Environmental adaptation of organisms relies on fast perception and response to external signals, which lead to developmental changes. Plant cell growth is strongly dependent on cell wall remodeling. However, little is known about cell wall‐related sensing of biotic stimuli and the downstream mechanisms that coordinate growth and defense responses. We generated genetically encoded pH sensors to determine absolute pH changes across the plasma membrane in response to biotic stress. A rapid apoplastic acidification by phosphorylation‐based proton pump activation in response to the fungus Fusarium oxysporum immediately reduced cellulose synthesis and cell growth and, furthermore, had a direct influence on the pathogenicity of the fungus. In addition, pH seems to influence cellulose structure. All these effects were dependent on the COMPANION OF CELLULOSE SYNTHASE proteins that are thus at the nexus of plant growth and defense. Hence, our discoveries show a remarkable connection between plant biomass production, immunity, and pH control, and advance our ability to investigate the plant growth‐defense balance.

Environmental adaptation of organisms relies on fast perception and response to external signals, which lead to developmental changes. Plant cell growth is strongly dependent on cell wall remodeling. However, little is known about cell wall-related sensing of biotic stimuli and the downstream mechanisms that coordinate growth and defense responses. We generated genetically encoded pH sensors to determine absolute pH changes across the plasma membrane in response to biotic stress. A rapid apoplastic acidification by phosphorylation-based proton pump activation was followed by an acidification of the cortical side of the plasma membrane in response to the fungus Fusarium oxysporum. The proton chemical gradient modulation immediately reduced cellulose synthesis and cell growth and, furthermore, had a direct influence on the pathogenicity of the fungus. All these effects were dependent on the COMPANION OF CELLULOSE SYNTHASE proteins that are thus at the nexus of plant growth and defense. Hence, our discoveries show a remarkable connection between plant biomass production, immunity, and pH control, and advance our ability to investigate the plant growth-defense balance. We are grateful to G. Sancho-Andrés, B. Pfister, and P. van Dam for technical support. We thank S. Persson for the cc1cc2 , cc1cc2 GFP-CC1 and cc1cc2 GFP-CC1ΔN120 lines and A. Molina, G. Bissoli and E. López-Solanilla for constructive discussions. Live cell imaging was performed with equipment maintained by

The apoplast is a continuous plant compartment that connects cells between tissues and organs and is one of the first sites of interaction between plants and microbes. The plant cell wall occupies most of the apoplast and is composed of polysaccharides and associated proteins and ions. This dynamic part of the cell constitutes an essential physical barrier and a source of nutrients for the microbe. At the same time, the plant cell wall serves important functions in the interkingdom detection, recognition, and response to other organisms. Thus, both plant and microbe modify the plant cell wall and its environment in versatile ways to benefit from the interaction. We discuss here crucial processes occurring at the plant cell wall during the contact and communication between microbe and plant. Finally, we argue that these local and dynamic changes need to be considered to fully understand plant-microbe interactions

Background 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). 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. Results Using 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. Conclusions Our 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.

Plant pathogens cause widespread yield losses in agriculture. Understanding the drivers of plantpathogen interactions requires decoding the molecular dialog leading to either resistance or disease.However, progress in deciphering pathogenicity genes has been severely hampered by suitable model systems and incomplete fungal genome assemblies. Here, we report a significant improvement of the assembly and annotation of the genome of the Fusarium oxysporum (Fo) strain Fo5176. Fo comprises a large number of serious plant pathogens on dozens of plant species with largely unresolved pathogenicity factors. The strain Fo5176 infects Arabidopsis thaliana and, hence, constitutes a highly promising model system. We use high-coverage Pacific Biosciences Sequel long-read sequencing to assemble the genome into 19 chromosome-scale contigs with a N50 of 5 Mb and a 99.1% complete BUSCO score. Phylogenomic analyses based on single-copy orthologs clearly place the Fo5176 strain in the Fo f sp. conglutinans clade as expected. We generated RNAseq data from culture medium and plant infections to train gene predictions and identified 19'069 genes including ten effector genes known from other Fo clades. We show that Fo5176 is able to infect cabbage and Brussel sprouts of the Brassica oleracea expanding the usefulness of the Fo5176 model pathosystem. Finally, we performed large-scale comparative genomics analyses comparing the Fo5176 to 103 additional Fo genomes to define core and accessory genomic regions. In conjunction with the molecular tool sets available for A. thaliana, the Fo5176 genome and annotation provides a crucial step towards the establishment of a highly promising pathosystem.