Quantitative Peptidomics Study Reveals That a Wound-Induced Peptide from PR-1 Regulates Immune Signaling in Tomato

Abstract

Many important cell-to-cell communication events in multicellular organisms are mediated by peptides, but only a few peptides have been identified in plants. In an attempt to address the difficulties in identifying plant signaling peptides, we developed a novel peptidomics approach and used this approach to discover defense signaling peptides in plants. In addition to the canonical peptide systemin, several novel peptides were confidently identified in tomato (Solanum lycopersicum) and quantified to be induced by both wounding and methyl jasmonate (MeJA). A wounding or wounding plus MeJA-induced peptide derived from the pathogenesis-related protein 1 (PR-1) family was found to induce significant antipathogen and minor antiherbivore responses in tomato. This study highlights a role for PR-1 in immune signaling and suggests the potential application of plant endogenous peptides in efforts to defeat biological threats in crop production. As PR-1 is highly conserved across many organisms and the putative peptide from At-PR1 was also found to be bioactive in Arabidopsis thaliana, our results suggest that this peptide may be useful for enhancing resistance to stress in other plant species.

The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions

“…For many years it was thought that tomato PR-1b encodes a 14-kD protein with antifungal activity (Niderman et al, 1995). Now it appears that it also encodes the CAPE1 peptide with antibacterial activity and antiherbivory activity and a role in the regulation of salt stress responses (Chen et al, 2014;Chien et al, 2015). At least 30 novel putative CAPE1-like peptides carrying the characteristic Pro-rich PxGNxxxxxPY motif were found in Solanoideae, Nicotianoideae, Viticeae, Brassicaceae, Fabaceae, and Poaceae (Chen et al, 2014) (Figure 3).…”

“…Such peptides, released from the precursor by proteolytic enzyme activity, are called cryptides (Samir and Link, 2011). In humans, ;35 cryptides have been reported (Pimenta and Lebrun, 2007), but in plants, only three have been reportedly identified (Figures 2 and 3) (Schmelz et al, 2006;Pearce et al, 2010a;Chen et al, 2014).…”

“…Although most known peptides are derived from nonfunctional precursors (see above), some studies reported the existence of unique peptides derived from functional precursor proteins (Schmelz et al, 2006;Pearce et al, 2010a;Chen et al, 2014) (Figure 1). In some cases, these functional precursors have a different primary function from that of the peptides buried within them.…”

“…Recently, a targeted and quantitative peptidomics strategy was employed to discover novel defense signaling peptides in tomato (Chen et al, 2014). CYSTEINE-RICH SECRETORY PROTEINS, ANTIGEN 5, AND PATHOGENESIS-RELATED 1 PROTEINS derived peptide 1 (CAPE1) was successfully identified as an 11-amino acid peptide derived from the preproprotein PATHOGENESIS-RELATED PROTEIN 1b (PR1b), a marker gene for the salicylic acid signaling pathway and systemic acquired resistance.…”

“…Despite the majority of reported plant peptides being derived from such nonfunctional precursors, different studies also point to the existence of peptides originating from a functional protein but with an activity differing from that of the precursor (Schmelz et al, 2006;Pearce et al, 2010a;Chen et al, 2014) (Figure 1). This phenomenon raises the question whether many other well-known protein-encoding genes could have a double function, both as parent protein and as derived peptide.…”