biochem. Physiol. 2007, 87, 220–228. [Google Scholar] [CrossRef]
  90. El-Mohamedya, R.S.R.; Abd El-Aziz, M.E.; Kamel, S. Antifungal activity of chitosan nanoparticles against some plant pathogenic fungi in vitro. Agric. Eng. Int. CIGR J. 2019, 21, 201–209. [Google Scholar]
  91. Berger, L.R.R.; Stanford, N.P.; Walladino, L.G.; Laranieira, D.; Barbosa de-Lima, M.A.; Malheiros, S.M.M.; Oliveria, W.J.D.; Stamford, T.C.M. Cowpea resistance induced against Fusarium oxysporum f. sp. tracheiphilum by crustaceous chitosan and by biomass and chitosan obtained from Cunninghamella elegans. Biol. Cont. 2016, 92, 45–54. [Google Scholar] [CrossRef]
  92. Hassni, M.; El Hadrami, A.; Daayf, F.; Barka, E.A.; El Hadrami, I. Chitosan, antifungal product against Fusarium oxysporum f. sp. albedinis and elicitor of defence reactions in date palm roots. Phytopathol. Mediterr. 2004, 43, 195–204. [Google Scholar]
  93. Dos Santos, N.S.T.; Aguiar, A.J.A.A.; de Oliveira, C.E.V.; de Sales, C.V.; de Melo e Silva, S.; da Silva, R.S.; Stamford, T.C.M.; de Souza, E.L. Efficacy of the application of a coating composed of chitosan and Origanum vulgare L. essential oil to control Rhizopus stolonifer and Aspergillus niger in grapes (Vitis labrusca L.). Food Microbiol. 2012, 32, 345–353. [Google Scholar] [CrossRef]
  94. Gutierrez-Martinez, P.; Ledezma-Morales, A.; Romero-Islas, L.d.L.; Ramos-Guerrero, A.; Romero-Islas, J.; Rodríguez-Pereida, C.; Casas-Junco, P.; Coronado-Partida, L.; González-Estrada, R. Antifungal activity of chitosan against postharvest fungi of tropical and subtropical fruits. In Chitin-Chitosan: Myriad Functionalities in Science and Technology; Dongre, R.S., Ed.; IntechOpen: London, UK, 2018. [Google Scholar]
  95. Kanetis, L.; Exarchou, V.; Charalambous, Z.; Goulas, V. Edible coating composed of chitosan and Salvia fruticosa Mill. extract for the control of grey mould of table grapes. J. Sci. Food Agric. 2017, 97, 452–460. [Google Scholar] [CrossRef]
  96. Falcon, A.B.; Cabrera, J.C.; Costales, D.; Ramirez, M.A.; Cabrera, G.; Toledo, V.; Martinez-Tellez, M.A. The effect of size and acetylation degree of chitosan derivatives on tobacco plant protection against Phytophthora parasitica nicotianae. World J. Microbiol. Biotechnol. 2008, 24, 103–112. [Google Scholar] [CrossRef] [Green Version]
  97. Kiprushkina, E.I.; Shestopalova, I.A.; Pekhotina, A.M.; Kuprina, E.E.; Nikitina, O.V. Protective-stimulating properties of chitosan in the vegetation and storing tomatoes. Prog. Chem. Appl. Chitin Deriv. 2017, 23, 77–81. [Google Scholar] [CrossRef] [Green Version]
  98. Guerra, I.C.D.; de Oliveira, P.D.L.; de Souza Pontes, A.L.; Lúcio, A.S.S.C.; Tavares, J.F.; Barbosa-Filho, J.M.; Madruga, M.S.; de Souza, E.L. Coatings comprising chitosan and Mentha piperita L. or Mentha×villosa Huds essential oils to prevent common postharvest mold infections and maintain the quality of cherry tomato fruit. Int. J. Food Microbiol. 2015, 214, 168–178. [Google Scholar] [CrossRef] [PubMed]
  99. Ing, L.Y.; Zin, N.M.; Sarwar, A.; Katas, H. Antifungal activity of chitosan nanoparticles and correlation with their physical properties. Int. J. Biomater. 2012, 2012, 632698. [Google Scholar] [CrossRef] [PubMed]
  100. Chowdappa, P.; Gowda, S.; Chethana, C.S.; Madhura, S. Antifungal activity of chitosan-silver nanoparticle composite against Colletotrichum gloeosporioides associated with mango anthracnose. Afr. J. Microbiol. Res. 2014, 8, 1803–1812. [Google Scholar]
  101. Cuero, R.G.; Duffus, E.; Osuji, G.; Pettit, R. Aflatoxin control in preharvest maize: Effects of chitosan and two microbial agents. J. Agric. Sci. 1991, 117, 165–169. [Google Scholar] [CrossRef]
  102. Meng, X.; Yang, L.; Kennedy, J.F.; Tian, S. Effects of chitosan and oligochitosan on growth of two fungal pathogens and physiological properties in pear fruit. Carbohydr. Polym. 2010, 81, 70–75. [Google Scholar] [CrossRef]
  103. Ma, Z.; Yang, L.; Yan, H.; Kennedy, J.F.; Meng, X. Chitosan and oligochitosan enhance the resistance of peach fruit to brown rot. Carbohydr. Polym. 2013, 94, 272–277. [Google Scholar] [CrossRef]
  104. Maia, A.J.; Botelho, R.V.; Faria, C.M.D.R.; Leite, C.D. Chitosan action on Plasmopara viticola and Elsinoe ampelina development in vitro and in grapevines cv. Isabel. Sum. Phytopathol. 2010, 36, 203–209. [Google Scholar] [CrossRef] [Green Version]
  105. Manjunatha, G.; Roopa, K.S.; Prashanth, G.N.; Shetty, H.S. Chitosan enhances disease resistance in pearl millet against downy mildew caused by Sclerospora graminicola and defence-related enzyme activation. Pest Manag. Sci. 2008, 64, 1250–1257. [Google Scholar] [CrossRef]
  106. Liu, H.; Tian, W.; Li, B.; Wu, G.; Ibrahim, M.; Tao, Z.; Wang, Y.; Xie, G.; Li, H.; Sun, G. Antifungal effect and mechanism of chitosan against the rice sheath blight pathogen, Rhizoctonia solani. Biotechnol. Lett. 2012, 34, 2291–2298. [Google Scholar] [CrossRef]
  107. Hadwiger, L.A.; McBride, P.O. Low-level copper plus chitosan applications provide protection against late blight of potato. Plant Health Prog. 2006, 7, 22. [Google Scholar] [CrossRef] [Green Version]
  108. Benhamou, N.; Theriault, G. Treatment with chitosan enhances resistance of tomato plants to the crown and root rot pathogen Fusarium oxysporum f. sp. radicis-lycopersici. Physiol. Mol. Plant Pathol. 1992, 41, 33–52. [Google Scholar] [CrossRef]
  109. Reglinski, T.; Elmer, P.A.G.; Taylor, J.T.; Wood, P.N.; Hoyte, S.M. Inhibition of Botrytis cinerea growth and suppression of botrytis bunch rot in grapes using chitosan. Plant Pathol. 2010, 59, 882–890. [Google Scholar] [CrossRef] [Green Version]
  110. Feliziani, E.; Landi, L.; Romanazzi, G. Preharvest treatments with chitosan and other alternatives to conventional fungicides to control postharvest decay of strawberry. Carbohydr. Polym. 2015, 132, 111–117. [Google Scholar] [CrossRef] [PubMed]
  111. Zahid, N.; Maqbool, M.; Siddiqui, Y.; Manickam, S.; Ali, A. Regulation of inducible enzymes and suppression of anthracnose using submicron chitosan dispersions. Sci. Hortic. 2015, 193, 381–388. [Google Scholar] [CrossRef]
  112. Sathiyabama, M.; Balasubramanian, R. Chitosan induces resistance components in Arachis hypogaea against leaf rust caused by Puccinia arachidis Speg. Crop Protec. 1998, 17, 307–313. [Google Scholar] [CrossRef]
  113. Dodgson, J.L.A.; Dodgson, W. Comparison of effects of chitin and chitosan for control of Colletotrichum sp. on cucumbers. J. Pure Appl. Microbiol. 2017, 11, 87–93. [Google Scholar] [CrossRef]
  114. Lopez-Moya, F.; Martin-Urdiroz, M.; Oses-Ruiz, M.; Fricker, M.D.; Littlejohn, G.R.; Lopez-Llorca, L.V.; Talbot, N.J. Chitosan inhibits septin-mediated plant infection by the rice blast fungus Magnaporthe oryzae in a protein kinase C and Nox1 NADPH oxidase-dependent manner. bioRxiv 2020. [Google Scholar] [CrossRef]
  115. Boonlertnirun, S.; Boonraung, C.; Suvanasara, R. Application of chitosan in rice production. J. Met. Mater. Miner. 2008, 18, 47–52. [Google Scholar]
  116. Chatterjee, S.; Chatterjee, B.P.; Guha, A.K. A study an antifungal activity of water-soluble chitosan against Macrophomina phaseolina. Int. J. Biol. Macromol. 2014, 67, 452–457. [Google Scholar] [CrossRef]
  117. Kheiri, A.; Moosawi Jorf, S.A.; Malihipour, A.; Saremi, H.; Nikkhah, A. Synthesis and characterization of chitosan nanoparticles and their effect on Fusarium head blight and oxidative activity in wheat. Int. J. Biol. Macromol. 2017, 102, 526–538. [Google Scholar] [CrossRef]
  118. Bhaskara Reddy, M.V.; Arul, J.; Angers, P.; Couture, L. Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. J. Agric. Food Chem. 1999, 47, 1208–1216. [Google Scholar] [CrossRef] [PubMed]
  119. Hassan, G.M.; Xiang, M.; Liu, X. Synergetic suppression of soybean cyst nematodes by chitosan and Hirsutella minnesotensis via the assembly of the soybean rhizosphere microbial communities. Biol. Control 2017, 115, 86–94. [Google Scholar]
  120. Benhamou, N.; Lafontaine, P.J.; Nicole, M. Induction of systemic resistance to Fusarium crown and root rot in tomato plants by seed treatment with chitosan. Phytopathology 1994, 84, 1432–1444. [Google Scholar] [CrossRef]
  121. Lafontaine, J.P.; Benhamou, N. Chitosan treatment: An emerging strategy for enhancing resistance of greenhouse tomato plants to infection by Fusarium oxysporum f. sp. radicislycopersici. Biocontrol Sci. Technol. 1996, 6, 111–124. [Google Scholar] [CrossRef]
  122. O’Herlihy, E.A.; Duffy, E.M.; Cassells, A.C. The effects of arbuscular mycorrhizal fungi band chitosan sprays on yield and late blight resistance in potato crops from microplants. Folia Geobot. 2003, 38, 201–208. [Google Scholar] [CrossRef]
  123. El-Mohamedy, R.S.R.; Shafeek, M.R.; Abd El-Samad, E.E.-D.H.; Salama, D.M.; Rizk, F.A. Field application of plant resistance inducers (PRIs) to control important root rot diseases and improvement growth and yield of green bean (Phaseolus vulgaris L.). Aust. J. Crop Sci. 2017, 11, 496–505. [Google Scholar] [CrossRef]
  124. Ben-Shalom, N.; Fallik, E. Further suppression of Botrytis cinerea disease in cucumber seedlings by chitosan-copper complex as compared with chitosan alone. Phytoparasitica 2003, 31, 99–102. [Google Scholar] [CrossRef]
  125. Moret, A.; Muñoz, Z.; Garcés, S. Control of powdery mildew on cucumber cotyledons by chitosan. J. Plant Pathol. 2009, 1, 375–380. [Google Scholar]
  126. Zohara, F.; Surovy, M.Z.; Khatun, A.; Prince, M.F.R.K.; Akanda, M.A.M.; Rahman, M.; Islam, M.T. Chitosan biostimulant controls infection of cucumber by Phytophthora capsici through suppression of asexual reproduction of the pathogen. Acta Agrobot. 2019, 72, 1763. [Google Scholar] [CrossRef]
  127. Long, L.T.; Tan, L.V.; Boi, V.N.; Trung, T.S. Antifungal activity of water-soluble chitosan against Colletotrichum capsici in post-harvest chili pepper. J. Food Process. Preserv. 2018, 42, e13339. [Google Scholar] [CrossRef]
  128. Sid Ahmed, A.; Ezziyyani, M.; Pérez Sánchez, C.; Candela, M.E. Effect of chitin on biological control activity of Bacillus spp. and Trichoderma harzianum against root rot disease in pepper (Capsicum annuum) plants. Eur. J. Plant Pathol. 2003, 109, 633–637. [Google Scholar] [CrossRef]
  129. Mandal, S. Induction of phenolics, lignin and key defense enzymes in eggplant (Solanum melongena L.) roots in response to elicitors. Afr. J. Biotechnol. 2010, 9, 8038–8047. [Google Scholar]
  130. Bautista-Baños, S.; Hernández-López, M.; Bosquez-Molina, E.; Wilson, C. Effects of chitosan and plant extracts on growth of Colletotrichum gloeosporioides, anthracnose levels and quality of papaya fruit. Crop Prot. 2003, 22, 1087–1092. [Google Scholar] [CrossRef]
  131. Sivakumar, D.; Sultanbawa, Y.; Ranasingh, N.; Wijesundera, R.L.C. Effect of the combined application of chitosan and carbonate salts on the incidence of anthracnose and on the quality of papaya during storage. J. Hortic. Sci. Biotechnol. 2005, 80, 447–452. [Google Scholar] [CrossRef]
  132. Cheah, L.; Page, B.; Shepherd, R. Chitosan coating for inhibition of sclerotinia rot of carrots. N. Z. J. Crop Hortic. Sci. 1997, 25, 89–92. [Google Scholar] [CrossRef]
  133. Aziz, A.; Trotel-Aziz, P.; Dhuicq, L.; Jeandet, P.; Couderchet, M.; Vernet, G. Chitosan oligomers and copper sulphate induce grapevine defense reaction and resistance to grey mould and down mildew. Phytopathology 2006, 96, 1188–1194. [Google Scholar] [CrossRef] [Green Version]
  134. Bell, A.A.; Hubbard, J.C.; Liu, L.; Davis, R.M.; Subbarao, K.V. Effects of chitin and chitosan on the incidence and severity of Fusarium yellows in celery. Plant Dis. 1998, 82, 322–328. [Google Scholar] [CrossRef] [Green Version]
  135. El Ghaouth, A.; Arul, J.; Grenier, J.; Asselin, A. Antifungal activity of chitosan on two postharvest pathogens of strawberry fruits. Phytopathology 1992, 82, 398–402. [Google Scholar] [CrossRef]
  136. Lowe, A.; Rafferty-McArdle, S.M.; Cassells, A.C. Effects of AMF- and PGPR-root inoculation and a foliar chitosan spray in single and combined treatments on powdery mildew disease in strawberry. Agric. Food Sci. 2012, 21, 28–38. [Google Scholar] [CrossRef]
  137. Du, J.; Gemma, H.; Iwahori, S. Effects of chitosan coating on the storage of peach Japanese pear and kiwifruit. J. Jpn. Soc. Hort. Sci. 1997, 66, 15–22. [Google Scholar] [CrossRef]
  138. Jinasena, D.; Pathirathna, P.; Wickramarachchi, S.; Marasinghe, E. Use of chitosan to control anthracnose on “Embul” banana. In Proceedings of the 2011 International Conference on Asia Agriculture and Animal IPCBEE, Hong Kong, China, 2 July 2011; pp. 56–60. [Google Scholar]
  139. Gutiérrez-Martínez, P.; Ramos-Guerrero, A.; Rodríguez-Pereida, C.; Coronado-Partida, L.; Angulo-Parra, J.; González-Estrada, R. Chitosan for postharvest disinfection of fruits and vegetables. Postharv. Disinfect. Fruits Veget. 2018, 1, 231–241. [Google Scholar]
  140. Jitareerat, P.; Paumchai, S.; Kanlayanarat, S.; Sangchote, S. Effect of chitosan on ripening, enzymatic activity, and disease development in mango (Mangifera indica) fruit. N. Z. J. Crop Hortic. Sci. 2007, 35, 211–218. [Google Scholar] [CrossRef]
  141. Jongsri, P.; Wangsomboondee, T.; Rojsitthisak, P.; Seraypheap, K. Effect of molecular weights of chitosan coating on postharvest quality and physicochemical characteristics of mango fruit. LWT Food Sci. Technol. 2016, 73, 28–36. [Google Scholar] [CrossRef]
  142. De Oliveira, K.Á.R.; Berger, L.R.R.; de Araújo, S.A.; Câmara, M.P.S.; de Souza, E.L. Synergistic mixtures of chitosan and Mentha piperita L. essential oil to inhibit Colletotrichum species and anthracnose development in mango cultivar Tommy Atkins. Food Microbiol. 2017, 66, 96–103. [Google Scholar] [CrossRef] [PubMed]
  143. Zeng, K.; Deng, Y.; Ming, J.; Deng, L. Induction of disease resistance and ROS metabolism in navel oranges by chitosan. Sci. Hortic. 2010, 126, 223–228. [Google Scholar] [CrossRef]
  144. Romanazzi, G.; Mlikota Gabler, F.; Smilanick, J.L. Preharvest chitosan and postharvest UV-C irradiation treatments suppress gray mold of table grapes. Plant Dis. 2006, 90, 445–450. [Google Scholar] [CrossRef] [Green Version]
  145. Romanazzi, G.; Nigro, F.; Ippolito, A. Short hypobaric treatments potentiate the effect of chitosan in reducing storage decay of sweet cherries. Postharvest Biol. Technol. 2003, 29, 73–80. [Google Scholar] [CrossRef]
  146. Chandra, S.; Chakraborty, N.; Panda, K.; Acharya, K. Chitosan-induced immunity in Camellia sinensis (L.) O. Kuntze against blister blight disease is mediated by nitric-oxide. Plant Physiol. Biochem. 2017, 115, 298–307. [Google Scholar] [CrossRef]
  147. Maluin, F.N.; Hussein, M.Z.; Yusof, N.A.; Fakurazi, S.; Idris, A.S.; Hilmi, N.H.Z.; Daim, L.D.J. Chitosan-based agronanofungicides as a sustainable alternative in the basal stem rot disease management. J. Agric. Food Chem. 2020, 68, 4305–4314. [Google Scholar] [CrossRef]
  148. Kishore, G.K.; Pande, S.; Podile, A.R. Chitin-supplemented foliar application of Serratia marcescens GPS 5 improves control of late leaf spot disease of groundnut by activating defense-related enzymes. J. Phytopathol. 2005, 153, 169–173. [Google Scholar] [CrossRef] [Green Version]
  149. Li, B.; Liu, B.; Shan, C.; Ibrahim, M.; Lou, Y.; Wang, Y.; Xie, G.; Li, H.Y.; Sun, G.C. Antibacterial activity of two chitosan solutions and their effect on rice bacterial leaf blight and leaf streak. Pest Manag. Sci. 2013, 69, 312–320. [Google Scholar] [CrossRef] [PubMed]
  150. Ramkissoon, A.; Francis, J.; Bowrin, V.; Ramjegathesh, R.; Ramsubhag, A.; Jayaraman, J. Bio efficacy of a chitosan based elicitor on Alternaria solani and Xanthomonas vesicatoria infections in tomato under tropical conditions. Ann. Appl. Biol. 2016, 169, 274–283. [Google Scholar] [CrossRef]
  151. Li, B.; Liu, B.; Su, T.; Fang, Y.; Xie, G.; Wang, G.; Wang, Y.; Sun, G. Effect of chitosan solution on the inhibition of Pseudomonas fluorescens causing bacterial head rot of broccoli. Plant Pathol. J. 2010, 26, 189–193. [Google Scholar] [CrossRef] [Green Version]
  152. Toan, N.V.; Hanh, T.T.; Thien, P.V.M. Antibacterial activity of chitosan on some common food contaminating microbes. Open Biomat. J. 2013, 4, 1–5. [Google Scholar] [CrossRef] [Green Version]
  153. Beausejour, J.; Clermont, N.; Beaulieu, C. Effect of Streptomyces melanosporofaciens strain EF-76 and of chitosan on common scab of potato. Plant Soil 2003, 256, 463–468. [Google Scholar] [CrossRef]
  154. Lou, M.M.; Zhu, B.; Muhammad, I.; Li, B.; Xie, G.L.; Wang, Y.L.; Li, H.Y.; Sun, G.C. Antibacterial activity and mechanism of action of chitosan solutions against apricot fruit rot pathogen Burkholderia seminalis. Carbohydr. Res. 2011, 346, 1294–1301. [Google Scholar] [CrossRef]
  155. Yang, C.; Li, B.; Ge, M.; Zhou, K.; Wang, Y.; Luo, J.; Ibrahim, M.; Xie, G.; Sun, G. Inhibitory effect and mode of action of chitosan solution against rice bacterial brown stripe pathogen Acidovorax avenae subsp. avenae RS-1. Carbohydr. Res. 2014, 391, 48–54. [Google Scholar] [CrossRef]
  156. Li, B.; Shi, S.; Shan, C.; Zhou, Q.; Ibrahim, M.; Wang, Y.; Wu, G.; Li, H. Effect of chitosan solution on the inhibition of Acidovorax citrulli causing bacterial fruit blotch of watermelon. J. Sci. Food Agric. 2013, 93, 1010–1015. [Google Scholar] [CrossRef]
  157. Farag, S.M.A.; Elhalag, K.M.A.; Mohamed, H.; Hagag, M.H.; Khairy, A.S.M.; Ibrahim, H.M.; Saker, M.T.; Messiha, N.A.S. Potato bacterial wilt suppression and plant health improvement after application of different antioxidants. J. Phytopathol. 2017, 65, 522–537. [Google Scholar] [CrossRef]
  158. Acar, O.; Aki, C.; Erdugan, H. Fungal and bacterial diseases control with ElexaTM plant booster. Fresenius Environ. Bull. 2008, 17, 797–802. [Google Scholar]
  159. Liu, N.; Chen, X.G.; Park, H.J.; Liu, C.G.; Liu, C.S.; Meng, X.H.; Yu, L.J. Effect of MW and concentration of chitosan on antibacterial activity of Escherichia coli. Carbohydr. Polym. 2006, 64, 60–65. [Google Scholar] [CrossRef]
  160. Shanmugam, A.; Kathiresan, K.; Nayak, L. Preparation, characterization and antibacterial activity of chitosan and phosphorylated chitosan from cuttlebone of Sepia kobiensis (Hoyle, 1885). Biotechnol. Rep. 2016, 9, 25–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  161. Sapers, G.M. Chitosan enhances control of enzymatic browning in apple and pear juice by filtration. J. Food Sci. 1992, 57, 1192–1193. [Google Scholar] [CrossRef]
  162. Rabea, E.I.; Steurbaut, W. Chemically modified chitosans as antimicrobial agents against some plant pathogenic bacteria and fungi. Plant Protect. Sci. 2010, 46, 149–158. [Google Scholar] [CrossRef]
  163. Chung, Y.C.; Wang, H.L.; Chen, Y.M.; Li, S.L. Effect of abiotic factors on the antibacterial activity of chitosan against waterborne pathogens. Bioresour. Technol. 2003, 88, 179–184. [Google Scholar] [CrossRef]
  164. Algam, S.; Xie, G.; Li, B.; Yu, S.; Su, T.; Larsen, J. Effects of Paenibacillus strains and chitosan on plant growth promotion and control of Ralstonia wilt in tomato. J. Plant Pathol. 2010, 92, 593–600. [Google Scholar]
  165. Coqueiro, D.S.O.; di Piero, M.R. Antibiotic activity against Xanthomonas gardneri and protection of tomato plants by chitosan. J. Plant Pathol. 2011, 93, 337–344. [Google Scholar]
  166. Ferrante, P.; Scortichini, M. Molecular and phenotypic features of Pseudomonas syringae pv. actinidiae isolated during recent epidemics of bacterial canker on yellow kiwifruit (Actinidia chinensis) in central Italy. Plant Pathol. 2010, 59, 954–962. [Google Scholar] [CrossRef]
  167. Li, B.; Wang, X.; Chen, R.; Huangfu, W.; Xie, G.L. Antibacterial activity of chitosan solution against Xanthomonas pathogenic bacteria isolated from Euphorbia pulcherrima. Carbohydr. Polym. 2008, 72, 287–292. [Google Scholar] [CrossRef]
  168. Chirkov, S.N. The antiviral activity of chitosan (review). Appl. Biochem. Microbiol. 2002, 38, 5–13. [Google Scholar] [CrossRef]
  169. Chirkov, S.N.; Il’ina, A.V.; Surgucheva, N.; Letunova, E.; Varitsev, Y.A.; Tatarinova, N.Y.; Varlamov, V. Effect of chitosan on systemic viral infection and some defense responses in potato plants. Russ. J. Plant Physiol. 2001, 48, 774–779. [Google Scholar] [CrossRef]
  170. Bondok, A. Response of tomato plants to salicylic acid and chitosan under infection with tomato mosaic virus. Am.-Eur. J. Agric. Environ. Sci. 2015, 15, 1520–1529. [Google Scholar]
  171. Mishra, S.; Jagadeesh, K.S.; Krishnaraj, P.U.; Prem, S. Biocontrol of tomato leaf curl virus (ToLCV) in tomato with chitosan supplemented formulations of Pseudomonas sp. under field conditions. Aust. J. Crop Sci. 2014, 8, 347–355. [Google Scholar]
  172. Firmansyah, D. Use of chitosan and plant growth promoting rhizobacteria to control squash mosaic virus on cucumber plants. Asian J. Plant Pathol. 2017, 11, 148–155. [Google Scholar] [CrossRef]
  173. Pospieszny, H.; Chirkov, S.; Atabekov, J. Induction of antiviral resistance in plants by chitosan. Plant Sci. 1991, 79, 63–68. [Google Scholar] [CrossRef]
  174. Nagorskaya, V.; Reunov, A.; Lapshina, L.; Davydova, V.; Yermak, I. Effect of chitosan on tobacco mosaic virus (TMV) accumulation, hydrolase activity, and morphological abnormalities of the viral particles in leaves of N. tabacum L. cv. Samsun. Virol. Sin. 2014, 29, 250–256. [Google Scholar] [CrossRef]
  175. Iriti, M.; Sironi, M.; Gomarasca, S.; Casazza, A.P.; Soave, C.; Faoro, F. Cell death-mediated antiviral effect of chitosan in tobacco. Plant Physiol. Biochem. 2006, 44, 893–900. [Google Scholar] [CrossRef]
  176. Scorza, R.; Callahan, A.; Levy, L.; Damsteegt, V.; Webb, K.; Ravelonandro, M. Post-transcriptional gene silencing in plum pox virus resistant transgenic European plum containing the plum pox potyvirus coat protein gene. Transgenic Res. 2001, 10, 201–209. [Google Scholar] [CrossRef]
  177. Kalaiarasan, P.; Lakshmanan, P.; Rajendran, G.; Samiyappan, R. Chitin and chitinolytic biocontrol agents for the management of root knot nematode, Meloidogyne arenaria in groundnut (Arachis hypogaea L.) cv. Co3. Indian J. Nematol. 2006, 36, 181–186. [Google Scholar]
  178. El-Sayed, S.M.; Mahdy, M.E. Effect of chitosan on root-knot nematode, Meloidogyne javanica on tomato plants. Int. J. ChemTech Res. 2015, 7, 1985–1992. [Google Scholar]
  179. Westerdahl, B.B.; Carlson, H.L.; Grant, J.; Radewald, J.D.; Welch, N.; Anderson, C.A.; Darso, J.; Kirby, D.; Shibuya, F. Management of plant-parasitic nematodes with a chitin-urea soil amendment and other materials. J. Nematol. 1992, 24, 669–680. [Google Scholar] [PubMed]
  180. Fan, Z.; Qin, Y.; Liu, S.; Xing, R.; Yu, H.; Li, P. Chitosan oligosaccharide fluorinated derivative control root-knot nematode (Meloidogyne incognita) disease based on the multi-efficacy strategy. Mar. Drugs 2020, 18, 273. [Google Scholar] [CrossRef] [PubMed]
  181. Liang, W.; Yu, A.; Wang, G.; Zheng, F.; Jia, J.; Xu, H. Chitosan-based nanoparticles of avermectin to control pine wood nematodes. Int. J. Biol. Macromol. 2018, 112, 258–263. [Google Scholar] [CrossRef] [PubMed]
  182. Ibrahim, A.Y.; Kurniawati, F. The efficacy of chitosan to control nematode Aphelenchoides besseyi Christie through seed treatment. IOP Conf. Ser. Earth Environ. Sci. 2020, 468, 012025. [Google Scholar] [CrossRef]
  183. Khalil, M.S.; Badawy, M.E. Nematicidal activity of a biopolymer chitosan at different molecular weights against root-knot nematode, Meloidogyne incognita. Plant Protect. Sci. 2012, 48, 170–178. [Google Scholar] [CrossRef] [Green Version]
  184. Escudero, N.; Lopez-Moya, F.; Ghahremani, Z.; Zavala-Gonzalez, E.A.; Alaguero-Cordovilla, A.; Ros-Ibañez, C.; Lacasa, A.; Sorribas, F.J.; Lopez-Llorca, L.V. Chitosan increases tomato root colonization by Pochonia chlamydosporia and their combination reduces root-knot nematode damage. Front. Plant Sci. 2017, 8, 1415. [Google Scholar] [CrossRef] [PubMed]
  185. Belair, G.; Tremblay, N. The influence of chitin-urea amendments applied to an organic soil on a Meloidogyne hapla population and on the growth of greenhouse tomato. Phytoprotection 1995, 76, 75–80. [Google Scholar] [CrossRef] [Green Version]
  186. Asif, M.; Ahmad, F.; Tariq, M.; Khan, A.; Ansari, T.; Khan, F.; Siddiqui, A.M. Potential of chitosan alone and in combination with agricultural wastes against the root-knot nematode, Meloidogyne incognita infesting eggplant. J. Plant Prot. Res. 2017, 57, 288–295. [Google Scholar] [CrossRef] [Green Version]
  187. El-Saedy, M.A.M.; Hammad, S.E.; Awd Allah, S.F.A. Nematicidal effect of abamectin, boron, chitosan, hydrogen peroxide and Bacillus thuringiensis against citrus nematode on Valencia orange trees. J. Plant Sci. Phytopathol. 2019, 3, 111–117. [Google Scholar]
  188. Hameed, A.; Sheikh, M.; Hameed, A.; Farooq, T.; Basra, S.; Jamil, A. Chitosan priming enhances the seed germination, antioxidants, hydrolytic enzymes, soluble proteins and sugars in wheat seeds. Agrochimica 2013, 67, 32–46. [Google Scholar]
  189. John, M.; Röhrig, H.; Schmidt, J.; Walden, R.; Schell, J. Cell signalling by oligosaccharides. Trends Plant Sci. 1997, 2, 111–115. [Google Scholar] [CrossRef]
  190. Dzung, N.A.; Khanh, V.T.P.; Dzung, T.T. Research on impact of chitosan oligomers on biophysical characteristics, growth, development and drought resistance of coffee. Carbohydr. Polym. 2011, 84, 751–755. [Google Scholar] [CrossRef]
  191. Amin, A.A.; Rashad EL-Sh, M.; EL-Abagy, H.M.H. Physiological effect of indole-3-butyric acid and salicylic acid on growth, yield and chemical constituents of onion plants. J. Appl. Sci. Res. 2007, 3, 1554–1563. [Google Scholar]
  192. Zeng, D.; Luo, X. Physiological effects of chitosan coating on wheat growth and activities of protective enzyme with drought tolerance. J. Soil Sci. 2012, 2, 282–288. [Google Scholar] [CrossRef] [Green Version]
  193. Dzung, N.A.; Thang, N.T. Effect of oligoglucosamine prepared by enzyme degradation on the growth of soybean. Adv. Chitin Sci. 2002, 5, 463–467. [Google Scholar]
  194. Xing, K.; Zhu, X.; Peng, X.; Qin, S. Chitosan antimicrobial and eliciting properties for pest control in agriculture: A review. Agron. Sustain. Dev. 2015, 35, 569–588. [Google Scholar] [CrossRef] [Green Version]
  195. Zhang, D.; Wang, H.; Hu, Y.; Liu, Y. Chitosan controls postharvest decay on cherry tomato fruit possibly via the mitogen-activated protein kinase signaling pathway. J. Agric. Food Chem. 2015, 63, 7399–7404. [Google Scholar] [CrossRef]
  196. Li, P.; Cao, Z.; Wu, Z.; Wang, X.; Li, X. The effect and action mechanisms of oligochitosan on control of stem dry rot of Zanthoxylum bungeanum. Int. J. Mol. Sci. 2016, 17, 1044. [Google Scholar] [CrossRef]
  197. Shahidi, F.; Arachchi, J.K.V.; Jeon, Y.J. Food applications of chitin and chitosan-review. Trends Food Sci. Technol. 1999, 10, 37–51. [Google Scholar] [CrossRef]
  198. Helander, I.M.; Nurmiaho-Lassila, E.L.; Ahvenainen, R.; Rhoades, J.; Roller, S. Chitosan disrupts the barrier properties of the outer membrane of Gram-negative bacteria. Int. J. Food Microbiol. 2001, 71, 235–244. [Google Scholar] [CrossRef]
  199. Xing, K.; Chen, X.G.; Liu, C.S.; Cha, D.S.; Park, H.J. Oleoyl-chitosan nanoparticles inhibits Escherichia coli and Staphylococcus aureus by damaging the cellmembrane and putative binding to extracellular or intracellular targets. Int. J. Food Microbiol. 2009, 132, 127–133. [Google Scholar] [CrossRef] [PubMed]
  200. García-Rincóna, J.; Vega-Pérez, J.; Guerra-Sánchez, M.G.; Hernández-Lauzardo, A.N.; Peña-Díaz, A.; Velázquez-Del Valle, M.G. Effect of chitosan on growth and plasma membrane properties of Rhizopus stolonifera (Ehrenb.:Fr.) Vuill. Pestic. Biochem. Phys. 2010, 97, 275–278. [Google Scholar]
  201. Rabea, E.I.; Badawy, M.E.-T.; Stevens, C.V.; Smagghe, G.; Steurbaut, W. Chitosan as antimicrobial agent: Applications and mode of action. Biomacromolecules 2003, 4, 1457–1465. [Google Scholar] [CrossRef] [PubMed]
  202. Chung, Y.C.; Su, Y.P.; Chen, C.C.; Jia, G.; Wang, H.L.; Wu, J.C.; Lin, J.G. Relationship between antibacterial activity of chitosan and surface characteristics of cell wall. Acta Pharmacol. Sin. 2004, 25, 932–936. [Google Scholar]
  203. Liu, H.; Du, Y.M.; Wang, X.H.; Sun, L.P. Chitosan kills bacteria through cell membrane damage. Int. J. Food Microbiol. 2004, 95, 147–155. [Google Scholar] [CrossRef]
  204. Gow, N.A.R.; Latge, J.-P.; Munro, C.A. The fungal cell wall: Structure, biosynthesis, and function. Microbiol. Spectr. 2017, 5, 267–292. [Google Scholar]
  205. Chung, Y.C.; Chen, C.Y. Antibacterial characteristics and activity of acid-soluble chitosan. Bioresour. Technol. 2008, 99, 2806–2814. [Google Scholar] [CrossRef]
  206. Hadwiger, L.A. Multiple effects of chitosan on plant systems: Solid science or hype. Plant Sci. 2013, 208, 42–49. [Google Scholar] [CrossRef]
  207. Sudarshan, N.R.; Hoover, D.G.; Knorr, D. Antibacterial action of chitosan. Food Biotechnol. 1992, 6, 257–272. [Google Scholar] [CrossRef]
  208. Goy, R.C.; Britto, D.; Assis, O.B.G. A review of the antimicrobial activity of chitosan. Polímeros 2009, 19, 241–247. [Google Scholar] [CrossRef]
  209. Come, V.; Deschamps, A.; Mertial, A. Bioactive packaging materials from edible chitosan polymer-antimicrobial activity assessment on dairy-related contaminants. J. Food Sci. 2003, 68, 2788–2792. [Google Scholar] [CrossRef]
  210. Issam, S.T.; Adele, M.G.; Adele, C.P.; Stephane, G.; Veronique, C. Chitosan polymer as bioactive coating and film against Aspergillus niger contamination. J. Food Sci. 2005, 70, 100–104. [Google Scholar]
  211. Qin, Y. The chelating properties of chitosan fibers. J. Appl. Polym. Sci. 1993, 49, 727–731. [Google Scholar] [CrossRef]
  212. Freeman, B.C.; Beattie, G.A. An overview of plant defenses against pathogens and herbivores. Plant Health Instr. 2008, 10, 1094. [Google Scholar] [CrossRef] [Green Version]
  213. Martins, A.; Facchi, S.; Follmann, H.; Pereira, A.; Rubira, A.; Muniz, E. Antimicrobial activity of chitosan derivatives containing N-quaternized moieties in its backbone: A review. Int. J. Mol. Sci. 2014, 15, 20800–20832. [Google Scholar] [CrossRef]
  214. El Ghaouth, A.; Ponnampalam, R.; Castaigne, F.; Arul, J. Chitosan coating to extend the storage life of tomatoes. HortScience 1992, 27, 1016–1018. [Google Scholar] [CrossRef] [Green Version]
  215. Dornenburg, H.; Knorr, D. Evaluation of elicitor- and high-pressure-induced enzymatic browning utilizing potato (Solanum tuberosum) suspension cultures as a model system for plant tissues. J. Agric. Food Chem. 1997, 45, 4173. [Google Scholar] [CrossRef]
  216. Bhaskara, M.V.; Arul, J.; Essaid, A.B.; Anger, P.; Richard, C.; Castaigne, F. Effect of chitosan on growth and toxin production by Alternaria alternata f. sp. lycopersici. Biocontrol Sci. Technol. 1998, 8, 33. [Google Scholar]
  217. El Ghaouth, A.; Arul, J.; Asselin, A.; Benhamou, N. Antifungal activity of chitosan on post-harvest pathogens: Induction of morphological and cytological alterations in Rhizopus stolonifera. Mycol. Res. 1992, 96, 769. [Google Scholar] [CrossRef]
  218. Lin, W.; Hu, X.; Zhang, W.; Rogers, W.J.; Cai, W. Hydrogen peroxide mediates defence responses induced by chitosans of different molecular weights in rice. J. Plant Physiol. 2005, 162, 937–944. [Google Scholar] [CrossRef]
  219. Burkhanova, G.F.; Yarullina, L.G.; Maksimov, I.V. The control of wheat defense responses during infection with Bipolaris sorokiniana by chitooligosaccharides. Russ. J. Plant Physiol. 2007, 54, 104–110. [Google Scholar] [CrossRef]
  220. Eilenberg, H.; Pnini-Cohen, S.; Rahamim, Y.; Sionov, E.; Segal, E.; Carmeli, S.; Zilberstein, A. Induced production of antifungal naphthoquinones in the pitchers of the carnivorous plant Nepenthes khasiana. J. Exp. Bot. 2009, 61, 911–922. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  221. Yin, H.; Zhao, X.; Du, Y. Oligochitosan: A plant diseases vaccine-a review. Carbohydr. Polym. 2010, 82, 1–8. [Google Scholar] [CrossRef]
  222. Romanazzi, G. Chitosan treatment for the control of postharvest decay of table grapes, strawberries and sweet cherries. Fresh Prod. 2010, 4, 111–115. [Google Scholar]
  223. Chang, T.; Kim, B.S. Application of chitosan preparations for eco-friendly control of potato late blight. Res. Plant Dis. 2012, 18, 338–348. [Google Scholar] [CrossRef] [Green Version]
  224. Rahman, M.; Punja, Z.K. Biochemistry of rusty root on American ginseng (Panax quinquefolius L.). Plant Physiol. Biochem. 2005, 43, 1103–1114. [Google Scholar] [CrossRef] [PubMed]
  225. Orzali, L.; Forni, C.; Riccioni, L. Effect of chitosan seed treatment as elicitor of resistance to Fusarium graminearum in wheat. Seed Sci. Technol. 2014, 42, 132–149. [Google Scholar] [CrossRef]
  226. Hoat, T.X.; Nakayashiki, H.; Yang, Q.; Tosa, Y.; Mayama, S. Molecular cloning of the apoptosis-related calcium-binding protein AsALG-2 in Avena sativa. Mol. Plant Pathol. 2013, 14, 222–229. [Google Scholar] [CrossRef]
  227. Hadwiger, L.A.; Beckman, J.M. Chitosan as a component of pea-Fusarium solani interactions. Plant Physiol. 1980, 66, 205–211. [Google Scholar] [CrossRef] [Green Version]
  228. Klessig, D.F.; Durner, J.; Shah, J.; Yang, Y. Salicylic Acid-Mediated Signal Transduction in Plant Disease Resistance. In Phytochemical Signals and Plant-Microbe Interactions; Romeo, T.J., Downum, R.K., Verpoorte, R., Eds.; Springer: New York, NY, USA, 1998; pp. 119–137. [Google Scholar]
  229. Lienart, Y.; Gautier, C.; Domard, A. Isolation from Rubus cell-suspension cultures of a lectin specific for glucosamine oligomers. Planta 1991, 184, 8–13. [Google Scholar] [CrossRef]
  230. Petutschnig, E.K.; Jones, A.M.; Serazetdinova, L.; Lipka, U.; Lipka, V. The Lysin Motif Receptor-Like Kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 2010, 285, 28902–28911. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  231. Rahman, M.; Rahman, M.; Islam, T. Improving yield and antioxidant properties of strawberries by utilizing microbes and natural products. In Strawberry: Pre- and Post-Harvest Management Techniques for Higher Fruit Quality; Asao, T., Asaduzzaman, M., Eds.; IntechOpen: London, UK, 2019. [Google Scholar] [CrossRef] [Green Version]
  232. Galván, M.I.; Akuaku, J.; Cruz, I.; Cheetham, J.; Golshani, A.; Smith, M.L. Disruption of protein synthesis as antifungal mode of action by chitosan. Int. J. Food Microbiol. 2013, 164, 108–112. [Google Scholar] [CrossRef] [PubMed]
  233. Geisberger, G.; Gyenge, E.B.; Hinger, D.; Käch, A.; Maake, C.; Patzke, G.R. Chitosan-thioglycolic acid as a versatile antimicrobial agent. Biomacromolecules 2013, 14, 1010–1017. [Google Scholar] [CrossRef] [PubMed]
  234. Palma-Guerrero, J.; Lopez-Jimenez, J.A.; Pérez-Berná, A.J.; Huang, I.C.; Jansson, H.B.; Salinas, J.; Villalaín, J.; Read, N.D.; Lopez-Llorca, L.V. Membrane fluidity determines sensitivity of filamentous fungi to chitosan. Mol. Microbiol. 2010, 75, 1021–1032. [Google Scholar] [CrossRef] [PubMed]
  235. Palma-Guerrero, J.; Huang, I.C.; Jansson, H.B.; Salinas, J.; Lopez-Llorca, L.V.; Read, N.D. Chitosan permeabilizes the plasma membrane and kills cells of Neurospora crassa in an energy dependent manner. Fungal Genet. Biol. 2009, 46, 585–594. [Google Scholar] [CrossRef] [PubMed]
  236. Vishu, K.A.B.; Varadaraj, M.C.; Gowda, L.R.; Tharanathan, R.N. Characterization of chito-oligosaccharides prepared by chitosanolysis with the aid of papain and pronase, and their bactericidal action against Bacillus cereus and Escherichia coli. Biochem. J. 2005, 391, 167–175. [Google Scholar]
  237. Liang, C.; Yuan, F.; Liu, F.; Wang, Y.; Gao, Y. Structure and antimicrobial mechanism of ε-polylysine-chitosan conjugates through Maillard reaction. Int. J. Biol. Macromol. 2014, 70, 427–434. [Google Scholar] [CrossRef]
  238. Kong, M.; Chen, X.G.; Liu, C.S.; Liu, C.G.; Meng, X.H.; Yu, L.J. Antibacterial mechanism of chitosan microspheres in a solid dispersing system against E. coli. Colloid Surf. B 2008, 65, 197–202. [Google Scholar] [CrossRef]
  239. Tang, H.; Zhang, P.; Kieft, T.L.; Ryan, S.J.; Baker, S.M.; Wiesmann, W.P.; Rogelj, S. Antibacterial action of a novel functionalized chitosanarginine against gram-negative bacteria. Acta Biomater. 2010, 6, 2562–2571. [Google Scholar] [CrossRef] [Green Version]
  240. Mansilla, A.Y.; Albertengo, L.; Rodríguez, M.S.; Debbaudt, A.; Zúñiga, A.; Casalongué, C.A. Evidence on antimicrobial properties and mode of action of a chitosan obtained from crustacean exoskeletons on Pseudomonas syringae pv. tomato DC3000. Appl. Microbiol. Biotechnol. 2013, 97, 6957–6966. [Google Scholar] [CrossRef]
  241. Raafat, D.; Bargen, K.V.; Haas, A.; Sahl, H.-G. Insights into the mode of action of chitosan as an antibacterial compound. Appl. Environ. Microbiol. 2008, 74, 3764–3773. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Agriculture 10 00624 g001 550
Figure 1. An overview of chitosan-mediated plant growth regulation under stress conditions.
Figure 1. An overview of chitosan-mediated plant growth regulation under stress conditions.
Agriculture 10 00624 g001
Agriculture 10 00624 g002 550
Figure 2. An overview of chitosan-mediated disease suppression in plants.
Figure 2. An overview of chitosan-mediated disease suppression in plants.
Agriculture 10 00624 g002
Table
Table 1. Effects of chitosan (CHT) on plant growth and development.
Table 1. Effects of chitosan (CHT) on plant growth and development.
Plant SpeciesCHT EffectsMode of ApplicationReferences
Rice (Oryza sativa L.)Increased plant growth,
higher photosynthesis rate		In vivo[55]
Soybean (Glycine max)Increased plant growthSoil application[56]
Rape (Brassica rapa L.)Increased plant growth and content of leaf chlorophyll Hydroponic pot application[57]
Maize (Zea mays L.)Increased plant growth and grain weightBiofertilization [52]
Improved seed germinationIn vivo[58]
Improved seed germination and vigor indexIn vivo[59]
Potato (Solanum tuberosum L.)Increased of tuber sizeIn vivo[60]
Increased plant growth and yieldIn vitro and in vivo[61]
Tomato (Solanum lycopersicum)Improved fruit quality and productivity In vivo[9,10]
Increased seed germination and vigor indexIn vivo[62]
Daikon radishes (Raphanus sativus)Increased plant growthIn vivo[47]
Cabbage (Brassica oleracea) Increased plant growth In vivo[48]
Soybean sprouts (Glycine max)Increased plant growth In vivo[49]
Okra (Hibiscus esculentus L.)Increased plant growth, and yieldIn vivo[63]
Eggplant (Solanum melongena)Increased plant growth, and yieldIn vivo[64]
Bean (Phaseolus vulgaris)Increased leaf area, and carotenoids and chlorophylls levelsIn vitro[65]
Chili (Capsicum frutescence L.)Increased plant growth, yield, and thousand seed weightIn vivo[66]
Increased leaf area, canopy diameter, and plant heightIn vivo[67]
Bell pepper (Capsicum annuum)Increased fruit weight, diameter, and yieldIn vivo [68]
Turmeric (Curcuma longa)Increased plant growth, and yieldIn vivo[69]
Ajowan (Carum copticum)Increased seed germination, vigor index, dry weight and radical lengthIn vivo[70]
Artichoke (Cynara scolymus)Improved seed germination and plant growthIn vivo[71]
Cucumber (Cucumis sativus)Increased plant growth and improved qualityIn vivo[72]
Chickpea (Cicer arietinum)Increased plant growth In vivo[73]
Increased seed germination and vigor indexIn vivo[74]
Coffee (Coffea arabica)Increased plant height and leaf area In vivo[75]
Strawberry (Fragaria × annanasa)Increased fruit yield and total antioxidant activitiesIn vivo[14]
Increased fruit yieldIn vivo[76]
Watermelon (Citrullus lanatus)Increased plant growthIn vivo[77]
Mango (Mangifera indica)Increased plant growth, fruit size and weightIn vivo[78]
Grapevine (Vitis vinifera L.)Increased plant growthIn vivo[45]
Basil (Ocimum ciliatum and
Ocimum basilicum)		Increased plant growth and
phenol content		In vivo[50]
Phyla dulcisIncreased plant growthIn vitro[79]
Freesia (Freesia corymbosa)Increased plant growthIn vivo[53]
Gerbera jamesoniiIncreased plant growthIn vivo[51]
Dendrobium aggregatumIncreased plant growthIn vitro[42]
Cymbidium insigneIncreased plant growthIn vitro[44]
Kemiri sunan (Reutealis trisperma)Increased plant growthIn vivo[80]
Scots pine (Pinus sylvestris L.)Increased plant growthIn vivo[81]
Table
Table 2. Effects of CHT on fungal plant pathogens.
Table 2. Effects of CHT on fungal plant pathogens.
Plant SpeciesFungiMode of ApplicationReferences
Rice (Oryza sativa)Magnaporthe oryzaeIn vitro[114]
M. oryzaeIn vivo[115]
Rhizoctonia solaniIn vitro and In vivo[106]
Jute (Corchorus olitorius)Macrophomina phaseolinaIn vivo[116]
Maize (Zea mays)Aspergillus flavusPre-harvest treatment [101]
Wheat (Triticum aestivum)Bipolaris sorokinianaIn vivo [87]
Fusarium graminearumIn vivo[117]
F. graminearumIn vivo[118]
Pearl millet (Pennisetum glaucum)Sclerospora graminicolaPost-harvest treatment [105]
Soybean (Glycine max L.) Heterodera glycinesIn vivo[119]
Cowpea (Vigna unguiculata)F. oxysporum f. sp.
tracheiphilum		In vivo[91]
Tobacco (Nicotiana tabacum)Phytophthora parasiticaIn vitro and In vivo[96]
Cherry tomato (Solanum
lycopersicum var. cerasiforme)		Botrytis cinereaPost-harvest treatment [98]
Tomato (S. lycopersicum)F. oxysporumIn vivo[108]
F. oxysporum f. sp. radicis-lycopersiciIn vivo[120]
F. oxysporum f. sp. radicislycopersiciIn vivo[121]
F. oxysporum f.
sp. lycopersici		In vivo [9]
Alternaria solaniIn vivo [10]
P. infestansIn vivo[97]
F. ox f. sp. lycopersiciIn vitro[90]
F. solani
F. oxf. radicis. lycopersici
A. solani
P. infestance
R. solani
Sclerotium rolfsii
Potato (S. tuberosum)F. sembaticumIn vitro[90]
P. infestans
A. solani,
R. solani
P. infestansIn vivo[122]
P. infestansIn vivo[107]
Green bean (Phaseolus vulgaris L.)F. oxysporiumIn vitro[90]
F. solani
R. solani
S. rolfsii
Sclerotina sclerotiorum
B. cienera
Macrophomina phaseolina
F. solaniIn vivo[123]
R. solani
Cucumber (Cucumis sativus L.)Colletotrichum spp. Foliar spraying[113]
B. cinereaFoliar spray [124]
Sphaerotheca fuligineaIn vitro[125]
Phytophthora capsiciIn vivo [126]
Pepper (Piper nigrum)P. capsiciIn vivo[89]
Chili pepper (Capsicum annuum)Colletotrichum capsiciIn vivo [127]
P. capsiciIn vivo [128]
Chilli (Capsicum frutescence L.)C. capsiciIn vivo [66]
Eggplant (Solanum melongena)Ralstonia solanacearumIn vitro[129]
Papaya (Carica papaya)C. gloeosporioidesIn situ [130]
C. gloeosporioidesPost-harvest treatment [131]
Carrot (Daucus carota)S. sclerotiorumIn vitro[132]
Grapevine (Vitis vinifera)Elsinoe ampelinaPost-harvest treatment [104]
Plasmopara viticola
B. cinereaIn vitro and In vivo [109]
B. cinereaIn vivo[133]
P. viticola
Celery (Apium graveolens)Fusarium oxysporum f. sp. apiiIn vivo[134]
Strawberry (Fragaria × ananassa)Rhizopus stoloniferPost-harvest treatment[135]
B. cinerea
B. cinereaPre-harvest treatment[110]
Sphaerotheca macularisIn vivo[136]
Dragon fruit (Hylocereus undatus)C. gleosporoidesIn vivo[111]
Kiwifruit (Actinidia deliciosa)B. cinereaPost-harvest treatment[137]
Pear (Pyrus communis)A. kikuchianaIn vitro and Post-harvest treatment [102]
P. piricola
B. cinereaPost-harvest treatment[137]
Peach (Prunus persica)Monilinia fructicolaPost-harvest treatment[103]
B. cinereaPost-harvest treatment[137]
Banana (Musa acuminate)P. viticolaIn vivo[138]
Colletotrichum sp. Post-harvest treatment[139]
Fusarium sp.
Mango (Mangifera indica)C. gloeosporioidesPost-harvest coating [140]
C. gloeosporioidesPost-harvest coating [141]
C. asianumPost-harvest coating [142]
C. dianesei
C. fructicola
C. tropicale
C. karstii
Orange (Citrus sinensis)Penicillium italicumPost-harvest coating [143]
P. digitatum
Grape (Vitis vinifera)Rhizopus stoloniferPost-harvest treatment [93]
Aspergillus niger
B. cinereaPre-harvest treatment [144]
Pomegranate (Punica
granatum L.)		Botrytis spp. Post-harvest coating [95]
Penicillium spp.
Pilidiella granati
Avocado (Persea americana mill.)C. gloeosporioidesPost-harvest treatment[16]
Soursop (Annona muricata L.)C. gloeosporioidesPost-harvest treatment[139]
Jackfruit (Artocarpus heterophyllus L.)Rhizopus sp.Post-harvest treatment[139]
Sweet cherry (Prunus avium)Monilinia fructicolaPost-harvest treatment [145]
B. cinerea
Tea (Camellia sinensis L.) Exobasidium vexansFoliar spraying[146]
Scots Pine (Pinus sylvestris L.)Fusarium spp.In vivo[81]
Date palm (Phoenix dactylifera)F. oxysporumIn vivo [92]
Oil palm (Elaeis guineensis)Ganoderma boninenseIn vivo [147]
Peanut (Arachis hypogaea)Puccinia arachidisIn vivo [112]
Groundnut (Arachis hypogaea)Phaeoisariopsis personataFoliar spraying[148]
Table
Table 3. Antibacterial effects of CHT on bacterial plant pathogens.
Table 3. Antibacterial effects of CHT on bacterial plant pathogens.
Plant SpeciesBacteriaMode of ApplicationReferences
Rice (Oryza sativa)Acidovorax avenae subsp. avenaeIn vitro[155]
Xanthomonas oryzae pv. oryzaeIn vitro and In vivo[149]
X. oryzae pv. oryzicola
Tomato (Solanum lycopersicum)RalstoniasolanacearumIn vivo[164]
X. vesicatoriaIn vivo[165]
X. vesicatoriaIn vitro and in vivo[150]
Potato (S. tuberosum)Streptomyces scabiesIn vivo [153]
Ralstonia solanacearumIn vitro and in vivo[157]
Broccoli (Brassica oleracea var. italic)Pseudomonas fluorescensIn vitro and In vivo[151]
Cucumber (Cucumis sativus)P. syringae pv. lachrymansIn vivo[158]
Kiwifruit (Actinidia chinensis)P. syringae pv. actinidiaeIn vitro [166]
Apricot (Prunus armeniaca)Burkholderia seminalisIn vitro [154]
Watermelon (Citrullus lanatus)A. citrulliIn vitro [156]
Banana (Musa acuminate)P. aeruginosaIn vitro[152]
Staphylococcus aureus
Apple (Malus domestica)P. aeruginosa
S. aureus
Poinsettia (Euphorbia pulcherrima)Xanthomonas spp.In vitro [167]
Table
Table 4. In vivo antiviral activities of CHT.
Table 4. In vivo antiviral activities of CHT.
Plant SpeciesVirusesReferences
Tomato
(Lycopersicum esculentum)		PVX, TYLCV[173]
ToLCV[171]
PSTV, TMV[168]
Potato
(Solanum tuberosum)		PVX[169]
PVY[168]
Bean
(Phuseolus vulgaris)		AMV[173]
AMV, BGMV, PSV, TNV, BYMV, TMV, BCMV[168]
BCMV[11]
Cucumber (Cucumis sativus)SMV[172]
Globe amaranth
(Gomphrena globosa L.) 		PVX[168]
Pea (Pisum sativum)AMV, PSV[173]
Quinoa
(Chenopodium quinoa)		TNV[173]
CMV, TNV, AMV[168]
Tobacco
(Nicotiana tabacum)		TMV[174]
TNV[175]
TMV[170]
PSV[173]
Stramony
(Datura stramonium L.)		FMV, TMV[168]
Plum (Prunus domestica)PPV[176]
Viruses: PVX, potato virus X; TYLCV, tomato yellow leaf curl virus; ToLCV, tomato leaf curl virus; PSTV, potato spindle tuber viroid; TMV, tobacco mosaic virus; PVY, potato virus Y; AMV, alfalfa mosaic virus; BGMV, bean goldish mosaic virus; PSV, peanut stunt virus; TNV, tobacco necrosis virus; BYMV, bean yellow mosaic virus; MV, squash mosaic virus; BCMV, bean common mosaic virus; CMV, cucumber mosaic virus; FMV, figwort mosaic virus; PPV, plum pox virus.
Table
Table 5. Nematicidal effect of CHT on nematode plant pathogens.
Table 5. Nematicidal effect of CHT on nematode plant pathogens.
Plant SpeciesNematodesMode of ApplicationReferences
Rice (Oryza sativa)Aphelenchoides besseyiIn vivo[182]
Tomato (Solanum lycopersicum)Meloidogyne incognitaIn vivo[180]
M. incognitaIn vitro and in vivo[178]
M. incognitaIn vitro and Fertigation[183]
M. incognitaFertigation[179]
Meloidogyne spp.In vivo[184]
M. javanicaFertigation[178]
M. haplaFertigation[185]
Potato (S. tuberosum)M. chitwoodFertigation[179]
Eggplant (S. melongena)M. incognitaFertigation[186]
Brussels sprouts (Brassica oleracea)Heterodera schachtiiFertigation[179]
Valencia orange (Citrus sinensis Valencia)Tylenchulus semipenetransFertigation[187]
Walnut (Juglans regia)Pratylenchus vulnusFertigation[179]
Groundnut (Arachis hypogaea L.)M. arenariaFertigation[177]
Pinewood (Pinus sp.)Bursaphelen chusxylophilusFertigation[12]
B. chusxylophilusFertigation[181]
Table
Table 6. Proposed antimicrobial mechanisms of CHT.
Table 6. Proposed antimicrobial mechanisms of CHT.
PathogensMechanismsReferences
Magnaporthe oryzaePermeabilized the cell plasma membrane and affected the NADPH oxidase-dependent synthesis of ROS[114]
Rhizoctonia solaniDisrupted cell plasma membrane, destroyed cell structures and induced defense-associated enzymes activity in plants[106]
Saccharomyces cerevisiaeDestroyed synthesis of protein, and integrity of cell membrane [232]
Candida albicansDisrupted the integrity of cell wall and intra-cellular ultrastructure [233]
Beauveria bassianaFluidity of the cell membrane determines the vulnerability of fungi to CHT [234]
Pochonia chlamydosporia
Fusarium oxysporum f. sp. radicis-lycopersici
F. oxysporumHad an attraction for lipids in the plasma membrane[7]
F. solani
Neurospora crassaFluidity of the cell membrane determines the vulnerability of fungi to CHT[234]
Permeabilized the cell membrane and destroyed cells [235]
Rhizopus stoloniferTriggered K+ efflux and inhibited the activity of H+-ATPase[200]
Aspergillus fumigatusHad an attraction for lipids in the plasma membrane [7]
Botrytis cinerea
Aspergillus
parasiticus
Penicillium verrusosum var. verrucosum
Alternaria alternataChelation of metals[216]
Bacillus cereusBlockage of nutrient flow[236]
Escherichia coliDisrupted cell membranes and leaked cellular cytoplasm [237]
Destroyed plasma membrane structure of cells, and bind to intracellular or extracellular targets[199]
Destroyed structure of cells, electrostatic interactions, induced enzyme and nucleotide leakages[205]
Disrupted cell membrane structures, and leaked cellular cytoplasm[238]
Destroyed cell membrane[198,203]
Blockage of nutrient flow[236]
Increased cell plasma membrane permeability by CHT-membrane interaction [239]
Neisseria subflavaDestroyed the integrity of cell wall, and intra-cellular ultrastructure[233]
Pseudomonas syringaeElectrostatic interactions, disrupted bacterial cell surface and induced morphological alterations [240]
P. fluorescensIncreased cell plasma membrane permeability by CHT-membrane interaction[239]
P. aeruginosaDisrupted outer cell membrane [198]
Streptococcus sobrinusDestroyed the integrity of cell wall, and intra-cellular ultrastructure [233]
Staphylococcus simulansElectrostatic interactions[241]
S. aureusElectrostatic interactions[241]
Destroyed cell plasma membrane[203]
Disrupted cell plasma membranes and leaked cellular cytoplasm [237]
Damaged structures of cell membrane, and bind to intracellular or extracellular targets[199]
Salmonella typhimuriumDestroyed the outer cell membrane[198]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Chakraborty, M.; Hasanuzzaman, M.; Rahman, M.; Khan, M.A.R.; Bhowmik, P.; Mahmud, N.U.; Tanveer, M.; Islam, T. Mechanism of Plant Growth Promotion and Disease Suppression by Chitosan Biopolymer. Agriculture 2020, 10, 624. https://doi.org/10.3390/agriculture10120624

AMA Style

Chakraborty M, Hasanuzzaman M, Rahman M, Khan MAR, Bhowmik P, Mahmud NU, Tanveer M, Islam T. Mechanism of Plant Growth Promotion and Disease Suppression by Chitosan Biopolymer. Agriculture. 2020; 10(12):624. https://doi.org/10.3390/agriculture10120624

Chicago/Turabian Style

Chakraborty, Moutoshi, Mirza Hasanuzzaman, Mahfuzur Rahman, Md. Arifur Rahman Khan, Pankaj Bhowmik, Nur Uddin Mahmud, Mohsin Tanveer, and Tofazzal Islam. 2020. "Mechanism of Plant Growth Promotion and Disease Suppression by Chitosan Biopolymer" Agriculture 10, no. 12: 624. https://doi.org/10.3390/agriculture10120624

APA Style

Chakraborty, M., Hasanuzzaman, M., Rahman, M., Khan, M. A. R., Bhowmik, P., Mahmud, N. U., Tanveer, M., & Islam, T. (2020). Mechanism of Plant Growth Promotion and Disease Suppression by Chitosan Biopolymer. Agriculture, 10(12), 624. https://doi.org/10.3390/agriculture10120624

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop