Yangyang Zhao
Pedro Laborda
Sang-Wook Han
Fengquan Liu- 1Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China
- 2School of Plant Protection, Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, Hainan University, Haikou, China
- 3School of Life Sciences, Nantong University, Nantong, China
- 4Department of Plant Science and Technology, Chung-Ang University, Anseong, Republic of Korea
Editorial on the Research Topic
Pathogenic mechanism and biocontrol of Xanthomonas on plants
Xanthomonas, a Gram-negative bacterium, belonging to the class Gammaproteobacteria, can infect more than 400 different plants including a wide variety of important crops such as rice, wheat, citrus, tomato, pepper, cabbage, banana, and bean (An et al., 2020 and Timilsina et al., 2020). Some devastating diseases caused by Xanthomonas have been reported from multiple important crops worldwide. In the top 10 plant pathogenic bacteria, the fourth, fifth, and sixth positions are Xanthomonas species (Mansfield et al., 2012). For example, X. oryzae pv. oryzae (Xoo) and X. oryzae pv. oryzicola (Xoc) are the causal agents of bacterial blight and bacterial leaf streak of rice, respectively, which are two severe diseases affecting rice production and quality in tropical and subtropical regions. Moreover, X. campestris pathovars cause diseases in a range of crops. The articles in the Research Topic on the pathogenic mechanisms and biocontrol of Xanthomonas on plants explore the diversity, virulence factors, and potential management of Xanthomonas. The results provide a broader insight into Xanthomonas pathogenicity in relation to host specificity and spread, and the alternative protection strategies of plants.
Xanthomonas diversity has been largely investigated through genome sequencing and characterized using advances in omics tools (An et al., 2020 and Timilsina et al., 2020). Xoo causes bacterial blight disease of rice (Oryza sativa), which is one of the major diseases affecting rice production. Song et al. employ whole-genome sequencing to explore the diversity and evolution of Xoo in the main rice-growing areas of China over the past 30 years. They reveal six lineages including CX-1 to CX-6, in which CX-5 and CX-6 were the most prevalent across all studied areas. Recent sporadic disease outbreaks have been primarily caused by Xoo isolates derived from lineages CX-5 and CX-6. The rapid virulence evolution of Xoo against rice is analyzed using large-scale virulence tests and is correlated to the genetic background of Xoo, rice resistance genes, and the planting environment of rice. The population genomic study together with a large-scale virulence evaluation of Xoo may help build durable resistance and management strategies against this pathogen.
Bacterial type IV secretion (T4S) systems are multiprotein complexes that deliver DNA, effectors, and protein–DNA complex to the extracellular milieu or into the eukaryotic and prokaryotic target cells (Costa et al., 2021). Drehkopf et al. demonstrate the existence of the T4S systems in the tomato and pepper pathogen X. euvesicatoria, which is the only known plant pathogen with a VirB/VirD4- and an Icm/Dot-like T4S system. The VirB/VirD4 T4S system acts as a conjugation system for plasmid transfer between X. euvesicatoria strains and shares substrate specificity with the Icm/Dot system which serves as an additional protein delivery system. VirB/VirD4 T4SS in X. citri provides strains with the ability to kill other Gram-negative bacteria in a contact-dependent manner (Souza et al., 2015), but there is no toxic effect of T4S systems in X. euvesicatoria on other bacteria. The study provides a perspective on the function of T4S systems in X. euvesicatoria, which helps us understand more about this plant pathogen.
The biocontrol strategies used for Xanthomonas increasingly depend on the application of microbial biocontrol agents, or microbiome engineering. The diffusible signal factor (DSF) family is an important type of quorum sensing (QS) signal found in diverse Gram-negative bacteria and mediates intraspecies, interspecies, and inter-kingdom communication (He et al., 2023). It has been reported that DSF in X. campestris elicits innate immunity in plants and is suppressed by the exopolysaccharide xanthan (Kakkar et al., 2015). However, another study showed that DSF produced by X. campestris pv. campestris (Xcc) can suppress pathogen-associated molecular pattern-triggered immunity (PTI) in Arabidopsis thaliana (Tran et al., 2020). Zhao et al. report that a low concentration (1–5 μM) of DSF could prime plant immunity against Xcc when interacting with plants and is mediated by the jasmonic acid signaling pathway. The finding provides new insight into the function of DSF and an alternative strategy for the control of black rot in plants.
Bacillus strains are always effective and reliable alternatives to develop as a microbial pesticide to fight against Xanthomonas (Marin et al., 2019). Zhou et al. report that Bacillus velezensis strain 504 exhibits apparent antagonistic activity against Xoc wild-type strain RS105, and is a potential biocontrol agent for bacterial leaf streak, exhibiting relative control efficiencies over 70% on two susceptible cultivars. Approximately 77% of the Xoc RS105 genes are differentially expressed in the presence of cell-free supernatants of B. velezensis 504, which sheds light on the mechanisms of biological control agent-impaired Xoc.
Essential oils (EOs) or EO-based products are promising candidates for being used as biocontrol agents due to their broad-spectrum activity against fungi, bacteria, viruses, pests, and weeds, and are environmentally friendly and economically viable (Chang et al., 2022). EOs have been isolated from citrus cultivars to inhibit the X. citri subsp. citri that causes citrus bacterial canker (Mirzaei-Najafgholi et al., 2017). Nagy et al. show that EOs, especially cinnamon, are effective against X. arboricola pv. pruni (Xap), which causes bacterial spots on stone fruits. They also report that direct bioautography is a fast and suitable method for screening anti-Xap components of complex matrices. The study offers a possibility that EOs could be used to control plant disease caused by Xap.
Xanthomonas spp. cover a variety of plant pathogens that utilize a wide range of virulence factors for pathogenicity and fitness in plant hosts. This Research Topic presents the latest research and perspectives on the diversity and pathogenicity of Xanthomonas and its potential biological control agents. This Research Topic will provide researchers with the opportunity to advance perspectives on the pathogenic mechanism and biocontrol of Xanthomonas.
Author contributions
YZ: Writing – original draft. PL: Writing – review & editing. S-WH: Writing – review & editing. FL: Funding acquisition, Supervision, Writing – review & editing.
Funding
This study was supported by the National Natural Science Foundation of China (32072379).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
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References
An, S. Q., Potnis, N., Dow., M., Vorhölter, F. J., He, Y. Q., Becker, A., et al. (2020). Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas. FEMS Microbiol. Rev. 44 (1), 1–32. doi: 10.1093/femsre/fuz024
Chang, Y., Harmon, P. F., Treadwell, D. D., Carrillo, D., Sarkhosh, A., Brecht, J. K. (2022). Biocontrol potential of essential oils in organic horticulture systems: from farm to fork. Front. Nutr. 8. doi: 10.3389/fnut.2021.805138
Costa, T. R. D., Harb, L., Khara, P., Zeng, L., Hu, B., Christie, P. J. (2021). Type IV secretion systems: advances in structure, function, and activation. Mol. Microbiol. 115, 436–452. doi: 10.1111/mmi.14670
He, Y. W., Deng, Y., Miao, Y., Chatterjee, S., Tran, T. M., Tian, J., et al. (2023). DSF family quorum sensing signal-mediated intraspecies, interspecies, and inter-kingdom communication. Trends Microbiol. 31, 36–50. doi: 10.1016/j.tim.2022.07.006
Kakkar, A., Nizampatnam, N. R., Kondreddy, A., Pradhan, B. B., Chatterjee, S. (2015). Xanthomonas campestris cell-cell signaling molecule DSF (diffusible signal factor) elicits innate immunity in plants and is suppressed by the exopolysaccharide xanthan. J. Exp. Bot. 66, 6697–6714. doi: 10.1093/jxb/erv377
Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., et al. (2012). Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13, 614–629. doi: 10.1111/j.1364-3703.2012.00804.x
Marin, V. R., Ferrarezi, J. H., Vieira, G., Sass, D. C. (2019). Recent advances in the biocontrol of Xanthomonas spp. World J. Microbiol. Biotechnol. 35 (5), 72. doi: 10.1007/s11274-019-2646-5
Mirzaei-Najafgholi, H., Tarighi, S., Golmohammadi, M., Taheri, P. (2017). The effect of citrus essential oils and their constituents on growth of Xanthomonas citri subsp. citri. Molecules 22 (4), 591. doi: 10.3390/molecules22040591
Souza, D. P., Oka, G. U., Alvarez-Martinez, C. E., Bisson-Filho, A. W., Dunger, G., Hobeika, L., et al. (2015). Bacterial killing via a type IV secretion system. Nat. Commun. 6, 6453. doi: 10.1038/ncomms7453
Timilsina, S., Potnis, N., Newberry, E. A., Liyanapathiranage, P., Iruegas-Bocardo, F., White, F. F., et al. (2020). Xanthomonas diversity, virulence and plant–pathogen interactions. Nat. Rev. Microbiol. 18, 415–427. doi: 10.1038/s41579-020-0361-8
Keywords: Xanthomonas, diversity, type IV secretion system (T4SS), quorum sensing (QS), biocontrol, Bacillus, Essential oils (EOs)
Citation: Zhao Y, Laborda P, Han S-W and Liu F (2023) Editorial: Pathogenic mechanism and biocontrol of Xanthomonas on plants. Front. Cell. Infect. Microbiol. 13:1270750. doi: 10.3389/fcimb.2023.1270750
Received: 01 August 2023; Accepted: 08 August 2023;
Published: 18 August 2023.
Edited and Reviewed by:
Alain Filloux, Imperial College London, United KingdomCopyright © 2023 Zhao, Laborda, Han and Liu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Fengquan Liu, ZnFsaXUyMDAxMUBzaW5hLmNvbQ==