The Alteration of Plant Morphology by Small Peptides Released from the Proteolytic Processing of the Bacterial Peptide TENGU  

Abstract

Phytoplasmas are insect-borne plant pathogenic bacteria that alter host morphology. TENGU, a small peptide of 38 residues, is a virulence factor secreted by phytoplasmas that induces dwarfism and witches' broom in the host plant. In this study, we demonstrate that plants process TENGU in order to generate small functional peptides. First, virus vector-mediated transient expression demonstrated that the amino-terminal 11 amino acids of TENGU are capable of causing symptom development in Nicotiana benthamiana plants. The deletion of the 11th residue significantly diminished the symptom-inducing activity of TENGU, suggesting that these 11 amino acids constitute a functional domain. Second, we found that TENGU undergoes proteolytic processing in vitro, generating peptides of 19 and 21 residues including the functional domain. Third, we observed similar processing of TENGU in planta, and an alanine substitution mutant of TENGU, for which processing was compromised, showed reduced symptom induction activity. All TENGU homologs from several phytoplasma strains possessed similar symptom induction activity and went through processing, which suggests that the processing of TENGU might be related to its function.

Decreasing Global Transcript Levels over Time Suggest that Phytoplasma Cells Enter Stationary Phase during Plant and Insect Colonization

“…Although the pathogenicity mechanisms are still largely unclear, phytoplasmas influence plant metabolism both directly, through a set of membrane proteins acting as molecular carriers (6), and indirectly, through secretion of effector proteins (8,9). In vitro studies have also shown that phytoplasma immunodominant membrane proteins interact with vector proteins (10, 11) and plant proteins (12) and are subjected to strong positive selection (13-15).…”

“…Consistent with this lifestyle, phytoplasmas have very small, A/T-rich genomes, ranging from 530 to 1,350 kb in size (5), that lack essential metabolic pathways, such as ATP synthesis. This genome condensation reflects the phytoplasma adaptation to nutrient-rich environments such as the plant phloem (6) and helps explain why these pathogens are not cultivable under axenic conditions (7).Although the pathogenicity mechanisms are still largely unclear, phytoplasmas influence plant metabolism both directly, through a set of membrane proteins acting as molecular carriers (6), and indirectly, through secretion of effector proteins (8,9). In vitro studies have also shown that phytoplasma immunodominant membrane proteins interact with vector proteins (10, 11) and plant proteins (12) and are subjected to strong positive selection (13-15).…”

Exploring the phytoplasmas, plant pathogenic bacteria

“…4) (Hoshi et al 2009). More recently, TENGU was found to be processed in planta into a small functional peptide, similar to the proteolytic processing of plant endogenous peptide signals (Sugawara et al 2013). As for phyllody symptoms, a previous study has shown the involvement of the floral homeotic MADS-domain transcription factors of the floral ABCE model (floral quartet model) .…”

“…TENGU induces witches' broom and dwarfism, which are typical of phytoplasma infection in Nicotiana benthamiana and Arabidopsis thaliana. TENGU homologs from several phytoplasma strains induce similar symptoms (Sugawara et al 2013). Microarray analysis of TENGU-transgenic Arabidopsis plants revealed that TENGU inhibits auxinrelated pathways, thereby affecting plant development (Fig.…”

Post-translational cleavage and self-interaction of the phytoplasma effector SAP11

“…10 The protein was found to be processed into small functional peptides, including an 11-amino acid sequence at the N-terminus that is necessary to induce branch proliferation. Previously, SAP11 was found to bind to and destabilize CIN-TCPs, which inhibits LOX2 expression and reduces JA biosynthesis.…”