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Organic Fertilizer Application Mediates Tomato Defense Against Pseudomonas syringae pv. Tomato, Possibly by Reshaping the Soil Microbiome.

ABSTRACT: Bacterial speck caused by Pseudomonas syringae pv. tomato is a serious foliar disease on tomato. However, it is still unknown how organic fertilizers application mediates plant defense against foliar pathogens by altering the composition of the soil microbial community. We conducted a 2-cycle pot experiment involving chemical and organic fertilizers and tracked tomato foliar pathogen incidence. Using microbiome sequencing, we then compared the differences in bulk and rhizosphere microbial communities. The results showed that, compared with soils amended with chemical fertilizer, soils amended with organic fertilizer gradually and significantly presented a reduction in tomato foliar disease, and the bacterial richness and diversity significantly increased. Moreover, the bacterial and fungal compositions of the bulk soil and rhizosphere soil of the organic fertilizer and chemical fertilizer treatments were different from each other. More importantly, the abundance of some potentially beneficial bacteria, such as Luteolibacter, Glycomyces, Flavobacterium, and Flavihumibacter, increased in the organic fertilizer-amended soil, and these genera were significantly negatively correlated with the incidence of tomato foliar disease. These results suggest that organic fertilizers can alter the taxonomy of the soil microbiome and that some specific beneficial microbial communities may play an important role in reducing the infection of foliar pathogens by inducing plant resistance.

SUBMITTER: Huang F

PROVIDER: S-EPMC9253564 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Chemotaxis has been associated with the pathogenicity of bacteria in plants and was found to facilitate bacterial entry through stomata and wounds. However, knowledge regarding the plant signals involved in this process is scarce. We have addressed this issue using Pseudomonas syringae pv. tomato, which is a foliar pathogen that causes bacterial speck in tomato. We show that the chemoreceptor P. syringae pv. tomato PscA (PsPto-PscA) recognizes specifically and with high affinity l-Asp, l-Glu, and d-Asp. The mutation of the chemoreceptor gene largely reduced chemotaxis to these ligands but also altered cyclic di-GMP (c-di-GMP) levels, biofilm formation, and motility, pointing to cross talk between different chemosensory pathways. Furthermore, the PsPto-PscA mutant strain showed reduced virulence in tomato. Asp and Glu are the most abundant amino acids in plants and in particular in tomato apoplasts, and we hypothesize that this receptor may have evolved to specifically recognize these compounds to facilitate bacterial entry into the plant. Infection assays with the wild-type strain showed that the presence of saturating concentrations of d-Asp also reduced bacterial virulence.IMPORTANCE There is substantive evidence that chemotaxis is a key requisite for efficient pathogenesis in plant pathogens. However, information regarding particular bacterial chemoreceptors and the specific plant signal that they sense is scarce. Our work shows that the phytopathogenic bacterium Pseudomonas syringae pv. tomato mediates not only chemotaxis but also the control of pathogenicity through the perception of the plant abundant amino acids Asp and Glu. We describe the specificity of the perception of l- and d-Asp and l-Glu by the PsPto-PscA chemoreceptor and the involvement of this perception in the regulation of pathogenicity-related traits. Moreover, a saturating concentration of d-Asp reduces bacterial virulence, and we therefore propose that ligand-mediated interference of key chemoreceptors may be an alternative strategy to control virulence.

Project description:UnlabelledPlant-pathogenic bacteria are able to integrate information about their environment and adjust gene expression to provide adaptive functions. AlgU, an extracytoplasmic function (ECF) sigma factor encoded by Pseudomonas syringae, controls expression of genes for alginate biosynthesis and genes involved with resisting osmotic and oxidative stress. AlgU is active while these bacteria are associated with plants, where its presence supports bacterial growth and disease symptoms. We found that AlgU is an important virulence factor for P. syringae pv. tomato DC3000 but that alginate production is dispensable for disease in host plants. This implies that AlgU regulates additional genes that facilitate bacterial pathogenesis. We used transcriptome sequencing (RNA-seq) to characterize the AlgU regulon and chromatin immunoprecipitation sequencing (ChIP-seq) to identify AlgU-regulated promoters associated with genes directly controlled by this sigma factor. We found that in addition to genes involved with alginate and osmotic and oxidative stress responses, AlgU regulates genes with known virulence functions, including components of the Hrp type III secretion system, virulence effectors, and the hrpL and hrpRS transcription regulators. These data suggest that P. syringae pv. tomato DC3000 has adapted to use signals that activate AlgU to induce expression of important virulence functions that facilitate survival and disease in plants.ImportancePlant immune systems produce antimicrobial and bacteriostatic conditions in response to bacterial infection. Plant-pathogenic bacteria are adapted to suppress and/or tolerate these conditions; however, the mechanisms controlling these bacterial systems are largely uncharacterized. The work presented here provides a mechanistic explanation for how P. syringae pv. tomato DC3000 coordinates expression of multiple genetic systems, including those dedicated to pathogenicity, in response to environmental conditions. This work demonstrates the scope of AlgU regulation in P. syringae pv. tomato DC3000 and characterizes the promoter sequence regulated by AlgU in these bacteria.

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Organic Fertilizer Application Mediates Tomato Defense Against Pseudomonas syringae pv. Tomato, Possibly by Reshaping the Soil Microbiome.

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