6533b856fe1ef96bd12b2291

RESEARCH PRODUCT

Investigation of the physiological impact and the mode of action of the pyoverdine from Pseudomonas fluorescens on Arabidopsis thaliana : links with iron homeostasis, growth and defense

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Siderophores are strong iron chelators produced by bacteria under iron deficiency conditions. In the present work, we studied the impact of the siderophore pyoverdine, produced by the plant growth promoting rhizobacteria Pseudomonas fluorescens C7R12, on plant physiology from phenotypic to molecular effects with a specific focus on plant growth, immune response and iron homeostasis. Based on our analysis of the mode of action of the non-protein amino acid β-aminobutyric acid (BABA), a priming inducer in plants, we studied more specifically the functional link between iron homeostasis and plant immunity. Under iron deficiency, P. fluorescens excretes the iron free form of pyoverdine (apo-pyo) in the soil. Once chelated with iron (ferri-pyo), the complex is internalized by the bacteria. We demonstrated that Arabidopsis thaliana plants treated by apo-pyo in a medium containing or not iron (Fe 25 or Fe 0) also internalize pyoverdine. Moreover, we observed that under iron deficiency, pyoverdine treated plants did not display the growth reduction induced by iron deficiency. In accordance with this phenotype, a microarray analysis revealed that the expression of genes related to growth and development was induced, as well as genes related to iron uptake and transport in planta. In contrast, the down regulation of the expression of genes related to defense was observed. Correspondingly, we demonstrated that the growth improvement induced by apo-pyo under iron deficiency depends on the expression of IRT1 and FRO2, two major genes involved in iron uptake mechanisms. Of interest, the resistance to Botrytis cinerea conferred by iron deficiency was lost following apo-pyo treatment. The overexpression of the HBI1 transcription factor, known to be involved in the growth-defense tradeoff, can be linked to the above observations. These apo-pyo effects were not observed after treatment of plants under sufficient iron conditions, indicating that in A. thaliana apo-pyo effects are dependent on the plant iron status. In the same time, the analysis of the mode of action of BABA that potentiates plant defense responses demonstrated that BABA is a powerful iron chelator. BABA treatment in A. thaliana triggered a transient iron deficiency response. Based on this assessment, we assume that iron deficiency response and priming of defense may be connected. In accordance with this hypothesis, we showed that plants cultivated under iron deficiency and BABA treated plants both displayed resistance to B. cinerea and produced secondary metabolites associated to defense. Hence, the BABA priming effects on plant defense may be due to the induction of transient iron deficiency. To conclude, this work draws first explications on pyoverdine effects on plant physiology and presents an original mode of action contributing to the priming effects of BABA. In a larger view, this work supports the recent concept of the existence of a cross-regulation between growth, immunity and iron homeostasis in plants.