PIRLs: A novel class of plant intracellular leucine-rich repeat proteins

Plant and Cell Physiology

Volumn 46, Issue 6, 2005, Pages 913-922

  Forsthoefel, Nancy R ^a   Cutler, Kerry ^a   Port, Martha D ^a,b   Yamamoto, Tori ^a   Vernon, Daniel M ^a  

^a WHITMAN COLLEGE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Arabidopsis thaliana; G proteins; Gene knockouts; Leucine rich repeats; Linker protein; Signal transduction

Indexed keywords

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; COMPLEMENTARY DNA; LEUCINE; PLANT DNA;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; CLASSIFICATION; GENE; GENE TARGETING; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY; TANDEM REPEAT;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; DNA, COMPLEMENTARY; DNA, PLANT; EVOLUTION, MOLECULAR; GENE TARGETING; GENES, PLANT; LEUCINE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; SEQUENCE HOMOLOGY, AMINO ACID; TANDEM REPEAT SEQUENCES;

EID: 24644483740     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pci097     Document Type: Article

References (60)

1. Abysalh, J.C., Kuchnicki, L.L. and Larochelle, D.A. (2003) The identification of Pats1, a novel gene locus required for cytokinesis in Dictyostelium discoideum. Mol. Biol. Cell 14: 14-25.
2. Acevedo, F.G., Gamboa, A. Paez-Valencia, J., Jimenez-Garcia, L.F., Izaguirre-Sierra, M. and Alvarez-Buylla, E.R. (2004) Flor1, a putative interaction partner of the floral homeotic protein AGAMOUS, is a plant-specific intracellular LRR. Plant Sci. 167: 225-231.
3. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
4. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
5. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-826.
6. Aruga, J., Yokota, N. and Mioshiba, K. (2003) Human SLITRK family genes: genomic organization and expression profiling in normal brain and brain tumor tissue. Gene 315: 87-94.
7. Askjaer, P., Galy, V., Hannak, E. and Mattaj, I.W. (2002) Tan GTPase cycle and importins are essential for spindle formation and nuclear envelope assembly in living C. elegans embryos. Mol. Biol. Cell 13: 4355-4370.
8. Baumberger, N., Ringli, C. and Keller, B. (2001) The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev. 15: 1128-1139.
9. Borg, J.P., Marchetto, S., Le Bivic, A., Ollendorff, V., Jaulin-Bastard, F., Saito, H., Fournier, E., Adelaide, J., Margolis, B. and Birnbaum, D. (2000) Erbin: a basolateral PDZ protein that interacts with the mammalian ERBB2/HER2 receptor. Nat. Cell Biol. 1: 407-414.
10. Chauhan, A., Forsthoefel, N., Ran, Y., Quigley, F., Nelson, D. and Bohnert, H.J. (2000) Na/myo-inositol symporters and Na/H-antiport in M. crystallinum. Plant J. 24: 511-522.
11. Claudianos, C. and Campbell, H.D. (1995) The novel flightless-I gene brings together two gene families, actin-binding proteins related to gelsolin and leucine-rich-repeat proteins involved in Ras signal transduction. Mol. Biol. Evol. 12: 405-414.
12. Cushing, D.A., Forsthoefel, N.R., Gestaut, D.R. and Vernon, D.M. (2005) Arabidopsis emb175 and embryo-defective ppr knockout mutants reveal essential roles for PPR proteins. Planta. In press. http://dx.doi.org/10.1007/s00425-004- 1452-x
13. Cutler, M.L., Bassin, R.H., Zanoni, L. and Talbot, N. (1992) Isolation of rsp-1, a novel cDNA capable of suppressing v-Ras transformation. Mol. Cell. Biol. 12: 3750-3756.
14. Dangle, J.L. (1995) Pièce de résistance: novel classes of plant disease resistance genes. Cell 80: 363-366.
15. Di Matteo, A., Federici, L., Mattei, B., Salvi, G., Johnson, K.A., Savino, C., De Lorenzo, G., Tsernoglou, D. and Cervone, F. (2003) The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc. Natl Acad. Sci. USA 100: 10124-10128.
16. Dievart, A. and Clark, S.E. (2004) LRR-containing receptors regulate plant development and defense. Development 131: 251-261.
17. Ellis, J., Dodds, P. and Pryor, T. (2000) The generation of plant disease resistance gene specificities. Trends Plant Sci. 5: 373-379.
18. Fluhr, R. (2001) Sentinels of disease: plant resistance genes. Plant Physiol. 127: 1367-1374.
19. Guyon, V., Tang, W., Monti, M.M., Raiola, A., De Lorenzo, G., McCormick, S. and Taylor, L.P. (2004) Antisense phenotypes reveal a role for SHY, a pollen-specific leucine-rich repeat protein, in pollen tube growth. Plant J. 39: 643-654.
20. Haberland, J. and Gerke, V. (1999) Conserved charged residues in the leucine-rich repeat domain of the Ran GTPase activating protein are required for Ran binding and GTPase activation. Biochem. J. 343: 653-662.
21. Hellmann, H. and Estelle, M. (2002) Plant development: regulation by protein degradation. Science 297: 793-797.
22. Howitt, H.A., Clout, N.J. and Hohenester, E. (2004) Binding site for Robo receptors revealed by dissection of the leucine-rich repeat region of Slit. EMBO J. 23: 4406-4412
23. Jaulin-Bastard, F., Arsanto, J.P, Le Bivic, A., Navarro, C., Vely, F., et al. (2002) Interaction between erbin and a catenin-related protein in epithelial cells. J. Biol. Chem. 277: 2869-2875.
24. Jeong, S., Trotochaud, A.E. and Clark, S.E. (1999) The Arabidopsis CLV2 gene encodes a receptor-like protein required for the stability of the CLV1 receptor-like kinase. Plant Cell 11: 1925-1933.
25. Jones, D.A., Thomas, C.M., Hammond-Kosack, K.E., Balint-Kurti, P.J. and Jones, J.D.G (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266: 789-793.
26. Kajava, A.V. (1998) Structural diversity of leucine-rich repeat proteins. J. Mol. Biol. 277: 519-27.
27. Kobe, B. and Deisenhofer, J. (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem. Sci. 19: 415-421.
28. Kobe, B. and Deisenhofer, J. (1995) A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature 374: 183-186.
29. Kobe, B. and Kajava, A.V. (2001) The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11: 725-732.
30. Krysan, P.J., Young, J.C. and Sussman, M.R. (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell. 11: 2283-2290.
31. Kuroda, H., Takahashi, N., Shimada, H., Motoaki, S., Shinozaki, K. and Matsui, M. (2002) Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol. 43: 1073-1085.
32. Kusano, A., Yoshioka, T., Nishijima, H., Nishitani, H. and Nishimoto, T. (2004) S. pombe RanGAP homologue SpRNA1 is required for centromeric silencing and chromosome segregation. Mol. Biol. Cell. 15: 4960-4970.
33. Lease, K., Ingham, E. and Walker, J.C. (1998) Challenges in understanding RLK function. Curr. Opin. Plant Biol. 1: 388-392.
34. Leckie, F., Mattei, B., Capodicasa, C., Hemmings, A., Nuss, L., Aracri, B., De Lorenzo, G. and Cervone, F. (1999) The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed β-strand/β-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J. 18: 2352-2363.
35. Li, H., Shen, J-J., Zheng, Z-L., Lin, Y. and Yang, Z. (2001) The Rop GTPase switch controls multiple developmental processes in Arabidopsis. Plant Physiol. 126: 670-684.
36. Li, J. and Chory, J. (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
37. Li, W., Han, M. and Guan, K. (2000) The leucine-rich repeat protein SUR-8 enhances MAP kinase activation and forms a complex with Ras and Raf. Genes Dev. 14: 895-900.
38. Liu, Y.T. and Yin, H.L. (1998) Identification of the binding partners for flightless I, a novel protein bridging the leucine-rich repeat and the gelsolin superfamilies. J. Biol. Chem. 273: 7920-7927.
39. McDowell, J.M. and Dangle, J.L. (2000) Signal transduction in the plant immune response. Trends Biochem. Sci. 25: 79-82
40. Mindrinos, M., Katagiri, F., Yu G. and Ausubel, F.M. (1994) The Arabidopsis disease resistance gene RPS2 encodes a protein containing a nucleotide binding site and leu-rich repeats. Cell 78: 1089-1099.
41. Morris, E.R. and Walker, J.C. (2003) Receptor-like protein kinases: the keys to response. Curr. Opin. Plant Biol. 6: 339-342.
42. Rose, A. and Meier, I. (2001) A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proc. Natl Acad. Sci. USA 98: 15377-15382.
43. Ruegger, M., Dewey, E., Gray, W.M., Hobbie, L., Turner, J. and Estelle, M. (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grrlp. Genes Dev. 12: 198-207.
44. Schuster, J.M. and Nelson, P.S. (2000) Toll receptors: an expanding role in our understanding of human disease. J. Leukoc. Biol. 67: 767-773.
45. Shiu, S.-H. and Bleecker, A.B. (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Proc. Natl Acad. Sci. USA 98: 10763-10768.
46. Shiu, S.-H. and Bleecker, A.B. (2003) Expansion of the receptor-like kinase/ pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132: 530-543.
47. Sieburth, D.S., Sun, Q. and Han, M. (1998) SUR-8, a conserved Ras-binding protein with leucine-rich repeats, positively regulates Ras-mediated signaling in C. elegans. Cell 94: 119-130.
48. Simillion, C., Vandepoele, K., Van Montagu, M.C.E., Zabeau, M. and Van der Peer, Y. (2002) The hidden duplication past of Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 99: 13627-13632.
49. Sternberg, P.W. and Alberola-Ila, J. (1998) Conspiracy theory: RAS and RAF do not act alone. Cell 95: 447-450.
50. Strack, S., Robison, A.J., Bass, M.A. and Colbran, R.J. (2000) Association of calium/calmodulin-dependent kinase II with developmentally regulated variants of the postsynaptic density protein densin-180. J. Biol. Chem. 275: 25061-25064.
51. Stratford, S., Barnes, W., Hohorst, D.L., Sagert, J.G., Cotter, R., Goubiewski, A., Showalter, A.M., McCormick, S. and Bedinger, P. (2001) A leucine-rich repeat region is conserved in pollen extensin-like (Pex) proteins in monocots and dicots. Plant Mol. Biol. 46: 43-56.
52. Sussman, M.R., Amasino, R.M., Young, J.C., Krysan, P.J. and Austin-Phillips, S. (2000) The Arabidopsis Knockout Facility at the University of Wisconsin. Plant Physiol. 124: 1465-1467.
53. Suzuki, N., Choe, H.R., Nishida, Y., Yamawaki-Kataoka, Y., Ohnishi, S., Tamaoki, T. and Kataoka, T. (1990) Leucine-rich repeats and carboxyl terminus are required for interaction of yeast adenylate cyclase with RAS proteins. Proc. Natl Acad. Sci. USA 87: 8711-8715.
54. Suzuki, T., Inagaki, S., Nakajima, S., Akashi, T., Ohto, M., et al. (2004) A novel Arabidopsis gene TONSOKU is required for proper cell arrangement in root and shoot apical meristems. Plant J. 38: 673-684.
55. Tax, F.E. and Vernon, D.M. (2001) T-DNA associated duplication/ rearrangements in Arabidopsis: implications for reverse genetics and functional genomics. Plant Physiol. 126: 1526-1537.
56. Tsuda, T. and Cutler, M.L. (1993) Human RSU1 is highly homologous to mouse RSP1 and localizes to human chromosome 10. Genomcis 18: 461-462.
57. Vernon, D.M. and Forsthoefel, N.R. (2002) Leucine-rich repeat proteins in plants: diverse roles in signaling and development. Res. Signpost: Recent Res. Dev. Plant Biol. 2: 201-214.
58. Vernon, D.M. and Meinke, D.W. (1995) The late embryo-defective mutants of Arabidopsis. Dev. Genet. 16: 311-320.
59. Vision, T.J., Brown, D.G. and Tanksley, S.D. (2000) The origins of genomic duplications in Arabidopsis. Science. 290: 2114-2117.
60. Zheng, Z.-L. and Yang, Z. (2000) The Rop GTPase: an emerging signaling switch in plants. Plant Mol. Biol. 44: 1-9.