Seed-mediated vertical transmission of Pantoea core endophytes

Abstract

Plant-associated microorganisms, particularly endophytes, are essential for plant health and development. Endophytic microbiota is intimately associated with host plants colonizing various tissues, including seeds. Seed endophytes are particularly noteworthy because of their potential for vertical transmission. This pathway may play a role in the long-term establishment and evolution of stable bacteria-host interactions across plant generations. Hundreds of seed-bacteria associations have been recently uncovered; however, most seem to be transient or unspecific. Although it is known that microorganisms can be transmitted from plant tissues to seeds and from seeds to seedlings, the experimental confirmation of bacterial transfer through successive plant generations by inoculation remains unreported. In this study, we identified Pantoea as the unique core endophytic bacteria inhabiting the endosperms of 24 wheat seed samples originally harvested in different worldwide locations. Pantoea is the genus with the highest relative average abundance in wheat seeds (61%) and in germinated roots and shoots grown under gnotobiotic conditions (45-38%). In the field, it was the only genus dwelling roots, shoots, spikes, and seeds of four different wheat varieties tested and its abundance progressively increased across these tissues. This genuine pattern of vertical enrichment, which was not found in other common wheat-associated taxa, suggests a role in the transfer of these endophytic bacteria through the seeds. To confirm intergenerational transmission, parental plants were inoculated with labelled Pantoea isolates, which specifically colonized the next generations of Poaceae plants, experimentally demonstrating bacterial vertical inheritance to the offspring generations and suggesting transmission specificity.