Type VI secretion system is not required for virulence on rice but for inter-bacterial competition in Xanthomonas oryzae pv. oryzicola

Zhu, Pingchuan; Li, Yiming; Xia, Yang; HaiFan, Zou; Zhu, Xiaoguang; Niu, Xiang-Na; Xu, Luzhou; Jiang, Wei; Huang, Sheng; Tang, Ji‐Liang; He, Yanan

doi:10.1016/j.resmic.2019.10.004

Cited by 18 publications

(21 citation statements)

References 39 publications

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“…oryzicola, T6SS i4 has been identified for its role in the interbacterial competition, whereas in X. oryzae pv. oryzae, it was identified for its role in virulence ( Choi et al, 2020 ; Zhu et al, 2020 ; Montenegro Benavides et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…Of these six systems, types II, III, and IV have been extensively studied in the genus Xanthomonas . In contrast, the role, distribution, and evolutionary history of the most recently identified type VI secretion system (T6SS) has been described only in few studies ( Bayer-Santos et al, 2018 ; Bansal et al, 2019 , 2020 ; Bayer-Santos et al, 2019 ; Ceseti et al, 2019 ; Alvarez-Martinez et al, 2020 ; Choi et al, 2020 ; Zhu et al, 2020 ; Montenegro Benavides et al, 2021 ). Most of the aforementioned studies used only representative Xanthomonas spp., to derive conclusions regarding the distribution of the T6SS clusters in the whole genus Xanthomonas .…”

Section: Introductionmentioning

confidence: 99%

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Phylogenetic Distribution and Evolution of Type VI Secretion System in the Genus Xanthomonas

et al. 2022

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The type VI secretion system (T6SS) present in many Gram-negative bacteria is a contact-dependent apparatus that can directly deliver secreted effectors or toxins into diverse neighboring cellular targets including both prokaryotic and eukaryotic organisms. Recent reverse genetics studies with T6 core gene loci have indicated the importance of functional T6SS toward overall competitive fitness in various pathogenic Xanthomonas spp. To understand the contribution of T6SS toward ecology and evolution of Xanthomonas spp., we explored the distribution of the three distinguishable T6SS clusters, i3*, i3***, and i4, in approximately 1,740 Xanthomonas genomes, along with their conservation, genetic organization, and their evolutionary patterns in this genus. Screening genomes for core genes of each T6 cluster indicated that 40% of the sequenced strains possess two T6 clusters, with combinations of i3*** and i3* or i3*** and i4. A few strains of Xanthomonas citri, Xanthomonas phaseoli, and Xanthomonas cissicola were the exception, possessing a unique combination of i3* and i4. The findings also indicated clade-specific distribution of T6SS clusters. Phylogenetic analysis demonstrated that T6SS clusters i3* and i3*** were probably acquired by the ancestor of the genus Xanthomonas, followed by gain or loss of individual clusters upon diversification into subsequent clades. T6 i4 cluster has been acquired in recent independent events by group 2 xanthomonads followed by its spread via horizontal dissemination across distinct clades across groups 1 and 2 xanthomonads. We also noted reshuffling of the entire core T6 loci, as well as T6SS spike complex components, hcp and vgrG, among different species. Our findings indicate that gain or loss events of specific T6SS clusters across Xanthomonas phylogeny have not been random.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Phylogenetic Distribution and Evolution of Type VI Secretion System in the Genus Xanthomonas

et al. 2022

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“…These observations together with the wide distribution of T6SS clusters in plant-associated bacteria could suggest that this system is crucial for optimal fitness during plant colonization, as the main role of T6SS in phytobacteria would be interbacterial competition rather than host manipulation (Bernal et al 2018) as also recently demonstrated in the rice pathogen X. oryzae pv. oryzicola (Zhu et al 2020). Since it was already reported that X. fragariae and X. arboricola pv.…”

Section: Discussionmentioning

confidence: 99%

Comparative genomics of Xanthomonas fragariae and Xanthomonas arboricola pv. fragariae reveals intra- and interspecies variations

et al. 2020

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The quarantine bacterium Xanthomonas fragariae causes angular leaf spots on strawberry. Its population structure was recently found to be divided into four (sub)groups resulting from two distinct main groups. Xanthomonas arboricola pv. fragariae causes bacterial leaf blight, but the bacterium has an unclear virulence status on strawberry. In this study, we use comparative genomics to provide an overview of the genomic variations of a set of 58 X. fragariae and five X. arboricola pv. fragariae genomes with a focus on virulence-related proteins. Structural differences within X. fragariae such as differential plasmid presence and large-scale genomic rearrangements were observed. On the other hand, the virulence-related protein repertoire was found to vary greatly at the interspecies level. In three out of five sequenced X. arboricola pv. fragariae strains, the major part of the Hrp type III secretion system was lacking. An inoculation test with strains from all four X. fragariae (sub)groups and X. arboricola pv. fragariae resulted in an interspecies difference in symptom induction since no symptoms were observed on the plants inoculated with X. arboricola pv. fragariae. Our analysis suggests that all X. fragariae (sub)groups are pathogenic on strawberry plants. On the other hand, the first genomic investigations of X. arboricola pv. fragariae revealed a potential lack of certain key virulence-related factors which may be related to the difficulties to reproduce symptoms on strawberry and could question the plant-host interaction of the pathovar.

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“…The results indicate that the T6SS-2 in Xoo PXO99 A is involved in competition with E. coli, consistent with the recent study in X. oryzae pv. oryzicola (Zhu et al, 2020).…”

Section: Sar Regulates the Expression Of T6ss-1 Related Genes But Not...mentioning

confidence: 99%

Transcriptional regulator Sar regulates the multiple secretion systems in Xanthomonas oryzae

Shao

Tang

Huang

et al. 2022

Molecular Plant Pathology

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Xanthomonas oryzae pv. oryzae (Xoo) is a notorious plant pathogen that causes leaf blight of rice cultivars. The pathogenic bacteria possess numerous transcriptional regulators to regulate various biological processes, such as pathogenicity in the host plant. Our previous study identified a new master regulator PXO_RS20790 that is involved in pathogenicity for Xoo against the host rice. However, the molecular functions of PXO_RS20790 are still unclear. Here, we demonstrate that transcriptional regulator Sar (PXO_RS20790) regulates multiple secretion systems. The RNA-sequencing analysis, bacterial one-hybrid assay, and electrophoretic mobility shift assay revealed that Sar enables binding of the promoters of the T1SS-related genes, the avirulence gene, raxX, and positively regulates these genes' expression.Meanwhile, we found that Sar positively regulated the T6SS-1 clusters but did not regulate the T6SS-2 clusters. Furthermore, we revealed that only T6SS-2 is involved in interbacterial competition. We also indicated that Sar could bind the promoters of the T3SS regulators, hrpG and hrpX, to activate these two genes' transcription.Our findings revealed that Sar is a crucial regulator of multiple secretion systems and virulence.

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Type VI secretion system is not required for virulence on rice but for inter-bacterial competition in Xanthomonas oryzae pv. oryzicola

Cited by 18 publications

References 39 publications

Phylogenetic Distribution and Evolution of Type VI Secretion System in the Genus Xanthomonas

Phylogenetic Distribution and Evolution of Type VI Secretion System in the Genus Xanthomonas

Comparative genomics of Xanthomonas fragariae and Xanthomonas arboricola pv. fragariae reveals intra- and interspecies variations

Transcriptional regulator Sar regulates the multiple secretion systems in Xanthomonas oryzae

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