Abstract

BackgroundCell walls (CWs) are protein-rich polysaccharide matrices essential for plant growth and environmental acclimation. The CW constitutes the first physical barrier as well as a primary source of nutrients for microbes interacting with plants, such as the vascular pathogen Fusarium oxysporum (Fo). Fo colonizes roots, advancing through the plant primary CWs towards the vasculature, where it grows causing devastation in many crops. The pathogenicity of Fo and other vascular microbes relies on their capacity to reach and colonize the xylem. However, little is known about the root-microbe interaction before the pathogen reaches the vasculature and the role of the plant CW during this process.ResultsUsing the pathosystem Arabidopsis-Fo5176, we show dynamic transcriptional changes in both fungus and root during their interaction. One of the earliest plant responses to Fo5176 was the downregulation of primary CW synthesis genes. We observed enhanced resistance to Fo5176 in Arabidopsis mutants impaired in primary CW cellulose synthesis. We confirmed that Arabidopsis roots deposit lignin in response to Fo5176 infection, but we show that lignin-deficient mutants were as susceptible as wildtype plants to Fo5176. Genetic impairment of jasmonic acid biosynthesis and signaling did not alter Arabidopsis response to Fo5176, whereas impairment of ethylene signaling did increase vasculature colonization by Fo5176. Abolishing ethylene signaling attenuated the observed resistance while maintaining the dwarfism observed in primary CW cellulose-deficient mutants.ConclusionsOur study provides significant insights on the dynamic root-vascular pathogen interaction at the transcriptome level and the vital role of primary CW cellulose during defense response to these pathogens. These findings represent an essential resource for the generation of plant resistance to Fo that can be transferred to other vascular pathosystems.

Highlights

  • Cell walls (CWs) are protein-rich polysaccharide matrices essential for plant growth and environmental acclimation

  • By Illumina sequencing of 3’mRNA libraries, we obtained more than 234 billion reads from all samples, which were mapped to the Arabidopsis TAIR10 gene models [32] and the Fo5176 genome [10] (Additional file 1: Table S1)

  • Many of these genes clustered together in cluster 3 (Figure 2B, Additional file 3: Table S2). These results suggest that infected Arabidopsis roots undergo major transcriptional reprogramming leading to overall repression of growth followed by activation of stress and defense responses

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Summary

Introduction

Cell walls (CWs) are protein-rich polysaccharide matrices essential for plant growth and environmental acclimation. The CW constitutes the first physical barrier as well as a primary source of nutrients for microbes interacting with plants, such as the vascular pathogen Fusarium oxysporum (Fo). All living organisms must adapt to their environment to survive and reproduce in their habitats This is challenging for sessile organisms like plants, which rely on remarkable plasticity to adjust to different and simultaneous external cues. Plant CW alteration directly influences growth and stress response pathways. This is especially relevant during plant response to microbes who mainly live in the apoplast, like the root vascular pathogen Fusarium oxysporum (Fo)

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