Guotian Li1*
Xiaodong Wang2*
Xiaojie Wang3*
Meixiang Zhang4*
Xiao-Ren Chen5*
Jianhui Wu6*
Jin-Ying Gou7*
Lisong Ma2,8*- 1State Key Laboratory of Agricultural Microbiology, Provincial Key Laboratory of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China
- 2State Key Laboratory of North China Crop Improvement and Regulation, College of Plant Protection, Hebei Agricultural University, Baoding, China
- 3State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest Agriculture and Forestry University, Xianyang, China
- 4National Engineering Laboratory for Endangered Medicinal Resource Development in Northwest China, Key Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry of Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi'an, China
- 5College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, China
- 6College of Agronomy, Northwest Agriculture and Forestry University, Xianyang, China
- 7State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Ministry of Education Engineering Research Center of Gene Technology, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai, China
- 8College of Horticulture, Hebei Agricultural University, Baoding, China
Editorial on the Research Topic
Molecular interactions between crops and phytopathogens, volume II: Rice
Crop diseases reduce the yield and quality of agricultural products, seriously threatening human, animal and ecological heath (Dean et al., 2012). Rice (Oryza sativa), as the staple that feeds more than half of the world's population, is often afflicted with multiple devastating diseases, including rice blast caused by Magnaporthe oryzae, false smut caused by Ustilaginoidea virens, and sheath blight caused by Rhizoctonia solani (Ms, 2014). Besides these three aforementioned fungal diseases, there are severe bacterial diseases, including rice bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo) and bacterial leaf streak caused by Xanthomonas oryzae pv. oryzicola (Xoc). Among these diseases, rice blast alone results in annual grain losses that are sufficient to feed more than 60 million people globally (Cook et al., 2011). Furthermore, rice false smut not only causes yield losses but also contaminates grains with mycotoxins (Sun et al., 2020), similar to notorious Fusarium head blight of wheat. To understand these diseases for better control strategies, researchers utilize bioinformatics, physiological, molecular, and biochemical tools to elucidate the complex pathogen-host interactions. In total, this Research Topic collects seven articles from researchers in the field and covers a broad range of subjects in the following three themes.
Transcriptional analysis of the M. oryzae-rice pathosysterm
The early availability of genome sequences of M. oryzae and rice, including the recently published high-quality genomes (Qin et al., 2021; Wang et al., 2022; Yang et al., 2022), facilitates basic research of the M. oryzae-rice pathosystem. Equally important is the accurate genome annotation. In this special issue, Li Z. et al. used RNA-seq data to annotate the M. oryzae genome, leading to the identification of 3,374 additional genes, most of which encode long non-coding RNAs and often show alternative splicing events that could be important for growth, conidiation, and pathogenesis. RNA-seq has long been used in studying pathogen-host interactions and uncovering immunity-related genes. From transcriptomes of the rice cultivar Nipponbare infected by three different M. oryzae strains, Liang et al. identified thousands of conserved differentially expressed genes of rice and uncovered that overexpression of one such gene enhances rice immunity against blast. The above two papers provide rich genomic and transcriptomic information for the M. oryzae-rice interaction study.
Molecular plant pathology of M. oryzae and U. virens
Three papers in this special issue cover molecular plant pathology of rice fungal pathogens M. oryzae and U. virens. Zhang et al. studied the MoPCS60 gene that encodes a peroxisomal-CoA synthase in M. oryzae. The Mopcs60 mutant is reduced in vegetative growth when the carbon source is limited to oleate and olive oil, and attenuated in virulence. The defects of the Mopcs60 mutant are likely resulted from its defective fatty acid metabolism. The importance of lipids in M. oryzae pathogenesis is also evidenced by another recent publication, which shows that the phosphatidate phosphatase MoPah1 is important for fungal development and pathogenesis (Zhao et al., 2022). In another paper collected this special issue, Liu et al. showed that the calcineurin regulator MoRCN1 is required for full fungal virulence by M. oryzae through regulating the calcineurin pathway that often plays a key role in fungal development and pathogenesis. The Morcn1 mutant is defective in appressorium formation, invasive growth, virulence, and suppressing reactive oxygen species (ROS) of the host. Mechanistically, MoRCN1 interacts directly with the calcineurin subunit A (MoCNA) in the calcineurin pathway of M. oryzae. Rice false smut recently emerges as a serious threat to rice production worldwide, particularly to those high-yielding cultivars. Effective resistance genes against rice false smut have not been widely deployed. Recently, molecular studies of U. virens pathogenesis provide valuable information for the development of novel control strategies. Recognition of fungal chitin by plant receptors triggers immune responses, which has been shown in multiple pathosystems (Gong et al., 2020). As a counteract, fungal pathogens have evolved various approaches to avoid the recognition. Li et al. elegantly showed that the chitin-binding protein UvCBP1 secreted by U. virens is important to attenuate chitin-triggered rice immunity including ROS burst, callose deposition, and expression of defense marker genes such as OsPR10b. When overexpressed, UvCBP1 promotes fungal infection. Mechanistically, UvCBP1 competes with OsCEBiP-the rice chitin receptor-for binding to free chitin and suppresses rice immunity. These three papers together deepen our understanding of fungal-rice interactions.
Plant immune inducers and phytohormones
Chemicals are an important means in disease control, but excessive uses of traditional fungicides lead to environmental pollution and health concerns. Wang et al. identified guanine-one nucleobase of the nucleic acids DNA and RNA-as a plant immune inducer from the crude extract of the endophytic fungus Paecilomyces variotii. Guanine induces a series of defense responses, including ROS burst, callose deposition, and activation of mitogen-activated protein kinases in Arabidopsis and rice, which enhance plant resistance to bacterial and fungal pathogens through a mechanism involved in ethylene and jasmonic acid signaling pathways. In another study, Xie et al. showed that salicylic acid (SA), jasmonate, and ethylene are important for rice resistance to the white tip nematode Aphelenchoides besseyi. Authors demonstrated that the SA-related genes are positively associated with rice resistance to the nematode by comparing expression of hormone-responsive genes in resistant and susceptible rice cultivars through quantitative real-time (qRT)-PCR assays. The exogenous application of analogs of the three plant hormones induces rice resistance to the nematode. In contrast, the hormone inhibitors make rice more susceptible to the nematode. The exogenous application results were further confirmed using genetic analyses. Taken together, results from these two papers demonstrate that plant hormones are important for rice resistance to bacteria, fungi and nematodes.
The results reported in this Research Topic provide key insights into pathogen-rice interactions. Yet, some cutting-edge techniques are awaiting researchers in this field to explore, including telomere-to-telomere (T2T) genome sequencing (Nurk et al., 2022), artificial intelligence, and synthetic biology, which will facilitate our deep understanding of pathogen-rice interactions and hence development of novel disease control strategies.
Author contributions
All authors have participated in the article writing and have acted as coeditors of this Research Topic. All authors contributed to the article and approved the submitted version.
Funding
GL was supported by the National Natural Science Foundation of China (32172373). XiaodW was supported by the Provincial Natural Science Foundation of Hebei (C2022204010, C2021204008) and State Key Laboratory of North China Crop Improvement and Regulation (NCCIR2021ZZ-4). XiaojW was supported by the Shaanxi Innovation Team Project (2018TD-004). MZ was supported by the National Natural Science Foundation of China (32072399, 31672008) and the Fundamental Research Funds for the Central Universities (GK202201017). X-RC was supported by the National Natural Science Foundation of China (31871907, 31671971) and Jiangsu Agriculture Science and Technology Innovation Fund (JASTIF) [CX(20)3125]. JW was supported by the Key R&D Program of Shaanxi Province in China (2021ZDLNY0-01). J-YG was supported by the National Natural Science Foundation of China (31972350). LM was supported by the Hundred Talents Program for the introduction of high-level overseas talents in Hebei Province (E2020100004).
Acknowledgments
We thank the Frontiers Editorial Office and reviewers for their assistance in completing this Research Topic.
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
Cook, D. C., Fraser, R. W., Paini, D. R., Warden, A. C., Lonsdale, W. M., and De Barro, P. J. (2011). Biosecurity and yield improvement technologies are strategic complements in the fight against food insecurity. PLoS ONE 6, e26084. doi: 10.1371/journal.pone.0026084
Dean, R., Van Kan, J. A. L., Pretorius, Z. A., Hammond-Kosack, K. E., Di Pietro, A., Spanu, P. D., et al. (2012). The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant. Pathol. 13, 414–430. doi: 10.1111/j.1364-3703.2011.00783.x
Gong, B. Q., Wang, F. Z., and Li, J. F. (2020). Hide-and-seek: chitin-triggered plant immunity and fungal counterstrategies. Trends Plant Sci. 25, 805–816. doi: 10.1016/j.tplants.2020.03.006
Ms, Y.. (2014). Rice sheath blight: a review of disease and pathogen management approaches. J. Plant Pathol. Microbiol. 5, 1. doi: 10.4172/2157-7471.1000241
Nurk, S., Koren, S., Rhie, A., Rautiainen, M., Bzikadze, A. V., Mikheenko, A., et al. (2022). The complete sequence of a human genome. Science 376, 44–53. doi: 10.1126/science.abj6987
Qin, P., Lu, H. W., Du, H. L., Wang, H., Chen, W. L., Chen, Z., et al. (2021). Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell 184, 3542–3558. doi: 10.1016/j.cell.2021.04.046
Sun, W., Fan, J., Fang, A. F., Li, Y. J., Tariqjaveed, M., Li, D. Y., et al. (2020). Ustilaginoidea virens: insights into an emerging rice pathogen. Annu. Rev. Phytopathol. 58, 363–385. doi: 10.1146/annurev-phyto-010820-012908
Wang, Y., Yang, L., Ma, C., Zhou, Y., Zhao, M., Bi, R., et al. (2022). Genome sequence of Magnaporthe oryzae EA18 virulent to multiple widely used rice varieties. Mol. Plant Microbe Interact. MPMI01220030A. doi: 10.1094/MPMI-01-22-0030-A
Yang, L., Zhao, M., Sha, G., Sun, Q., Gong, Q., Yang, Q., et al. (2022). The genome of the rice variety LTH provides insight into its universal susceptibility mechanism to worldwide rice blast fungal strains. Comput. Struct. Biotechnol. J. 20, 1012–1026. doi: 10.1016/j.csbj.2022.01.030
Keywords: Oryza sativa, fungal pathogen, multiple omics, hypersensitive response, plant hormone
Citation: Li G, Wang X, Wang X, Zhang M, Chen X-R, Wu J, Gou J-Y and Ma L (2022) Editorial: Molecular interactions between crops and phytopathogens, volume II: Rice. Front. Plant Sci. 13:984072. doi: 10.3389/fpls.2022.984072
Received: 01 July 2022; Accepted: 14 July 2022;
Published: 29 July 2022.
Edited and reviewed by: Leo Marcelis, Wageningen University and Research, Netherlands
Copyright © 2022 Li, Wang, Wang, Zhang, Chen, Wu, Gou and Ma. 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: Guotian Li, bGk0JiN4MDAwNDA7bWFpbC5oemF1LmVkdS5jbg==; Xiaodong Wang, emhid3hkJiN4MDAwNDA7aGViYXUuZWR1LmNu; Xiaojie Wang, d2FuZ3hpYW9qaWUmI3gwMDA0MDtud3N1YWYuZWR1LmNu; Meixiang Zhang, bWVpeGlhbmd6aGFuZyYjeDAwMDQwO3NubnUuZWR1LmNu; Xiao-Ren Chen, eHJjaGVuJiN4MDAwNDA7eXp1LmVkdS5jbg==; Jianhui Wu, d3VqaCYjeDAwMDQwO253YWZ1LmVkdS5jbg==; Jin-Ying Gou, anlnb3UmI3gwMDA0MDtmdWRhbi5lZHUuY24=; Lisong Ma, bGlzb25nLm1hJiN4MDAwNDA7YW51LmVkdS5hdQ==