Jianuan Zhou
Steffen Kolb
Xiaofan Zhou- 1National Key Laboratory of Green Pesticide, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, China
- 2Microbial Biogeochemistry, Research Area Landscape Functioning, Leibniz Center for Agricultural Landscape Research e.V. (ZALF), Müncheberg, Germany
Editorial on the Research Topic
Pathogen co-infections and plant diseases
Plant-microbe interaction has always been the focus of agricultural life science and has continuously increased the knowledge of human cognition about the nature. However, previous efforts in this regard have mostly focused on “one-to-one” binary relationships, such as the most classical plant-pathogen interaction “zigzag” model proposed by Jones and Dangl (2006). However, interactions between microbes are important components of the complexity of nature. With the development of microbe separation techniques and especially the metagenomic sequencing technology, communities of co-occurring pathogens are increasingly identified in diseased plants, and co-occurrence patterns and inter- and intra-species interactions have started to draw attention. Disease outbreaks may be incited by a certain mixture of microbes that are spatially aggregated in the field and migrate patch to patch in a short time (Burdon, 1993; Morris et al., 2017). Moreover, in reality, the distribution and composition of such microbe metapopulations are dynamic with changes in climate and environmental conditions.
In this special issue, four articles were published. Zhang et al. in their article “Co-infection of Fusarium aglaonematis sp. nov. and Fusarium elaeidis causing stem rot in Aglaonema modestum in China” obtained multiple Fusarium isolates from the diseased A. modestum, and determined F. aglaonematis and F. elaeidis belonging to different Fusarium species complex as the pathogens. Co-infection of the two species enhanced the disease severity of the host compared to single inoculation. Similar examples of synergistic interactions of pathogen-pathogen in plants that lead to increased disease severity have often been reported. For instance, co-infection of F. oxysporum f. sp. medicaginis and Rhizoctonia solani resulted in more severe disease incidence and growth reduction in commercial alfalfa production compared to a single infection (Fang et al., 2021). For tomato pith necrosis, co-infection of Pseudomonas corrugate with P. marginalis or P. mediterranea greatly enhanced the severity of the disease in tomato (Moura et al., 2005; Kudela et al., 2010). Co-inoculations with Pythium and Fusarium species caused increased disease symptoms compared to either pathogen alone (Lerch-Olson and Robertson, 2020). More commonly, different pathogens with imperceptible relationships have been purified from the same disease plant tissue, such as the recent studies identifying Dickeya zeae and Stenotrophomonas maltophilia as the soft rot pathogens on Clivia minita (Hu et al., 2021a), Xanthomonas perforans and Pantoea ananatis as the causal agents on water spinach (Ipomoea aquatic) (Hu et al., 2021b), and Enterobacter asburiae and Pa. ananatis causing rice bacterial blight in China (Xue et al., 2021).
In the next article “Effect of disease severity on the structure and diversity of the phyllosphere microbial community in tobacco” by Sun et al., amplicon sequencing-based analysis of ITS and 16S rRNA markers was employed to investigate the structure of microbiomes involved in tobacco target spot disease. The study revealed significant differences in the composition and diversity of phyllospheric fungi and bacteria between healthy plants and plants with varying levels of disease severity. In addition, critical fungal and bacterial biomarkers were identified for health and disease plants. High-throughput sequencing-based techniques such as amplicon sequencing and shotgun metagenomic sequencing are powerful tools that alleviate the limitations of traditional microbe separation techniques and can provide a complete picture of the microbial communities in samples of interest. These approaches not only help to elucidate the mechanisms of plant-pathogen and pathogen-pathogen interactions, but can also facilitate the monitoring of disease development and the evaluation of disease management strategies.
The complexity of the pathogen-host interaction is not only reflected in the change of the composition of the pathogen mixture at different stages on the same plant, but also in the different gene expression profiles of the resistant and susceptible plant varieties responding to the same pathogen. Gong et al. in the article “Transcriptional profiling of resistant and susceptible cultivars of grapevine (Vitis L.) reveals hypersensitive responses to Plasmopara viticola” revealed that the resistant grape variety “Kober 5BB” has significantly different gene expression profiles from the susceptible variety “Zitian Seedless”, and Caspase-like proteases mediating plant hypersensitive response (HR) cell death is the key strategy in the process of grape defense against downy mildew. Besides HR, reactive oxygen species (ROS) and plant hormones like salicylic acid (SA) and jasmonic acid (JA) have been reported to be involved in plant defense (Sherif et al., 2016; Rahman et al., 2019; Gupta et al., 2020; Hu et al., 2022). Additionally, Xu et al. in the article “Mutations in PpAGO3 Lead to Enhanced Virulence of Phytophthora parasitica by Activation of 25–26 nt sRNA-Associated Effector Genes” examined the AGO3 gene of Phytophthora parasitica, and revealed an underappreciated role of small RNA (sRNA) silencing pathways in regulating the expression of effectors in pathogenic oomycetes.
In conclusion, this special issue focusing on pathogen co-Infections of plant diseases highlights the importance of the interactions between multiple pathogens and plant-pathogen and calls for future endeavors in this area. The underlying mechanisms resulting from pathogen co-infection that can lead to complex disease epidemiology are important topics for investigation and for the development of novel disease management approaches.
Author contributions
JZ, SK, and XZ contributed to the manuscript preparation and finalizing. All authors contributed to the article and approved the submitted version.
Funding
JZ acknowledges the support by National Key Research and Development Program (2022YFA1304400).
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
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Burdon, J. J. (1993). The structure of pathogen populations in natural plant communities. Annu. Rev. Phytopathol. 31, 305–323. doi: 10.1146/annurev.py.31.090193.001513
Fang, X., Zhang, C., Wang, Z., Duan, T., Yu, B., Jia, X., et al. (2021). Co-infection by soil-borne fungal pathogens alters disease responses among diverse Alfalfa varieties. Front. Microbiol. 12, 664385. doi: 10.3389/fmicb.2021.664385
Gupta, A., Bhardwaj, M., and Tran, L. S. P. (2020). Jasmonic acid at the crossroads of plant immunity and Pseudomonas syringae virulence. Int. J. Mol. Sci. 21, 7482. doi: 10.3390/ijms21207482
Hu, A., Hu, M., Chen, S., Xue, Y., Tan, X., and Zhou, J. (2022). Five plant natural products are potential Type III secretion system inhibitors to effectively control soft-rot disease caused by Dickeya. Front. Microbiol. 13, 839025. doi: 10.3389/fmicb.2022.839025
Hu, M., Li, C., Xue, Y., Hu, A., Chen, S., Chen, Y., et al. (2021a). Isolation, characterization, and genomic investigation of a phytopathogenic strain of Stenotrophomonas maltophilia. Phytopathol. 111, 2088–2099. doi: 10.1094/PHYTO-11-20-0501-R
Hu, M., Li, C., Zhou, X., Xue, Y., Wang, S., Hu, A., et al. (2021b). Microbial diversity analysis and genome sequencing identify Xanthomonas perforans as the pathogen of bacterial leaf canker of water spinach (Ipomoea aquatic). Front. Microbiol. 12, 752760. doi: 10.3389/fmicb.2021.752760
Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323–329. doi: 10.1038/nature05286
Kudela, V., Krejzar, V., and Pánkov,á, I. (2010). Pseudomonas corrugate and Pseudomonas marginalis associated with the collapse of tomato plants in rockwool slab hydroponic culture. Plant Prot. Sci. 46, 1–11. doi: 10.17221/44/2009-PPS
Lerch-Olson, E. R., and Robertson, A. E. (2020). Effect of co-inoculations with Pythium and Fusarium species on seedling disease development of soybean. Can. J. Plant Pathol. 42, 408–418. doi: 10.1080/07060661.2019.1668858
Morris, C. E., Barny, M., Berge, O., Kinkel, L. L., and Lacroix, C. (2017). Frontiers for research on the ecology of plant-pathogenic bacteria: fundamentals for sustainability. Mol. Plant Pathol. 18, 308–319. doi: 10.1111/mpp.12508
Moura, M. L., Jacques, L. A., Brito, L. M., Mourao, I. M., and Duclos, J. (2005). Tomato pith necrosis caused by P. corrugata and P. mediterranea: severity of damages and crop loss assessment. Acta Hort. 695, 365–372. doi: 10.17660/ActaHortic.2005.695.45
Rahman, M. U., Hanif, M., Shah, F., and Wang, X. P. (2019). Botrytis cinerea structural development and host responses in resistant and susceptible grapevine cultivars: a physiological and structural study. Fresenius Environ. Bull. 28, 3162–3171.
Sherif, S. M., Shukla, M. R., Murch, S. J., Bernier, L., and Saxena, P. K. (2016). Simultaneous induction of Jasmonic acid and disease-responsive genes signifies tolerance of American elm to Dutch elm disease. Sci. Rep. 6, 21934. doi: 10.1038/srep21934
Keywords: plant diseases, co-infection, microbial community, interactions, synergism
Citation: Zhou J, Kolb S and Zhou X (2023) Editorial: Pathogen co-infections and plant diseases. Front. Microbiol. 14:1189476. doi: 10.3389/fmicb.2023.1189476
Received: 19 March 2023; Accepted: 12 April 2023;
Published: 10 May 2023.
Edited and reviewed by: Jesús Navas-Castillo, IHSM La Mayora, CSIC, Spain
Copyright © 2023 Zhou, Kolb and Zhou. 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: Jianuan Zhou, amlhbnVhbnpob3UmI3gwMDA0MDtzY2F1LmVkdS5jbg==; Steffen Kolb, U3RlZmZlbi5Lb2xiJiN4MDAwNDA7emFsZi5kZQ==; Xiaofan Zhou, eGlhb2Zhbl96aG91JiN4MDAwNDA7c2NhdS5lZHUuY24=