A role in immunity for arabidopsis cysteine protease RD21, the ortholog of the tomato immune protease C14

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Shindo, Takayuki ^a   Misas Villamil, Johana C ^a   Hörger, Anja C ^a   Song, Jing ^b   van der Hoorn, Renier A L ^a  

^a CHEMICAL GENOMICS CENTRE OF THE MAX PLANCK SOCIETY   (Germany)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATIN; CYSTEINE PROTEINASE; PAPAIN; PROTEINASE; ARABIDOPSIS PROTEIN; RD21 PROTEIN, ARABIDOPSIS; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BOTRYTIS CINEREA; CONTROLLED STUDY; DIVERSIFYING SELECTION; ENZYME INHIBITION; ENZYME RELEASE; GENE MUTATION; INFECTION SENSITIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PHENOTYPE; PLANT DISEASE; PLANT IMMUNITY; PLANT LEAF; PROTEIN INTERACTION; PROTEIN MOTIF; PSEUDOMONAS SYRINGAE; SOLANACEAE; TOMATO; AMINO ACID SEQUENCE; BOTRYTIS; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; SEQUENCE HOMOLOGY; TRANSGENIC PLANT;

ARABIDOPSIS; BOTRYOTINIA FUCKELIANA; HYALOPERONOSPORA; LYCOPERSICON ESCULENTUM; PHYTOPHTHORA INFESTANS; PSEUDOMONAS SYRINGAE PV. TOMATO; SOLANACEAE; SOLANUM JAMESII;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BOTRYTIS; CYSTEINE PROTEASES; IMMUNITY, INNATE; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PSEUDOMONAS SYRINGAE; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84855467361     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029317     Document Type: Article

References (42)

1. Gilroy EM, Hein I, Van der Hoorn R, Boeving PC, Venter E, et al. (2007) Involvement of cathepsin B in the plant disease resistance hypersensitive response. Plant J 52: 1-13.
2. Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, et al. (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296: 744-747.
3. Bernoux M, Timmers T, Jauneau A, Briere C, De Wit PJGM, et al. (2008) RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell 20: 2252-2264.
4. Rooney HCE, Van't Klooster JW, Van der Hoorn RAL, Joosten MHAJ, Jones JDG, et al. (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308: 1783-1786.
5. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, et al. (2008) Fungal effector protein AVR2 targets diversifying defence-related Cys proteases of tomato. Plant Cell 20: 1169-1183.
6. Van Esse HP, Van't Klooster JW, Bolton MD, Yadeta KA, Van Baarlen P, et al. (2008) The Cladosporium fulvum virulence protein AVR2 inhibits host proteases required for basal defence. Plant Cell 20: 1948-1963.
7. Tian M, Win J, Van der Hoorn R, Van der Knaap E, Kamoun S, (2007) A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol 143: 364-377.
8. Song J, Win J, Tian M, Schornack S, Kaschani F, et al. (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci USA 106: 1654-1659.
9. Kaschani F, Shabab M, Bozkurt T, Shindo T, Schornack S, et al. (2010) An effector-targeted protease contributes to defense against Phytophthora infestans and is under diversifying selection in natural hosts. Plant Physiol 154: 1794-1804.
10. Schaffer MA, Fischer RL, (1988) Analysis of mRNAs that accumulate in response to low temperature identifies a thiol protease gene in tomato. Plant Physiol 87: 431-436.
11. Schaffer MA, Fischer RL, (1990) Transcriptional activation by heat and cold of a thiol protease gene in tomato. Plant Physiol 93: 1486-1491.
12. Drake R, John I, Farrell A, Cooper W, Schuch W, et al. (1996) Isolation and analysis of cDNAs encoding tomato cysteine proteases expressed during leaf senescence. Plant Mol Biol 30: 755-767.
13. Harrak H, Azelmat S, Baker EN, Tabaeizadh Z, (2001) Isolation and characterization of a gene encoding a drought-induced cysteine protease in tomato (Lycopersicon esculentum). Genome 44: 368-374.
14. Kaschani F, Van der Hoorn RAL, (2011) A model of the C14-EPIC complex indicates hotspots for a protease-inhibitor arms race in the oomycete-potato interaction. Plant Signal Behav 6: 1-4.
15. Misas-Villamil JC, Van der Hoorn RAL, (2008) Enzyme-inhibitor interactions at the plant-pathogen interface. Curr Opin Plant Biol 11: 380-388.
16. Coates ME, Beynon JL, (2010) Hyaloperonospora arabidopsidis as a pathogen model. Annu Rev Phytopathol 48: 329-345.
17. Holub EB, (2008) Natural history of Arabidopsis thaliana and oomycete symbioses. Eur J Plant Pathol 122: 91-109.
18. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, et al. (2010) Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
19. Koizumi M, Yamaguchi-Shinozaki K, Tsuji H, Shinozaki K, (1993) Structure and expression of two genes that encode distinct drought-inducible cysteine proteinases in Arabidopsis thaliana. Gene 129: 175-182.
20. Van der Hoorn RAL, Leeuwenburgh MA, Bogyo M, Joosten MHAJ, Peck SC, (2004) Activity profiling of papain-like cysteine proteases in plants. Plant Physiol 135: 1170-1178.
21. Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, et al. (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nature Genetics in press.
22. Wang Z, Gu C, Colby T, Shindo T, Balamurugan R, et al. (2008) Beta-lactone probes identify a papain-like peptide ligase in Arabidopsis thaliana. Nat Chem Biol 4: 557-563.
23. Yamada K, Matsushima R, Nishimura M, Hara-Nishimura I, (2001) A slow maturation of a cysteine protease with a granulin domain in the vacuoles of senescing Arabidopsis leaves. Plant Physiol 127: 1626-1634.
24. Greenbaum D, Medzihradszky KF, Burlingame A, Bogyo M, (2000) Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem Biol 7: 569-581.
25. Carter C, Pan S, Zouhar J, Avila EL, Girke T, et al. (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16: 3285-3303.
26. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, et al. (2009) A novel membrane-fusion-mediated plant immunity against bacterial pathogens. Gene Dev 23: 2496-2506.
27. Wildermuth MC, Dewdney J, Wu G, Ausubel FM, (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-751.
28. Zhou N, Tootle TL, Glazebrook J, (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11: 2419-2428.
29. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, et al. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3: e196.
30. Schmid KJ, Ramos-Onsins S, Ringys-Beckstein H, Weisshaar B, Mitchell-Olds T, (2005) A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism. Genetics 166: 373-88.
31. Ramos-Onsins SE, Puerma E, Balañá-Alcaide D, Salguero D, Aguadé M, (2008) Multilocus analysis of variation using a large empirical data set: phenylpropanoid pathway genes in Arabidopsis thaliana. Mol Ecol 17: 1211-23.
32. François O, Blum MG, Jakobsson M, Rosenberg NA, (2008) Demographic history of european populations of Arabidopsis thaliana. PLoS Genet 4: e1000075.
33. Boller T, He SY, (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742-744.
34. Hayashi Y, Yamada K, Shimada T, Matsushima R, Nishizawa NK, et al. (2001) A proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis. Plant Cell Physiol 42: 894-899.
35. Boudart G, Jamet E, Rossignol M, Lafitte C, Borderies B, et al. (2005) Cell wall proteomics in apoplastic fluids of Arabidopsis thaliana rosettes identification by mass spectrometry and bioinformatics. Proteomics 5: 212-221.
36. Rawlings ND, Barrett AJ, Bateman A, (2010) MEROPS: the peptidase database. Nucleic Acids Res 38: D227-D233.
37. Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, et al. (2011) Genomic Analysis of the necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230.
38. Van Kan JAL, (2006) Licenced to kill the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11: 247-253.
39. Maddison WP, Maddison DR, (2007) Mesquite: a modular system for evolutionary analysis. Version 2.0 Mesquite website http://mesquiteproject.org. Accessed 2011 Dec 12.
40. Librado P, Rozas J, (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
41. Hey J, Wakeley J, (1997) A coalescent estimator of the population recombination rate. Genetics 145: 833-846.
42. Parker JE, Szabo V, Staskawicz BJ, Lister C, Dean C, et al. (1993) Phenotypic characterization and molecular mapping of the Arabidopsis thaliana locus RPP5, determining disease resistance to Peronospora parasitica. Plant J 4: 821-831.