Bacterial outer membrane vesicles induce a transcriptional shift in arabidopsis towards immune system activation leading to suppression of pathogen growth in planta

Abstract

Gram-negative bacteria form spherical blebs on their cell periphery, which later dissociate from the bacterial cell wall to form extracellular vesicles. These nano scale structures, known as outer membrane vesicles (OMVs), have been shown to promote infection and disease and can induce typical immune outputs in both mammal and plant hosts. To better understand the broad transcriptional change plants undergo following exposure to OMVs, we treated Arabidopsis thaliana (Arabidopsis) seedlings with OMVs purified from the Gram-negative plant pathogenic bacterium Xanthomonas campestris pv. campestris and performed RNA-seq analysis on OMVand mock-treated plants at 2, 6 and 24 h post challenge. The most pronounced transcriptional shift occurred at the first two time points tested, as reflected by the number of differentially expressed genes and the average fold change. OMVs induce a major transcriptional shift towards immune system activation, upregulating a multitude of immune-related pathways including a variety of immune receptors. Comparing the response of Arabidopsis to OMVs and to purified elicitors, revealed that OMVs induce a similar suite of genes and pathways as single elicitors, however, pathways activated by OMVs and not by other elicitors were detected. Pretreating Arabidopsis plants with OMVs and subsequently infecting with a bacterial pathogen led to a significant reduction in pathogen growth. Mutations in the plant elongation factor receptor (EFR), flagellin receptor (FLS2), or the brassinosteroid-insensitive 1associated kinase (BAK1) co-receptor, did not significantly affect the immune priming effect of OMVs. All together these results show that OMVs induce a broad transcriptional shift in Arabidopsis leading to upregulation of multiple immune pathways, and that this transcriptional change may facilitate resistance to bacterial infection.

Hydrogel-exosome system in tissue engineering: A promising therapeutic strategy

“…Outer membrane vesicles (OMVs) purified from Xanthomonas campestris pv , a Gram-negative plant pathogenic bacterium, could induce significant transcriptional changes in Arabidopsis. This activation has involved the immune system and upregulation of related pathways including multiple immune receptors [ 60 ]. Compared to mammalian exosomes, microbial-derived exosomes offer greater convenience for engineering modifications.…”

Insights into Bacterial Extracellular Vesicle Biogenesis, Functions, and Implications in Plant–Microbe Interactions

“…Campestris ( Xcc ), and Xoo and virulence factors purified from these EVs have been shown to trigger immune responses in plants, including callose deposition, the alkalinization of the medium, increased transcription of pattern recognition receptors, the activation of Mitogen-Activated Protein Kinase (MAPK), and the release of reactive oxygen species [ 21 , 22 ]. Alterations in crucial receptors like the plant elongation factor receptor (EFR), flagellin receptor (FLS2), or brassinosteroid-insensitive 1–associated kinase (BAK1) co-receptor had minimal effect on the immune priming ability of Xcc EVs [ 86 ]. These findings suggest that Xcc EVs elicit a widespread transcriptional shift in Arabidopsis , stimulating the activation of multiple immune pathways.…”

“…Xcc EVs were shown to induce the expression of multiple WRKY transcription factors. This transcriptional modulation holds promise for enhancing the plant’s defense mechanisms against bacterial infections [ 86 ]. Tran et al [ 87 ] elucidated that the structured lipid composition of EVs enables direct interaction and integration of Xcc EVs into the Arabidopsis plasma membrane (PM), thereby enhancing its lipid organization.…”

Extracellular Vesicles and Bacteriophages: New Directions in Environmental Biocolloid Research

“…3 Other studies demonstrated a similar phenomena for Xanthomonas campestris and X. oryzae OMVs, which inhibited the growth of Arabidopsis thaliana. 116,117 Other nonplant associated bacteria P. aeruginosa, S. aureus, and enterotoxigenic E. coli also induced plant immune responses, albeit to different extents. 3 OMVs and plants more thoroughly elsewhere.…”

“…For instance, Samuel et al and An et al discuss fungal–plant interactions: how sometimes vesicular structures aid in the dissemination of fungal pathogens but also how similar structures can induce immune responses to combat the growth of harmful fungi on plants. , More recently, McMillan et al demonstrated that OMVs from P. syringae and P. fluorescens can elicit protective plant immune responses . Other studies demonstrated a similar phenomena for Xanthomonas campestris and X. oryzae OMVs, which inhibited the growth of Arabidopsis thaliana . , Other nonplant associated bacteria P. aeruginosa, S. aureus , and enterotoxigenic E. coli also induced plant immune responses, albeit to different extents . McMillan et al and Bahar et al further suggest that OMV-associated protein may not be the primary category of molecules that stimulates a response preventing plant infection.…”