Bacterial Outer Membrane Vesicles Induce Plant Immune Responses

Abstract

Gram-negative bacteria continuously pinch off portions of their outer membrane, releasing membrane vesicles. These outer membrane vesicles (OMVs) are involved in multiple processes including cell-to-cell communication, biofilm formation, stress tolerance, horizontal gene transfer, and virulence. OMVs are also known modulators of the mammalian immune response. Despite the well-documented role of OMVs in mammalian-bacterial communication, their interaction with plants is not well studied. To examine whether OMVs of plant pathogens modulate the plant immune response, we purified OMVs from four different plant pathogens and used them to treat Arabidopsis thaliana. OMVs rapidly induced a reactive oxygen species burst, medium alkalinization, and defense gene expression in A. thaliana leaf discs, cell cultures, and seedlings, respectively. Western blot analysis revealed that EF-Tu is present in OMVs and that it serves as an elicitor of the plant immune response in this form. Our results further show that the immune coreceptors BAK1 and SOBIR1 mediate OMV perception and response. Taken together, our results demonstrate that plants can detect and respond to OMV-associated molecules by activation of their immune system, revealing a new facet of plant-bacterial interactions.

Spheres of Hope, Packets of Doom: the Good and Bad of Outer Membrane Vesicles in Interspecies and Ecological Dynamics

“…On evolutionary time scales, public goods provided by OMVs may select for cooperative behavior, driving the establishment of mutualisms. Finally, we note that the preponderance of research has examined OMVs in the context of animal symbioses; to date, only a few studies have focused on OMV-plant interactions (23,(99)(100)(101)(102)(103). Extending the role of OMVs in the biology of other multicellular lineages is a budding area for future investigation.…”

Bacterial outer membrane vesicles at the plant–pathogen interface

“…The perception of OMVs in mammalian systems is facilitated by cell surface and cytosolic receptor recognition of OMV MAMPs and was recently reviewed [13]. Plants have only recently been shown to recognize and respond to OMVs purified from plant pathogens by activating typical innate immune responses [14]. MAMP diversity in OMVs is large and ranges from integral elements like LPS and PG to variable proteinaceous cargo such as Elongation Factor-Tu (EF-Tu) and flagellin, which have been found to be associated with purified OMVs [3,4,10,13].…”

“…Functions related to bacterial cell–cell interactions, such as regulation of biofilm, horizontal gene transfer, removal of damaged molecules, and so on, have been demonstrated in several bacterial species [2][3]. OMVs have been shown to activate the plant immune system [14]. A close-up illustration of an OMV (upper right) shows it contains various known microbe-associated molecular patterns (MAMPs) such as lipopolysaccharides (LPS), peptidoglycans (PG), and proteinaceous MAMPs that can potentially interact with pattern recognition receptors (PRRs) and induce MAMP-triggered immunity (MTI).…”

“…This observation, together with biochemical evidence for the association of known MAMPs with OMVs, may suggest that OMVs can activate multiple PRRs, reflecting the redundancy of immune receptor signaling pathways potentially activated by OMVs [14]. Furthermore, an Arabidopsis mutant line producing a nonfunctional version of the co-receptor brassinosteroid-insensitive 1–associated kinase (BAK1), which is known to be a signalling hub for multiple PRRs, showed a significantly reduced response to OMVs, strengthening the hypothesis that multiple PRRs are responsive to and activated by OMVs [14]. A similar response, albeit slightly less significant, was seen with an Arabidopsis knockout line of the co-receptor Suppressor of BIR1-1 (SOBIR1) [14].…”

“…Furthermore, an Arabidopsis mutant line producing a nonfunctional version of the co-receptor brassinosteroid-insensitive 1–associated kinase (BAK1), which is known to be a signalling hub for multiple PRRs, showed a significantly reduced response to OMVs, strengthening the hypothesis that multiple PRRs are responsive to and activated by OMVs [14]. A similar response, albeit slightly less significant, was seen with an Arabidopsis knockout line of the co-receptor Suppressor of BIR1-1 (SOBIR1) [14]. Intriguingly, EF-Tu was found to be associated with OMVs and to be recognized by its respective plant immune receptor [14].…”