Secretomic Insights into the Pathophysiology of Venturia inaequalis: The Causative Agent of Scab, a Devastating Apple Tree Disease

Abstract

Apple scab, caused by Venturia inaequalis, is one of the world's most commercially significant apple diseases. The fungi have a catastrophic impact on apples, causing considerable losses in fruit quality and productivity in many apple-growing locations despite numerous control agents. Fungi secrete various effectors and other virulence-associated proteins that suppress or alter the host's immune system, and several such proteins were discovered in this work. Using state-of-the-art bioinformatics techniques, we examined the V. inaequalis reference genome (EU-B04), resulting in the identification of 647 secreted proteins, of which 328 were classified as small secreted proteins (SSPs), with 76.52% of SSPs identified as anticipated effector proteins. The more prevalent CAZyme proteins were the enzymes engaged in plant cell wall disintegration (targeting pectin and xylanase), adhesion and penetration (Cutinases/acetyl xylan esterase), and reactive oxygen species formation (multicopper oxidases). Furthermore, members of the S9 prolyl oligopeptidase family were identified as the most abundant host defense peptidases. Several known effector proteins were discovered to be expressed during the V. inaequalis infection process on apple leaves. The present study provides valuable data that can be used to develop new strategies for controlling apple scab.

Keywords: Venturia inaequalis; genome annotation; secreted proteins; transposable elements; virulence.

Figure 1

Distribution of transposable elements in the V. inaequalis genome. The repeats of the analyzed genomes are shown alongside (from the innermost ring outwards). Pie 1–5 represent LTR elements, DNA transposons, Unclassified, Small RNA and Satellites, respectively.

Figure 2

An in silico workflow used to dissect the secretome of V. inaequalis.

Figure 3

Relative abundance of CAZymes and peptidases of V. inaquealis. Distribution of the CAZyme family in the (A) genome and (B) secretome of V. inaquealis. (C) Frequencies of different classes of CAZymes in the V. inaquealis secretome. The bars indicate the number of CAZymes (D) Prevalence of the peptidase families in the V. inaequalis genome.

Figure 4

Variation in protein length across the secretome, small secreted proteins (SSPs), and effectome of V. inaequalis.

Figure 5

Gene expression profiles (logFC) of differentially expressed effector candidates from V. inaequalis during apple leaf invasion.