Regulation of Cell Wall-Bound Invertase in Pepper Leaves by Xanthomonas campestris pv. vesicatoria Type Three Effectors

Abstract

Xanthomonas campestris pv. vesicatoria (Xcv) possess a type 3 secretion system (T3SS) to deliver effector proteins into its Solanaceous host plants. These proteins are involved in suppression of plant defense and in reprogramming of plant metabolism to favour bacterial propagation. There is increasing evidence that hexoses contribute to defense responses. They act as substrates for metabolic processes and as metabolic semaphores to regulate gene expression. Especially an increase in the apoplastic hexose-to-sucrose ratio has been suggested to strengthen plant defense. This shift is brought about by the activity of cell wall-bound invertase (cw-Inv). We examined the possibility that Xcv may employ type 3 effector (T3E) proteins to suppress cw-Inv activity during infection. Indeed, pepper leaves infected with a T3SS-deficient Xcv strain showed a higher level of cw-Inv mRNA and enzyme activity relative to Xcv wild type infected leaves. Higher cw-Inv activity was paralleled by an increase in hexoses and mRNA abundance for the pathogenesis-related gene PRQ. These results suggest that Xcv suppresses cw-Inv activity in a T3SS-dependent manner, most likely to prevent sugar-mediated defense signals. To identify Xcv T3Es that regulate cw-Inv activity, a screen was performed with eighteen Xcv strains, each deficient in an individual T3E. Seven Xcv T3E deletion strains caused a significant change in cw-Inv activity compared to Xcv wild type. Among them, Xcv lacking the xopB gene (Xcv ΔxopB) caused the most prominent increase in cw-Inv activity. Deletion of xopB increased the mRNA abundance of PRQ in Xcv ΔxopB-infected pepper leaves, but not of Pti5 and Acre31, two PAMP-triggered immunity markers. Inducible expression of XopB in transgenic tobacco inhibited Xcv-mediated induction of cw-Inv activity observed in wild type plants and resulted in severe developmental phenotypes. Together, these data suggest that XopB interferes with cw-Inv activity in planta to suppress sugar-enhanced defense responses during Xcv infection.

Functional Analysis of Plant Defense Suppression and Activation by the Xanthomonas Core Type III Effector XopX

“…In order to take advantage of the genome sequence and annotation of Xe strain 85-10 during our study of XopX (Thieme et al, 2005), we used an Xe 85-10 strain with a genomic deletion in the xopX coding sequence (Δ xopX ) (Sonnewald et al, 2012). Consistent with prior work, Δ xopX grew less and caused reduced leaf chlorosis and necrotic spots during infection of tomato culivar (cv.)…”

Xanthomonas perforans Colonization Influences Salmonella enterica in the Tomato Phyllosphere

“…If the former is true, then S. enterica may utilize limited nutrients liberated by X. perforans in a compatible interaction. During the infection process, phytopathogens manipulate plant metabolism to benefit their ability to colonize, both by suppressing plant defenses (compatible interaction) and by reallocating photoassimilates to supply the pathogen with nutrients (29). The compatible interaction increases apoplastic carbohydrate levels in infected leaves by converting the leaves from sources to sinks (30).…”

Plant-Mediated Systemic Interactions Between Pathogens, Parasitic Nematodes, and Herbivores Above- and Belowground

“…Moreover, these sugars function as priming molecules leading to MTI (sweet priming) (113), making it sometimes difficult to distinguish whether systemic within-or crosscompartment effects of phytophages are mediated by modulation of defense signaling pathways or by modulation of source-sink relationships (130). Some pathogens have also evolved effectors that suppress CW-Inv activity to prevent sugar-mediated defense signaling (148). Cell wall invertases also play an important role in interactions with nematodes (21) and insect herbivores.…”