Abstract
The current reports on phytopathogens multidrug resistance have become a significant issue for plant health and global food security. Antimicrobial peptides (AMPs) have recently gained generous attention as potential alternatives to prevent plant disease resistance because of their potent, multifarious antimicrobial activity. AMPs are low-weight protein molecules. Living organisms secrete a wide range of AMPs, with some synthesised by canonical gene expression, known as ribosomal AMPs, and non-ribosomal AMPs, synthesised by modular enzyme-generating systems. Plants produce an array of AMPs, yet they are still unknown to many infection processes of causal agents. Plant-derived AMPs have a wide range of structures and functions, and they induce an innate immune system in plants. The biologically active AMPs in plants mainly depend on direct and indirect interactions with membrane lipids. Transgenic plants have expressed several AMPs, the basis for the model of new synthetic analogues, to provide support against diseases. These peptides have shown significant ability to manage plant diseases and can provide an eco-friendly alternative to hazardous conventional methods. Here, we have a comprehensive study on AMPs to identify their role in plant pathogen stress suppression activities and their mode of action. This would surely facilitate a bottomless insight into AMPs' mode of action against pathogen infections. An improved understanding of the mechanism will facilitate the development of the next generation of antimicrobial peptides, potentially employing a multitargeted approach.
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1 Introduction
The world food security of a continuously growing global population is a major concern in the current scenario. According to recent studies, the growing human population is expected to reach ten billion by 2050 [1, 2]. The current agricultural food grain production is not fully supporting global food demand because the global population is rising by 1.13% per year. To fulfill human food demand, humans are called to increase grain production in huge amounts and also to develop novel and sustainable approaches that can raise crop yields and product quality with few changes in climate [3, 4]. Globally, 1.3 billion metric tons of food production are lost annually. Among them, approximately 34% are due to plant diseases caused by fungal, bacterial, and viral causal agents and nematodes [5,6,7]. The management of plant diseases through the excessive use of synthetic chemical pesticides, which are petroleum-based compounds, may destroy our ecosystem and agricultural suitable soil structure [8]. The continuous use of these hazardous chemicals promotes the emergence, genetic variation, and coevolution of pathogens, which leads to the origin of newly virulent species of phytopathogens [9]. Developing drug-resistant microbes is a challenging task for growers and scientific communities and requires alternative practices to combat formidable pathogens [10, 11]. As a result, in the current agriculture system, we require to develop a variety of highly potent techniques to improve global food production and manage the growth of plant pathogens.
Antimicrobial peptides (AMPs), emerging as newly optimistic candidates to resolve these concerns, play a crucial role in plant disease management (Fig. 1). Peptides with antimicrobial activities, also called host defense peptides (HDPs), have emerged as key elements that provide an innate immunity response [12,13,14]. Natural synthesis produces AMPs, which are short-sequence peptides of up to 100 amino acid residues with broad-spectrum activity. They act as protectors against microbe infections [15, 16]. AMPs are low-weight protein molecules. Structural and biochemical analysis reveals that AMPs are highly diverse groups of biologically active substances found in a wide array of life, including microbes, animals and plants [17, 18]. Folded peptides typically have one side positively charged due to the presence of lysine and arginine amino acids, and the other side primarily consists of hydrophilic or hydrophobic moieties consolidated with negatively charged microbial cell membranes [19, 20]. Their wide diversity makes them more effective in disrupting and rupturing the targeted phytopathogen cell membrane through the secretion of cell-degrading compounds [21].
Antimicrobial peptides (AMPs) roles in plant disease management
Cells classify AMPs into two groups, ribosomal and non-ribosomal, based on their mode of synthesis [22]. Gene-encoded peptides synthesise ribosomal AMPs during pre-protein cleavage, enabling the creation of R-AMPs, while modular enzymes, specifically non-ribosomal peptide synthetases (NRPS), efficiently utilize enzymes to assemble non-ribosomal AMPs [23, 24]. NRPS can produce macrocyclic antimicrobial peptides; typically, these NRPS form in one operon in bacteria or eukaryotes, gene clusters, and mostly synthesise (one peptide per gene cluster or operon) [25]. Prediction of ribosomal peptides is quite challenging but there are some reports which discussed the in-silico prediction of antimicrobial role of AMPs. The in-silico prediction offered valuable visions and methodologies to improve accuracy to better understanding and address the challenges related with ribosomal peptides prediction from genomic and transcriptomic data [26, 27]. Currently, a publicly available harnessing AMPs database, named ADAM, provides all necessary information, contains 7007 unprecedented peptide sequences, and comprises 759 peptide structures (http://bioinformatics.cs.ntou.edu.tw/ADAM/links.html) [28, 29]. The mass spectra (MS) imaging technique can identify new AMPs and their isoforms, providing useful information such as molecular weight of peptides, length of fatty acids in the peptide chain, and amino acid sequences [30,31,32]. According to their structures, the 8000 AMPs reported today [33] fall into three categories: (i) linear AMPs, which form helical structures, (ii) cyclopeptides, which adopt ring peptides, and (iii) open-ended cysteine peptides, which form structures resembling disulfide bridges [34]. Generally, fatty acid chains known as lipopeptides link both linear and cyclic peptides, forming complex molecules known as pseudopeptides [35, 36].
2 Classification and types of antimicrobial peptides (AMPs)
Thousands of AMPs have been discovered and used to confer resistance in a variety of plants. Certain factors enable the classification of AMPs. AMPs are classified into two major antimicrobial groups based on the composition of amino acids and peptide structures [37]. There are diverse group of AMPs reported which have ability to inhibit or kill diverse range of pathogens such as parasites, fungi, bacteria and viruses. AMPs have specific sequences, domains, and structures, which helps them to interface and disrupt the structural integrity and cellular processes [38]. Here are some unique features of AMPs that contribute to their specific activities. In addition to the classification above, we can also group AMPs into the following categories based on their mode of action and target:
2.1 Antibacterial peptides
Antibacterial peptides are among the most evaluated antimicrobial peptides today. These are mostly cationic in nature and target the cell membranes of different bacteria, leading to the disintegration of the lipid two-layer structure [15, 39, 40]. The majority of the antibacterial peptides are also amphipathic in nature, having both hydrophilic and hydrophobic domains. AMPs with these kinds of structures can bind to lipid parts (hydrophobic region) and phospholipid groups (hydrophilic region) [41, 42]. Investigations also proved that, at low concentrations, some AMPs can kill bacteria with their membranes intact. In this instance, AMPs do not directly interact with the bacterial membrane. They eliminate the bacteria by inhibiting some important pathways inside the cell, such as DNA replication and protein synthesis [43]. Some examples of this type of AMPs are buforin II, drosocin, pyrrhocoricin, and apidaecin. These AMPs have 18–20 amino acid residues with an active site and can diffuse into target bacterial cells and bind to DNA and RNA without disintegrating their cell membrane [44, 45].
2.2 Antifungal peptides
Antifungal peptides work exactly resemble to antibacterial peptides. These AMPs may either disrupt fungal cell wall [46, 47] or affect the intracellular components [48]. Some antifungal peptides can bind to chitin, which is the main part of the fungal cell wall [49,50,51]. This makes it easier for the antimicrobial peptides to target the fungal cells effectively. Cell wall targeting AMPs kills the target fungal cells by disintegrating the cell membranes [52, 53]; either increasing plasma membrane permeability or directly forming pores in the cell membrane [54]. Similar to antibacterial peptides, these antifungal AMPs also affect the fungal cells by inhibiting some important pathways inside the fungal cells. Some examples of antifungal peptides are D-V13K, P18, indolicin, and defensins [55,56,57,58].
2.3 Antiviral peptides
Antiviral AMPs have the potential to neutralize viruses by integrating either into the viral envelope or the host cell membrane. Antiviral peptides can target both enveloped RNA and DNA viruses [59, 60]. AMPs can integrate into viral envelopes and make the membrane instable, which leads to the viruses losing their ability to infect host cells [61,62,63]. These peptides can also reduce the ability of viruses to bind to host cells [64]. In addition to dissolving viral envelopes and obstructing viral receptors, certain antiviral peptides can obstruct viral particles, preventing their entry into the host cells by occupying specific receptors, a phenomenon commonly observed in most mammalian cells [65]. Other than AMPs, which bind to viral receptors on the cell surface, some antiviral peptides could not compete with viral glycoproteins to bind to heparin sulfate receptors on the cell surface [66]. Instead, these antiviral peptides can get through the cell membrane and settle in the cytoplasm and organelles of the host cell [67]. They may change the gene expression of the host cell, which can either help the cell's defense system fight viruses or stop the expression of viral genes [68, 69]. Certain antiviral peptides stop the virus by preventing the transport of an important viral protein into the host nucleus [70, 71]. In order to form complexes with the host transcriptional factors and induce the expression of immediate early viral genes, the virus needs this viral protein to defeat the first-stage cellular response [72, 73]. Hence, such antiviral peptides prevent cell-to-cell movement of the viral particles instead of competing with them to bind to the receptor on the cell surface [74, 75].
2.4 Antiparasitic peptides
Compared to the above three classes of AMPs, the group consisting of antiparasitic peptides is a smaller one. Magainin, the first antiparasitic peptide reported, has ability to kill Paramecium caudatum [15, 76]. Later, scientists developed a synthetic peptide to combat the Leishmania parasite [77]. Cathelicidin is another antiparasitic peptide that is very effective against Caernohabditis elegans. This antiparasitic peptide kills C. elegans by forming pores in the cell membrane [78]. Antiparasitic peptides have the same mode of action as other AMPs, despite the fact that some parasitic microorganisms are multicellular. They kill cells by directly interacting with the cell membrane [78].
2.5 Simulated antimicrobial peptides
Newly designed simulated AMPs with 6–47 amino acids have been synthesised. A solid-phase method is the best method for the synthesis of simulated AMPs [79, 80]. Combinatorial chemistry is a powerful tool for designing new molecules that can enhance its activity regarding to selected target pathogens, minimizing susceptibility to protease digestion and toxicity for animals and plant pathogens [81,82,83,84]. Many simulated AMPs have been produced based on animal origin. Cecropin A-melittin hybrid Pep3 is an active compound against several plant pathogens, including Phytophthora infestans, Thielaviopsis basicola, and Fusarium species [85,86,87]. Cecropin B inhibits Verticillium dahlia, Fusarium moniliforme, T. basicola, Xanthomonas campestris pv. malvacearum, and Pseudomonas syringae pv. tabaci [46, 88, 89]. Another cecropin analogue, MP39, is active against many bacterial plant pathogens such as P. syringae, Erwinia carotvora, and X. campestris, as well as phytopathogenic fungi like Rhizoctonia solani and P. infestens.
Many tachyplesin derivatives are active against Fusarium spp. [90]. Synthetic derivative of magainin, MS1-99, is efficient against the fungal causal agents e.g., Alternaria solani, P. infestans, and some bacterial plant pathogens [91, 92]. Kamysz et al. [93] found that CAMEL, a cecropin-melittin hybrid peptide, and iseganan, a simulated variant of porcine protegrin I, may kill soft-rot bacteria such as Pectobacterium spp. [94]. White shrimp produced Pe4-1, an isomorph of penaedin that inhibits F. oxysporum and numerous plant pathogenic bacteria [95]. Derivatives of phyto AMPs have also been prepared. A peptide, Rs-AFP2, derived from radish defensin, restricts growth of fungi [96]. According to Vila-Perello et al. [97], D32R, which is similar to Pyrularia pubera thionin, can kill Botrytis cinerea, F. oxysporum, Plectosphaerella cucumerina, and a number of bacterial causal agents, such as Clavibacter michiganensis and X. campestris pv. translucens. Reed et al. [98] implied that the hexapeptide PEP6 can kill Pythium ultimum, R. solani, Ceratocystis fagacearum, and F. oxysporum f. sp. lycopersici. ESF12 is active against Agrobacterium tumefaciens, Erwinia amylovora, and P. syringae [99]. ESF1 has antifungal activity against A. solani, P. infestans, and Septoria musiva. A synthetic hexapeptide, PAF26, is effective against B. cinerea, Penicillium digitatum, and Penicillium italicum [100,101,102]. The 2S albumins AMPs, derived from seeds of both monocotyledonous and dicotyledonous plants, exhibit antimicrobial properties against fungal phytopathogens including Fusarium oxysporum, F. solani, and Colletotrichum spp. [103]. Under both laboratory and greenhouse conditions, AsR416 obtained from Allium sativum reduced the disease severity of the rice sheath blight and the pathogen infection process [104]. The application of GMA4CG_V6 by spraying on tobacco and tomato plants effectively prevented and cured indicators of grey mould disease [102]. According to Yang et al. [105], inducing the MdDEF25-YFP fusion enhanced the resistance against F. solani in apples, providing a novel approach for future prevention and biological control of apple replant disease. Recently, Panthi et al. [106] found that applying three plant-derived AMPs (β-purothionin, defensing-2, and purothionin-α2) to the leaves of wheat reduced rust infections by increasing the expression of genes related to defense reactions.
3 Mechanisms of action of AMPs
Investigate the mechanism of action of antimicrobial peptides in combating plant diseases, which has significantly contributed to the development of sustainable approaches. The targeting action of AMPs directly interacts and massively degrades some pervasive pathways in living cells, such as protein synthesis and DNA replication, which inhibit pathogen growth at low concentrations [20]. Various microbes produce different AMPs that act as protectors in response to invading pathogens by causing cell wall death or by targeting intracellular processes [46, 47]. Bacillus sp. is a microbe that may secrete many AMPs, such as iturins, polymixins, fusaricidins, agrastatins, and fengycins [107]. These AMPs are very important because they prevent a wide range of plant pathogens by eliminating fungal causal agents [108,109,110]. Until now, the activation of antifungal AMPs with target cells, such as antifungal peptides with β-sheet and α-helical structures, remains an unresolved story due to their unique structures [111, 112]. Indeed, scientists have reported interesting mechanisms, by which AMPs interact and bind with fungal membrane cells, then macerate the fungal membranes by inducing pores or altering membrane permeabilization [113,114,115]. The crucial role of lipopeptides under in vitro conditions has a strong dilemma effect on plant disease-causing microbes such as F. oxysporum, Alternaria spp., P. ultimum, B. cinerea, and R. solani [116]. The potential application of AMPs for inhibiting the bacteria under in vitro conditions required a low quantity that was sufficient for the inhibition of bacteria, ranging from 0.25 to 4 μg/ml. Pre-treatment of bean seedlings with Bacillus subtilis M4 gives superior results for improving plant disease status and suppressing pathogen growth [117]. The multifarious benefits of AMPs include destructive effects on host cells, broad-spectrum activity, and potential resistance to reported antibiotic-resistant microbes [118] (Fig. 2). AMPs activity is not only limited to the inhibition of pathogens, but they also have other promising modes of action e.g., systemic resistance and huge production of phenolic compounds that enhance disease resistance in vitally strategic plants [119,120,121].
Multifarious roles of AMPs
The mechanism of AMPs is dependent on several physiochemical properties, such as charge, amino acid sequence, amphipathic nature and structure [122, 123]. These peptides involve various mechanisms for membrane disruption [124, 125]. Positively charged AMPs bind to the microorganism's surface with receptor-mediated interaction and insert into the cytoplasmic membrane [126, 127]. Several AMPs inhibit enzymatic activity, nucleic acid, or protein synthesis through membrane disruption, while others have a non-membrane disruptive nature and cross the cell membrane to interact with intracellular targets [43, 128, 129]. Several researchers conclude that the AMPs ability to bind the bacterial membrane plays an essential role in the exploitation of AMPs in plant disease control [130,131,132]. The interaction capacity of bacterial cell walls and membranes determines AMPs' ability to kill bacteria. AMPs typically prefer binding to negatively charged bacterial membranes (due to the presence of phospholipids such as phosphatidyl glycerol and cardiolopin), as they possess a net positive charge and a high ratio of hydrophobic amino acids [54, 133]. This electrostatic interaction between anionic-charged phospholipids in the bacterial membrane and cationic-charged AMPs is a significant driving force for cellular contact and interaction [134,135,136]. When the amphipathic structure of AMPs contacts the bacterial surface, hydrophilic segments of the peptide interact with charged head groups of phospholipids, and hydrophobic peptide domains interact with the lipid bilayer [12, 137, 138].
AMPs binding to the bacterial membrane leads to non-enzymatic disruption. Various microbes differ in cell types and membrane compositions, which govern the selectivity of specific species. Several AMPs employ an immediate microbicidal effect by disrupting target organism membrane unity or translocating across the microbial membrane to reach intracellular targets [139]. A few AMPs' binding mechanisms to the bacterial membrane include barrel stave, toroidal pore wormhole, carpet, and detergent-like models [80, 140]. The barrel-stave model forms ion channels by locating the peptides in a specific direction between the membranes and joining them together [141, 142]. The toroidal pore wormhole model places peptides in a parallel direction with a two-layer membrane [143], while the carpet model places peptides on the membrane surface to cause chaos and disorder [141]. Aggregation of peptides in a suitable concentration expands the membrane curvature, which leads to enhanced production of the spiral pore of the membrane [143, 144]. In this mechanism, peptides envelop the carpet by creating a membrane surface that resembles the early stages of a “spiral hole”. It breaks the membrane into tiny pieces [40]. Furthermore, peptides gathered together, increased concentration, and formed micelles due to amphipathic properties [40].
AMPs play an important role in destabilizing the bacterial membrane by increasing or decreasing its thickness [145]. Furthermore, AMPs produce complexes with minute organic anions, causing membrane permeability and allowing them to carry across the membrane [146, 147], or by inducing molecular electroporation, where the charged AMPs create a transmembrane potential, resulting in pore formation and molecular translocation [148, 149]. Furthermore, non-bilayer intermediates collapse after internalizing the peptide within the membrane, and AMPs can generate peptide release [40, 150], while AMPs also cause the membrane to disintegrate without significantly altering the membrane's structure [12, 129, 151]. Notably, most AMPs directly interact with lipids, transforming the lipid phase stage in the bacterial membrane, which includes both positive and negative membrane curvature, as well as the cubic liquid phase [40]. Peptides that induce positive curvature strain can facilitate the production of toroidal pores and micelles; however, negative curvature stress and the induction of the cubic lipid phase by AMPs can produce non-bilayer intermediates, resulting in membrane porosity [40, 150, 152]. AMPs cause permeability of the membrane, resulting in leakage of metabolites, dysfunction of the membrane, and finally leakage, rupturing, and lysis of the bacterial cell membrane [37, 153, 154]. Membrane permeability plays an important role in allowing specific AMPs to move into the cytoplasm of bacteria for various target intracellular processes such as RNA, DNA, protein, and cell wall synthesis, as well as enzymatic activity and protein folding [153, 155]. There are several types of intracellular target AMPs, such as teixobactin, which stops the production of cell walls by attaching to peptidoglycan precursor lipids [156], indolicidin, which stops DNA replication by interacting with DNA [129], Lser-PRP2 (larvae peptide), which stops protein production by connecting to the bacterial chaperone Dnak [157], and protein-rich peptide Bac5, which stops translation by attaching to ribosomes [158]. In addition to direct bactericidal action, several AMPs employ complex immunomodulatory functions (Fig. 3). The immunomodulatory activities of AMPs include the formation of increased immune cell chemotaxis, the initiation of immune cell differentiation, dendritic cell maturation, activation of adaptive immunity, repression of cytokine-mediated and Toll-like receptor (TLR)-mediated cytokines, release of proinflammatory cytokines and reactive oxygen species (ROS), induction of anti-inflammatory cytokines, scavenging of bacterial endotoxins, stimulating angiogenesis, enhancing wound healing, and reducing scar formation [159, 160].
Mechanism of action and immunomodulatory activities of antimicrobial peptides (AMPs)
Cathelicidins and defensins encompass the major families of membrane-disrupting peptides [161]. The electrostatic interaction between clusters of cationic charge in defensin and anionic charge in the phospholipid band can produce pores in the bacterial membrane that destroy the membrane's coherence and support the lysis of the target microorganisms [162]. Cathelicidins disrupt the bacterial cell membrane similarly to defensins. Enzymatic digestion through a few AMPs results in disruption of the bacterial membrane [163]. For example, lysosomes break down the β-glycosidic linkage between N-acetyl glucosamine in the peptidoglycan of bacterial cell walls and phospholipase A2 (PLA2) released from human platelets [164]. This breaks down the bacterial cell membrane phospholipids and disrupts the bacteria. From the seeds of Impatiens balsamina, AMPs named as Ib-AMP1-4 contains four short peptides. It reduces the growth of a wide range of bacteria and fungi. Ib-AMP1 penetrate the fungal cell surface/ cell membranes without forming any amphipathic helix. The activity of AMPs determines by the presence of disulfide bonds [165]. Most of the antimicrobial peptide families also showed antifungal properties due to multiple cysteine-bridge defensins and pro-rich peptides [166].
4 AMPs mode of action and gene expression
AMPs are considered as an essential component of the plant defense system. These compact and typically simple peptides may serve as a general defense mechanism, providing permanent and direct protection from environmental stresses. When a pathogen attacks the host plant during plant-pathogen interaction, the host activates several defense mechanisms to provide durable and direct protection against a diverse range of pathogens. A high degree of heterogeneous mechanisms of action characterizes these chemical and morphological defense mechanisms [144, 167, 168] (Table 1). The spatiotemporal analysis of AMPs gene expression reveals their presence in all plant parts and their tissue-specific identification [169, 196]. Few AMPs are readily accessible at the infection site in such a diverse condition, while others activate only after the attack to restrict tissue-specific invaders [197]. The availability of the distinctive AMPs inside the compromised organs, along with a dynamic peptide complex with different patterns of expression and modes of action, enables the AMPs to mediate this form of defense [198,199,200].
4.1 AMPs as morphological and chemical defense shields
In the plant immune system, plants show a type of adaptation to the attack mechanism, i.e., an increase in the production of different morphological and chemical defense shields when the plant is attacked by pathogens [201]. Most AMPs genes exhibit this type of dynamic response because their production increases rapidly, specifically by herbivore or microbial attacks [202,203,204]. AMP genes are incorporated into the general network of defense signaling because their production appears to be controlled by a similar signaling mechanism that regulates many other plant immune responses [205, 206]. For instance, several plant species frequently classify various plant hormones that control the immune system, such as salicylic acid, ethylene, and jasmonic acid, as potential inducers of AMP gene expression [207,208,209]. Indeed, there is an effective connection between AMPs and the activation of defense hormones. Some of the AMP genes, such as PDF1.2 and Thi2.1, are generally considered as very important genes for the evaluation of signaling pathways in the plant's immune system and hormonal activation [210]. The mechanisms of plant AMPs communicate to monitor defense responses with mitogen-activated protein kinase (MAPK) signaling cascades and ROS are not fully understood yet [207]. For instance, when plant pattern recognition receptors (PRRs) detect microbial pathogens, they activate multiple MAPK signaling cascades, which increase the expression of AMP genes. The molecular level has shown that MAPKs are powerful inducers of transcription factors linked to plant AMP expression. Along with this, AMPs interact with components of the ROS-activated MAPK signaling cascade, which may interact with AMPs to control plants' defense mechanisms [207]. The interactions of AMPs with membrane are vital to show antimicrobial activity, these interactions are:
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(a) AMPs interactions with the cell membrane
Plant AMPs also act as a protective chemical shield that resists a broad range of causal agents [211, 212]. This is essentially based on two main principles: (1) the diversity of their mode of action, and (2) their exceptional structural stability. One of the most interesting characteristics of plant AMPs is that they can perform different types of functions depending on the various targets and factors they communicate with. The 'peptide promiscuity' demonstrated by Franco [213] enables the AMPs to function according to the attacking organism through various modes of action to characterize various weak points. The plant AMPs may effectively interact with bacterial membranes [163, 214]. The bacterial membrane’s outermost layer consists of phospholipid head groups, which are negatively charged, whereas the AMPs are positively charged [164, 215, 216]. This type of electrostatic disparity results in lipid dislocation, surface tension, and membrane organization modifications (Fig. 4A). This AMP membrane interaction contributes to cellular material leakage and fatal microbial membrane destruction. Plant AMPs, such as some lipid forms of plasma membranes and construction blocks of cell walls, may also affect the specific structural components on the cell surface [165, 217]. This feature enables certain classes of AMPs to target specific groups of pathogens specifically. For instance, defensins, a well-known group of AMPs with plant origin, work well as an antifungal peptide because they bind to specific sphingolipids in the fungal cell membrane [173, 218, 219]. AMPs may not choose one membrane or lipid group over another based-on differences in charges. Instead, they choose based on the structure and sequence of amino acids in the peptide, except when it comes to interactions between AMPS and bacterial membranes [167]. This type of interaction forms transient pores, allowing AMPs to freely move and interact with intracellular components in the membrane. Sphingolipids, in addition to controlling the cell cycle, play a significant role as secondary messenger molecules [217, 220, 221]. A suggested mode of action of defensin indicates that such peptides interact with the sphingolipids upon cellular uptake to activate signaling cascades that eventually lead to programmed cell death in fungal cells [222, 223] (Fig. 4B). The binding of plant AMPs to sphingolipids also influences the ion influx and efflux of the pathogen cell [224, 225]. The fungal pathogenic growth and multiplication depend on the persistence of the intracellular Ca2+ concentration gradients, which seems to be essential for accelerating the tip growth. For example, defensins similar to dahlia Dm-AMP1 and radish Rs-AFP2 bind to the sphingolipids of typical types of fungal membranes, causing a significant and swift rise in the influx of Ca2+ in the fungus cell, resulting in gradient dispersion and inhibition of pathogenic cell growth [226]. Contrary to insect and mammal defensins, Dm-AMP1 and Rs-AFP2 may develop ion-permeable pores and therefore do not alter the electrical characteristics of the lipid bilayers, suggesting a distinct mechanism that results from plant AMP-induced alteration in Ca2+ fluxes [227].
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(b) AMPs affecting the inner cell components
Action mechanisms of plant AMPs. A Interaction is facilitated by electrostatic variations between AMPs (positively charged) and the bacterial outer membrane (negatively charged). AMPs can dislocate membrane lipids upon interaction to alter the structure of the microbial membrane or to form structures similar to pores in the membrane. Both mechanisms result in cellular part leakage and fatal microbial membrane destruction. B Interaction with specific membrane targets in fungal cells such as sphingolipid types (indicated in red in the inset) can lead to the cellular uptake of AMPs that further interact with internal cell components to initiate signaling cascades resulting in the programmed death of cells
Plant AMPs have evolved plants that operate by explicitly disrupting the role of their inner cell components. This mechanism of action may be activated by a variety of mechanisms, including the interaction of peptides with specific membrane receptors that transmit the signal to the internal components of the cell, the AMP internalization pathways that use membrane receptors, or the endocytic uptakes that require energy loss [228,229,230]. For example, Koo et al. [231] found that AMP-PPn-AMP1 (an anti-fungal compound), produced in the seeds of morning glory (Ipomoea nil), causes sudden and rapid depolarization of the actin cytoskeleton, which is further associated with the retardation of fungal multiplication and growth. Pn-AMP1 transmits the external peptide signal via an internal signaling network in combination with membrane receptors located in the fungal cell membrane, which alters the status of the actin filament. Another example of this type of mechanism is the defensin PsD1, which is constitutively produced in pea (Pisum sativum) leaves and seeds and crosses the fungal membranes to interact with nuclear proteins responsible for controlling the fungal cell cycle and cell division, inhibiting the growth of pathogenic cells [232, 233]. The AMPs of plants modulate the activity of internal cell components e.g., mitochondria, nucleus, vacuole, protein synthesis initiation and elongation steps [234,235,236].
4.2 AMPs as passive defense weapons
Besides directly attacking pests and microorganisms, plant AMPs may also serve as passive defense mechanisms. They can indirectly change the body functions of insects and herbivores intestines by stopping enzymes e.g., trypsin, chemotrypsin, and α-amylase from doing their jobs. This hinders their ability to absorb nutrients, thereby restricting their growth [237]. It also modifies the electrophysiology of intestinal cells, resulting in a decrease in nutrient absorption [238], and it also impacts the midgut epithelium cells of insects [199]. It has been shown that insects can strongly block alpha-amylase activity using, a defensin (VuD1) from cowpea (Vigna unguiculata). The passive action of plant AMPs includes their ability to stop the activity of proteins released that are directly associated with fungal pathogenicity in plants and their ability to cause allergenic responses in mammals [174, 239].
5 Transgenic plants expressing antimicrobial peptides
Serious environmental concerns have led to the ban on many global agrochemicals, and, at the same time, the growing demands for sustainable crop protection strategies have inspired the idea of using AMPs to improve plant health [240]. This research talks about the different ways that AMP stops pathogens from attacking and gives an overview of the effects of AMPs expression in transgenic plants that are important for changing different plant immune pathways (Table 2).
5.1 Modulation of different cascades of the immune system in the corresponding transgenic plants
Some reports show that the host gene's profile changes after AMP penetration. Expression of the metchnikowin gene from Drosophila melanogaster in barley to encode a peptide with antimicrobial activity was used to improve plant defense against microbial attack. This is supported by an assessment of the effect of metchnikowin on powdery mildew during its interaction with transgenic barley. Researchers reported that the anti-fungal peptide enhanced plant resistance, potentially impeding the development of a functional cusp through an increased rate of hypersensitivity reaction (HR) and the development of cell wall apposition [16, 254]. Rahnamaeian et al. [255] conducted a comprehensive study on the potential latent effect of metchnikowin on plant defense systems, revealing that interaction with mould improves the SAR and ISR pathways, as well as the redox state of barley plants expressing metchnikowin. In the phenylpropanoid signaling pathway, the PAL-1 gene expression profile showed that the activity of PAL in transgenic metchnikowin plants increases upon infection with Bgh. De Beer and Viver [256] made a similar observation for the PAL gene, suggesting that highly activated ISR may be one of the reasons for increased resistance in these transgenic plants. The higher expression of PR-6 in metchnikowin plants compared to wild-type individuals supports this assumption [257]. Higher ROS levels, up to the expression of AMPs, support the idea that these peptides play a role by modulating the redox environment, which can lead to cell death [223]. Those inhibitors, MLO and Bax, in Metchnikowin barley showed that the sensitivity or resistance of these plants does not depend on these factors. A comparative analysis of gene expression between transgenic cecropin A. Plants and wild rice plants that were grown in ideal conditions and during a rice outbreak caused by Magnaporthe oryzae infection showed overexpression of several genes. These genes are involved in (1) protecting against oxidative stress, (2) making proteins that go into the secretory pathway, (3) the translation mechanism, and (4) the genes that code for the parts of the vesiculate vegetable garden graft in rice Cecropin A [258]. Overall, these relationships suggest an impaired immune status in plants expressing AMP. The findings revealed that the PRR-activated MAPK cascade (MEKK1-MKK1/2-MPK4) may inhibit SUMM2-NLR activation, representing a unique example of coordinated regulation between RLK and NLR activation. To investigate the mechanism underlying cell death mediated by the PRR coreceptors BAK1 and SERK4, we employed a virus-induced gene silencing (VIGS) approach for temporal RNAi. This enabled us to develop an innovative high-throughput screening method for identifying cell death suppressors using collections of mutants marked by the DNA transfer sequence (T-DNA) of Arabidopsis. The findings revealed that the PRR-activated MAPK cascade (MEKK1-MKK1/2-MPK4) may inhibit SUMM2-NLR activation, representing a unique example of coordinated regulation between RLK and NLR activation. To investigate the mechanism underlying cell death mediated by the PRR coreceptors BAK1 and SERK4, we employed a virus-induced gene silencing (VIGS) approach for temporal RNAi. This enabled us to develop an innovative high-throughput screening method for identifying cell death suppressors using collections of mutants marked by the DNA transfer sequence (T-DNA) of Arabidopsis. [259]. DrsB1-CBD, a recombinant peptide showed highest antifungal activity. Expression of recombinant peptides provides protection to transgenic plants against Pythium aphanidermatum. Expression of new recombinant peptides led to a delay in fungal colonization and the appearance of symptoms of fungal disease take from 6 days to more than 7 weeks [260]. Fujimura et al. [261] found two isoforms, Fa-AMP1 and Fa-AMP2, in buck wheat (Fagopyrum esculentum) that were very good at the inhibition of bacteria and fungi.
Plant defensins, besides their antimicrobial activity, exhibit sensitivity to abiotic stress and play a crucial role in plant growth and development [262, 263]. Several reports also describe the multigenic transformation of disease-resistant genes. The co-expression of the transgenes Rs-AFP2 (Rhapanus sativus) and Dm-AMP1 (from Dahlia merckii) in processed rice caused greater resistance to fungal pathogens than only transformed plants [264]. Similarly, a transgenic potato that expressed the antifungal defensin Ms-Def1 (Medicago sativa seeds) inhibited the growth of V. dahlia [226].
6 Exploiting antimicrobial peptides in plant disease control
Antimicrobial compounds are significant to plant disease management because of their mechanism of action against the target microorganism. The phytotoxic nature of microbial-origin AMPs (e.g., LCPs and peptaibols) restricts their direct use as plant protection products. Furthermore, synthetic procedures, primarily using AMPs as a basis, can produce shorter and less toxic analogues. Other AMPs play a role as biocontrol agents for plant diseases [265]. The AMPs of plant and animal origin have provided tools for developing transgenic plants with genes coding for total or partial resistance to plant pathogens [266, 267]. Various categories of antimicrobial peptides (AMPs), including plant defensins [268, 269], thionin [270, 271], lipid transfer proteins [272, 273], snakins [191, 274], hevein-type [177, 275], knottin-like family [276, 277], 2S albumins [278, 279], glycine-rich cysteine-free antimicrobial peptides MiAMP2c [280,281,282], Ib-AMP1 and Ib-AMP4 [165, 283], and cyclotide [36, 284], have significant efficacy against several fungal and bacterial phytopathogens (Table 3).
7 Conclusion and future prospect
AMPs have been playing a vital role in strengthening the plant's defense against phytopathogens. With modern genome-targeting tools and genetic engineering, it is now possible to overexpress the AMPs in the desired crop plant for enhanced resistance against biotic stress. Different plant species have reported overexpressing various classes of AMPs to manage an array of fungal and bacterial pathogens. Different parts of the plant, including the flower, shoot, root, and seed, have expressed these AMPs in response to biotic stress. Transgenic crops have integrated multiple AMPs to provide long-lasting and effective resistance against a wide range of pathogens. Researchers have investigated different classes of AMPs for their potential antagonistic activity against multiple drug-resistant bacterial pathogens. With such potential, we can now expect a new generation of versatile, potent, and durable antimicrobial drugs to be available on the market. A vast community of researchers is investigating the AMPs due to their significant role in plant immunity. The ability of AMPs to evolve and their wide spectrum of activity and mechanisms make them an excellent tool for plant defense against a wide range of pathogens and agriculture, clearly indicating a very promising future for research.
Data availability
No datasets were generated or analysed during the current study.
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Acknowledgements
The author M.M. gratefully acknowledges the financial support provided by the funding agency Science and Engineering Research Board (SERB), State University Research Excellence (SURE) (File Number: SUR/2022/005216) for this study. The author M.M. is also highly thankful to the Ministry of Education and SPD-RUSA Rajasthan for the financial support received under the RUSA-2.0 project. C.K. gratefully acknowledges the financial support from the project of the Ministry of Science and Higher Education of the Russian Federation on the Young Scientist Laboratory within the framework of the Interregional Scientific and Educational Center of the South of Russia (No. FENW-2024-0001). All the authors acknowledge their host institute for infrastructure support. All the authors read and approved the content of the manuscript for the publication.
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SK: conceptualization, writing—original draft, writing draft—review and editing, prepared figures. LB: writing—original draft, writing draft—review and editing. RK: writing draft—review and editing. DB: writing draft—review and editing. VS: writing draft—review and editing. CK: writing draft—review and editing, project administration. TM: writing draft—review and editing. ACB: writing draft—review and editing. PD: writing draft—review and editing. YN: writing draft—review and editing. R: review and editing. UBS: review and editing. AB: review and editing. H: writing draft—review and editing. AS: review and editing, prepared figures. PS: writing draft—review and editing, prepared figures. MM: conceptualization, writing—original draft, writing draft—review and editing, prepared figures, investigation, resources, data curation, supervision. All the authors reviewed and edited the contents. All authors have read and agreed to the published version of the manuscript.
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Kumar, S., Behera, L., Kumari, R. et al. Unraveling the role of antimicrobial peptides in plant resistance against phytopathogens. Discov Sustain 5, 243 (2024). https://doi.org/10.1007/s43621-024-00456-3
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DOI: https://doi.org/10.1007/s43621-024-00456-3