留言板

尊敬的读者、作者、审稿人, 关于本刊的投稿、审稿、编辑和出版的任何问题, 您可以本页添加留言。我们将尽快给您答复。谢谢您的支持!

姓名
邮箱
手机号码
标题
留言内容
验证码

Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae

Xiaojuan Zheng,  Zhaoyang Zhou,  Zhen Gong,  Meijuan Hu,  Ye Jin Ahn,  Xiaojuan Zhang,  Yan Zhao,  Guoshu Gong,  Jian Zhang,  Jianru Zuo,  Guan-Zhu Han,  Sohn Kee Hoon,  Jian-Min Zhou

downloadPDF
文章导航 > 机械工程学报  > 优先出版
Xiaojuan Zheng, Zhaoyang Zhou, Zhen Gong, Meijuan Hu, Ye Jin Ahn, Xiaojuan Zhang, Yan Zhao, Guoshu Gong, Jian Zhang, Jianru Zuo, Guan-Zhu Han, Sohn Kee Hoon, Jian-Min Zhou. Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae[J]. 机械工程学报. doi: 10.1016/j.jgg.2022.06.006
引用本文: Xiaojuan Zheng, Zhaoyang Zhou, Zhen Gong, Meijuan Hu, Ye Jin Ahn, Xiaojuan Zhang, Yan Zhao, Guoshu Gong, Jian Zhang, Jianru Zuo, Guan-Zhu Han, Sohn Kee Hoon, Jian-Min Zhou. Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae[J]. 机械工程学报. doi: 10.1016/j.jgg.2022.06.006
shu
Xiaojuan Zheng, Zhaoyang Zhou, Zhen Gong, Meijuan Hu, Ye Jin Ahn, Xiaojuan Zhang, Yan Zhao, Guoshu Gong, Jian Zhang, Jianru Zuo, Guan-Zhu Han, Sohn Kee Hoon, Jian-Min Zhou. Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae[J]. JOURNAL OF MECHANICAL ENGINEERING. doi: 10.1016/j.jgg.2022.06.006
Citation: Xiaojuan Zheng, Zhaoyang Zhou, Zhen Gong, Meijuan Hu, Ye Jin Ahn, Xiaojuan Zhang, Yan Zhao, Guoshu Gong, Jian Zhang, Jianru Zuo, Guan-Zhu Han, Sohn Kee Hoon, Jian-Min Zhou. Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae[J]. JOURNAL OF MECHANICAL ENGINEERING. doi: 10.1016/j.jgg.2022.06.006
shu

Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae

doi: 10.1016/j.jgg.2022.06.006

  • a. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China;

  • b. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China;

  • c. College of Horticulture, China Agricultural University, Beijing 100193, China;

  • d. College of Life Sciences, Jiangsu Key Laboratory for Microbes and Functional Genomics, Nanjing Normal University, Nanjing, Jiangsu 210023, China;

  • e. Department of Life Sciences, Pohang University of Science and Technology, Pohang 37673, Republic of Korea;

  • f. School of Interdisciplinary Bioscience and Bioengineering, Pohang University of Science and Technology, Pohang 37673, Republic of Korea;

  • g. Plant Protection Department and Major Crop Disease Laboratory, College of Agronomy, Sichuan Agricultural University, Chengdu, Sichuan 611130, China;

  • h. Hainan Yazhou Bay Seed Laboratory, Sanya, Hainan 572025, China

基金项目: 

We thank Yuxin Hu for the sze1 sze2 mutant and Brian Staskawicz for the Nbzar1 mutant. We thank Qi-Jun Chen for providing the CRISPR/Cas9 vectors. The work was supported by grants from the National Key R&

D Program of China (2021YFA1300701) to J.M.Z., the National Natural Science Foundation of China (31872654) to Z.Y.Z., and the Hainan Excellent Talent Team, and the State Key Laboratory of Plant Genomics (SKLPG2016B-2) to J.M.Z.

详细信息
    通讯作者:

    Jian-Min Zhou,E-mail:jmzhou@genetics.ac.cn

Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae

  • a. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100101, China;

  • b. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China;

  • c. College of Horticulture, China Agricultural University, Beijing 100193, China;

  • d. College of Life Sciences, Jiangsu Key Laboratory for Microbes and Functional Genomics, Nanjing Normal University, Nanjing, Jiangsu 210023, China;

  • e. Department of Life Sciences, Pohang University of Science and Technology, Pohang 37673, Republic of Korea;

  • f. School of Interdisciplinary Bioscience and Bioengineering, Pohang University of Science and Technology, Pohang 37673, Republic of Korea;

  • g. Plant Protection Department and Major Crop Disease Laboratory, College of Agronomy, Sichuan Agricultural University, Chengdu, Sichuan 611130, China;

  • h. Hainan Yazhou Bay Seed Laboratory, Sanya, Hainan 572025, China

Funds: 

We thank Yuxin Hu for the sze1 sze2 mutant and Brian Staskawicz for the Nbzar1 mutant. We thank Qi-Jun Chen for providing the CRISPR/Cas9 vectors. The work was supported by grants from the National Key R&

D Program of China (2021YFA1300701) to J.M.Z., the National Natural Science Foundation of China (31872654) to Z.Y.Z., and the Hainan Excellent Talent Team, and the State Key Laboratory of Plant Genomics (SKLPG2016B-2) to J.M.Z.

    摘要
  • 摘要: Pseudomonas syringae pv. actinidiae (Psa) causes bacterial canker, a devastating disease threatening the Actinidia fruit industry. In a search for non-host resistance genes against Psa, we find that the nucleotide-binding leucine-rich repeat receptor (NLR) protein ZAR1 from both Arabidopsis and Nicotiana benthamiana (Nb) recognizes HopZ5 and triggers cell death. The recognition requires ZED1 in Arabidopsis and JIM2 in Nb plants, which are members of the ZRK pseudokinases and known components of the ZAR1 resistosome. Surprisingly, Arabidopsis ZAR1 and RPM1, another NLR known to recognize HopZ5, confer disease resistance to HopZ5 in a strain-specific manner. Thus, ZAR1, but not RPM1, is solely required for resistance to P.s. maculicola ES4326 (Psm) carrying hopZ5, whereas RPM1 is primarily required for resistance to P.s. tomato DC3000 (Pst) carrying hopZ5. Furthermore, the ZAR1-mediated resistance to Psm hopZ5 in Arabidopsis is insensitive to SOBER1, which encodes a deacetylase known to suppress the RPM1-mediated resistance to Pst hopZ5. In addition, hopZ5 enhances P.syringae virulence in the absence of ZAR1 or RPM1 and that SOBER1 abolishes such virulence function. Together the study suggests that ZAR1 may be used for improving Psa resistance in Actinidia and uncovers previously unknown complexity of effector-triggered immunity and effector-triggered virulence.

     

    Abstract: Pseudomonas syringae pv. actinidiae (Psa) causes bacterial canker, a devastating disease threatening the Actinidia fruit industry. In a search for non-host resistance genes against Psa, we find that the nucleotide-binding leucine-rich repeat receptor (NLR) protein ZAR1 from both Arabidopsis and Nicotiana benthamiana (Nb) recognizes HopZ5 and triggers cell death. The recognition requires ZED1 in Arabidopsis and JIM2 in Nb plants, which are members of the ZRK pseudokinases and known components of the ZAR1 resistosome. Surprisingly, Arabidopsis ZAR1 and RPM1, another NLR known to recognize HopZ5, confer disease resistance to HopZ5 in a strain-specific manner. Thus, ZAR1, but not RPM1, is solely required for resistance to P.s. maculicola ES4326 (Psm) carrying hopZ5, whereas RPM1 is primarily required for resistance to P.s. tomato DC3000 (Pst) carrying hopZ5. Furthermore, the ZAR1-mediated resistance to Psm hopZ5 in Arabidopsis is insensitive to SOBER1, which encodes a deacetylase known to suppress the RPM1-mediated resistance to Pst hopZ5. In addition, hopZ5 enhances P.syringae virulence in the absence of ZAR1 or RPM1 and that SOBER1 abolishes such virulence function. Together the study suggests that ZAR1 may be used for improving Psa resistance in Actinidia and uncovers previously unknown complexity of effector-triggered immunity and effector-triggered virulence.

     

    • HTML全文
    • 参考文献(53)
  • Adachi, H., Sakai, T., Kourelis, J., Pai, H., Gonzalez Hernandez, J.L., Maqbool, A., Kamoun, S. (2022). Jurassic NLR:conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1. bioRxiv 2020.10.12.333484
    Axtell, M.J., and Staskawicz, B.J. (2003). Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369-377
    Bi, G., Su, M., Li, N., Liang, Y., Dang, S., Xu, J., Hu, M., Wang, J., Zou, M., Deng, Y., et al., (2021). The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell 184, 3528-3541
    Bisgrove, S.R., Simonich, M.T., Smith, N.M., Sattler, A., Innes, R.W. (1994). A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6, 927-933
    Burger, M., Willige, B.C., Chory, J. (2017). A hydrophobic anchor mechanism defines a deacetylase family that suppresses host response against YopJ effectors. Nature Commun. 8, 2201
    Butler, M.I., Stockwell, P.A., Black, M.A., Day, R.C., Lamont, I.L., Poulter, R.T. (2013). Pseudomonas syringae pv. actinidiae from recent outbreaks of kiwifruit bacterial canker belong to different clones that originated in China. PloS One 8, e57464
    Choi, S., Jayaraman, J., Sohn, K.H. (2018). Arabidopsis thaliana SOBER1 (SUPPRESSOR OF AVRBST-ELICITED RESISTANCE 1) suppresses plant immunity triggered by multiple bacterial acetyltransferase effectors. New Phytol. 219, 324-335
    Choi, S., Prokchorchik, M., Lee, H., Gupta, R., Lee, Y., Chung, E.H., Cho, B., Kim, M.S., Kim, S.T., Sohn, K.H. (2021). Direct acetylation of a conserved threonine of RIN4 by the bacterial effector HopZ5 or AvrBsT activates RPM1-dependent immunity in Arabidopsis. Mol. Plant 14, 1951-1960
    Cui, H., Tsuda, K., Parker, J.E. (2015). Effector-triggered immunity:from pathogen perception to robust defense. Annu. Rev. Plant Boil. 66, 487-511
    Dou, D., Zhou, J.M. (2012). Phytopathogen effectors subverting host immunity:different foes, similar battleground. Cell Host Microbe, 12, 484-495
    Duxbury, Z., Wu, C.H., Ding, P. (2021). A comparative overview of the intracellular guardians of plants and animals:NLRs in innate immunity and beyond. Annu. Rev. Plant Biol. 72, 155-184
    Felix, G., Duran, J.D., Volko, S., and Boller, T. (1999). Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276
    Gomez-Gomez, L., Boller, T. (2000). FLS2:an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003-1011
    Gong, Z., Qi, J., Hu, M., Bi, G., Zhou, J.M., Han, G.Z. (2022). The origin and evolution of a plant resistosome. Plant Cell 34, 1600-1620
    He, P., Shan, L., Sheen, J. (2007). The use of protoplasts to study innate immune responses. Methods Mol. Biol. 354, 1-9
    Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q., Vinh, L.S. (2018). UFBoot2:improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518-522
    Horsefield, S., Burdett, H., Zhang, X., Manik, M.K., Shi, Y., Chen, J., Qi, T., Gilley, J., Lai, J.S., Rank, M. X., et al., (2019). NAD+ cleavage activity by animal and plant TIR domains in cell death pathways. Science 365, 793-799
    Hu, M., Qi, J., Bi, G., Zhou, J.M. (2020). Bacterial effectors induce oligomerization of immune receptor ZAR1 in vivo. Mol. Plant 13, 793-801
    Jacob, P., Kim, N.H., Wu, F., El-Kasmi, F., Chi, Y., Walton, W.G., Furzer, O.J., Lietzan, A.D., Sunil, S., Kempthorn, K., et al., (2021). Plant "helper" immune receptors are Ca2+-permeable nonselective cation channels. Science 373, 420-425
    Jayaraman, J., Choi, S., Prokchorchik, M., Choi, D. S., Spiandore, A., Rikkerink, E.H., Templeton, M.D., Segonzac, C., Sohn, K.H. (2017). A bacterial acetyltransferase triggers immunity in Arabidopsis thaliana independent of hypersensitive response. Sci. Rep. 7, 3557
    Jayaraman, J., Yoon, M., Applegate, E.R., Stroud, E.A., Templeton, M.D. (2020). AvrE1 and HopR1 from Pseudomonas syringae pv. actinidiae are additively required for full virulence on kiwifruit. Mol. Plant Pathol. 21, 1467-1480
    Jubic, L.M., Saile, S., Furzer, O.J., El Kasmi, F., Dangl, J.L. (2019). Help wanted:helper NLRs and plant immune responses. Curr. Opin. Plant Biol. 50, 82-94
    Katoh, K., Standley, D.M. 2013. MAFFT multiple sequence alignment software version 7:improvements in performance and usability. Mol. Biol. Evol. 30, 772-780
    Kirik, A., Mudgett, M.B. (2009). SOBER1 phospholipase activity suppresses phosphatidic acid accumulation and plant immunity in response to bacterial effector AvrBsT. Proc. Natl. Acad. Sci. USA 106, 20532-20537
    Kourelis, J., and van der Hoorn, R. (2018). Defended to the nines:25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30, 285-299
    Laflamme, B., Dillon, M.M., Martel, A., Almeida, R., Desveaux, D., Guttman, D.S. (2020). The pan-genome effector-triggered immunity landscape of a host-pathogen interaction. Science 367, 763-768
    Lapin, D., Bhandari, D.D., Parker, J.E. (2020). Origins and immunity networking functions of EDS1 family proteins. Annu. Rev. Phytopathol. 58, 253-276
    Lewis, J.D., Abada, W., Ma, W., Guttman, D.S., Desveaux, D. (2008). The HopZ family of Pseudomonas syringae type III effectors require myristoylation for virulence and avirulence functions in Arabidopsis thaliana. J. Bacteriol. 190, 2880-2891
    Lewis, J.D., Lee, A.H., Hassan, J.A., Wan, J., Hurley, B., Jhingree, J.R., Wang, P.W., Lo, T., Youn, J.Y., Guttman, D.S., et al., (2013). The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. Proc. Natl. Acad. Sci. USA 110, 18722-18727
    Lewis, J.D., Lee, A., Ma, W., Zhou, H., Guttman, D.S., Desveaux, D. (2011). The YopJ superfamily in plant-associated bacteria. Mol. Plant Pathol. 12, 928-937
    Li, L., Habring, A., Wang, K., Weigel, D. (2020). Atypical resistance protein RPW8/HR triggers oligomerization of the NLR immune receptor RPP7 and autoimmunity. Cell Host Microbe 27, 405-417. e6
    Liu, C., Cui, D., Zhao, J., Liu, N., Wang, B., Liu, J., Xu, E., Hu, Z., Ren, D., Tang, D., et al., (2019). Two Arabidopsis receptor-like cytoplasmic kinases SZE1 and SZE2 associate with the ZAR1-ZED1 complex and are required for effector-triggered immunity. Mol. Plant 12, 967-983
    Ma, S., Lapin, D., Liu, L., Sun, Y., Song, W., Zhang, X., Logemann, E., Yu, D., Wang, J., Jirschitzka, J., et al., (2020). Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science 370, eabe3069
    Macho, A.P., Zumaquero, A., Ortiz-Martin, I., Beuzon, C.R. (2007). Competitive index in mixed infections:a sensitive and accurate assay for the genetic analysis of Pseudomonas syringae-plant interactions. Mol. Plant Pathol. 8, 437-450
    Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R., Dangl, J.L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379-389
    Mackey, D., Holt, B.F., 3rd, Wiig, A., Dangl, J.L. (2002). RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743-754
    Martel, A., Laflamme, B., Seto, D., Bastedo, D.P., Dillon, M.M., Almeida, R., Guttman, D.S., Desveaux, D. (2020). Immunodiversity of the Arabidopsis ZAR1 NLR is conveyed by receptor-like cytoplasmic kinase sensors. Front. Plant Sci. 11, 1290
    Martin, R., Qi, T., Zhang, H., Liu, F., King, M., Toth, C., Nogales, E., Staskawicz, B.J. (2020). Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Science 370, eabd9993
    McCann, H.C., Rikkerink, E.H., Bertels, F., Fiers, M., Lu, A., Rees-George, J., Andersen, M. T., Gleave, A.P., Haubold, B., Wohlers, M. W., et al., (2013). Genomic analysis of the Kiwifruit pathogen Pseudomonas syringae pv. actinidiae provides insight into the origins of an emergent plant disease. PLoS Pathog. 9, e1003503
    Nguyen, L.T., Schmidt, H.A., von Haeseler, A., Minh, B.Q. 2015. IQ-TREE:a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268-274
    Pilkington, S.M., Crowhurst, R., Hilario, E., Nardozza, S., Fraser, L., Peng, Y., Gunaseelan, K., Simpson, R., Tahir, J., Deroles, S.C., et al., (2018). A manually annotated Actinidia chinensis var. chinensis (kiwifruit) genome highlights the challenges associated with draft genomes and gene prediction in plants. BMC Genomics 19, 257
    Price, M.N., Dehal, P.S., Arkin, A.P. (2010). FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5, e9490
    Reuber, T.L., Ausubel, F.M. (1996). Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell 8:241-249
    Schultink, A., Qi, T., Bally, J., Staskawicz, B.J. (2019). Using forward genetics in Nicotiana benthamiana to uncover the immune signaling pathway mediating recognition of the Xanthomonas perforans effector XopJ4. New Phytol. 221, 1001-1009
    Seto, D., Koulena, N., Lo, T., Menna, A., Guttman, D.S., Desveaux, D. (2017). Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases. Nat. Plants 3, 17027
    Tang, W., Sun, X., Yue, J., Tang, X., Jiao, C., Yang, Y., Niu, X., Miao, M., Zhang, D., Huang, S., et al., (2019) Chromosome-scale genome assembly of kiwifruit Actinidia eriantha with single-molecule sequencing and chromatin interaction mapping. GigaScience 8, giz027
    Wan, L., Essuman, K., Anderson, R. G., Sasaki, Y., Monteiro, F., Chung, E.H., Nishimura, E.O., DiAntonio, A., Milbrandt, J., Dangl, J. L., et al., (2019). TIR domains of plant immune receptors are NAD+-cleaving enzymes that promote cell death. Science 365, 799-803
    Wang, G., Roux, B., Feng, F., Guy, E., Li, L., Li, N., Zhang, X., Lautier, M., Jardinaud, M.F., Chabannes, M., et al., (2015a). The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18, 285-295
    Wang, J., Hu, M., Wang, J., Qi, J., Han, Z., Wang, G., Qi, Y., Wang, H. W., Zhou, J.M., Chai, J. (2019). Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364, eaav5870
    Wang, Z. P., Xing, H. L., Dong, L., Zhang, H. Y., Han, C. Y., Wang, X. C., Chen, Q. J. (2015b). Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 16, 144
    Wei, H. L., Zhang, W., Collmer, A. (2018). Modular study of the type III effector repertoire in Pseudomonas syringae pv. tomato DC3000 reveals a matrix of effector interplay in pathogenesis. Cell Rep. 23, 1630-1638
    Wu, H., Ma, T., Kang, M., Ai, F., Zhang, J., Dong, G., Liu, J. (2019). A high-quality Actinidia chinensis (kiwifruit) genome. Hort. Res. 6, 117
    Zhou, H., Morgan, R. L., Guttman, D. S., Ma, W. (2009). Allelic variants of the Pseudomonas syringae type III effector HopZ1 are differentially recognized by plant resistance systems. Mol. Plant Microbe Interact. 22, 176-189
    • 相关文章
    • 施引文献
  • 资源附件(0)
  • 加载中
WeChat 点击查看大图
计量
  • 文章访问数:  69
  • HTML全文浏览量:  41
  • PDF下载量:  0
  • 被引次数: 0
出版历程
  • 收稿日期:  2022-05-13
  • 修回日期:  2022-06-06
  • 录用日期:  2022-06-15
  • 网络出版日期:  2023-03-17

目录

    /

    返回文章
    返回

    Copyright © 2008 北京仁和汇智信息技术有限公司

    地址：邮政编码：100101

    电话：010-84988317，84988356，84988357传真：021-64253812Email：syzt@vip.163.com

    京公网安备 11010502036328号　京ICP备17033152号

    本系统由 北京仁和汇智信息技术有限公司 开发