The timing of bacterial mesophyll infection shapes the leaf chemical landscape.

Autor: Roman-Reyna V; Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA.; Infectious Diseases Institute, The Ohio State University, Columbus, Ohio, USA., Heiden N; Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA.; Infectious Diseases Institute, The Ohio State University, Columbus, Ohio, USA., Butchacas J; Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA.; Infectious Diseases Institute, The Ohio State University, Columbus, Ohio, USA., Toth H; Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA.; Infectious Diseases Institute, The Ohio State University, Columbus, Ohio, USA., Cooperstone JL; Department of Horticulture and Crop Science, The Ohio State University, Columbus, Ohio, USA.; Department of Food Science and Technology, The Ohio State University, Columbus, Ohio, USA., Jacobs JM; Department of Plant Pathology, The Ohio State University, Columbus, Ohio, USA.; Infectious Diseases Institute, The Ohio State University, Columbus, Ohio, USA.
Jazyk: angličtina
Zdroj: Microbiology spectrum [Microbiol Spectr] 2024 Apr 02; Vol. 12 (4), pp. e0413823. Date of Electronic Publication: 2024 Mar 01.
DOI: 10.1128/spectrum.04138-23
Abstrakt: Chemistry in eukaryotic intercellular spaces is shaped by both hosts and symbiotic microorganisms such as bacteria. Pathogenic microorganisms like barley-associated Xanthomonas translucens (Xt) swiftly overtake the inner leaf tissue becoming the dominant microbial community member during disease development. The dynamic metabolic changes due to Xt pathogenesis in the mesophyll spaces remain unknown. Genomic group I of Xt consists of two barley-infecting lineages: pathovar translucens (Xtt) and pathovar undulosa (Xtu). Xtu and Xtt, although genomically distinct, cause similar water-soaked lesions. To define the metabolic signals associated with inner leaf colonization, we used untargeted metabolomics to characterize Xtu and Xtt metabolism signatures associated with mesophyll growth. We found that mesophyll apoplast fluid from infected tissue yielded a distinct metabolic profile and shift from catabolic to anabolic processes over time compared to water-infiltrated control. The pathways with the most differentially expressed metabolites by time were glycolysis, tricarboxylic acid cycle, sucrose metabolism, pentose interconversion, amino acids, galactose, and purine metabolism. Hierarchical clustering and principal component analysis showed that metabolic changes were more affected by the time point rather than the individual colonization of the inner leaves by Xtt compared to Xtu. Overall, in this study, we identified metabolic pathways that explain carbon and nitrogen usage during host-bacterial interactions over time for mesophyll tissue colonization. This foundational research provides initial insights into shared metabolic strategies of inner leaf colonization niche occupation by related but phylogenetically distinct phyllosphere bacteria.
Importance: The phyllosphere is a habitat for microorganisms including pathogenic bacteria. Metabolic shifts in the inner leaf spaces for most plant-microbe interactions are unknown, especially for Xanthomonas species in understudied plants like barley ( Hordeum vulgare ). Xanthomonas translucens pv. translucens (Xtt) and Xanthomonas translucens pv. undulosa (Xtu) are phylogenomically distinct, but both colonize barley leaves for pathogenesis. In this study, we used untargeted metabolomics to shed light on Xtu and Xtt metabolic signatures. Our findings revealed a dynamic metabolic landscape that changes over time, rather than exhibiting a pattern associated with individual pathovars. These results provide initial insights into the metabolic mechanisms of X. translucens inner leaf pathogenesis.
Competing Interests: The authors declare no conflict of interest.
Databáze: MEDLINE