1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Phytopathology
  4. Volume 59, 2021
  5. Article

Annual Review of Phytopathology

Volume 59, 2021

Regulation of Cell Death and Signaling by Pore-Forming Resistosomes

Abstract

Nucleotide-binding leucine-rich repeat receptors (NLRs) are the largest class of immune receptors in plants. They play a key role in the plant surveillance system by monitoring pathogen effectors that are delivered into the plant cell. Recent structural biology and biochemical analyses have uncovered how NLRs are activated to form oligomeric resistosomes upon the recognition of pathogen effectors. In the resistosome, the signaling domain of the NLR is brought to the center of a ringed structure to initiate immune signaling and regulated cell death (RCD). The N terminus of the coiled-coil (CC) domain of the NLR protein HOPZ-ACTIVATED RESISTANCE 1 likely forms a pore in the plasma membrane to trigger RCD in a way analogous to animal pore-forming proteins that trigger necroptosis or pyroptosis. NLRs that carry TOLL-INTERLEUKIN1-RECEPTOR as a signaling domain may also employ pore-forming resistosomes for RCD execution. In addition, increasing evidence supports intimate connections between NLRs and surface receptors in immune signaling. These new findings are rapidly advancing our understanding of the plant immune system.

Keyword(s): immune signaling, ion channel, NLR, plant disease resistance, regulated cell death
Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-020620-095952
2021-08-25
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/phyto/59/1/annurev-phyto-020620-095952.html?itemId=/content/journals/10.1146/annurev-phyto-020620-095952&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adachi H, Contreras MP, Harant A, Wu CH, Derevnina L et al. 2019. An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species. eLife 8:e49956
     [Google Scholar]
  2. 2. 
    Ashikawa I, Hayashi N, Yamane H, Kanamori H, Wu J et al. 2008. Two adjacent nucleotide-binding site–leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics 180:2267–76
     [Google Scholar]
  3. 3. 
    Axtell MJ, Staskawicz BJ. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–77
     [Google Scholar]
  4. 4. 
    Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar S. 1997. Signaling in plant-microbe interactions. Science 276:726–33
     [Google Scholar]
  5. 5. 
    Bastedo DP, Khan M, Martel A, Seto D, Kireeva I et al. 2019. Perturbations of the ZED1 pseudokinase activate plant immunity. PLOS Pathog 15:e1007900
     [Google Scholar]
  6. 6. 
    Bayless AM, Nishimura MT. 2020. Enzymatic functions for Toll/interleukin-1 receptor domain proteins in the plant immune system. Front. Genet 11:539
     [Google Scholar]
  7. 7. 
    Bendahmane A, Farnham G, Moffett P, Baulcombe DC. 2002. Constitutive gain-of-function mutants in a nucleotide binding site–leucine rich repeat protein encoded at the Rx locus of potato. Plant J 32:195–204
     [Google Scholar]
  8. 8. 
    Bentham AR, Zdrzalek R, De la Concepcion JC, Banfield MJ. 2018. Uncoiling CNLs: structure/function approaches to understanding CC domain function in plant NLRs. Plant Cell Physiol 59:2398–408
     [Google Scholar]
  9. 9. 
    Bernoux M, Burdett H, Williams SJ, Zhang X, Chen C et al. 2016. Comparative analysis of the flax immune receptors L6 and L7 suggests an equilibrium-based switch activation model. Plant Cell 28:146–59
     [Google Scholar]
  10. 10. 
    Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379–406
     [Google Scholar]
  11. 11. 
    Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL. 2011. Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. PNAS 108:16463–68
     [Google Scholar]
  12. 12. 
    Botella MA, Parker JE, Frost LN, Bittner-Eddy PD, Beynon JL et al. 1998. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10:1847–60
     [Google Scholar]
  13. 13. 
    Broz P, Pelegrin P, Shao F. 2020. The gasdermins, a protein family executing cell death and inflammation. Nat. Rev. Immunol. 20:143–57
     [Google Scholar]
  14. 14. 
    Burdett H, Bentham AR, Williams SJ, Dodds PN, Anderson PA et al. 2019. The plant “resistosome”: structural insights into immune signaling. Cell Host Microbe 26:193–201
     [Google Scholar]
  15. 15. 
    Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K et al. 2015. Chloroplast stromules function during innate immunity. Dev. Cell 34:45–57
     [Google Scholar]
  16. 16. 
    Catanzariti A-M, Dodds PN, Ve T, Kobe B, Ellis JG, Staskawicz BJ. 2010. The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol. Plant-Microbe Interact. 23:49–57
     [Google Scholar]
  17. 17. 
    Cesari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V et al. 2014. The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J 33:1941–59
     [Google Scholar]
  18. 18. 
    Cesari S, Moore J, Chen C, Webb D, Periyannan S et al. 2016. Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC-NLR proteins. PNAS 113:10204–9
     [Google Scholar]
  19. 19. 
    Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C et al. 2013. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25:1463–81
     [Google Scholar]
  20. 20. 
    Chen X, He W-T, Hu L, Li J, Fang Y et al. 2016. Pyroptosis is driven by non-selective gasdermin-D pore and its morphology is different from MLKL channel-mediated necroptosis. Cell Res 26:1007–20
     [Google Scholar]
  21. 21. 
    Choi HW, Klessig DF. 2016. DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biol 16:232
     [Google Scholar]
  22. 22. 
    Chung E-H, da Cunha L, Wu A-J, Gao Z, Cherkis K et al. 2011. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9:125–36
     [Google Scholar]
  23. 23. 
    Coll NS, Epple P, Dangl JL. 2011. Programmed cell death in the plant immune system. Cell Death Differ 18:1247–56
     [Google Scholar]
  24. 24. 
    Collier SM, Hamel L-P, Moffett P. 2011. Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol. Plant-Microbe Interact. 24:918–31
     [Google Scholar]
  25. 25. 
    Costanzo S, Jia Y. 2010. Sequence variation at the rice blast resistance gene Pi-km locus: implications for the development of allele specific markers. Plant Sci 178:523–30
     [Google Scholar]
  26. 26. 
    Cui H, Tsuda K, Parker JE. 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511
     [Google Scholar]
  27. 27. 
    Daskalov A, Habenstein B, Sabaté R, Berbon M, Martinez D et al. 2016. Identification of a novel cell death-inducing domain reveals that fungal amyloid-controlled programmed cell death is related to necroptosis. PNAS 113:2720–25
     [Google Scholar]
  28. 28. 
    Day B, Dahlbeck D, Huang J, Chisholm ST, Li D, Staskawicz BJ 2005. Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell 17:1292–305
     [Google Scholar]
  29. 29. 
    Deng Y, Zhai K, Xie Z, Yang D, Zhu X et al. 2017. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355:962–65
     [Google Scholar]
  30. 30. 
    Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M et al. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. PNAS 100:8024–29
     [Google Scholar]
  31. 31. 
    Dickman MB, Fluhr R. 2013. Centrality of host cell death in plant-microbe interactions. Annu. Rev. Phytopathol. 51:543–70
     [Google Scholar]
  32. 32. 
    Ding J, Wang K, Liu W, She Y, Sun Q et al. 2016. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535:111–16
     [Google Scholar]
  33. 33. 
    Ding X, Jimenez-Gongora T, Krenz B, Lozano-Duran R. 2019. Chloroplast clustering around the nucleus is a general response to pathogen perception in Nicotiana benthamiana. Mol. Plant Pathol. 20:1298–306
     [Google Scholar]
  34. 34. 
    Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Wang C-I et al. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. PNAS 103:8888–93
     [Google Scholar]
  35. 35. 
    Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11:539–48
     [Google Scholar]
  36. 36. 
    Dou D, Zhou J-M. 2012. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12:484–95
     [Google Scholar]
  37. 37. 
    Durrant WE, Dong X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185–209
     [Google Scholar]
  38. 38. 
    Duxbury Z, Ma Y, Furzer OJ, Huh SU, Cevik V et al. 2016. Pathogen perception by NLRs in plants and animals: parallel worlds. BioEssays 38:769–81
     [Google Scholar]
  39. 39. 
    Duxbury Z, Wang S, MacKenzie CI, Tenthorey JL, Zhang X et al. 2020. Induced proximity of a TIR signaling domain on a plant-mammalian NLR chimera activates defense in plants. PNAS 117:18832–39
     [Google Scholar]
  40. 40. 
    El Kasmi F, Chung E-H, Anderson RG, Li J, Wan L et al. 2017. Signaling from the plasma-membrane localized plant immune receptor RPM1 requires self-association of the full-length protein. PNAS 114:E7385–94
     [Google Scholar]
  41. 41. 
    Essuman K, Summers DW, Sasaki Y, Mao X, DiAntonio A, Milbrandt J. 2017. The SARM1 Toll/interleukin-1 receptor domain possesses intrinsic NAD+ cleavage activity that promotes pathological axonal degeneration. Neuron 93:1334–43e5
     [Google Scholar]
  42. 42. 
    Feng F, Yang F, Rong W, Wu X, Zhang J et al. 2012. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485:114–18
     [Google Scholar]
  43. 43. 
    Fischer NL, Naseer N, Shin S, Brodsky IE. 2020. Effector-triggered immunity and pathogen sensing in metazoans. Nat. Microbiol. 5:14–26
     [Google Scholar]
  44. 44. 
    Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G. 2009. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 10:241–47
     [Google Scholar]
  45. 45. 
    Frost D, Way H, Howles P, Luck J, Manners J et al. 2004. Tobacco transgenic for the flax rust resistance gene L expresses allele-specific activation of defense responses. Mol. Plant-Microbe Interact. 17:224–32
     [Google Scholar]
  46. 46. 
    Gabriels SH, Vossen JH, Ekengren SK, van Ooijen G, Abd-El-Haliem AM et al. 2007. An NB-LRR protein required for HR signalling mediated by both extra- and intracellular resistance proteins. Plant J 50:14–28
     [Google Scholar]
  47. 47. 
    Gantner J, Ordon J, Kretschmer C, Guerois R, Stuttmann J. 2019. An EDS1-SAG101 complex is essential for TNL-mediated immunity in Nicotiana benthamiana. Plant Cell 31:2456–74
     [Google Scholar]
  48. 48. 
    Gao X, Chen X, Lin W, Chen S, Lu D et al. 2013. Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLOS Pathog 9:e1003127
     [Google Scholar]
  49. 49. 
    Gao Y, Wang W, Zhang T, Gong Z, Zhao H, Han G-Z. 2018. Out of water: the origin and early diversification of plant R-genes. Plant Physiol 177:82–89
     [Google Scholar]
  50. 50. 
    Gao Z, Chung E-H, Eitas TK, Dangl JL. 2011. Plant intracellular innate immune receptor Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. PNAS 108:7619–24
     [Google Scholar]
  51. 51. 
    Gassmann W, Hinsch ME, Staskawicz BJ. 1999. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J 20:265–77
     [Google Scholar]
  52. 52. 
    Goritschnig S, Steinbrenner AD, Grunwald DJ, Staskawicz BJ. 2016. Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector. New Phytol 210:984–96
     [Google Scholar]
  53. 53. 
    Grant JJ, Chini A, Basu D, Loake GJ. 2003. Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol. Plant-Microbe Interact. 16:669–80
     [Google Scholar]
  54. 54. 
    Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J 2000. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23:441–50
     [Google Scholar]
  55. 55. 
    Guo H, Ahn HK, Sklenar J, Huang J, Ma Y et al. 2020. Phosphorylation-regulated activation of the Arabidopsis RRS1-R/RPS4 immune receptor complex reveals two distinct effector recognition mechanisms. Cell Host Microbe 27:769–81.e6
     [Google Scholar]
  56. 56. 
    Halff EF, Diebolder CA, Versteeg M, Schouten A, Brondijk TH, Huizinga EG. 2012. Formation and structure of a NAIP5-NLRC4 inflammasome induced by direct interactions with conserved N- and C-terminal regions of flagellin. J. Appl. Biol. Chem. 287:38460–72
     [Google Scholar]
  57. 57. 
    Hander T, Fernandez-Fernandez AD, Kumpf RP, Willems P, Schatowitz H et al. 2019. Damage on plants activates Ca2+-dependent metacaspases for release of immunomodulatory peptides. Science 363:6433eaar7486
     [Google Scholar]
  58. 58. 
    Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K et al. 2009. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23:2496–506
     [Google Scholar]
  59. 59. 
    Hayashi N, Inoue H, Kato T, Funao T, Shirota M et al. 2010. Durable panicle blast-resistance gene Pb1 encodes an atypical CC-NBS-LRR protein and was generated by acquiring a promoter through local genome duplication. Plant J 64:498–510
     [Google Scholar]
  60. 60. 
    He S, Wang L, Miao L, Wang T, Du F et al. 2009. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell 137:1100–11
     [Google Scholar]
  61. 61. 
    Horsefield S, Burdett H, Zhang X, Manik MK, Shi Y et al. 2019. NAD+ cleavage activity by animal and plant TIR domains in cell death pathways. Science 365:793–99
     [Google Scholar]
  62. 62. 
    Hou X, Pedi L, Diver MM, Long SB. 2012. Crystal structure of the calcium release–activated calcium channel Orai. Science 338:1308–13
     [Google Scholar]
  63. 63. 
    Howles P, Lawrence G, Finnegan J, McFadden H, Ayliffe M et al. 2005. Autoactive alleles of the flax L6 rust resistance gene induce non-race-specific rust resistance associated with the hypersensitive response. Mol. Plant-Microbe Interact. 18:570–82
     [Google Scholar]
  64. 64. 
    Hu L, Wu Y, Wu D, Rao W, Guo J et al. 2017. The coiled-coil and nucleotide binding domains of BROWN PLANTHOPPER RESISTANCE14 function in signaling and resistance against planthopper in rice. Plant Cell 29:3157–85
     [Google Scholar]
  65. 65. 
    Hu M, Qi J, Bi G, Zhou JM. 2020. Bacterial effectors induce oligomerization of immune receptor ZAR1 in vivo. Mol. Plant 13:793–801
     [Google Scholar]
  66. 66. 
    Hu Z, Yan C, Liu P, Huang Z, Ma R et al. 2013. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 341:172–75
     [Google Scholar]
  67. 67. 
    Hu Z, Zhou Q, Zhang C, Fan S, Cheng W et al. 2015. Structural and biochemical basis for induced self-propagation of NLRC4. Science 350:399–404
     [Google Scholar]
  68. 68. 
    Hwang C-F, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM. 2000. Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12:1319–29
     [Google Scholar]
  69. 69. 
    Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A et al. 2013. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. PNAS 110:9577–82
     [Google Scholar]
  70. 70. 
    Jones JD, Dangl JL. 2006. The plant immune system. Nature 444:323–29
     [Google Scholar]
  71. 71. 
    Jones JD, Vance RE, Dangl JL. 2016. Intracellular innate immune surveillance devices in plants and animals. Science 354:6316aaf6395
     [Google Scholar]
  72. 72. 
    Jubic LM, Saile S, Furzer OJ, El Kasmi F, Dangl JL. 2019. Help wanted: helper NLRs and plant immune responses. Curr. Opin. Plant Biol. 50:82–94
     [Google Scholar]
  73. 73. 
    Kadota Y, Liebrand TWH, Goto Y, Sklenar J, Derbyshire P et al. 2019. Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector- and PAMP-triggered immunity in plants. New Phytol 221:2160–75
     [Google Scholar]
  74. 74. 
    Kanneganti A, Malireddi R, Saavedra PH, Vande Walle L, Van Gorp H et al. 2018. GSDMD is critical for autoinflammatory pathology in a mouse model of familial Mediterranean fever. J. Exp. Med. 215:1519–29
     [Google Scholar]
  75. 75. 
    Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A et al. 2012. Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J 72:894–907
     [Google Scholar]
  76. 76. 
    Khan M, Subramaniam R, Desveaux D. 2016. Of guards, decoys, baits and traps: pathogen perception in plants by type III effector sensors. Curr. Opin. Microbiol. 29:49–55
     [Google Scholar]
  77. 77. 
    Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S et al. 2005. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121:749–59
     [Google Scholar]
  78. 78. 
    Kofoed EM, Vance RE. 2011. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477:592–95
     [Google Scholar]
  79. 79. 
    Kourelis J, van der Hoorn RAL. 2018. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30:285–99
     [Google Scholar]
  80. 80. 
    Krasileva KV, Dahlbeck D, Staskawicz BJ. 2010. Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22:2444–58
     [Google Scholar]
  81. 81. 
    Krysko O, Love Aaes T, Bachert C, Vandenabeele P, Krysko DV 2013. Many faces of DAMPs in cancer therapy. Cell Death Dis 4:e631
     [Google Scholar]
  82. 82. 
    Künstler A, Bacsó R, Gullner G, Hafez YM, Király L. 2016. Staying alive: Is cell death dispensable for plant disease resistance during the hypersensitive response?. Physiol. Mol. Plant Pathol. 93:75–84
     [Google Scholar]
  83. 83. 
    Laflamme B, Dillon MM, Martel A, Almeida RN, Desveaux D, Guttman DS. 2020. The pan-genome effector-triggered immunity landscape of a host-pathogen interaction. Science 367:763–68
     [Google Scholar]
  84. 84. 
    Lapin D, Bhandari DD, Parker JE. 2020. Origins and immunity networking functions of EDS1 family proteins. Annu. Rev. Phytopathol. 58:253–76
     [Google Scholar]
  85. 85. 
    Lapin D, Kovacova V, Sun X, Dongus JA, Bhandari D et al. 2019. A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. Plant Cell 31:2430–55
     [Google Scholar]
  86. 86. 
    Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D et al. 2015. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161:1074–88
     [Google Scholar]
  87. 87. 
    Leibman-Markus M, Pizarro L, Schuster S, Lin ZJD, Gershony O et al. 2018. The intracellular nucleotide-binding leucine-rich repeat receptor (SlNRC4a) enhances immune signalling elicited by extracellular perception. Plant Cell Environ 41:2313–27
     [Google Scholar]
  88. 88. 
    Lewis JD, Abada W, Ma W, Guttman DS, Desveaux D. 2008. The HopZ family of Pseudomonas syringae type III effectors require myristoylation for virulence and avirulence functions in Arabidopsis thaliana. J. Bacteriol. Res. 190:2880–91
     [Google Scholar]
  89. 89. 
    Lewis JD, Lee AH-Y, Hassan JA, Wan J, Hurley B et al. 2013. The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. PNAS 110:18722–27
     [Google Scholar]
  90. 90. 
    Li B, Meng X, Shan L, He P. 2016. Transcriptional regulation of pattern-triggered immunity in plants. Cell Host Microbe 19:641–50
     [Google Scholar]
  91. 91. 
    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 27:405–17.e6
     [Google Scholar]
  92. 92. 
    Li M, Ma X, Chiang Y-H, Yadeta KA, Ding P et al. 2014. Proline isomerization of the immune receptor-interacting protein RIN4 by a cyclophilin inhibits effector-triggered immunity in Arabidopsis. Cell Host Microbe 16:473–83
     [Google Scholar]
  93. 93. 
    Li X, Clarke JD, Zhang Y, Dong X. 2001. Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol. Plant-Microbe Interact. 14:1131–39
     [Google Scholar]
  94. 94. 
    Li X, Kapos P, Zhang Y. 2015. NLRs in plants. Curr. Opin. Immunol. 32:114–21
     [Google Scholar]
  95. 95. 
    Liang X, Zhou J-M. 2018. Receptor-like cytoplasmic kinases: central players in plant receptor kinase–mediated signaling. Annu. Rev. Plant Biol. 69:267–99
     [Google Scholar]
  96. 96. 
    Liu C, Cui D, Zhao J, Liu N, Wang B 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 12:967–83
     [Google Scholar]
  97. 97. 
    Liu J, Elmore JM, Lin Z-JD, Coaker G. 2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:137–46
     [Google Scholar]
  98. 98. 
    Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L et al. 2015. Fungal effectors and plant susceptibility. Annu. Rev. Plant Biol. 66:513–45
     [Google Scholar]
  99. 99. 
    Lolle S, Greeff C, Petersen K, Roux M, Jensen MK et al. 2017. Matching NLR immune receptors to autoimmunity in camta3 mutants using antimorphic NLR alleles. Cell Host Microbe 21:518–29.e4
     [Google Scholar]
  100. 100. 
    Lu D, Wu S, Gao X, Zhang Y, Shan L, He P. 2010. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. PNAS 107:496–501
     [Google Scholar]
  101. 101. 
    Lu X, Kracher B, Saur IM, Bauer S, Ellwood SR et al. 2016. Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen. PNAS 113:E6486–95
     [Google Scholar]
  102. 102. 
    Ma S, Lapin D, Liu L, Sun Y, Song W et al. 2020. Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science 370:6521eabe3069
     [Google Scholar]
  103. 103. 
    Ma Y, Guo H, Hu L, Martinez PP, Moschou PN et al. 2018. Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors. PNAS 115:10218–27
     [Google Scholar]
  104. 104. 
    Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–89
     [Google Scholar]
  105. 105. 
    Mackey D, Holt BF III, Wiig A, Dangl JL. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–54
     [Google Scholar]
  106. 106. 
    Maekawa T, Cheng W, Spiridon LN, Toller A, Lukasik E et al. 2011. Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe 9:187–99
     [Google Scholar]
  107. 107. 
    Mahdi LK, Huang M, Zhang X, Nakano RT, Kopp LB et al. 2020. Discovery of a family of mixed lineage kinase domain-like proteins in plants and their role in innate immune signaling. Cell Host Microbe 28:6813–24.e6
     [Google Scholar]
  108. 108. 
    Maqbool A, Saitoh H, Franceschetti M, Stevenson C, Uemura A et al. 2015. Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor. eLife 4:e08709
     [Google Scholar]
  109. 109. 
    Martel A, Laflamme B, Seto D, Bastedo DP, Dillon MM et al. 2020. Immunodiversity of the Arabidopsis ZAR1 NLR is conveyed by receptor-like cytoplasmic kinase sensors. Front. Plant Sci. 11:1290
     [Google Scholar]
  110. 110. 
    Martin R, Qi T, Zhang H, Liu F, King M et al. 2020. Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Science 370:6521eabd9993
     [Google Scholar]
  111. 111. 
    Mestre P, Baulcombe DC. 2006. Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:491–501
     [Google Scholar]
  112. 112. 
    Muñoz-Planillo R, Kuffa P, Martínez-Colón G, Smith BL, Rajendiran TM, Núñez G. 2013. K+ efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 38:1142–53
     [Google Scholar]
  113. 113. 
    Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E 2008. The hypersensitive response; the centenary is upon us but how much do we know?. J. Exp. Bot. 59:501–20
     [Google Scholar]
  114. 114. 
    Murphy JM, Czabotar PE, Hildebrand JM, Lucet IS, Zhang JG et al. 2013. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39:443–53
     [Google Scholar]
  115. 115. 
    Ngou BPM, Ahn H-K, Ding P, Jones JDG. 2020. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. bioRxiv 034173 https://doi.org/10.1101/2020.04.10.034173
  116. 116. 
    Okuyama Y, Kanzaki H, Abe A, Yoshida K, Tamiru M et al. 2011. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J 66:467–79
     [Google Scholar]
  117. 117. 
    Oxenoid K, Dong Y, Cao C, Cui T, Sancak Y et al. 2016. Architecture of the mitochondrial calcium uniporter. Nature 533:269–73
     [Google Scholar]
  118. 118. 
    Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. 2013. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLOS Pathog 9:e1003235
     [Google Scholar]
  119. 119. 
    Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC. 2005. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr. Biol. 15:968–73
     [Google Scholar]
  120. 120. 
    Peng W, Shen H, Wu J, Guo W, Pan X et al. 2016. Structural basis for the gating mechanism of the type 2 ryanodine receptor RyR2. Science 354:6310aah5324
     [Google Scholar]
  121. 121. 
    Petrie EJ, Czabotar PE, Murphy JM. 2019. The structural basis of necroptotic cell death signaling. Trends Biochem. Sci. 44:53–63
     [Google Scholar]
  122. 122. 
    Petrie EJ, Sandow JJ, Jacobsen AV, Smith BJ, Griffin MDW et al. 2018. Conformational switching of the pseudokinase domain promotes human MLKL tetramerization and cell death by necroptosis. Nat. Commun. 9:2422
     [Google Scholar]
  123. 123. 
    Pruitt RN, Zhang L, Saile SC, Karelina D, Fröhlich K et al. 2020. Arabidopsis cell surface LRR immune receptor signaling through the EDS1-PAD4-ADR1 node. bioRxiv 391516 https://doi.org/10.1101/2020.11.23.391516
  124. 124. 
    Qi D, DeYoung BJ, Innes RW. 2012. Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol 158:1819–32
     [Google Scholar]
  125. 125. 
    Qi J, Wang J, Gong Z, Zhou J-M. 2017. Apoplastic ROS signaling in plant immunity. Curr. Opin. Plant Biol. 38:92–100
     [Google Scholar]
  126. 126. 
    Qi T, Seong K, Thomazella DPT, Kim JR, Pham J et al. 2018. NRG1 functions downstream of EDS1 to regulate TIR-NLR-mediated plant immunity in Nicotiana benthamiana. PNAS 115:E10979–87
     [Google Scholar]
  127. 127. 
    Rairdan GJ, Moffett P. 2006. Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18:2082–93
     [Google Scholar]
  128. 128. 
    Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR et al. 2005. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17:1839–50
     [Google Scholar]
  129. 129. 
    Roberts M, Tang S, Stallmann A, Dangl JL, Bonardi V. 2013. Genetic requirements for signaling from an autoactive plant NB-LRR intracellular innate immune receptor. PLOS Genet 9:e1003465
     [Google Scholar]
  130. 130. 
    Ruan J, Xia S, Liu X, Lieberman J, Wu H. 2018. Cryo-EM structure of the gasdermin A3 membrane pore. Nature 557:62–67
     [Google Scholar]
  131. 131. 
    Saile SC, Jacob P, Castel B, Jubic LM, Salas-Gonzales I et al. 2020. Two unequally redundant “helper” immune receptor families mediate Arabidopsis thaliana intracellular “sensor” immune receptor functions. PLOS Biol 18:e3000783
     [Google Scholar]
  132. 132. 
    Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C et al. 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:1089–100
     [Google Scholar]
  133. 133. 
    Schultink A, Qi T, Bally J, Staskawicz B. 2019. Using forward genetics in Nicotiana benthamiana to uncover the immune signaling pathway mediating recognition of the Xanthomonas perforans effector XopJ4. New Phytol 221:1001–9
     [Google Scholar]
  134. 134. 
    Schultink A, Qi T, Lee A, Steinbrenner AD, Staskawicz B. 2017. Roq1 mediates recognition of the Xanthomonas and Pseudomonas effector proteins XopQ and HopQ1. Plant J 92:787–95
     [Google Scholar]
  135. 135. 
    Schwartz AR, Potnis N, Timilsina S, Wilson M, Patané J et al. 2015. Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front. Microbiol. 6:535
     [Google Scholar]
  136. 136. 
    Seto D, Koulena N, Lo T, Menna A, Guttman DS, Desveaux D. 2017. Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases. Nat. Plants 3:17027
     [Google Scholar]
  137. 137. 
    Shen Q-H, Saijo Y, Mauch S, Biskup C, Bieri S et al. 2007. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315:1098–103
     [Google Scholar]
  138. 138. 
    Shen W, Liu J, Li JF. 2019. Type-II metacaspases mediate the processing of plant elicitor peptides in Arabidopsis. Mol. Plant 12:1524–33
     [Google Scholar]
  139. 139. 
    Shi J, Zhao Y, Wang K, Shi X, Wang Y et al. 2015. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526:660–65
     [Google Scholar]
  140. 140. 
    Shirano Y, Kachroo P, Shah J, Klessig DF. 2002. A gain-of-function mutation in an Arabidopsis Toll interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 14:3149–62
     [Google Scholar]
  141. 141. 
    Sohn KH, Segonzac C, Rallapalli G, Sarris PF, Woo JY et al. 2014. The nuclear immune receptor RPS4 is required for RRS1 SLH1-dependent constitutive defense activation in Arabidopsis thaliana. PLOS Genet 10:e1004655
     [Google Scholar]
  142. 142. 
    Steinbrenner AD, Goritschnig S, Staskawicz BJ. 2015. Recognition and activation domains contribute to allele-specific responses of an Arabidopsis NLR receptor to an oomycete effector protein. PLOS Pathog 11:e1004665
     [Google Scholar]
  143. 143. 
    Steuernagel B, Witek K, Krattinger S, Ramirez-Gonzalez R, Schoonbeek H et al. 2018. Physical and transcriptional organisation of the bread wheat intracellular immune receptor repertoire. bioRxiv 339424 https://doi.org/10.1101/339424
  144. 144. 
    Su J, Yang L, Zhu Q, Wu H, He Y et al. 2018. Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity. PLOS Biol 16:e2004122
     [Google Scholar]
  145. 145. 
    Su L, Quade B, Wang H, Sun L, Wang X, Rizo J 2014. A plug release mechanism for membrane permeation by MLKL. Structure 22:1489–500
     [Google Scholar]
  146. 146. 
    Sun Q, Collins NC, Ayliffe M, Smith SM, Drake J et al. 2001. Recombination between paralogues at the Rp1 rust resistance locus in maize. Genetics 158:423–38
     [Google Scholar]
  147. 147. 
    Sun T, Zhang Y, Li Y, Zhang Q, Ding Y, Zhang Y. 2015. ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nat. Commun. 6:10159
     [Google Scholar]
  148. 148. 
    Tameling WI, Elzinga SD, Darmin PS, Vossen JH, Takken FL et al. 2002. The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14:2929–39
     [Google Scholar]
  149. 149. 
    Tang D, Kang R, Berghe TV, Vandenabeele P, Kroemer G. 2019. The molecular machinery of regulated cell death. Cell Res 29:347–64
     [Google Scholar]
  150. 150. 
    Tang D, Wang G, Zhou J-M. 2017. Receptor kinases in plant-pathogen interactions: more than pattern recognition. Plant Cell 29:618–37
     [Google Scholar]
  151. 151. 
    Tenthorey JL, Haloupek N, López-Blanco JR, Grob P, Adamson E et al. 2017. The structural basis of flagellin detection by NAIP5: a strategy to limit pathogen immune evasion. Science 358:888–93
     [Google Scholar]
  152. 152. 
    Torres MA, Dangl JL, Jones JD. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. PNAS 99:517–22
     [Google Scholar]
  153. 153. 
    Van de Weyer A-L, Monteiro F, Furzer OJ, Nishimura MT, Cevik V et al. 2019. A species-wide inventory of NLR genes and alleles in Arabidopsis thaliana. Cell 178:1260–72.e14
     [Google Scholar]
  154. 154. 
    van Wersch R, Li X, Zhang Y 2016. Mighty dwarfs: Arabidopsis autoimmune mutants and their usages in genetic dissection of plant immunity. Front. Plant Sci. 7:1717
     [Google Scholar]
  155. 155. 
    Wan L, Essuman K, Anderson RG, Sasaki Y, Monteiro F et al. 2019. TIR domains of plant immune receptors are NAD+-cleaving enzymes that promote cell death. Science 365:799–803
     [Google Scholar]
  156. 156. 
    Wang G, Roux B, Feng F, Guy E, Li L et al. 2015. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:285–95
     [Google Scholar]
  157. 157. 
    Wang J, Chen T, Han M, Qian L, Li J et al. 2020. Plant NLR immune receptor Tm-22 activation requires NB-ARC domain-mediated self-association of CC domain. PLOS Pathog 16:e1008475
     [Google Scholar]
  158. 158. 
    Wang J, Hu M, Wang J, Qi J, Han Z et al. 2019. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364:6435eaav5870
     [Google Scholar]
  159. 159. 
    Wang J, Wang J, Hu M, Wu S, Qi J et al. 2019. Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364:6435eaav5868
     [Google Scholar]
  160. 160. 
    Wei CF, Kvitko BH, Shimizu R, Crabill E, Alfano JR et al. 2007. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J 51:32–46
     [Google Scholar]
  161. 161. 
    Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF et al. 2014. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344:299–303
     [Google Scholar]
  162. 162. 
    Williams SJ, Sornaraj P, deCourcy-Ireland E, Menz RI, Kobe B et al. 2011. An autoactive mutant of the M flax rust resistance protein has a preference for binding ATP, whereas wild-type M protein binds ADP. Mol. Plant-Microbe Interact. 24:897–906
     [Google Scholar]
  163. 163. 
    Wu C-H, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R et al. 2017. NLR network mediates immunity to diverse plant pathogens. PNAS 114:8113–18
     [Google Scholar]
  164. 164. 
    Wu C-H, Belhaj K, Bozkurt TO, Birk MS, Kamoun S. 2016. Helper NLR proteins NRC 2a/b and NRC 3 but not NRC 1 are required for Pto-mediated cell death and resistance in Nicotiana benthamiana. New Phytol 209:1344–52
     [Google Scholar]
  165. 165. 
    Wu C-H, Derevnina L, Kamoun S. 2018. Receptor networks underpin plant immunity. Science 360:1300–1
     [Google Scholar]
  166. 166. 
    Wu Y, Gao Y, Zhan Y, Kui H, Liu H et al. 2020. Loss of the common immune coreceptor BAK1 leads to NLR-dependent cell death. PNAS 117:27044–53
     [Google Scholar]
  167. 167. 
    Wu Z, Li M, Dong OX, Xia S, Liang W et al. 2019. Differential regulation of TNL-mediated immune signaling by redundant helper CNLs. New Phytol 222:938–53
     [Google Scholar]
  168. 168. 
    Xia B, Fang S, Chen X, Hu H, Chen P et al. 2016. MLKL forms cation channels. Cell Res 26:517–28
     [Google Scholar]
  169. 169. 
    Xiao J, Wang C, Yao J-C, Alippe Y, Xu C et al. 2018. Gasdermin D mediates the pathogenesis of neonatal-onset multisystem inflammatory disease in mice. PLOS Biol 16:e3000047
     [Google Scholar]
  170. 170. 
    Xie T, Peng W, Yan C, Wu J, Gong X, Shi Y. 2013. Structural insights into RIP3-mediated necroptotic signaling. Cell Rep 5:70–78
     [Google Scholar]
  171. 171. 
    Xiong Y, Han Z, Chai J. 2020. Resistosome and inflammasome: platforms mediating innate immunity. Curr. Opin. Plant Biol. 56:47–55
     [Google Scholar]
  172. 172. 
    Xu F, Kapos P, Cheng YT, Li M, Zhang Y, Li X. 2014. NLR-associating transcription factor bHLH84 and its paralogs function redundantly in plant immunity. PLOS Pathog 10:e1004312
     [Google Scholar]
  173. 173. 
    Yamada K, Yamashita-Yamada M, Hirase T, Fujiwara T, Tsuda K et al. 2016. Danger peptide receptor signaling in plants ensures basal immunity upon pathogen-induced depletion of BAK 1. EMBO J 35:46–61
     [Google Scholar]
  174. 174. 
    Yang X, Yang F, Wang W, Lin G, Hu Z et al. 2018. Structural basis for specific flagellin recognition by the NLR protein NAIP5. Cell Res 28:35–47
     [Google Scholar]
  175. 175. 
    Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H et al. 2009. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21:1573–91
     [Google Scholar]
  176. 176. 
    Yuan M, Jiang Z, Bi G, Nomura K, Liu M et al. 2020. Pattern-recognition receptors are required for NLR-mediated plant immunity. bioRxiv 031294. https://doi.org/10.1101/2020.04.10.031294
  177. 177. 
    Zhai K, Deng Y, Liang D, Tang J, Liu J et al. 2019. RRM transcription factors interact with NLRs and regulate broad-spectrum blast resistance in rice. Mol. Cell 74:996–1009.e7
     [Google Scholar]
  178. 178. 
    Zhang D-W, Shao J, Lin J, Zhang N, Lu B-J et al. 2009. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325:332–36
     [Google Scholar]
  179. 179. 
    Zhang J, Li W, Xiang T, Liu Z, Laluk K et al. 2010. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301
     [Google Scholar]
  180. 180. 
    Zhang L, Chen S, Ruan J, Wu J, Tong AB et al. 2015. Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization. Science 350:404–9
     [Google Scholar]
  181. 181. 
    Zhang X, Dodds PN, Bernoux M. 2017. What do we know about NOD-like receptors in plant immunity?. Annu. Rev. Phytopathol. 55:205–29
     [Google Scholar]
  182. 182. 
    Zhang Y, Chen X, Gueydan C, Han J. 2018. Plasma membrane changes during programmed cell deaths. Cell Res 28:9–21
     [Google Scholar]
  183. 183. 
    Zhang Y, Goritschnig S, Dong X, Li X 2003. A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1–1, constitutive 1. Plant Cell 15:2636–46
     [Google Scholar]
  184. 184. 
    Zhang Y, Han J. 2016. Electrophysiologist shows a cation channel function of MLKL. Cell Res 26:643–44
     [Google Scholar]
  185. 185. 
    Zhang Y, Xu S, Ding P, Wang D, Cheng YT et al. 2010. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. PNAS 107:18220–25
     [Google Scholar]
  186. 186. 
    Zhu Z, Xu F, Zhang Y, Cheng YT, Wiermer M et al. 2010. Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. PNAS 107:13960–65
     [Google Scholar]
  187. 187. 
    Zipfel C, Oldroyd GE. 2017. Plant signalling in symbiosis and immunity. Nature 543:328–36
     [Google Scholar]
/content/journals/10.1146/annurev-phyto-020620-095952
Loading
Regulation of Cell Death and Signaling by Pore-Forming Resistosomes
Annual Review of Phytopathology 59, 239 (2021); https://doi.org/10.1146/annurev-phyto-020620-095952
/content/journals/10.1146/annurev-phyto-020620-095952
/content/journals/10.1146/annurev-phyto-020620-095952
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error