Early senescence and cell death in arabidopsis saul1 mutants involves the PAD4-dependent salicylic acid pathway

Plant Physiology

Volumn 159, Issue 4, 2012, Pages 1477-1487

  Vogelmann, Katja ^a   Drechsel, Gabriele ^b,e   Bergler, Johannes ^a   Subert, Christa ^b   Philippar, Katrin ^c   Soll, Jürgen ^c   Engelmann, Julia C ^d   Engelsdorf, Timo ^b   Voll, Lars M ^b   Hoth, Stefan ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF REGENSBURG   (Germany)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84864657734     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.196220     Document Type: Article

References (82)

1. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148-2152
2. 2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol Plant 4: 346-360
3. Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, Zanor MI, Köhler B, Mueller-Roeber B (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62: 250-264
4. Bassham DC (2007) Plant autophagy: more than a starvation response. Curr Opin Plant Biol 10: 587-593
5. Benjamini Y, Hochberg Y (2000) On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Educ Behav Stat 25: 60-83
6. Bisson MM, Bleckmann A, Allekotte S, Groth G (2009) EIN2, the central regulator of ethylene signalling, is localized at the ER membrane where it interacts with the ethylene receptor ETR1. Biochem J 424: 1-6
7. Blanco F, Salinas P, Cecchini NM, Jordana X, Van Hummelen P, Alvarez ME, Holuigue L (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70: 79-102
8. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, et al (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42: 567-585
9. Coates JC (2003) Armadillo repeat proteins: beyond the animal kingdom. Trends Cell Biol 13: 463-471
10. Deeken R, Engelmann JC, Efetova M, Czirjak T, Müller T, Kaiser WM, Tietz O, Krischke M, Mueller MJ, Palme K, et al (2006) An integrated view of gene expression and solute profiles of Arabidopsis tumors: a genome-wide approach. Plant Cell 18: 3617-3634
11. de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bögre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26: 1434-1443
12. Drechsel G, Bergler J, Wippel K, Sauer N, Vogelmann K, Hoth S (2011) C-terminal armadillo repeats are essential and sufficient for association of the plant U-box armadillo E3 ubiquitin ligase SAUL1 with the plasma membrane. J Exp Bot 62: 775-785
13. Duy D, Wanner G, Meda AR, von Wirén N, Soll J, Philippar K (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19: 986-1006
14. Feys BJ, Moisan LJ, Newman MA, Parker JE (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J 20: 5400-5411
15. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
16. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205-227
17. Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143: 973-982
18. González-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JD (2006) The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 18: 1067-1083
19. Grune T, Jung T, Merker K, Davies KJ (2004) Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and 'aggresomes' during oxidative stress, aging, and disease. Int J Biochem Cell Biol 36: 2519-2530
20. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46: 601-612
21. He Y, Gan S (2002) A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. Plant Cell 14: 805-815
22. Hoppe T, Rape M, Jentsch S (2001) Membrane-bound transcription factors: regulated release by RIP or RUP. Curr Opin Cell Biol 13: 344-348
23. Hoth S, Morgante M, Sanchez JP, Hanafey MK, Tingey SV, Chua NH (2002) Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci 115: 4891-4900
24. Huber AH, Nelson WJ, Weis WI (1997) Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell 90: 871-882
25. Huber W, von Heydebreck A, Sültmann H, Poustka A, Vingron M (2002) Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics (Suppl 1) 18: S96-S104
26. Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29: 649-659
27. Hyun DH, Gray DA, Halliwell B, Jenner P (2004) Interference with ubiquitination causes oxidative damage and increased protein nitration: implications for neurodegenerative diseases. J Neurochem 90: 422-430
28. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264
29. Jin Z, Li Y, Pitti R, Lawrence D, Pham VC, Lill JR, Ashkenazi A (2009) Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 137: 721-735
30. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci USA 96: 13583-13588
31. Jirage D, Zhou N, Cooper B, Clarke JD, Dong X, Glazebrook J (2001) Constitutive salicylic acid-dependent signaling in cpr1 and cpr6 mutants requires PAD4. Plant J 26: 395-407
32. Kesarwani M, Yoo J, Dong X (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol 144: 336-346
33. Kim HS, Delaney TP (2002) Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora para-sitica. Plant J 32: 151-163
34. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323: 1053-1057
35. Kim M, Ahn JW, Jin UH, Choi D, Paek KH, Pai HS (2003) Activation of the programmed cell death pathway by inhibition of proteasome function in plants. J Biol Chem 278: 19406-19415
36. Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9: 631-638
37. Lee DH, Choi HW, Hwang BK (2011) The pepper E3 ubiquitin ligase RING1 gene, CaRING1, is required for cell death and the salicylic acid-dependent defense response. Plant Physiol 156: 2011-2025
38. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58: 115-136
39. Lin SS, Martin R, Mongrand S, Vandenabeele S, Chen KC, Jang IC, Chua NH (2008) RING1 E3 ligase localizes to plasma membrane lipid rafts to trigger FB1-induced programmed cell death in Arabidopsis. Plant J 56: 550-561
40. Mateo A, Mühlenbock P, Rustérucci C, Chang CC, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136: 2818-2830
41. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55: 853-867
42. Morris K, MacKerness SA, Page T, John CF, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J 23: 677-685
43. Mosher S, Moeder W, Nishimura N, Jikumaru Y, Joo SH, Urquhart W, Klessig DF, Kim SK, Nambara E, Yoshioka K (2010) The lesion-mimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid-dependent manner. Plant Physiol 152: 1901-1913
44. Mühlenbock P, Szechynska-Hebda M, Plaszczyca M, Baudo M, Mateo A, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2008) Chloro-plast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20: 2339-2356
45. Ng G, Seabolt S, Zhang C, Salimian S, Watkins TA, Lu H (2011) Genetic dissection of salicylic acid-mediated defense signaling networks in Arabidopsis. Genetics 189: 851-859
46. Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301: 969-972
47. Noh YS, Amasino RM (1999) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol Biol 41: 181-194
48. Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287: 795-801
49. Ochsenbein C, Przybyla D, Danon A, Landgraf F, Göbel C, Imboden A, Feussner I, Apel K (2006) The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J 47: 445-456
50. Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 12: 527-535
51. Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76: 789-791
52. Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50: 320-337
53. Phillips AR, Suttangkakul A, Vierstra RD (2008) The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabi-dopsis thaliana. Genetics 178: 1339-1353
54. Raab S, Drechsel G, Zarepour M, Hartung W, Koshiba T, Bittner F, Hoth S (2009) Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. Plant J 59: 39-51
55. Raab S, Toth Z, de Groot C, Stamminger T, Hoth S (2006) ABA-responsive RNA-binding proteins are involved in chloroplast and stromule function in Arabidopsis seedlings. Planta 224: 900-914
56. Rietz S, Stamm A, Malonek S, Wagner S, Becker D, Medina-Escobar N, Vlot AC, Feys BJ, Niefind K, Parker JE (2011) Different roles of Enhanced Disease Susceptibility1 (EDS1) bound to and dissociated from Phytoalexin Deficient4 (PAD4) in Arabidopsis immunity. New Phytol 191: 107-119
57. Riggleman B, Wieschaus E, Schedl P (1989) Molecular analysis of the armadillo locus: uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev 3: 96-113
58. Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16: 1139-1149
59. Rustérucci C, Aviv DH, Holt BF, Dangl JL, Parker JE (2001) The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13: 2211-2224
60. Salt JN, Yoshioka K, Moeder W, Goring DR (2011) Altered germination and subcellular localization patterns for PUB44/SAUL1 in response to stress and phytohormone treatments. PLoS ONE 6: e21321
61. Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55: 555-590
62. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3
63. Stirnberg P, Furner IJ, Ottoline Leyser HM (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50: 80-94
64. Sullivan JA, Shirasu K, Deng XW (2003) The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nat Rev Genet 4: 948-958
65. Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8: 165-173
66. Trujillo M, Ichimura K, Casais C, Shirasu K (2008) Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabi-dopsis. Curr Biol 18: 1396-1401
67. Trujillo M, Shirasu K (2010) Ubiquitination in plant immunity. Curr Opin Plant Biol 13: 402-408
68. van der Graaff E, Schwacke R, Schneider A, Desimone M, Flügge UI, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141: 776-792
69. Vernace VA, Schmidt-Glenewinkel T, Figueiredo-Pereira ME (2007) Aging and regulated protein degradation: who has the UPPer hand? Aging Cell 6: 599-606
70. Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10: 385-397
71. Voll LM, Zell MB, Engelsdorf T, Saur A, Wheeler MG, Drincovich MF, Weber APM, Maurino VG (2012) Loss of cytosolic NADP-malic enzyme 2 in Arabidopsis thaliana is associated with enhanced susceptibility to Colletotrichum higginsianum. New Phytol 195: 189-202
72. Wagstaff C, Yang TJ, Stead AD, Buchanan-Wollaston V, Roberts JA (2009) A molecular and structural characterization of senescing Arabi-dopsis siliques and comparison of transcriptional profiles with senesc-ing petals and leaves. Plant J 57: 690-705
73. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17: 1784-1790
74. Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37: 455-469
75. Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol 8: 383-389
76. Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13: 1779-1790
77. Yee D, Goring DR (2009) The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J Exp Bot 60: 1109-1121
78. Yoshida S (2003) Molecular regulation of leaf senescence. Curr Opin Plant Biol 6: 79-84
79. Yoshida S, Ito M, Callis J, Nishida I, Watanabe A (2002) A delayed leaf senescence mutant is defective in arginyl-tRNA:protein arginyltransferase, a component of the N-end rule pathway in Arabidopsis. Plant J 32: 129-137
80. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21: 2914-2927
81. Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL (2004) 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 16: 2795-2808
82. Zhu S, Jeong RD, Venugopal SC, Lapchyk L, Navarre D, Kachroo A, Kachroo P (2011) SAG101 forms a ternary complex with EDS1 and PAD4 and is required for resistance signaling against turnip crinkle virus. PLoS Pathog 7: e1002318