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Professor Shannong Ding Xinhua's team revealed the mechanism of rice's recognition of "self" exosome small proteins, stimulating immunity, and improving broad-spectrum disease resistance

author:Frontiers of Plant Science

Plants are constantly threatened by various pathogenic bacteria during the growth and development process, and in the long-term co-evolution process of plants-pathogens, plants have accumulated abundant potential disease resistance resources. The essence of plant immunity is that the body recognizes 'self' and 'non-self', and when a plant is attacked by a pathogen, the plant as a host will recognize the 'non-self' and produce corresponding signals, which in turn will cause a series of immune responses. At present, there have been some reports of plant recognition of DAMP (damage-associated molecular pattern) to elicit immunity, but there are few reports of plant recognition of "self" eliciting immunity. As the "frontier battlefield" of the interaction between plants and pathogens, the apoplast space contains a wealth of immune proteins. Although some studies have shown that the expression and application of plant proteins with antibacterial or immuno-inducing activity in plants can effectively reduce the occurrence of diseases, the identification and mechanism of exoexosome disease resistance proteins in rice are still very limited.

2024年4月25日,Molecular Plant在线发表了山东农业大学丁新华教授团队题为“Recognition of the inducible, secretory small protein OsSSP1 by the membrane receptor OsSSR1 and coreceptor OsBAK1 confers rice resistance to the blast fungus”的研究论文。 该研究揭示了一个水稻分泌小蛋白OsSSP1在稻瘟病菌侵染阶段从细胞内被分泌到质外体空间中,被植物自身膜受体OsSSR1及共受体OsBAK1所识别,激发植物免疫的分子机制。 同时发现,植物的这种对自身分泌蛋白的自我识别过程产生的抗性具有很好的广谱性。 该工作对丰富水稻广谱抗性资源、控制水稻病害,保证粮食安全具有重要意义。

Professor Shannong Ding Xinhua's team revealed the mechanism of rice's recognition of "self" exosome small proteins, stimulating immunity, and improving broad-spectrum disease resistance

https://doi.org/10.1016/j.molp.2024.04.009

In this study, it was first found that Oryza sativa secretory small protein 1 (Oryza sativa secretory small protein 1) can be secreted into the apoplast space during blast infection to stimulate plant immunity (Fig. 1A-1F). Exogenous expression of this small protein could significantly reduce the incidence of rice blast without affecting the yield-related phenotype of rice (Fig. 1G), and it was found that OsSSP1 protein could be stored in an open environment for 7 days and still had a good resistance induction effect, suggesting that it is feasible for OsSSP1 protein treatment to enhance rice disease resistance in vitro. Furthermore, the overexpression of OsSSP1 (SSP1-OE) and CRISPR-edited (ssp1) lines showed that SSP1-OE had a stronger immune response and resistance to rice blast during the infection process, while the ssp1 line showed a lower immune response and more susceptibility (Fig. 1H-1I), indicating that OsSSP1 positively regulated rice resistance to rice blast.

Professor Shannong Ding Xinhua's team revealed the mechanism of rice's recognition of "self" exosome small proteins, stimulating immunity, and improving broad-spectrum disease resistance

Fig.1 Rice exosome protein OsSSP1 can be secreted into the apoplast space to stimulate plant immunity and enhance rice disease resistance

In order to clarify the mechanism by which OsSSP1 stimulates plant immunity, the research team screened two membrane proteins that directly interact with OsSSP1: the membrane receptor OsSSR1 and the co-receptor OsBAK1. Bimolecular fluorescence complementation, luciferase complementation imaging, and Co-IP showed that the interaction between OsSSP1 and the membrane receptors OsSSR1 and OsBAK1 occurred in their extracellular regions, and OsSSR1 and OsBAK1 also interacted through the extracellular part (Figs. 2A-2F). It was further found that the plant immunity and rice disease resistance induced by OsSSP1 were significantly affected in the gene-edited lines of OsSSR1 and OsBAK1 (Fig. 2G-2H), indicating that the plant immunity stimulated by OsSSP1 was dependent on the membrane receptor OsSSR1 and the co-receptor OsBAK1.

Professor Shannong Ding Xinhua's team revealed the mechanism of rice's recognition of "self" exosome small proteins, stimulating immunity, and improving broad-spectrum disease resistance

Fig.2 OsSSP1-mediated plant immune stimulation and disease resistance depend on membrane receptor OsSSR1 and co-receptor OsBAK1OsSSP1The protein encoded by OsSSP1 belongs to the DIR protein family and is related to lignin and lignanin synthesis. However, the research team found that OsSSP1 is not involved in the synthesis of lignin and lignans, which is also an expansion of the function of the DIR protein family.

Professor Shannong Ding Xinhua's team revealed the mechanism of rice's recognition of "self" exosome small proteins, stimulating immunity, and improving broad-spectrum disease resistance

Fig.3 Recognition of OsSSP1 membrane receptor OsSSR1 and co-receptor OsBAK1 in rice

A working model to enhance broad-spectrum disease resistance in plants

In view of the fact that the elicitors that can induce plant immune responses are mainly derived from pathogenic bacteria, the small exosome protein OsSSP1 found in this study can be recognized by the plant's own membrane receptor protein OsSSR1 and co-receptor OsBAK1, which can stimulate plant immunity and enhance plant resistance to diseases (Fig. 3), so it is a new expansion of plant immune defense strategy. At the same time, the expression of this protein in vitro had good stability and resistance induction effect, and the overexpressed transgenic plants had good resistance to different field physiological races of B. oryzae and other major rice diseases, which not only further enriched the related materials of rice disease resistance, but also laid a theoretical foundation for the establishment of new disease control strategies based on exocrine disease resistance proteins.

Zhao Tianfeng, a master's student from the College of Plant Protection of Shandong Agricultural University, is the first author of the paper, and Professor Yin Ziyi, Associate Professor Li Yang and Professor Ding Xinhua of the College of Plant Protection of Shandong Agricultural University are the co-corresponding authors of the paper. His research was supported by the National Key R&D Program of China, the National Natural Science Foundation of China, the Natural Science Foundation of Shandong Province, and the Taishan Scholars Program.

About the Contact:

尹梓屹博士,山东农业大学植物保护学院教授,围绕稻瘟病菌与水稻相互作用机制及病害绿色防控开展工作,主要成果发表在Autophagy、Journal of Nanobiotechnology、Horticulture Research等期刊。

Dr. Yang Li is an associate professor at the College of Plant Protection, Shandong Agricultural University, focusing on plant-microbial interactions, and his main results have been published in journals such as Horticulture Research.

丁新华博士,山东农业大学植物保护学院教授,围绕植物-微生物互作及病害绿色防控开展工作,主要成果发表在Nature Genetics、The Plant Cell、Molecular Plant等期刊。

Professor Shannong Ding Xinhua's team revealed the mechanism of rice's recognition of "self" exosome small proteins, stimulating immunity, and improving broad-spectrum disease resistance

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