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A Hormone and Proteome Approach to Picturing the Initial Metabolic Events During Plasmodiophora brassicae Infection on Arabidopsis

¹Laboratory of Plant Physiology and Plant Biochemistry, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium; ²CEPROMA, Center for Proteome Analysis and Mass Spectrometry, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium; ³Unit Plant Hormone Signaling and Bio-imaging, Department of Molecular Genetics, University of Ghent, K.L. Ledeganckstraat 35, B-9000 Ghent, Belgium; ⁴VIB, Department of Plant Systems Biology, University of Ghent, Technologiepark 927, B-9052 Ghent, Belgium

We report on the early response of Arabidopsis thaliana to the obligate biotrophic pathogen Plasmodiophora brassicae at the hormone and proteome level. Using a CYCB1;1::GUS construct, the re-initiation of infection-related cell division is shown from 4 days after inoculation on. Sensitivity to cytokinins and auxins as well as the endogenous hormone levels are evaluated. Both an enhanced cytokinin gene response and an accumulation of isopentenyl adenine and adenosine precede this re-initiation of cell division, whereas an enhanced auxin gene response is observed from 6 days after inoculation on. The alh1 mutant, impaired in the cross talk between ethylene and auxins, is resistant to P. brassicae. A differential protein analysis of infected versus noninfected roots and hypocotyls was performed using two-dimensional gel electrophoresis and quantitative image analysis, coupled to matrix-assisted laser desorption ionization time of flight-time of flight mass spectrometry-based protein identification. Of the visualized proteins, 12% show altered abundance compared with the nonin-fected plants, including proteins involved in metabolism, cell defense, cell differentiation, and detoxification. Combining the hormone and proteome data, we postulate that, at the very first stages of Plasmodiophora infection, plasmodial-produced cytokinins trigger a local re-initiation of cell division in the root cortex. Consequently, a de novo meristematic area is established that acts as a sink for host-derived indole-3-acetic acid, carbohydrates, nitrogen, and energy to maintain the pathogen and to trigger gall development.