The Role Of Peptides

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By Irina Lyapina Irina Lyapina Scilit Preprints.org Google Scholar View Publications † , Anna Filippova Anna Filippova Scilit Preprints.org Google Scholar View Publications † and Igor Fesenko Igor Fesenko Scilit Preprints.org Google Publication *

Department of Functional Genomics and Proteomics of Plants, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry Russian Academy of Sciences, Moscow 117997, Russia

Antimicrobial Host Defence Peptides: Functions And Clinical Potential

Submission Received: 5 August 2019 / Revised: 2 September 2019 / Accepted: 3 September 2019 / Published: 5 September 2019

Plants have developed a sophisticated innate immune system to combat a variety of phytopathogens and insect herbivores. Plasma-membrane-localized pattern recognition receptors (PRRs), such as receptor-like kinases (RLK), recognize unique signals, pathogen- or damage-associated molecular patterns (PAMPs or DAMPs), and trigger immune responses. A growing body of evidence shows that many peptides hidden in plant and pathogen functional protein sequences belong to such a group of immune signals. However, the origin, evolution, and release mechanisms of peptide sequences from functional and nonfunctional protein precursors known as cryptic peptides remain largely unknown. Various specialized proteases, such as metacaspases or subtilisin-like proteases, are involved in the release of peptides upon activation during defense responses. In this review, we discuss the roles of cryptic peptide sequences hidden in the structure of functional proteins in plant defense and plant-pathogen interactions.

Although there is no adaptive immune system, plants have developed an innate immune system to combat potential pathogens. Several models have been proposed to explain the response of plants to pathogens. The classical “zigzag model” describes two modes of plant resistance mechanisms, PTI (sample-triggered immunity) and ETI (effector-triggered immunity), both of which lead to the development of systemic acquired resistance (SAR). Innate immunity relies on the recognition of conserved pathogen molecular patterns. These molecules are called microbe-associated patterns (MAMPs) or also called pathogen-associated molecular patterns (PAMPs), which are recognized by pattern recognition receptors (PRRs) on the cell surface [1]. Some well-known examples of MAMPs are fragments of flagellin, EF-Tu, DNA, lipoproteins, lipopolysaccharides, and fungal chitin [2]. Recognition of MAMPs and PAMPs by PRRs triggers signaling pathways for downstream defense responses, known as the PAMP-triggered immunity system (PTI) [3]. PTI is the first line of defense against pathogen attack, involving complex physiological changes to confer pathogen resistance. Such changes promote Ca influx

, production of reactive oxygen species (ROS) and NO, biosynthesis of antimicrobial molecules and defense hormones, activation of mitogen-activated protein kinases (MAPKs) and recruitment of transcription factors such as WRKY, BES, ASR, ERF, ORA, or MYC to induce the expression of defense genes [4 ]. However, the co-evolution of plant-pathogen interactions has helped pathogens acquire specialized means to avoid receptor recognition and suppress PTI. To prevent pathogen invasion, ETI is activated upon recognition of pathogen effector proteins in the cytoplasm by intracellular nucleotide binding leucine-rich repeat (NB-LRR) proteins. NB-LRR proteins are encoded by R genes [5]. Once activated, ETI triggers the synthesis of signaling molecules that are transported from infected to neighboring cells. Perception of these signals leads to the activation of MAP kinases cascades similar to the PTI mechanism, which induces the accumulation of molecules such as salicylic acid, as well as the transcription of pathogen-related (PR)-genes. Released PR-proteins are mostly non-pathogen-specific, they may have antibacterial, antifungal or antiviral activity and are found in the extracellular space as well as in vacuoles [6]. Antimicrobial peptides, defensins, cyclotides, thionins, snackins, lipid transfer and heain-like proteins, form another important component of plant defense mechanisms. These antimicrobial agents are gene-encoded, may consist of 10–50 amino acids, and are expressed in various parts of plants [7]. Compared to PTI, ETI mediates chronic responses, such as a hypersensitive response, which ultimately leads to the programmed death of infected cells [8].

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The release of endogenous molecules into the extracellular space as a result of damage to host cells triggers a signal to alert neighboring cells of danger. The original “zigzag model” does not take into account any damage-associated molecular patterns (DAMPs), which indeed play an important role in inducing or amplifying host immune responses [9]. Nowadays, endogenous plant signaling peptides have attracted special interest. These peptides are derived from functional and nonfunctional precursor proteins and can trigger antiherbivore or antimicrobial defense pathways. Systemin, the hydroxyproline-rich systemin and plant elicitor peptides (PEPs) are the best studied plant peptide DAMPS [10]. Such plant immune peptides have recently been called phytocytokines because they have many similarities to metazoan cytokines [11]. These peptides are effective at low concentrations, are absorbed by specific receptors, and are mainly derived from inactive protein precursors upon injury or pathogen infection. Their precursors are usually small proteins with no known functions. For example, AtPEP1 is derived from a 92 amino acid protein precursor [ 12 ]. The exact mechanism of Pep1 release was unknown until a recent study by Hander et al., which described a mechanism involving calcium-induced activation of metacaspase-4. Conserved AtPEP1 has been shown to be released from its cytoplasmic precursor PROPEP1 upon wounding by metacaspase-4 (MC-4), which is activated by calcium influx into the damaged cell. Under normal conditions, MC4 is inactive in the cytosol and the protein precursor PROPEP1 is attached to the vacuolar membrane. MC4-mediated processing of PROPEP1 occurs in leaves, but not in roots [13]. As there are nine metacaspase genes and eight PROPEPs in Arabidopsis, this suggests complex protease networks involved in peptide DAMP signaling. Moreover, metacaspases are only involved in the release of PROPEP family peptides. An extracellular metacapse-9 cleaves from its precursor a bioactive peptide GRI (GRIM REAPER), which plays an important role in cell death in Arabidopsis [ 14 ]. In addition to metacaspases, other types of proteases are involved in the release of peptide DAMPs. A recent study revealed a novel type of peptide DAMP in cells of Zea mays, immune signaling peptide 1 (Zip1). It is produced by papain-like proteases (PLCPs) after salicylic acid (SA) treatment. Zip1 only stimulates the transcription of SA-responsive genes [15]. Despite the examples mentioned above, the plant proteases involved in the release of plant peptide DAMPs have not yet been elucidated.

Phytocytokines interact with receptor complexes and transmit their signals downstream. Membrane-localized leucine-rich repeat receptor-like kinases (LRR-RLKs) have been shown to play a key role in environmental stress responses, as they are involved in the perception of highly secreted peptides. For example, in rice, maize and Arabidopsis thaliana , PEPs transduce their signals by binding to the plant elicitor peptide receptor (PEPR) LRR receptor kinases (RK) — PEPR1 and PEPR2 [ 12 , 16 ]. Both receptors cooperate with the co-receptor BRI1-associated kinase 1 (BAK1), which is also involved in developmental regulation through interaction with the plant brassinosteroid receptor BRI [ 17 ]. The DAMP is an 18 amino acid peptide, systemin, which is recognized by distinct LRR-RKs—SYR1 and SYR2 [ 18 , 19 ]. This pair of receptors triggers an intracellular signaling cascade: depolarization of the plasma membrane, an increase in Ca influx

, activation of MAP kinase and phospholipase A2 activities [20]. In vitro studies have shown that systemin is released from its precursors by subtilisin-like phytospacers [21]; However, there is no such evidence in vivo.

Precursors of hydroxyproline-rich glycopeptide systems (Hypsis), which represent another family of defense signal peptides, undergo hydroxylation and glycosylation of prolines and are processed by the secretory pathway [22]. This suggests that post-translational modification of immune peptides plays an important role in plant defense response. Some antimicrobial, insecticidal and quorum sensing peptides are known to belong to the group of ribosomally synthesized and post-translationally modified peptides (RiPPs). their propeptides

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