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Povzetek: Background Potato virus Y (PVY) is a major pathogen that causes substantial economic losses in worldwide potato production. Different potato cultivars differ in resistance to PVY, from severe susceptibility, through tolerance, to complete resistance. The aim of this study was to better define the mechanisms underlying tolerant responses of potato to infection by the particularly aggressive PVYNTN strain. We focused on the dynamics of the primary metabolism-related processes during PVYNTN infection. Results A comprehensive analysis of the dynamic changes in primary metabolism was performed, which included whole transcriptome analysis, nontargeted proteomics, and photosynthetic activity measurements in potato cv. Désirée and its transgenic counterpart depleted for accumulation of salicylic acid (NahG-Désirée). Faster multiplication of virus occurred in the NahG-Désirée, with these plants developing strong disease symptoms. We show that while the dynamics of responses at the transcriptional level are extensive and bimodal, this is only partially translated to the protein level, and to the final functional outcome. Photosynthesis-related genes are transiently induced before viral multiplication is detected and it is down-regulated later on. This is reflected as a deficiency of the photosynthetic apparatus at the onset of viral multiplication only. Interestingly, specific and constant up-regulation of some RuBisCO transcripts was detected in Désirée plants, which might be important, as these proteins have been shown to interact with viral proteins. In SA-deficient and more sensitive NahG-Désirée plants, consistent down-regulation of photosynthesis-related genes was detected. A constant reduction in the photochemical efficiency from the onset of viral multiplication was identified; in nontransgenic plants this decrease was only transient. The transient reduction in net photosynthetic rate occurred in both genotypes with the same timing, and coincided with changes in stomatal conductivity. Conclusions Down-regulation of photosynthesis-related gene expression and decreased photosynthetic activity is in line with other studies that have reported the effects of biotic stress on photosynthesis. Here, we additionally detected induction of light-reaction components in the early stages of PVYNTN infection of tolerant interaction. As some of these components have already been shown to interact with viral proteins, their overproduction might contribute to the absence of symptoms in cv. Désirée.
Ključne besede: plant-pathogen interactions, Potato virus Y, potyviridae, salicylic acid, whole transcriptome analysis, shot-gun proteomics, photosynthetic parameters
Objavljeno v DiRROS: 29.07.2024; Ogledov: 121; Prenosov: 149
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Povzetek: Background The Dickeya genus is part of the Pectobacteriaceae family that is included in the newly described enterobacterales order. It comprises a group of aggressive soft rot pathogens with wide geographic distribution and host range. Among them, the new Dickeya fangzhongdai species groups causative agents of maceration-associated diseases that impact a wide variety of crops and ornamentals. It affects mainly monocot plants, but D. fangzhongdai strains have also been isolated from pear trees and water sources. Here, we analysed which genetic novelty exists in this new species, what are the D. fangzhongdai-specific traits and what is the intra-specific diversity. Results The genomes of eight D. fangzhongdai strains isolated from diverse environments were compared to 31 genomes of strains belonging to other Dickeya species. The D. fangzhongdai core genome regroups approximately 3500 common genes, including most genes that encode virulence factors and regulators characterised in the D. dadantii 3937 model strain. Only 38 genes are present in D. fangzhongdai and absent in all other Dickeyas. One of them encodes a pectate lyase of the PL10 family of polysaccharide lyases that is found only in a few bacteria from the plant environment, soil or human gut. Other D. fangzhongdai-specific genes with a known or predicted function are involved in regulation or metabolism. The intra-species diversity analysis revealed that seven of the studied D. fangzhongdai strains were grouped into two distinct clades. Each clade possesses a pool of 100–150 genes that are shared by the clade members, but absent from the other D. fangzhongdai strains and several of these genes are clustered into genomic regions. At the strain level, diversity resides mainly in the arsenal of T5SS- and T6SS-related toxin-antitoxin systems and in secondary metabolite biogenesis pathways. Conclusion This study identified the genome-specific traits of the new D. fangzhongdai species and highlighted the intra-species diversity of this species. This diversity encompasses secondary metabolites biosynthetic pathways and toxins or the repertoire of genes of extrachromosomal origin. We however didn’t find any relationship between gene content and phenotypic differences or sharing of environmental habitats. Background Soft rot Pectobacteriaceae are Enterobacterales responsible for considerable economic losses in several important crops and ornamental plants [1,2,3]. Their virulence is mainly due to the production and secretion of a battery of plant cell wall degrading enzymes (PCWDEs) that cause maceration of the plant tissue; however, several other virulence factors have also been characterized [2, 4]. These bacteria often exhibit a very broad host range, and recent outbreaks in potato, for example, resulted from the action of a cohort of bacteria belonging to different Pectobacteriaceae species in a complex population dynamics history [5]. The Pectobacteriaceae family includes two genera comprising soft rot bacteria, Pectobacterium and Dickeya. The Dickeya genus was formed in 2005 by the reclassification of former Erwinia chrysanthemi into six species [6]. It has recently undergone multiple phylogenetic changes, including the addition of three new species, Dickeya solani [7], Dickeya aquatica [8] and, more recently, Dickeya fangzhongdai [9]. The description of this last new species was based on three isolates from pear trees in China with bleeding canker necrosis [9], but it was extended by a large number of strains isolated from monocot plants from Japan [10, 11]. D. fangzhongdai strains were associated with soft rot symptoms of many ornamental and economically important staple food plants [10, 12, 13], thereby highlighting the broad host range of the species. While there is little information regarding associated economic damages and the extent of its occurrence in different host plants outside of Asia, Alič et al. [14] recently identified D. fangzhongdai as the causative agent of soft rot of orchids in commercial production in Europe, starting with material from Asia [11]. Moreover, as previously reported, bacteriophages of different families, and active against D. fangzhongdai, were isolated from a wastewater treatment plant not associated to the orchid production site. This would suggest that D. fangzhongdai bacteria may be more widespread in nature than could currently be concluded on the basis of symptoms in plants. Its occurrence in water would suggest that it may potentially have a wider ecological niche than genomically close Dickeya spp., that is, Dickeya dadantii, Dickeya dianthicola, and D. solani. Previous experience with D. solani has shown that novel species or isolates can lead to clonal spread and high losses in affected host plants [15]. Together with repeated introductions of D. fangzhongdai, the co-occurrence of genetically and phenotypically diverse strains on the same plants (e.g., B16 and S1 on orchids, as reported by Alič et al. [11]) increases the probability of the development of recombined strains with novel pathogenic potential and may present a risk to agriculturally important plants. Their aggressiveness, high maceration potential on various plant tissues, and persistence in potato plants further exacerbate the risk for agriculture. Therefore, in this paper, we analysed the genomic characteristics of the D. fangzhongdai species, compared it to the other Dickeya species and determine the inter- and intra- species diversity. The study addressed the question whether the presence of the isolates in a specific environment is associated to a specific set of genes (water vs plant symptoms, monocots vs dicots, different geographical origin). We also analysed the virulence gene arsenal, in order to evaluate the virulence potential of this species. Methods Dickeya strain selection All D. fangzhongdai genomes publicly available in the NCBI database were included in this study. These genomes were compared to five D. solani, four D. dadantii, five D. dianthicola, five D. chrysanthemi, seven D. zeae, one D. aquatica, two D. paradisiaca and two unassigned Dickeya genomes extracted from the NCBI database. Information on the provenance and genomic data of the D. fangzhongdai strains used in this study are summarized in Table 1. The accession numbers and phylogenetic position of the other Dickeya strains used for the SiLix analyses are presented in Additional file 1: Figure S1.
Ključne besede: T5SS, T6SS, NRPS/PKS, zeamine, oocydin A, plant-bacteria interactions, plasmid, Dickeya fangzhongdai
Objavljeno v DiRROS: 23.07.2024; Ogledov: 130; Prenosov: 101
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