Pseudomonas fluorescens Induces Strain-Dependent and Strain-Independent Host Plant Responses in Defense Networks, Primary Metabolism, Photosynthesis, and Fitness

• Published in: Molecular plant-microbe interactions Vol. 25; no. 6; pp. 765 - 778
• Main Authors: WESTON, David J, PELLETIER, Dale A, KARVE, Abhijit A, CHEN, Jin-Gui, XIAOHAN YANG, DOKTYCZ, Mitchel J, TUSKAN, Gerald A, MORRELL-FALVEY, Jennifer L, TSCHAPLINSKI, Timothy J, JAWDY, Sara S, LU, Tse-Yuan, ALLEN, Sara M, MELTON, Sarah J, MARTIN, Madhavi Z, SCHADT, Christopher W
• Format: Journal Article
• Language: English
• Published: St. Paul, MN APS Press 01-06-2012; The American Phytopathological Society
• Subjects: Abundance; Amino acids; Arabidopsis - classification; Arabidopsis - metabolism; Arabidopsis - microbiology; Arabidopsis thaliana; Auxins; Biological and medical sciences; Calcium Signaling; Calcium signalling; Carbohydrates; Carbon; Colonization; Data processing; Fitness; Fundamental and applied biological sciences. Psychology; Gene Expression Profiling; Gene Expression Regulation, Fungal - physiology; Gene Expression Regulation, Plant - physiology; Hormones; Host plants; Host-Pathogen Interactions; Light effects; Metabolites; Nutrients; Pathogens; Phenylalanine; Photosynthesis; Photosynthesis - physiology; Phylogeny; Phytopathology. Animal pests. Plant and forest protection; Plant Diseases - immunology; Plant Roots - metabolism; Plant Roots - microbiology; Protein turnover; Pseudomonas fluorescens; Pseudomonas fluorescens - genetics; Pseudomonas fluorescens - physiology; RNA; RNA, Fungal - genetics; RNA, Fungal - metabolism; Roots; Shoots; Signal transduction; Sugar; Transcription; Tryptophan; Pseudomonadales; Plant; Bacteria; Pseudomonadaceae; Pseudomonas fluorescens; Metabolism; Photosynthesis; Fitness; Strain
• ISSN: 0894-0282; 1943-7706
• DOI: 10.1094/MPMI-09-11-0253

Colonization of plants by nonpathogenic Pseudomonas fluorescens strains can confer enhanced defense capacity against a broad spectrum of pathogens. Few studies, however, have linked defense pathway regulation to primary metabolism and physiology. In this study, physiological data, metabolites, and transcript profiles are integrated to elucidate how molecular networks initiated at the root-microbe interface influence shoot metabolism and whole-plant performance. Experiments with Arabidopsis thaliana were performed using the newly identified P. fluorescens GM30 or P. fluorescens Pf-5 strains. Co-expression networks indicated that Pf-5 and GM30 induced a subnetwork specific to roots enriched for genes participating in RNA regulation, protein degradation, and hormonal metabolism. In contrast, only GM30 induced a subnetwork enriched for calcium signaling, sugar and nutrient signaling, and auxin metabolism, suggesting strain dependence in network architecture. In addition, one subnetwork present in shoots was enriched for genes in secondary metabolism, photosynthetic light reactions, and hormone metabolism. Metabolite analysis indicated that this network initiated changes in carbohydrate and amino acid metabolism. Consistent with this, we observed strain-specific responses in tryptophan and phenylalanine abundance. Both strains reduced host plant carbon gain and fitness, yet provided a clear fitness benefit when plants were challenged with the pathogen P. syringae DC3000.