The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity

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• 作者：Jing Wang (1) (2)
  Baoyuan Qu (3)
  Shijuan Dou (4)
  Liyun Li (4)
  Dedong Yin (1)
  Zhiqian Pang (1) (5)
  Zhuangzhi Zhou (1)
  Miaomiao Tian (1)
  Guozhen Liu (4)
  Qi Xie (1)
  Dingzhong Tang (3)
  Xuewei Chen (2)
  Lihuang Zhu (1)
  
  1. State Key Laboratory of Plant Genomics and National Center for Plant Gene Research ; Institute of Genetics and Developmental Biology ; Chinese Academy of Sciences ; Beijing ; 100101 ; China
  2. Rice Research Institute ; Sichuan Agricultural University ; Chengdu ; Sichuan ; 611130 ; China
  3. State Key Laboratory for Plant Cell and Chromosome Engineering ; Institute of Genetics and Developmental Biology ; Chinese Academy of Sciences ; Beijing ; 100101 ; China
  4. College of Life Sciences ; Hebei Agricultural University ; Baoding ; Hebei ; 071001 ; China
  5. CAS Key Laboratory of Genome Sciences and Information ; Beijing Institute of Genomics ; Chinese Academy of Sciences ; Beijing ; 100029 ; China
  
• 关键词：U ; box ; E3 ligase ; Protein interaction ; Blast resistance ; Cell death ; Rice
• 刊名：BMC Plant Biology
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：15
• 期：1
• 全文大小：2,096 KB
• 参考文献：1. Liu W, Liu J, Ning Y, Ding B, Wang X, Wang Z, et al. Recent progress in understanding PAMP- and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Mol Plant. 2013;6(3):605鈥?0. CrossRef
  2. Dodds PN, Rathjen JP. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet. 2010;11(8):539鈥?8. CrossRef
  3. Nurnberger T, Brunner F. Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol. 2002;5(4):318鈥?4. CrossRef
  4. Medzhitov R, Janeway Jr CA. Innate immunity: the virtues of a nonclonal system of recognition. Cell. 1997;91(3):295鈥?. CrossRef
  5. Abramovitch RB, Anderson JC, Martin GB. Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol. 2006;7(8):601鈥?1. CrossRef
  6. Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol. 2009;60:379鈥?06. CrossRef
  7. Delteil A, Zhang J, Lessard P, Morel J-B. Potential Candidate Genes for Improving Rice Disease Resistance. Rice. 2010;3(1):56鈥?1. CrossRef
  8. Jones JD, Dangl JL. The plant immune system. Nature. 2006;444(7117):323鈥?. CrossRef
  9. Dangl JL, Dietrich RA, Richberg MH. Death Don鈥檛 Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell. 1996;8(10):1793鈥?07. CrossRef
  10. Johal GS, Hulbert SH, Briggs SP. Disease lesion mimics of maize: A model for cell death in plants (pages 685鈥?92). Bioessays. 1995;17:685鈥?2. CrossRef
  11. Moeder W, Yoshioka K. Lesion mimic mutants: A classical, yet still fundamental approach to study programmed cell death. Plant Signal Behav. 2008;3(10):764鈥?. CrossRef
  12. Lorrain S, Vailleau F, Balague C, Roby D. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 2003;8(6):263鈥?1. CrossRef
  13. Mittler R, Rizhsky L. Transgene-induced lesion mimic. Plant Mol Biol. 2000;44(3):335鈥?4. CrossRef
  14. Dreher K, Callis J. Ubiquitin, hormones and biotic stress in plants. Ann Bot. 2007;99(5):787鈥?22. CrossRef
  15. Smalle J, Vierstra RD. The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol. 2004;55:555鈥?0. CrossRef
  16. Vierstra RD. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol. 2009;10(6):385鈥?7. CrossRef
  17. Downes B, Vierstra RD. Post-translational regulation in plants employing a diverse set of polypeptide tags. Biochem Soc Trans. 2005;33(Pt 2):393鈥?.
  18. Stone SL, Callis J. Ubiquitin ligases mediate growth and development by promoting protein death. Curr Opin Plant Biol. 2007;10(6):624鈥?2. CrossRef
  19. Moon J, Parry G, Estelle M. The ubiquitin-proteasome pathway and plant development. Plant Cell. 2004;16(12):3181鈥?5. CrossRef
  20. Hatakeyama S, Nakayama KI. U-box proteins as a new family of ubiquitin ligases. Biochem Biophys Res Commun. 2003;302(4):635鈥?5. CrossRef
  21. Koegl M, Hoppe T, Schlenker S, Ulrich HD, Mayer TU, Jentsch S. A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell. 1999;96(5):635鈥?4. CrossRef
  22. Yee D, Goring DR. The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J Exp Bot. 2009;60(4):1109鈥?1. CrossRef
  23. Zeng LR, Park CH, Venua RC, Goughc J, Wang GL. Classification, Expression Pattern, and E3 Ligase activity Assay of Rice U-Box-Containing Proteins. Mol Plant. 2008;1:800鈥?5. CrossRef
  24. Huber AH, Weis WI. The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell. 2001;105(3):391鈥?02. CrossRef
  25. Liu P, Sherman-Broyles S, Nasrallah ME, Nasrallah JB. A cryptic modifier causing transient self-incompatibility in Arabidopsis thaliana. Curr Biol. 2007;17(8):734鈥?0. CrossRef
  26. Stone SL, Anderson EM, Mullen RT, Goring DR. ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell. 2003;15(4):885鈥?8. CrossRef
  27. Kitano H, Fujioka S, Sakamoto T. An E3 ubiquitin ligase, ERECT LEAF1, functions in brassinosteroid signaling of rice. Plant Signal Behav. 2013;8(11):e27117. CrossRef
  28. Liu YC, Wu YR, Huang XH, Sun J, Xie Q. AtPUB19, a U-box E3 ubiquitin ligase, negatively regulates abscisic acid and drought responses in Arabidopsis thaliana. Mol Plant. 2011;4(6):938鈥?6. CrossRef
  29. Raab S, Drechsel G, Zarepour M, Hartung W, Koshiba T, Bittner F, et al. Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. Plant J. 2009;59(1):39鈥?1. CrossRef
  30. Amador V, Monte E, Garcia-Martinez JL, Prat S. Gibberellins signal nuclear import of PHOR1, a photoperiod-responsive protein with homology to Drosophila armadillo. Cell. 2001;106(3):343鈥?4. CrossRef
  31. Seo DH, Ryu MY, Jammes F, Hwang JH, Turek M, Kang BG, et al. Roles of four Arabidopsis U-box E3 ubiquitin ligases in negative regulation of abscisic acid-mediated drought stress responses. Plant Physiol. 2012;160(1):556鈥?8. CrossRef
  32. Park JJ, Yi J, Yoon J, Cho LH, Ping J, Jeong HJ, et al. OsPUB15, an E3 ubiquitin ligase, functions to reduce cellular oxidative stress during seedling establishment. Plant J. 2011;65(2):194鈥?05. CrossRef
  33. Ni X, Tian Z, Liu J, Song B, Li J, Shi X, et al. StPUB17, a novel potato UND/PUB/ARM repeat type gene, is associated with late blight resistance and NaCl stress. Plant Sci. 2010;178(2):158鈥?9. CrossRef
  34. Cho SK, Ryu MY, Song C, Kwak JM, Kim WT. Arabidopsis PUB22 and PUB23 are homologous U-Box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell. 2008;20(7):1899鈥?14. CrossRef
  35. Cho SK, Chung HS, Ryu MY, Park MJ, Lee MM, Bahk YY, et al. Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-Box E3 ubiquitin ligase homolog. Plant Physiol. 2006;142(4):1664鈥?2. CrossRef
  36. Li W, Ahn IP, Ning Y, Park CH, Zeng L, Whitehill JG, et al. The U-Box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol. 2012;159(1):239鈥?0. CrossRef
  37. Vega-Sanchez ME, Zeng L, Chen S, Leung H, Wang GL. SPIN1, a K homology domain protein negatively regulated and ubiquitinated by the E3 ubiquitin ligase SPL11, is involved in flowering time control in rice. Plant Cell. 2008;20(6):1456鈥?9. CrossRef
  38. Salt JN, Yoshioka K, Moeder W, Goring DR. Altered germination and subcellular localization patterns for PUB44/SAUL1 in response to stress and phytohormone treatments. PLoS One. 2011;6(6):e21321. CrossRef
  39. Trujillo M, Ichimura K, Casais C, Shirasu K. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr Biol. 2008;18(18):1396鈥?01. CrossRef
  40. Yang CW, Gonzalez-Lamothe R, Ewan RA, Rowland O, Yoshioka H, Shenton M, et al. The E3 ubiquitin ligase activity of arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. Plant Cell. 2006;18(4):1084鈥?8. CrossRef
  41. Gonzalez-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JD. The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell. 2006;18(4):1067鈥?3. CrossRef
  42. Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, et al. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell. 2004;16(10):2795鈥?08. CrossRef
  43. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, et al. The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. 2012;13(4):414鈥?0. CrossRef
  44. Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, et al. A B-lectin receptor kinase gene conferring rice blast resistance. Plant J. 2006;46(5):794鈥?04. CrossRef
  45. Ding X, Richter T, Chen M, Fujii H, Seo YS, Xie M, et al. A rice kinase-protein interaction map. Plant Physiol. 2009;149(3):1478鈥?2. CrossRef
  46. Kim M, Cho HS, Kim DM, Lee JH, Pai HS. CHRK1, a chitinase-related receptor-like kinase, interacts with NtPUB4, an armadillo repeat protein, in tobacco. Biochim Biophys Acta. 2003;1651(1鈥?):50鈥?. CrossRef
  47. Wang H, Lu Y, Jiang T, Berg H, Li C, Xia Y. The Arabidopsis U-box/ARM repeat E3 ligase AtPUB4 influences growth and degeneration of tapetal cells, and its mutation leads to conditional male sterility. Plant J. 2013;74(3):511鈥?3. CrossRef
  48. Mudgil Y, Shiu SH, Stone SL, Salt JN, Goring DR. A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family. Plant Physiol. 2004;134(1):59鈥?6. CrossRef
  49. Hatakeyama S, Yada M, Matsumoto M, Ishida N, Nakayama KI. U box proteins as a new family of ubiquitin-protein ligases. J Biol Chem. 2001;276(35):33111鈥?0. CrossRef
  50. Wu C, Bordeos A, Madamba MR, Baraoidan M, Ramos M, Wang GL, et al. Rice lesion mimic mutants with enhanced resistance to diseases. Mol Genet Genomics. 2008;279(6):605鈥?9. CrossRef
  51. Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A, Sugano S, et al. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proc Natl Acad Sci U S A. 2013;110(23):9577鈥?2. CrossRef
  52. Kawano Y, Akamatsu A, Hayashi K, Housen Y, Okuda J, Yao A, et al. Activation of a Rac GTPase by the NLR family disease resistance protein Pit plays a critical role in rice innate immunity. Cell Host Microbe. 2010;7(5):362鈥?5. CrossRef
  53. Jia Y, Martin R. Identification of a new locus, Ptr(t), required for rice blast resistance gene Pi-ta-mediated resistance. Mol Plant-Microbe Interact. 2008;21(4):396鈥?03. CrossRef
  54. Yin Z, Chen J, Zeng L, Goh M, Leung H, Khush GS, et al. Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol Plant-Microbe Interact. 2000;13(8):869鈥?6. CrossRef
  55. Kotchoni SO, Gachomo EW. The reactive oxygen species network pathways: an essential prerequisite for perception of pathogen attack and the acquired disease resistance in plants. J Biosci (Bangalore). 2006;31(3):389鈥?04. CrossRef
  56. Van Breusegem F, Dat JF. Reactive oxygen species in plant cell death. Plant Physiol. 2006;141(2):384鈥?0. CrossRef
  57. Kojo K, Yaeno T, Kusumi K, Matsumura H, Fujisawa S, Terauchi R, et al. Regulatory mechanisms of ROI generation are affected by rice spl mutations. Plant Cell Physiol. 2006;47(8):1035鈥?4. CrossRef
  58. Liu GZ, Pi LY, Walker JC, Ronald PC, Song WY. Biochemical characterization of the kinase domain of the rice disease resistance receptor-like kinase XA21. J Biol Chem. 2002;277(23):20264鈥?. CrossRef
  59. Chen X, Zuo S, Schwessinger B, Chern M, Canlas PE, Ruan D, et al. An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors. Mol Plant. 2014;7(5):874鈥?2. CrossRef
  60. Oh MH, Ray WK, Huber SC, Asara JM, Gage DA, Clouse SD. Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. Plant Physiol. 2000;124(2):751鈥?6. CrossRef
  61. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell. 2002;110(2):213鈥?2. CrossRef
  62. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A, et al. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 2011;7(4):e1002046. CrossRef
  63. Cao Y, Aceti DJ, Sabat G, Song J, Makino S, Fox BG, et al. Mutations in FLS2 Ser-938 dissect signaling activation in FLS2-mediated Arabidopsis immunity. PLoS Path. 2013;9(4):e1003313. CrossRef
  64. Abramovitch RB, Janjusevic R, Stebbins CE, Martin GB. Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Natl Acad Sci U S A. 2006;103(8):2851鈥?. CrossRef
  65. Guais A, Siegrist S, Solhonne B, Jouault H, Guellaen G, Bulle F. h-Goliath, paralog of GRAIL, is a new E3 ligase protein, expressed in human leukocytes. Gene. 2006;374:112鈥?0. CrossRef
  66. Liu T, Liu Z, Song C, Hu Y, Han Z, She J, et al. Chitin-induced dimerization activates a plant immune receptor. Science. 2012;336(6085):1160鈥?. CrossRef
  67. Endres NF, Engel K, Das R, Kovacs E, Kuriyan J. Regulation of the catalytic activity of the EGF receptor. Curr Opin Struct Biol. 2011;21(6):777鈥?4. CrossRef
  68. Petutschnig EK, Jones AM, Serazetdinova L, Lipka U, Lipka V. The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem. 2010;285(37):28902鈥?1. CrossRef
  69. Bae JH, Schlessinger J. Asymmetric tyrosine kinase arrangements in activation or autophosphorylation of receptor tyrosine kinases. Mol Cells. 2010;29(5):443鈥?. CrossRef
  70. Wang X, Li X, Meisenhelder J, Hunter T, Yoshida S, Asami T, et al. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev Cell. 2005;8(6):855鈥?5. CrossRef
  71. Surette MG, Levit M, Liu Y, Lukat G, Ninfa EG, Ninfa A, et al. Dimerization is required for the activity of the protein histidine kinase CheA that mediates signal transduction in bacterial chemotaxis. J Biol Chem. 1996;271(2):939鈥?5. CrossRef
  72. Chen X, Ronald PC. Innate immunity in rice. Trends Plant Sci. 2011;16(8):451鈥?. CrossRef
  73. Dardick C, Ronald P. Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Path. 2006;2(1):e2. CrossRef
  74. Schwessinger B, Ronald PC. Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol. 2012;63:451鈥?2. CrossRef
  75. Dardick C, Schwessinger B, Ronald P. Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures. Curr Opin Plant Biol. 2012;15(4):358鈥?6. CrossRef
  76. Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, et al. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science. 2011;332(6036):1439鈥?2. CrossRef
  77. Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, De Leon AL, et al. Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell. 2006;18(12):3635鈥?6. CrossRef
  78. Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, et al. SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell. 2007;19(6):1912鈥?9. CrossRef
  79. Xie Q, Guo HS, Dallman G, Fang S, Weissman AM, Chua NH. SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature. 2002;419(6903):167鈥?0. CrossRef
  80. Bart R, Chern M, Park CJ, Bartley L, Ronald PC. A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods. 2006;2:13. CrossRef
  81. Lee LY, Fang MJ, Kuang LY, Gelvin SB. Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells. Plant Methods. 2008;4:24. CrossRef
  82. Citovsky V, Lee LY, Vyas S, Glick E, Chen MH, Vainstein A, et al. Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta. J Mol Biol. 2006;362(5):1120鈥?1. CrossRef
  83. Wang Z, Chen CB, Xu YY, Jiang RX, Han Y, Xu ZH, et al. A Practical Vector for Efficient Knockdown of Gene Expression in Rice (Oryza sativa L.). Plant Mol Biol Rep. 2004;22(22):409鈥?7. CrossRef
  84. Hiei Y, Ohta S, Komari T, Kumashiro T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 1994;6(2):271鈥?2. CrossRef
  85. Yang C, Li D, Mao D, Liu X, Ji C, Li X, et al. Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ. 2013;36(12):2207鈥?8. CrossRef
  86. Qiao Y, Jiang W, Lee J, Park B, Choi MS, Piao R, et al. SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit micro 1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa). New Phytol. 2010;185(1):258鈥?4. CrossRef
  87. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28(10):2731鈥?. CrossRef
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background Rice blast disease is one of the most destructive diseases of rice worldwide. We previously cloned the rice blast resistance gene Pid2, which encodes a transmembrane receptor-like kinase containing an extracellular B-lectin domain and an intracellular serine/threonine kinase domain. However, little is known about Pid2-mediated signaling. Results Here we report the functional characterization of the U-box/ARM repeat protein OsPUB15 as one of the PID2-binding proteins. We found that OsPUB15 physically interacted with the kinase domain of PID2 (PID2K) in vitro and in vivo and the ARM repeat domain of OsPUB15 was essential for the interaction. In vitro biochemical assays indicated that PID2K possessed kinase activity and was able to phosphorylate OsPUB15. We also found that the phosphorylated form of OsPUB15 possessed E3 ligase activity. Expression pattern analyses revealed that OsPUB15 was constitutively expressed and its encoded protein OsPUB15 was localized in cytosol. Transgenic rice plants over-expressing OsPUB15 at early stage displayed cell death lesions spontaneously in association with a constitutive activation of plant basal defense responses, including excessive accumulation of hydrogen peroxide, up-regulated expression of pathogenesis-related genes and enhanced resistance to blast strains. We also observed that, along with plant growth, the cell death lesions kept spreading over the whole seedlings quickly resulting in a seedling lethal phenotype. Conclusions These results reveal that the E3 ligase OsPUB15 interacts directly with the receptor-like kinase PID2 and regulates plant cell death and blast disease resistance.