A novel simple extracellular leucine-rich repeat (eLRR) domain protein from rice (OsLRR1) enters the endosomal pathway and interacts with the hypersensitive-induced reaction protein 1 (OsHIR1)

Plant, Cell and Environment

Volumn 32, Issue 12, 2009, Pages 1804-1820

  Zhou, Liang ^a   Cheung, Ming Yan ^a   Zhang, Qi ^b   Lei, Cai Lin ^b   Zhang, Shi Hong ^a,c   Sun, Samuel Sai Ming ^a   Lam, Hon Ming ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c JILIN UNIVERSITY   (China)

Author keywords

Endosome; HIR1; Plant defence response

Indexed keywords

LEUCINE RICH REPEAT PROTEINS; LEUCINE-RICH REPEAT PROTEINS; PLANT RNA; PROTEIN; VEGETABLE PROTEIN;

DICOTYLEDON; DISEASE RESISTANCE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; PLANT DEFENSE; PROTEIN; RICE; YEAST;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; ENDOSOME; GENE EXPRESSION REGULATION; GENETICS; INNATE IMMUNITY; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PLANT DISEASE; PROTEIN ANALYSIS; PSEUDOMONAS SYRINGAE; RICE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; ARABIDOPSIS; CLONING, MOLECULAR; ENDOSOMES; GENE EXPRESSION REGULATION, PLANT; IMMUNITY, INNATE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN INTERACTION MAPPING; PROTEINS; PSEUDOMONAS SYRINGAE; RNA, PLANT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS);

EID: 70449134854     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2009.02039.x     Document Type: Article

References (69)

1. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A. Struhl K. (1995) Phenol/SDS method for plant RNA preparation. Current Protocols in Molecular Biology, Vol. 1. John Wiley & Sons, Inc., New York, UK, pp. 43.1-4.
2. Baumberger N., Ringli C. Keller B. (2001) The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes & Development 15, 1128 1139.
3. Baumberger N., Doesseger B., Guyot R., et al. (2003) Whole-genome comparison of leucine-rich repeat extensins in Arabidopsis and rice. A conserved family of cell wall proteins form a vegetative and a reproductive clade. Plant Physiology 131, 1313 1326.
4. Bechtold N. Pelletier G. (1998) In planta, Agrobacterium-mediated transformation of adult Arabidopsis 7 plants by vacuum infiltration. Methods in Molecular Biology 82, 259 266.
5. Brears T., Liu C., Knight T.J. Coruzzi G.M. (1993) Ectopic overexpression of asparagine synthetase in transgenic tobacco. Plant Physiology 103, 1285 1290.
6. Chen F., Yuan Y., Li Q. He Z. (2007) Proteomic analysis of rice plasma membrane reveals proteins involved in early defense response to bacterial blight. Proteomics 7, 1529 1539.
7. Cheung M.Y., Zeng N.Y., Tong S.W., Li F.W., Zhao K.J., Zhang Q., Sun S.S. Lam H.M. (2007) Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana. Journal of Experimental Botany 58, 4147 4159.
8. Cheung M.Y., Zeng N.Y., Tong S.W., et al. (2008) Constitutive expression of a rice GTPase-activating protein induces defense responses. New Phytologist 179, 530 545.
9. Dangl J.L. Jones J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature 411, 826 833.
10. Dhonukshe P., Baluska F., Schlicht M., Hlavacka A., Samaj J., Friml J. Gadella T.W. Jr. 2006) Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Developmental Cell 10, 137 150.
11. Dunning F.M., Sun W., Jansen K.L., Helft L. Bent A.F. (2007) Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeat domain residues that contribute to flagellin perception. The Plant Cell 19, 3297 3313.
12. Emans N., Zimmermann S. Fischer R. (2002) Uptake of a fluorescent marker in plant cells is sensitive to brefeldin A and wortmannin. The Plant Cell 14, 71 86.
13. Emanuelsson O., Brunak S., von Heijne G. Nielsen H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocol 2, 953 971.
14. 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. Proceedings of the National Academy of Sciences of the United States of America 96, 3292 3297.
15. Federici L., Di Matteo A., Fernandez-Recio J., Tsernoglou D. Cervone F. (2006) Polygalacturonase inhibiting proteins: players in plant innate immunity? Trends in Plant Science 11, 65 70.
16. Finckh U., Lingenfelter P.A. Myerson D. (1991) Producing single-stranded DNA probes with the Taq DNA polymerase: a high yield protocol. Biotechniques 10, 35 38.
17. Forsthoefel N.R., Cutler K., Port M.D., Yamamoto T. Vernon D.M. (2005) PIRLs: a novel class of plant intracellular leucine-rich repeat proteins. Plant Cell Physiology 46, 913 922.
18. Geldner N. Robatzek S. (2008) Plant receptors go endosomal: a moving view on signal transduction. Plant Physiology 147, 1565 1574.
19. Geldner N., Hyman D.L., Wang X., Schumacher K. Chory J. (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes & Development 21, 1598 1602.
20. Gietz R.D., Triggs-Raine B., Robbins A., Graham K.C. Woods R.A. (1997) Identification of proteins that interact with a protein of interest: applications of the yeast two-hybrid system. Molecular and Cellular Biochemistry 172, 67 79.
21. Gifford M.L., Robertson F.C., Soares D.C. Ingram G.C. (2005) ARABIDOPSIS CRINKLY4 function, internalization, and turnover are dependent on the extracellular crinkly repeat domain. The Plant Cell 17, 1154 1166.
22. Gómez-Gómez L., Bauer Z. Boller T. (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. The Plant Cell 13, 1155 1163.
23. Guy G.R., Philip R. Tan Y.H. (1994) Analysis of cellular phosphoproteins by two-dimensional gel electrophoresis: applications for cell signaling in normal and cancer cells. Electrophoresis 15, 417 440.
24. Hipskind J.D., Nicholson R.L. Goldsbrough P.B. (1996) Isolation of a cDNA encoding a novel leucine-rich repeat motif from Sorghum bicolor inoculated with fungi. Molecular Plant-Microbe Interactions 9, 819 825.
25. van der Hoorn R.A., Wulff B.B., Rivas S., Durrant M.C., van der Ploeg A., de Wit P.J. Jones J.D. (2005) Structure-function analysis of cf-9, a receptor-like protein with extracytoplasmic leucine-rich repeats. The Plant Cell 17, 1000 1015.
26. Jacques A., Ghannam A., Erhardt M., de Ruffray P., Baillieul F. Kauffmann S. (2006) NtLRP1, a tobacco leucine-rich repeat gene with a possible role as a modulator of the hypersensitive response. Molecular Plant-Microbe Interactions 19, 747 757.
27. Jain M., Nijhawan A., Tyagi A.K. Khurana J.P. (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochemical and Biophysical Research Communications 345, 646 651.
28. Jiang L. Rogers J.C. (1998) Integral membrane protein sorting to vacuoles in plant cells: evidence for two pathways. Journal of Cell Biology 143, 1183 1199.
29. Jones D.A. Jones J.D.G. (1997) The role of leucine rich repeat proteins in plant defenses. Advances in Botanical Research 24, 89 167.
30. Jung E.H., Jung H.W., Lee S.C., Han S.W., Heu S. Hwang B.K. (2004) Identification of a novel pathogen-induced gene encoding a leucine-rich repeat protein expressed in phloem cells of Capsicum annuum. Biochimica et Biophysica Acta 1676, 211 222.
31. Jung H.W. Hwang B.K. (2007) The leucine-rich repeat (LRR) protein, CaLRR1, interacts with the hypersensitive induced reaction (HIR) protein, CaHIR1, and suppresses cell death induced by the CaHIR1 protein. Molecular Plant Pathology 8, 503 514.
32. Kajava A.V. (1998) Structural diversity of leucine-rich repeat proteins. Journal of Molecular Biology 277, 519 527.
33. Kauffman H.E., Reddy A.P.K., Hsieh S.P.Y. Merca S.D. (1973) An improved technique for evaluating resistance to rice varieties of Xanthomonas oryzae. Plant Disease Reporter 57, 537 541.
34. Kim H.S. Delaney T.P. (2002) Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. The Plant Cell 14, 1469 1482.
35. Kobe B. Kajava A.V. (2001) The leucine-rich repeat as a protein recognition motif. Current Opinion in Structural Biology 11, 725 732.
36. Koch E. Slusarenko A. (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. The Plant Cell 2, 437 445.
37. Lam S.K., Siu C.L., Hillmer S., Jang S., An G., Robinson D.G. Jiang L. (2007) Rice SCAMP1 defines clathrin-coated, trans-Golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. The Plant Cell 19, 296 319.
38. Landschulz W.H., Johnson P.F. McKnight S.L. (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240, 1759 1764.
39. Li J., Brader G., Kariola T. Palva E.T. (2006) WRKY70 modulates the selection of signaling pathways in plant defense. The Plant Journal 46, 477 491.
40. -ΔΔCT method. Methods 25, 402 408.
41. Mayo K.J., Gonzales B.J. Mason H.S. (2006) Genetic transformation of tobacco NT1 cells with Agrobacterium tumefaciens. Nature Protocol 1, 1105 1111.
42. Miao Y. Jiang L. (2007) Transient expression of fluorescent fusion proteins in protoplasts of suspension cultured cells. Nature Protocol 2, 2348 2353.
43. Nadimpalli R., Yalpani N., Johal G.S. Simmons C.R. (2000) Prohibitins, stomatins, and plant disease response genes compose a protein superfamily that controls cell proliferation, ion channel regulation, and death. Journal of Biological Chemistry 275, 29579 29586.
44. Nebenführ A., Ritzenthaler C. Robinson D.G. (2002) Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiology 130, 1102 1108.
45. Nürnberger T., Brunner F., Kemmerling B. Piater L. (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunological Reviews 198, 249 266.
46. Remans T., Smeets K., Opdenakker K., Mathijsen D., Vangronsveld J. Cuypers A. (2008) Normalisation of real-time RT-PCR gene expression measurements in Arabidopsis thaliana exposed to increased metal concentrations. Planta 227, 1343 1349.
47. Robatzek S., Chinchilla D. Boller T. (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes & Development 20, 537 542.
48. Rooke L., Byrne D. Salgueiro S. (2000) Marker gene expression driven by the maize ubiquitin promoter in transgenic wheat. Annals of Applied Biology 136, 167 172.
49. Rostoks N., Schmierer D., Kudrna D. Kleinhofs A. (2003) Barley putative hypersensitive induced reaction genes: genetic mapping, sequence analyses and differential expression in disease lesion mimic mutants. Theoretical and Applied Genetics 107, 1094 1101.
50. Russinova E., Borst J.W., Kwaaitaal M., Caño-Delgado A., Yin Y., Chory J. de Vries S.C. (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). The Plant Cell 16, 3216 3229.
51. Saitou N. Nei M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406 425.
52. Sambrook J. Russel D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York, NY, USA.
53. Schenk P.M., Kazan K., Manners J.M., Anderson J.P., Simpson R.S., Wilson I.W., Somerville S.C. Maclean D.J. (2003) Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiology 132, 999 1010.
54. Shah K., Russinova E., Gadella T.W. Jr., Willemse J. De Vries S.C. (2002) The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes & Development 16, 1707 1720.
55. Shanmugam V. (2005) Role of extracytoplasmic leucine rich repeat proteins in plant defence mechanisms. Microbiological Research 160, 83 94.
56. Song W.Y., Wang G.L., Chen L.L., et al. (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804 1806.
57. Spoel S.H., Johnson J.S. Dong X. (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences of the United States of America 104, 18842 18847.
58. Sun X., Cao Y., Yang Z., Xu C., Li X., Wang S. Zhang Q. (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. The Plant Journal 37, 517 527.
59. Tamura K., Dudley J., Nei M. Kumar S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596 1599.
60. Tornero P., Mayda E., Gómez M.D., Cañas L., Conejero V. Vera P. (1996) Characterization of LRP, a leucine-rich repeat (LRR) protein from tomato plants that is processed during pathogenesis. The Plant Journal 10, 315 330.
61. Tse Y.C., Mo B., Hillme S., Zhao M., Lo S.W., Robinson D.G. Jiang L. (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. The Plant Cell 16, 672 693.
62. Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., Chandler D., Slusarenko A., Ward E. Ryals J. (1992) Acquired resistance in Arabidopsis. The Plant Cell 4, 645 656.
63. Wang Z.Y., Seto H., Fujioka S., Yoshida S. Chory J. (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410, 380 383.
64. Weigel D. Glazebrook J. (2006) Transformation of Agrobacterium using the freeze-thaw method. Cold Spring Harbor Protocols doi: 10.1101/pdb.prot4666.
65. Xiao F., Tang X. Zhou J.M. (2001) Expression of 35S::Pto globally activates defense-related genes in tomato plants. Plant Physiology 126, 1637 1645.
66. Yoo S.D., Cho Y.H. Sheen J. (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocol 2, 1565 1572.
67. Yoshimura S., Yamanouchi U., Katayose Y., Toki S., Wang Z.X., Kono I., Kurata N., Yano M., Iwata N. Sasaki T. (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proceedings of the National Academy of Sciences of the United States of America 95, 1663 1668.
68. Zhang Q., Shi A.N., Yang W.C. Wang C.L. (1996) Breeding of three near-isogenic japonica rice lines with different major genes for resistance to bacterial blight. Acta Agronomica Sinica 22, 135 141.
69. Zipfel C., Kunze G., Chinchilla D., Caniard A., Jones J.D., Boller T. Felix G. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749 760.