A stage-dependent seed defense response to explain efficient seed transmission of Xanthomonas citri pv. fuscans to common bean.

ABSTRACT

Although seed represents an important means of plant pathogen dispersion, the seed-pathogen dialogue remains largely unexplored. A multiomic approach was performed at different seed developmental stages of common bean (Phaseolus vulgaris L.) during asymptomatic colonization by Xanthomonas citri pv. fuscans (Xcf), At the early seed developmental stages, we observed high transcriptional changes both in seeds with bacterial recognition and defense signal transduction genes, and in bacteria with up-regulation of the bacterial type 3 secretion system. This high transcriptional activity of defense genes in Xcf-colonized seeds during maturation refutes the widely diffused assumption considering seeds as passive carriers of microbes. At later seed maturation stages, few transcriptome changes indicated a less intense molecular dialogue between the host and the pathogen, but marked by changes in DNA methylation of plant defense genes, in response to Xcf colonization. We showed examples of pathogen-specific DNA methylations in colonized seeds acting as plant defense silencing to repress plant immune response during the germination process. Finally, we propose a novel plant-pathogen interaction model, specific to the seed tissues, highlighting the existence of distinct phases during seed-pathogen interaction with seeds being actively interacting with colonizing pathogens, then both belligerents switching to more passive mode at later stages.