-Establishment of resistance to various pathogens using immune receptors-
□ Pathogen recognition and resistance formation by plant immune receptors
o Unlike animals, which have immune cells and adaptive immunity, plants recognize pathogens and initiate immune responses with various types of immune receptors present in each cell. Pathogens secrete specific proteins, called effectors, into plant cells to inhibit various plant functions or manipulate them in favor of survival. In response, immune receptors present in plant cells recognize the effector secreted by the pathogen and trigger a strong immune response.
o It has been reported that immune receptors indirectly recognize pathogens by detecting changes in bait proteins in plant cells when recognizing effectors. The most studied decoy protein is a protein called RIN4 found in the cruciferous plant Arabidopsis, and various bacterial effectors change RIN4 through post-translational modifications. The change is recognized by immune receptors called RPS2 and RPM1 and triggers an immune response. Bacterial effectors that induce an immune response in Arabidopsis have been reported to cause a strong immune response in tobacco, a plant of the Solanaceae family. However, recognition mechanisms for these effectors have not been studied in tobacco.
□ Discovery of Ptr1 and ZAR1 that recognize various bacterial effectors
o In this study, to study how bacterial effectors that change RIN4 in Arabidopsis thaliana are recognized in tobacco, effector recognition for 300 known tobacco immune receptors was explored. Virus-induced gene silencing was used to screen many immune receptors in a fast and effective reverse genetics method. As a result, it was found that among the tobacco immune receptors, an immune receptor called Ptr1 recognizes the effectors AvrRpt2, AvrRpm1 and AvrB of the pathogen Pseudomonas.
o Furthermore, it was found that the Pseudomonas effector HopZ5 and the Xanthomonas effector AvrBsT are also recognized by Ptr1, and that these effectors are additionally recognized by another immune receptor called ZAR1 in an independent mechanism. It was also reported that the intensity of the immune response caused by each receptor was different in tobacco and pepper. The important effector of Xanthomonas that causes bacterial spot in tomatoes and peppers is known as AvrBsT, and it was also confirmed that Ptr1 and ZAR1 recognize AvrBsT to form resistance to this pathogen.
□ Convergent evolution of pathogen effector recognition in Arabidopsis and tobacco
o In this study, we reported that effectors recognized in Arabidopsis are recognized by Ptr1 and ZAR1, which have no genetic similarity to Arabidopsis immune receptors RPS2 and RPM1, through convergent evolution in tobacco. Furthermore, the process in which various effectors in tobacco are recognized by one immune receptor Ptr1 seems to be a special recognition mechanism different from the previously reported recognition patterns of immune receptors and effectors. In the future, we plan to explore decoy proteins required for the recognition mechanism of Ptr1 and ZAR1 and proteins involved in immune response. Such studies will give a deeper understanding of how the two receptors form a broad effector recognition spectrum. It is expected that Ptr1 and ZAR1, which recognize various bacterial pathogens, will be utilized in solanaceous crops to greatly contribute to disease resistance and crop protection research. This study was supported by the National Research Foundation of Korea, the Center for Plant Immunity Research at Seoul National University, and the Rural Development Administration, and was published in New Phytologist, an internationally renowned journal.
<서울대학교 손기훈 교수>
Results
Ptr1 and ZAR1 immune receptors confer overlapping and distinct bacterial pathogen effector specificities
Ye Jin Ahn*, Haseong Kim*, Sera Choi*, Carolina Mazo-Molina, Maxim Prokchorchik, Ning Zhang, Boyoung Kim, Hyunggon Mang, Naio Koehler, Jieun Kim, Soeui Lee, Hayeon Yoon, Doil Choi, Min-Sung Kim, Cécile Segonzac, Gregory B. Martin§, Alex Schultink§, and Kee Hoon Sohn§
(New Phytologist; https://doi.org/10.1111/nph.19073)
● Some nucleotide-binding and leucine-rich repeat receptors (NLRs) indirectly detect pathogen effectors by monitoring their host targets. In Arabidopsis thaliana, RIN4 is targeted by multiple sequence-unrelated effectors and activates immune responses mediated by RPM1 and RPS2. These effectors trigger cell death in Nicotiana benthamiana, but the corresponding NLRs have yet not been identified. To identify N. benthamiana NLRs (NbNLRs) that recognize Arabidopsis RIN4-targeting effectors, we conducted a rapid reverse genetic screen using an NbNLR VIGS library.
● We identified that the N. benthamiana homolog of Ptr1 (Pseudomonas tomato race 1) recognizes the Pseudomonas effectors AvrRpt2, AvrRpm1, and AvrB.
● We demonstrated that recognition of the Xanthomonas effector AvrBsT and the Pseudomonas effector HopZ5 is conferred independently by the N. benthamiana homolog of Ptr1 and ZAR1. Interestingly, the recognition of HopZ5 and AvrBsT is contributed unequally by Ptr1 and ZAR1 in N. benthamiana and Capsicum annuum. In addition, we showed that the RLCK XII family protein JIM2 is required for the NbZAR1-dependent recognition of AvrBsT and HopZ5.
● The recognition of sequence-unrelated effectors by NbPtr1 and NbZAR1 provides an additional example of convergently evolved effector recognition. Identification of key components involved in Ptr1 and ZAR1-mediated immunity could reveal unique mechanisms of expanded effector recognition.
● Plant immune receptor nucleotide-binding and leucine-rich repeat receptor (NLR) indirectly recognizes effectors by detecting proteins in plant cells targeted by pathogenic effectors. In Arabidopsis, a protein called RIN4 undergoes post-translational modification by several effectors with no genetic similarity, and this change activates an immune response through RPM1 and RPS2 immune receptors. Effectors targeting RIN4 in Arabidopsis cause an immune response accompanied by apoptosis in tobacco, but immune receptors in tobacco that recognize these effectors have not yet been studied. In order to search for tobacco immune receptors that recognize effectors targeting Arabidopsis RIN4, the NbNLR VIGS library designed by reverse genetics was used.
● As a result, NbPtr1 (Nicotiana benthamiana homolog of Ptr1), which is homologous to Ptr1 (Pseudomonas tomato race 1) found in wild tomatoes, was found to recognize the Pseudomonas effectors AvrRpt2, AvrRpm1, and AvrB.
● It was confirmed that the Xanthomonas effector AvrBsT and the Pseudomonas effector HopZ5 are recognized by NbPtr1 and NbZAR1 as independent mechanisms. What was more interesting was that the recognition of HopZ5 and AvrBsT and the intensity of the immune response in tobacco and pepper differed depending on the immune receptors Ptr1 and ZAR1. We also showed that JIM2, a receptor-like cytoplasmic kinase XII protein, is required for NbZAR1 to recognize HopZ5 and AvrBsT.
● NbPtr1 and NbZAR1, which recognize genetically dissimilar pathogen effectors, show that effector recognition has evolved convergently in various plant species. The study of important proteins that contribute to the immune activation mechanism of Ptr1 and ZAR1 is expected to be important for understanding the mechanism of effector recognition expansion of immune receptors.
Convergent evolution of pathogen effector recognition in Arabidopsis and tobacco
Differences in immune receptors and recognition processes that recognize Pseudomonas effectors AvrRpt2, AvrB, AvrRpm1, and HopZ5 and Xanthomonas effector AvrBsT in Arabidopsis and tobacco were summarized. In Arabidopsis, five effectors undergo post-translational modification of a protein called RIN4, and the changes in RIN4 are detected by RPM1 and RPS2, resulting in an immune response. In contrast, in tobacco, one immune receptor Ptr1 recognizes five effectors, and HopZ5 and AvrBsT are additionally recognized by ZAR1 as an independent mechanism. It has been confirmed that the RLCK XII family protein in plant cells called JIM2 is required for the immune activity of ZAR1.
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