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Many phytopathogens' gene products that contribute to plant-pathogen interactions remain unexplored. In one of the most harmful phytopathogenic bacterium Pectobacterium atrosepticum ( Pba ), phosphonate-related genes have been previously shown to be among the most upregulated following host plant colonization. However, phosphonates, compounds characterized by a carbon-phosphorus bond in their composition, have not been described in Pectobacterium species and other phytopathogenic bacteria, with the exception of Pseudomonas syringae and Pantoea ananatis . Our study aimed to determine whether Pba synthesizes extracellular phosphonates and, if so, to analyze their physiological functions. We demonstrated that Pba produces two types of extracellular phosphonates: 2-diethoxyphosphorylethanamine and phenylphosphonic acid. Notably, such structures have not been previously described among natural phosphonates. The production of Pba phosphonates was shown to be positively regulated by quorum sensing and in the presence of pectic compounds. Pba phosphonates were found to have a positive effect on Pba stress resistance and a negative effect on Pba virulence. The discovered Pba phosphonates are discussed as metabolites that enable Pba to control its "harmful properties", thereby maintaining its ecological niche (the host plant) in a relatively functional state for an extended period.

The alternative sigma factor RpoS is considered to be one of the major regulators providing stress resistance and cross-protection in bacteria. In phytopathogenic bacteria, the effects of RpoS have not been analyzed with regard to cross-protection, and genes whose expression is directly or indirectly controlled by RpoS have not been determined at the whole-transcriptome level. Our study aimed to determine RpoS-regulated genes and phenotypes in the phytopathogenic bacterium Pectobacterium atrosepticum . Knockout of the rpoS gene in P. atrosepticum affected the long-term starvation response, cross-protection, and virulence toward plants with enhanced immune status. The whole-transcriptome profiles of the wild-type P. atrosepticum strain and its Δ rpoS mutant were compared under different experimental conditions, and functional gene groups whose expression was affected by RpoS were determined. The RpoS promoter motif was inferred within the promoter regions of the genes affected by rpoS deletion, and the P. atrosepticum RpoS regulon was predicted. Based on RpoS-controlled phenotypes, transcriptome profiles, and RpoS regulon composition, the regulatory role of RpoS in P. atrosepticum is discussed.

Pectobacterium and Dickeya species belonging to the Soft Rot Pectobacteriaceae (SRP) are one of the most devastating phytopathogens. They degrade plant tissues by producing an arsenal of plant cell wall degrading enzymes. However, SRP-plant interactions are not restricted to the production of these "brute force" weapons. Additionally, these bacteria apply stealth behavior related to (1) manipulation of the host plant via induction of susceptible responses and (2) formation of heterogeneous populations with functionally specialized cells. Our review aims to summarize current knowledge on SRP-induced plant susceptible responses and on the heterogeneity of SRP populations. The review shows that SRP are capable of adjusting the host's hormonal balance, inducing host-mediated plant cell wall modification, promoting iron assimilation by the host, stimulating the accumulation of reactive oxygen species and host cell death, and activating the synthesis of secondary metabolites that are ineffective in limiting disease progression. By this means, SRP facilitate host plant susceptibility. During host colonization, SRP populations produce various functionally specialized cells adapted for enhanced virulence, increased resistance, motility, vegetative growth, or colonization of the vascular system. This enables SRP to perform self-contradictory tasks, which benefits a population's overall fitness in various environments, including host plants. Such stealthy tactical actions facilitate plant-SRP interactions and disease progression., Competing Interests: Conflict of Interest The authors declare that they have no competing interests., (Copyright © 2023 Elsevier Ltd. All rights reserved.)

Phytopathogenic microorganisms, being able to cause plant diseases, usually interact with hosts asymptomatically, resulting in the development of latent infections. Knowledge of the mechanisms that trigger a switch from latent to typical, symptomatic infection is of great importance from the perspectives of both fundamental science and disease management. No studies to date have compared, at the systemic molecular level, the physiological portraits of plants when different infection types (typical and latent) are developed. The only phytopathogenic bacterium for which latent infections were not only widely described but also at least fluently characterized at the molecular level is Pectobacterium atrosepticum ( Pba ). The present study aimed at the comparison of plant transcriptome responses during typical and latent infections caused by Pba in order to identify and then experimentally verify the key molecular players that act as switchers, turning peaceful plant- Pba coexistence into a typical infection. Based on RNA-Seq, we predicted plant cell wall-, secondary metabolism-, and phytohormone-related genes whose products contributed to the development of the disease or provided asymptomatic plant- Pba interactions. By treatment tests, we confirmed that a switch from latent to typical Pba -caused infection is determined by the plant susceptible responses mediated by the joint action of ethylene and jasmonates.

Bacterial adaptation is regulated at the population level with the involvement of intercellular communication (quorum sensing). When the population density is insufficient for adaptation under starvation, bacteria can adjust it to a quorum level through cell divisions at the expense of endogenous resources. This phenomenon has been described for the phytopathogenic bacterium Pectobacterium atrosepticum ( Pba ), and it is called, in our study, adaptive proliferation. An important attribute of adaptive proliferation is its timely termination, which is necessary to prevent the waste of endogenous resources when the required level of population density is achieved. However, metabolites that provide the termination of adaptive proliferation remained unidentified. We tested the hypothesis of whether quorum sensing-related autoinducers prime the termination of adaptive proliferation and assessed whether adaptive proliferation is a common phenomenon in the bacterial world. We showed that both known Pba quorum sensing-related autoinducers act synergistically and mutually compensatory to provide the timely termination of adaptive proliferation and formation of cross-protection. We also demonstrated that adaptive proliferation is implemented by bacteria of many genera and that bacteria with similar quorum sensing-related autoinducers have similar signaling backgrounds that prime the termination of adaptive proliferation, enabling the collaborative regulation of this adaptive program in multispecies communities.

Stringent response (SR), a primary stress reaction in bacteria and plant chloroplasts, is a molecular switch that provides operational stress-induced reprogramming of transcription under conditions of abiotic and biotic stress. Because the infection is a stressful situation for both partners (the host plant and the pathogen), we analyzed the expression of bacterial and plastid SR-related genes during plant-microbial interaction. In the phytopathogenic bacterium Pectobacterium atrosepticum , SpoT-dependent SR was induced after contact with potato or tobacco plants. In plants, two different scenarios of molecular events developed under bacterial infection. Plastid SR was not induced in the host plant potato Solanum tuberosum , which co-evolved with the pathogen for a long time. In this case, the salicylic acid defense pathway was activated and plants were more resistant to bacterial infection. SR was activated in the tobacco Nicotiana tabacum (experimental host) along with activation of jasmonic acid-related genes, resulting in plant death. These results are important to more fully understand the evolutionary interactions between plants and symbionts/pathogens.

Siderophores produced by microorganisms to scavenge iron from the environment have been shown to contribute to virulence and/or stress resistance of some plant pathogenic bacteria. Phytopathogenic bacteria of Pectobacterium genus possess genes for the synthesis of siderophore enterobactin, which role in plant-pathogen interactions has not been elucidated. In the present study we characterized the phenotype of the mutant strain of Pba deficient for the enterobactin-biosynthetic gene entA . We showed that enterobactin may be considered as a conditionally beneficial virulence factor of Pba . The entA knockout did not reduce Pba virulence on non-primed plants; however, salicylic acid-primed plants were more resistant to Δ entA mutant than to the wild type Pba . The reduced virulence of Δ entA mutant towards the primed plants is likely explained by its compromised resistance to oxidative stress.

Our study is the first to consider the changes in the entire set of matrix plant cell wall (PCW) polysaccharides in the course of a plant infectious disease. We compared the molecular weight distribution, monosaccharide content, and the epitope distribution of pectic compounds and cross-linking glycans in non-infected potato plants and plants infected with Pectobacterium atrosepticum at the initial and advanced stages of plant colonization by the pathogen. To predict the gene products involved in the modification of the PCW polysaccharide skeleton during the infection, the expression profiles of potato and P. atrosepticum PCW-related genes were analyzed by RNA-Seq along with phylogenetic analysis. The assemblage of P. atrosepticum biofilm-like structures-the bacterial emboli-and the accumulation of specific fragments of pectic compounds that prime the formation of these structures were demonstrated within potato plants (a natural host of P. atrosepticum ). Collenchyma was shown to be the most "vulnerable" tissue to P. atrosepticum among the potato stem tissues. The infection caused by the representative of the Soft Rot Pectobacteriaceae was shown to affect not only pectic compounds but also cross-linking glycans; the content of the latter was increased in the infected plants compared to the non-infected ones., Competing Interests: The authors declare no conflict of interest

Soft rot caused by Pectobacterium species is a devastating plant disease poorly characterized in terms of host plant responses. In this study, changes in the transcriptome of tobacco plants after infection with Pectobacterium atrosepticum ( Pba ) were analyzed using RNA-Seq. To draw a comprehensive and nontrivially itemized picture of physiological events in Pba -infected plants and to reveal novel potential molecular "players" in plant- Pba interactions, an original functional gene classification was performed. The classifications present in various databases were merged, enriched by "missed" genes, and divided into subcategories. Particular changes in plant cell wall-related processes, perturbations in hormonal and other regulatory systems, and alterations in primary, secondary, and redox metabolism were elucidated in terms of gene expression. Special attention was paid to the prediction of transcription factors (TFs) involved in the disease's development. Herewith, gene expression was analyzed within the predicted TF regulons assembled at the whole-genome level based on the presence of particular cis-regulatory elements (CREs) in gene promoters. Several TFs, whose regulons were enriched by differentially expressed genes, were considered to be potential master regulators of Pba -induced plant responses. Differential regulation of genes belonging to a particular multigene family and encoding cognate proteins was explained by the presence/absence of the particular CRE in gene promoters.