Neofusicoccum parvum Colonization of the Grapevine Woody Stem Triggers Asynchronous Host Responses at the Site of Infection and in the Leaves.

Mélanie Massonnet,Rosa Figueroa-Balderas,Dario Cantu,Kendra Baumgartner,Daniel P Lawrence,Erin R A Galarneau,Christopher M Wallis,Shiho Miki,Qiang Sun

doi:10.3389/fpls.2017.01117

Abstract

Grapevine trunk diseases cause important economic losses in vineyards worldwide. Neofusicoccum parvum, one of the most aggressive causal agents of the trunk disease Botryosphaeria dieback, colonizes cells and tissues of the grapevine wood, leading to the formation of an internal canker. Symptoms then extend to distal shoots, with wilting of leaves and bud mortality. Our aim was to characterize the transcriptional dynamics of grapevine genes in the woody stem and in the leaves during Neofusicoccum parvum colonization. Genome-wide transcriptional profiling at seven distinct time points (0, 3, and 24 hours; 2, 6, 8, and 12 weeks) showed that both stems and leaves undergo extensive transcriptomic reprogramming in response to infection of the stem. While most intense transcriptional responses were detected in the stems at 24 hours, strong responses were not detected in the leaves until the next sampling point at 2 weeks post-inoculation. Network co-expression analysis identified modules of co-expressed genes common to both organs and showed most of these genes were asynchronously modulated. The temporal shift between stem vs. leaf responses affected transcriptional modulation of genes involved in both signal perception and transduction, as well as downstream biological processes, including oxidative stress, cell wall rearrangement and cell death. Promoter analysis of the genes asynchronously modulated in stem and leaves during N. parvum colonization suggests that the temporal shift of transcriptional reprogramming between the two organs might be due to asynchronous co-regulation by common transcriptional regulators. Topology analysis of stem and leaf co-expression networks pointed to specific transcription factor-encoding genes, including WRKY and MYB, which may be associated with the observed transcriptional responses in the two organs.

Highlights

Grapevine trunk diseases cause important economic losses in vineyards worldwide (Hofstetter et al, 2012; Fontaine et al, 2016; Kaplan et al, 2016)
N. parvum was recovered from the inoculation site (0 cm) of all stems at all timepoints for the Inoculated-Wounded plants (IW) plants, while it was recovered beyond the inoculation site (1 cm above and below) starting at 2 wpi (Data S1 Table A)
The apparent decline of mean lesion size observed at 12 wpi is likely due to mortality of IW plants, which were removed from the study, between 8 and 12 wpi

Summary

Introduction

Grapevine trunk diseases cause important economic losses in vineyards worldwide (Hofstetter et al, 2012; Fontaine et al, 2016; Kaplan et al, 2016). The infection causes foliar chlorosis and necrosis, but more often what appears in the vineyard is “dieback,” the death of shoots and buds distal to the wood canker (Larignon et al, 2001; Úrbez-Torres, 2011). N. parvum was shown to produce a variety of phytotoxins in vitro (Andolfi et al, 2011; Bénard-Gellon et al, 2015) These compounds belong to different chemical classes, including but not limited to dihydrotoluquinones, epoxylactones, dihydroisocoumarins, hydroxybenzoic acids, and fatty esters (Evidente et al, 2010; Abou-Mansour et al, 2015; Uranga et al, 2016). The dihydrotoluquinones terremutin and mullein were detected in wood from grapevines with Botryosphaeria dieback symptoms and were shown to cause severe necrosis when applied to leaf disks (Abou-Mansour et al, 2015)

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Conclusion