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ABSTRACT Type VI secretion system (T6SS) is a versatile, contact-dependent contractile nano-weapon in Gram-negative bacteria that fires proteinaceous effector molecules directly into prokaryotic and eukaryotic cells aiding in manipulation of the host and killing of competitors in complex niches. In plant pathogenic xanthomonads, T6SS has been demonstrated to play these diverse roles in individual pathosystems. However, the molecular network underlying the regulation of T6SS is still elusive inXanthomonasspp. To bridge this knowledge gap, we conducted anin vitrotranscriptome screen using plant apoplast mimicking minimal medium, XVM2 medium, to decipher the effect oftssMdeletion, a core gene belonging to T6SS-cluster i3*, on the regulation of gene expression inXanthomonas perforansstrain AL65. Transcriptomic data revealed that a total of 277 and 525 genes were upregulated, while 307 and 392 genes were downregulated in the mutant strain after 8 and 16 hours of growth in XVM2 medium. The transcript abundance of several genes associated with flagellum and pilus biogenesis as well as type III secretion system was downregulated in the mutant strain. Deletion oftssMof cluster-i3* resulted in upregulation of several T6SS genes belonging to cluster-i3*** and genes involved in biofilm and cell wall biogenesis. Similarly, transcription regulators likerpoN, Pho regulon,rpoE, andcsrAwere identified to be upregulated in the mutant strain. Our results suggest that T6SS modulates the expression of global regulators likecsrA,rpoN, andphoregulons, triggering a signaling cascade, and co-ordinates the expression of suite of virulence factors, stress response genes, and metabolic genes. IMPORTANCET6SS has received attention due to its significance in mediating interorganismal competition through contact-dependent release of effector molecules into prokaryotic and eukaryotic cells. Reverse-genetic studies have indicated the role of T6SS in virulence in a variety of plant pathogenic bacteria, including the one studied here,Xanthomonas. However, it is not clear whether such effect on virulence is merely due to a shift in the microbiome-mediated protection or if T6SS is involved in a complex virulence regulatory network. In this study, we conducted in vitro transcriptome profiling in minimal medium to decipher the signaling pathways regulated by tssM-i3* inX. perforansAL65. We show that TssM-i3* regulates the expression of a suite of genes associated with virulence and metabolism either directly or indirectly by altering the transcription of several regulators. These findings further expand our knowledge on the intricate molecular circuits regulated by T6SS in phytopathogenic bacteria. 

The emergence of plant pathogens is often associated with waves of unique evolutionary and epidemiological events. Xanthomonas hortorum pv. gardneri is one of the major pathogens causing bacterial spot disease of tomatoes. After its first report in the 1950s, there were no formal reports on this pathogen until the 1990s, despite active global research on the pathogens that cause tomato and pepper bacterial spot disease. Given the recently documented global distribution of X. hortorum pv. gardneri, our objective was to examine genomic diversification associated with its emergence. We sequenced the genomes of X. hortorum pv. gardneri strains collected in eight countries to examine global population structure and pathways of emergence using phylodynamic analysis. We found that strains isolated post-1990 group by region of collection and show minimal impact of recombination on genetic variation. A period of rapid geographic expansion in X. hortorum pv. gardneri is associated with acquisition of a large plasmid conferring copper tolerance by horizontal transfer and coincides with the burgeoning hybrid tomato seed industry through the 1980s. The ancestry of X. hortorum pv. gardneri is consistent with introduction to hybrid tomato seed production and dissemination during the rapid increase in trade of hybrid seeds. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license . 

Xanthomonas perforans is a seed-borne hemi-biotrophic pathogen that successfully establishes infection in the phyllosphere of tomato. While the majority of the studies investigating mechanistic basis of pathogenesis have focused on successful apoplastic growth, factors important during asymptomatic colonization in the early stages of disease development are not well understood. In this study, we show that tssM gene of the type VI secretion system cluster i3* (T6SS-i3*) plays a significant role during initial asymptomatic epiphytic colonization at different stages during the life cycle of the pathogen. Mutation in a core gene, tssM of T6SS-i3*, imparted higher aggressiveness to the pathogen, as indicated by higher overall disease severity, higher in planta growth as well as shorter latent infection period compared to the wild-type upon dip-inoculation of 4-5-week-old tomato plants. Contribution of tssM towards aggressiveness was evident during vertical transmission from seed-to-seedling with wild-type showing reduced disease severity as well as lower in planta populations on seedlings compared to the mutant. Presence of functional TssM offered higher epiphytic fitness as well as higher dissemination potential to the pathogen when tested in an experimental setup mimicking transplant house high-humidity conditions. We showed higher osmotolerance being one mechanism by which TssM offers higher epiphytic fitness. Taken together, these data reveal that functional TssM plays a larger role in offering ecological advantage to the pathogen. TssM prolongs the association of hemi-biotrophic pathogen with the host, minimizing overall disease severity, yet facilitating successful dissemination. 

Bacterial spot is an endemic seedborne disease responsible for recurring outbreaks on tomato and pepper around the world. The disease is caused by four diverse species, Xanthomonas gardneri, Xanthomonas euvesicatoria, Xanthomonas perforans, and Xanthomonas vesicatoria. There are no commercially available disease-resistant tomato varieties, and the disease is managed by chemical/biological control options, although these have not reduced the incidence of outbreaks. The disease on peppers is managed by disease-resistant cultivars that are effective against X. euvesicatoria but not X. gardneri. A significant shift in composition and prevalence of different species and races of the pathogen has occurred over the past century. Here, I attempt to review ecological and evolutionary processes associated with the population dynamics leading to disease emergence and spread. The goal of this review is to integrate the knowledge on population genomics and molecular plant–microbe interactions for this pathosystem to tailor disease management strategies.