Mitigating effects of Bean yellow mosaic virus infection in faba bean using new carboxymethyl chitosan-titania nanobiocomposites

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Abstract

Bean yellow mosaic virus (BYMV) is the main cause of the mosaic and malformation of many plants, worldwide. Thus, the triggering of plant systemic resistance against BYMV is of great interest. In this endeavor, we aimed to explore the capacity of new carboxymethyl chitosan-titania nanobiocomposites (NBCs, NBC1,2) to trigger faba bean plants resistance against BYMV. Effects of NBCs on faba bean (Vicia faba L.) disease severity (DS), growth parameters, and antioxidant defense system activity were investigated under BYMV stress. Noticeably that the DS in NBCs-treated faba bean was significantly reduced compared to untreated plants. Moreover, treatment with NBCs was remarkably increased growth indices, photosynthetic pigments, membrane stability index, and relative water content compared to challenge control. Additionally, enzymatic and non-enzymatic antioxidants and total soluble protein were significantly increased. Contrary, electrolyte leakage, hydrogen peroxide, and lipid peroxidation were reduced. Interestingly that NBC1 has higher efficacy than NBC2 in triggering plant immune-system against BYMV as indicated from DS percentage (DS = 10.66% and 19.33% in case of plants treated with NBC1 and NBC2, respectively). This could be attributed to the higher content of TNPs in NBC1 (21.58%) as compared to NBC2 (14.32%). Overall, NBCs offer safe and economic antiviral agents against BYMV.

Introduction

Faba bean (Vicia faba L. Fabaceae) is one of the largest food crops in Egypt and around the world. It is highly susceptible to viral diseases, leading to a significant reduction in productivity worldwide [1,2]. Bean yellow mosaic virus (BYMV) is the most common and prevalent virus among faba bean viruses [3,4]. Makkouk et al. reported BYMV in about 89% of the Egyptian faba bean fields surveyed with high-level BYMV symptoms (80–100% infection) [5]. BYMV is difficult to be controlled due to its fairly large host range and the ability to transmit non-persistently the aphid species as well as the seeds of some legumes species [4,6]. The number of chemical pesticides used in the management of plant virus diseases is limited. New strategies to manage viral diseases have been called for better and more sustainable control of viral diseases. It is therefore investigated for the management of plant viral diseases by inducing natural plant protection, e.g. systemically acquired resistance (SAR) [7].

Interestingly, a plethora of engineered nanomaterials has been used to induce plant-systemic resistance, combat phytopathogens and promote crop yield [8,9]. Particularly, titania (TiO2) nanoparticles (TNPs) have recently demonstrated prominent roles in the agroecosystem such as enhancing the plant immune system, controlling phytopathogens and thus plant diseases, and increasing plant growth and yield, as well [10,11]. In recent times, few engineered nanoparticles (ENPs) including TNP were used as elicitors for enhancing of the plant immune-system against phytoviruses [[11], [12], [13], [14]]. However, the direct utilization of TNPs in the agricultural applications is restricted due to their potential health risk to mammals [15] and some toxic impacts on plants [16]. Therefore, agricultural researchers have focused on the fabrication of TNPs with new morphological and functional features to makes them suitable for green agricultural applications for limiting plant diseases. Among the strategies followed to fabricate green TNPs, coating of TNPs with biodegradable polymers such as chitosan (CS), to fabricate nanobiocomposite (NBC), act as the promising one [17]. Coating with CS can offer multiple synergistic beneficial effects for TNPs as reducing their risks on the agroecosystem to achieve sustainable plant growth by promoting the intrinsic potential of plants such as systematic-resistance to phytoviruses [14,18]. For instance, the native chitosan was effectively induced resistance against viral infection in several plants such as cucumber, tomato, potato, tobacco, and sunflower [[18], [19], [20]]. On the other hand, the engineered CS-based nanomaterials have given many plants a strong immunity against phytopathogens (bacteria, fungi, and viruses), leading to sustainable plant protection and growth [21]. However, several shortcomings have restricted the wide application of neat chitosan in the engineered coating for NPs such as its low mechanical strength, poor chemical stability, and weakness of the NPs-CS binding [22]. Different chemical approaches have been adopted to escalate the intrinsic properties of CS to tackle these drawbacks [23]. In this context, carboxymethyl chitosan (CMC) derivatives, obtained by chemical modification of CS, were proven as promising alternatives for chitosan in the fabrication of the ENPs due to their higher stability, higher hydrophilicity, larger specific surface area, higher chelation capacities due to possession of multiple functional groups (carboxyl, amino, and hydroxyl groups) enabling it to efficiently interacted with metal ion, metal nanoparticles (MNPs). and metal oxide nanoparticles (MONPs), and cosequently, can be used as templates for building up of any MNP-/MONP-based composites [24,25]. This strong CMC-nanoparticles interaction helps in avoiding several serious health and environmental impacts, such as (i) leaching of higher concentrations of these nanoparticles into the environment; (ii) agglomeration into highly toxic massive particles.

So and in continuity for our outgoing program to explore new safe antiviral candidates [26], the main aims of this study are to fabricate and characterize novel engineered CMC-TiO2 nanobiocomposites (NBCs) and to investigate the capacity of these NBCs to effectively trigger resistance in faba bean plants against the Bean yellow mosaic virus (BYMV) infection. The advantages of using CMC-based nanocomposites, in this study, over chitosan-based ones are the promoted biocompatibility and superior antimicrobial activity of CMC as compared to chitosan [27].

Section snippets

Materials and methods

Materials and the details for the instrumentation used in this work along with the experimental protocols utilized for the extraction of chitin from crab shells, partial deacetylation chitin to give chitosan and it partial degradation into low molecular weight chitosan (LMWC) were described in the electronic Supplementary information (ESI†).

Synthesis of nanocomposites (NBC1,2)

The protocol used for the synthesis of NBCs is comprised of two consequent processes (see Scheme 1). In the first process, the carboxymethyl derivatives of low molecular weight chitosan (CMLMWCs) were prepared via a two-steps reaction, keeping in mind, the caboxymethylation product depends on the reaction conditions. For instance, if the LMWC was initially treated with a mixture of NaOH and SDS, which acts as an activating agent for C6-OH group, followed by dilution with isopropanol, which

Conclusion

Two types of carboxymethyl derivatives for low molecular weight chitosan (N,O-CMLMWC and O-CMLMWC) were successfully synthesized, for use as templates for fabrication of the corresponding TiO2-CMLMWC nanobiocomposites (NBCs, NBC1,2) via in situ incorporation of titania (TiO2) nanoparticles (TNPs) into the matrix of CMLMWC. FTIR, XRD, EDX, SEM, and TEM measurements clearly showed the successful formation of TNPs with the size range of 39–52 nm into the CMLMWC network. The efficacy of these NBCs (

Author statement

Ahmed R. Sofy: Conceptualization, Methodology, Software, Data curation, Validation, Visualization, Writing - Original Draft, Writing - Review & Editing.

Ahmed A. Hmed: Methodology, Data curation, Validation, Writing - Original Draft.

Abd EL-Aleem M. Alnaggar: Methodology, Data curation, Validation, Writing - Original Draft.

Rehab A. Dawoud: Methodology, Data curation, Validation, Writing - Original Draft.

Reda F. M. Elshaarawy: Conceptualization, Methodology, Software, Data curation, Validation,

Declaration of competing interest

The author(s) declared no potential conflicts of interest.

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