Regulation of plant defense responses in Arabidopsis by EDR2, a PH and START domain-containing protein

Plant Journal

Volumn 44, Issue 2, 2005, Pages 245-257

  Tang, Dingzhong ^a   Ade, Jules ^a   Frye, Catherine A ^a,b   Innes, Roger W ^a  

^a INDIANA UNIVERSITY   (United States)

^b SYNGENTA CROP PROTECTION   (United States)

Author keywords

Defense responses; Disease resistance; Powdery mildew; Programmed cell death; Salicylic acid; Senescence

Indexed keywords

CARBOXYLIC ACIDS; DISEASES; ENZYME INHIBITION; FUNGI; TISSUE;

DEFENSE RESPONSES; DISEASE RESISTANCE; SENESCENCE;

PLANT CELL CULTURE;

CARBOXYLIC ACIDS; DISEASES; ENZYMATIC ACTIVITY; PLANTS; SALICYLIC ACID; TISSUE;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); ERYSIPHALES; FUNGI; GOLOVINOMYCES CICHORACEARUM; LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO;

ARABIDOPSIS PROTEIN; ERD2 PROTEIN, ARABIDOPSIS; MEMBRANE PROTEIN; PHYTOHORMONE; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; ASCOMYCETES; CHEMISTRY; CHROMOSOME MAP; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETIC PREDISPOSITION; GENETICS; METABOLISM; MICROBIOLOGY; MITOCHONDRION; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PLANT DISEASE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; CHROMOSOME MAPPING; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; GENETIC PREDISPOSITION TO DISEASE; MEMBRANE PROTEINS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; PLANT DISEASES; PLANT GROWTH REGULATORS; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

EID: 33644796704     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02523.x     Document Type: Article

References (75)

1. Adam L. Somerville S.C. ( 1996) Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J. 9, 341 356.
2. Adam L. Ellwood S. Wilson I. Saenz G. Xiao S. Oliver R.P. Turner J.G. Somerville S. ( 1999) Comparison of Erysiphe cichoracearum and E. cruciferarum and a survey of 360 Arabidopsis thaliana accessions for resistance to these two powdery mildew pathogens. Mol. Plant Microbe Interact. 12, 1031 1043.
3. Alonso J.M. Hirayama T. Roman G. Nourizadeh S. Ecker J.R. ( 1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science, 284, 2148 2152.
4. Alonso J.M. Stepanova A.N. Leisse T.J. et al. ( 2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
5. Altschul S.F. Madden T.L. Schäffer A.A. Zhang J. Zhang Z. Miller W. Lipman D.J. ( 1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389 3402.
6. Ashfield T. Danzer J.R. Held D. Clayton K. Keim P. Saghai Maroof M.A. Webb P.M. Innes R.W. ( 1998) Rpg1, a soybean gene effective against races of bacterial blight, maps to a cluster of previously identified disease resistance genes. Theor. Appl. Genet. 96, 1013 1021.
7. Bancroft I. Love K. Bent E. Sherson S. Lister C. Cobbett C. Goodman H.M. Dean C. ( 1997) A strategy involving the use of high redundancy YAC subclone libraries facilitates the contiguous representation in cosmid and BAC clones of 1.7 Mb of the genome of the plant Arabidopsis thaliana. Weeds World, 4ii, 1 9.
8. Bannai H. Tamada Y. Maruyama O. Nakai K. Miyano S. ( 2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics, 18, 298 305.
9. Bowling S.A. Guo A. Cao H. Gordon A.S. Klessig D.F. Dong X. ( 1994) A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell, 6, 1845 1857.
10. Bowling S.A. Clarke J.D. Liu Y. Klessig D.F. Dong X. ( 1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1- independent resistance. Plant Cell, 9, 1573 1584.
11. Cao H. Glazebrook J. Clarke J.D. Volko S. Dong X. ( 1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell, 88, 57 63.
12. Clarke J.D. Liu Y. Klessig D.F. Dong X. ( 1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell, 10, 557 569.
13. Clarke J.D. Volko S.M. Ledford H. Ausubel F.M. Dong X. ( 2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell, 12, 2175 2190.
14. Clough S.J. Bent A.F. ( 1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
15. Consortium I.H.G. ( 2001) Initial sequencing and analysis of the human genome. Nature, 409, 860 921.
16. Delaney T.P. Friedrich L. Ryals J.A. ( 1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl Acad. Sci. USA, 92, 6602 6606.
17. Dong X. ( 1998) SA, JA, ethylene, and disease resistance in plants. Curr. Opin. Plant Biol. 1, 316 323.
18. Emanuelsson O. Nielsen H. Brunak S. von Heijne G. ( 2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005 1016.
19. Falk A. Feys B.J. Frost L.N. Jones J.D. Daniels M.J. Parker J.E. ( 1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl Acad. Sci. USA, 96, 3292 3297.
20. Ferri K.F. Kroemer G. ( 2001) Mitochondria-the suicide organelles. BioEssays, 23, 111 115.
21. Feys B.J.F. Benedetti C.E. Penfold C.N. Turner J.G. ( 1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate and resistant to a bacterial pathogen. Plant Cell, 6, 751 759.
22. Frye C.A. Innes R.W. ( 1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell, 10, 947 956.
23. Frye C.A. Tang D. Innes R.W. ( 2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl Acad. Sci. USA, 98, 373 378.
24. Glazebrook J. Zook M. Mert F. Kagan I. Rogers E.E. Crute I.R. Holub E.B. Hammerschmidt R. Ausubel F.M. ( 1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics, 146, 381 392.
25. Green D.R. ( 2000) Apoptotic pathways: paper wraps stone blunts scissors. Cell, 102, 1 4.
26. Hanada K. Kumagai K. Yasuda S. Miura Y. Kawano M. Fukasawa M. Nishijima M. ( 2003) Molecular machinery for non-vesicular trafficking of ceramide. Nature, 426, 803 809.
27. Hannun Y.A. Luberto C. ( 2000) Ceramide in the eukaryotic stress response. Trends Cell Biol. 10, 73 80.
28. Haslam R.J. Koide H.B. Hemmings B.A. ( 1993) Pleckstrin domain homology. Nature, 363, 309 310.
29. Jefferson R.A. Kavanagh T.A. Bevan M.W. ( 1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901 3907.
30. Jirage D. Tootle T.L. Reuber T.L. Frost L.N. Feys B.J. Parker J.E. Ausubel F.M. 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. Kachroo P. Shanklin J. Shah J. Whittle E.J. Klessig D.F. ( 2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc. Natl Acad. Sci. USA, 98, 9448 9453.
32. Kachroo A. Venugopal S.C. Lapchyk L. Falcone D. Hildebrand D. Kachroo P. ( 2004) Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc. Natl Acad. Sci. USA, 101, 5152 5157.
33. Koch E. Slusarenko A. ( 1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell, 2, 437 445.
34. Lacomme C. Santa Cruz S. ( 1999) Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc. Natl Acad. Sci. USA, 96, 7956 7961.
35. Leister R.T. Ausubel F.M. Katagiri F. ( 1996) Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. Proc. Natl Acad. Sci. USA, 93, 15497 15502.
36. Lemmon M.A. ( 2003) Phosphoinositide recognition domains. Traffic, 4, 201 213.
37. Lemmon M.A. Ferguson K.M. Abrams C.S. ( 2002) Pleckstrin homology domains and the cytoskeleton. FEBS Lett. 513, 71 76.
38. Liang H. Yao N. Song J.T. Luo S. Lu H. Greenberg J.T. ( 2003) Ceramides modulate programmed cell death in plants. Genes Dev. 17, 2636 2641.
39. Loewen C.J. Roy A. Levine T.P. ( 2003) A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 22, 2025 2035.
40. Maffucci T. Falasca M. ( 2001) Specificity in pleckstrin homology (PH) domain membrane targeting: a role for a phosphoinositide-protein co-operative mechanism. FEBS Lett. 506, 173 179.
41. Maldonado A.M. Doerner P. Dixon R.A. Lamb C.J. Cameron R.K. ( 2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature, 419, 399 403.
42. Maleck K. Neuenschwander U. Cade R.M. Dietrich R.A. Dangl J.L. Ryals J.A. ( 2002) Isolation and characterization of broad-spectrum disease-resistant Arabidopsis mutants. Genetics, 160, 1661 1671.
43. Mathias S. Pena L.A. Kolesnick R.N. ( 1998) Signal transduction of stress via ceramide. Biochem J. 335 ( Pt 3 465 480.
44. Mayer B.J. Ren R. Clark K.L. Baltimore D. ( 1993) A putative modular domain present in diverse signaling proteins. Cell, 73, 629 630.
45. Nandi A. Krothapalli K. Buseman C.M. Li M. Welti R. Enyedi A. Shah J. ( 2003) Arabidopsis sfd mutants affect plastidic lipid composition and suppress dwarfing, cell death, and the enhanced disease resistance phenotypes resulting from the deficiency of a fatty acid desaturase. Plant Cell, 15, 2383 2398.
46. Nandi A. Welti R. Shah J. ( 2004) The Arabidopsis thaliana dihydroxyacetone phosphate reductase gene suppressor of fatty acid desaturase deficiency1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell, 16, 465 477.
47. Nawrath C. Metraux J.P. ( 1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell, 11, 1393 1404.
48. Nawrath C. Heck S. Parinthawong N. Metraux J.P. ( 2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell, 14, 275 286.
49. Nishimura M.T. Stein M. Hou B.H. Vogel J.P. Edwards H. Somerville S.C. ( 2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science, 301, 969 972.
50. Parker J.E. Holub E.B. Frost L.N. Falk A. Gunn N.D. Daniels M.J. ( 1996) Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell, 8, 2033 2046.
51. Penninckx I.A. Thomma B.P. Buchala A. Metraux J.P. Broekaert W.F. ( 1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell, 10, 2103 2113.
52. Philip F. Guo Y. Scarlata S. ( 2002) Multiple roles of pleckstrin homology domains in phospholipase C-beta function. FEBS Lett. 531, 28 32.
53. Ponting C.P. Aravind L. ( 1999) START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem. Sci. 24, 130 132.
54. Rebecchi M.J. Scarlata S. ( 1998) Pleckstrin homology domains: a common fold with diverse functions. Annu. Rev. Biophys. Biomol. Struct. 27, 503 528.
55. Rogers E.E. Ausubel F.M. ( 1997) Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell, 9, 305 316.
56. Ryals J. Weymann K. Lawton K. et al. ( 1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell, 9, 425 439.
57. Schrick K. Nguyen D. Karlowski W.M. Mayer K.F. ( 2004) START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol. 5, R41.
58. Schulze-Lefert P. Vogel J. ( 2000) Closing the ranks to attack by powdery mildew. Trends Plant Sci. 5, 343 348.
59. Shah J. Kachroo P. Nandi A. Klessig D.F. ( 2001) A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J. 25, 563 574.
60. Soccio R.E. Breslow J.L. ( 2003) StAR-related lipid transfer (START) proteins: mediators of intracellular lipid metabolism. J. Biol. Chem. 278, 22183 22186.
61. Staswick P.E. Yuen G.Y. Lehman C.C. ( 1998) Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J. 15, 747 754.
62. Stocco D.M. ( 2001) StAR protein and the regulation of steroid hormone biosynthesis. Annu. Rev. Physiol. 63, 193 213.
63. Tang D. Innes R.W. ( 2002) Overexpression of a kinase-deficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J. 32, 975 983.
64. Thomma B.P.H.J. Eggermont K. Tierens K.F.M.-J. Broekaert W.F. ( 1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121, 1093 1101.
65. Thompson J.D. Gibson T.J. Plewniak F. Jeanmougin F. Higgins D.G. ( 1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876 4882.
66. Vogel J. Somerville S. ( 2000) Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc. Natl Acad. Sci. USA, 97, 1897 1902.
67. Vogel J.P. Raab T.K. Schiff C. Somerville S.C. ( 2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell, 14, 2095 2106.
68. Vogel J.P. Raab T.K. Somerville C.R. Somerville S.C. ( 2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J. 40, 968 978.
69. Wildermuth M.C. Dewdney J. Wu G. Ausubel F.M. ( 2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562 565.
70. Xiang C. Han P. Lutziger I. Wang K. Oliver D.J. ( 1999) A mini binary vector series for plant transformation. Plant Mol. Biol. 40, 711 717.
71. Xiao S. Ellwood S. Calis O. Patrick E. Li T. Coleman M. Turner J.G. ( 2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science, 291, 118 120.
72. Xiao S. Calis O. Patrick E. Zhang G. Charoenwattana P. Muskett P. Parker J.E. Turner J.G. ( 2005) The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. Plant J. 42, 95 110.
73. Yao N. Eisfelder B.J. Marvin J. Greenberg J.T. ( 2004) The mitochondrion - an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J. 40, 596 610.
74. Yu J.W. Mendrola J.M. Audhya A. Singh S. Keleti D. DeWald D.B. Murray D. Emr S.D. Lemmon M.A. ( 2004) Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol. Cell. 13, 677 688.
75. Zhou N. Tootle T.L. Tsui F. Klessig D.F. Glazebrook J. ( 1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell, 10, 1021 1030.