A novel “ceasefire” model to explain efficient seed transmission ofXanthomonas citripv.fuscansto common bean

Abstract

SummaryAlthough seed represents an important means of plant pathogen dispersion, the seed-pathogen dialogue remains largely unexplored.A multi-omic approach (i.e.dual RNAseq, plant small RNAs and methylome) was performed at different seed developmental stages of common bean (Phaseolus vulgarisL.) during asymptomatic colonization byXanthomonas citripv.fuscans(Xcf).In this condition,Xcfdid not produce disease symptoms, neither affect seed development. Although, an intense molecular dialogue, via important transcriptional changes, was observed at the early seed developmental stages with down-regulation of plant defense signal transduction, via action of plant miR, and upregulation of the bacterial Type 3 Secretion System. At later seed maturation stages, molecular dialogue between host and pathogen was reduced to few transcriptome changes, but marked by changes in DNA methylation of plant defense and germination genes, in response toXcfcolonization, potentially acting as defense priming to prepare the host for the post-germination battle. This distinct response of infected seeds during maturation, with a more active role at early stages refutes the widely diffused assumption considering seeds as passive carriers of microbes.Finally, our data support a novel plant-pathogen interaction model, specific to the seed tissues, which differs from others by the existence of distinct phases during seed-pathogen interaction with seeds first actively interacting with colonizing pathogens, then both belligerents switch to more passive mode at later stages. We contextualized this observed scenario in a novel hypothetical model that we called “ceasefire”, where both the pathogen and the host benefit from temporarily laying down their weapons until the moment of germination.