A novel link between tomato GRAS genes, plant disease resistance and mechanical stress response

Molecular Plant Pathology

Volumn 7, Issue 6, 2006, Pages 593-604

  Mayrose, Maya ^a   Ekengren, Sophia K ^b,d   Melech Bonfil, Shiri ^a   Martin, Gregory B ^b,c   Sessa, Guido ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; SOLANUM;

EID: 33750216254     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2006.00364.x     Document Type: Article

References (49)

1. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J. and Harberd, N.P. (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science, 311, 91-94.
2. Bolle, C. (2004) The role of GRAS proteins in plant signal transduction and development. Planta, 218, 683-692.
3. Bolle, C., Koncz, C. and Chua, N.H. (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev. 14, 1269-1278.
4. Bonshtien, A., Lev, A., Gibly, A., Debbie, P., Avni, A. and Sessa, G. (2005) Molecular properties of the Xanthomonas AvrRxv effector and global transcriptional changes determined by its expression in resistant tomato plants. Mol. Plant-Microbe Interact. 18, 300-310.
5. Cai, X.Z., Xu, Q.F., Wang, C.C. and Zeng, Z. (2006) Development of a virus-induced gene-silencing system for functional analysis of the RPS2-dependent resistance signaling pathways in Arabidopsis. Plant Mol. Biol. 62, 223-232.
6. Day, R.B., Shibuya, N. and Minami, E. (2003) Identification and characterization of two new members of the GRAS gene family in rice responsive to N-acetylchitooligosaccharide elicitor. Biochim. Biophys. Acta, 1625, 261-268.
7. Devoto, A., Ellis, C., Magusin, A., Chang, H.S., Chilcott, C., Zhu, T. and Turner, J.G. (2005) Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol. Biol. 58, 497-513.
8. Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A. and Benfey, P.N. (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell, 86, 423-433.
9. Ekengren, S.K., Liu, Y., Schiff, M., Dinesh-Kumar, S.P. and Martin, G.B. (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J. 36, 905-917.
10. Eulgem, T. (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 10, 71-78.
11. Gibly, A., Bonshtien, A., Balaji, V., Debbie, P., Martin, G.B. and Sessa, G. (2004) Identification and expression profiling of tomato genes differentially regulated during a resistance response to Xanthomonas campestris pv. vesicatoria. Mol. Plant-Microbe Interact. 17, 1212-1222.
12. Heery, D.M., Kalkhoven, E., Hoare, S. and Parker, M.G. (1997) A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature, 387, 733-736.
13. Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.T. and Benfey, P.N. (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell, 101, 555-567.
14. Huang, G., Dong, R., Allen, R., Davis, E.L., Baum, T.J. and Hussey, R.S. (2006) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol. Plant-Microbe Interact. 19, 463-470.
15. Itoh, H., Shimada, A., Ueguchi-Tanaka, M., Kamiya, N., Hasegawa, Y., Ashikari, M. and Matsuoka, M. (2005) Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice. Plant J. 44, 669-679.
16. Itoh, H., Ueguchi-Tanaka, M., Sato, Y., Ashikari, M. and Matsuoka, M. (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell, 14, 57-70.
17. Kalo, P., Gleason, C., Edwards, A., Marsh, J., Mitra, R.M., Hirsch, S., Jakab, J., Sims, S., Long, S.R., Rogers, J., Kiss, G.B., Downie, J.A. and Oldroyd, G.E. (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science, 308, 1786-1789.
18. Kim, Y.J., Lin, N.C. and Martin, G.B. (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell, 109, 589-598.
19. Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Pichersky, E. and Howe, G.A. (2004) The tomato homolog of CORONATINE- INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell, 16, 126-143.
20. Lim, J., Jung, J.W., Lim, C.E., Lee, M.H., Kim, B.J., Kim, M., Bruce, W.B. and Benfey, P.N. (2005) Conservation and diversification of SCARECROW in maize. Plant Mol. Biol. 59, 619-630.
21. Liu, Y., Schiff, M. and Dinesh-Kumar, S.P. (2002) Virus-induced gene silencing in tomato. Plant J. 31, 777-786.
22. Liu, Y., Schiff, M. and Dinesh-Kumar, S.P. (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1. N-mediated resistance to tobacco mosaic virus. Plant J. 38, 800-809.
23. Marathe, R., Guan, Z., Anandalakshmi, R., Zhao, H. and Dinesh-Kumar, S.P. (2004) Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Mol. Biol. 55, 501-520.
24. Mayrose, M., Bonshtien, A. and Sessa, G. (2004) LeMPK3 is a mitogenactivated protein kinase with dual specificity induced during tomato defense and wounding responses. J. Biol. Chem. 279, 14819-14827.
25. Morohashi, K., Minami, M., Takase, H., Hotta, Y. and Hiratsuka, K. (2003) Isolation and characterization of a novel GRAS gene that regulates meiosis-associated gene expression. J. Biol. Chem. 278, 20865-20873.
26. Mysore, K.S., Crasta, O.R., Tuori, R.P., Folkerts, O., Swirsky, P.B. and Martin, G.B. (2002) Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. Plant J. 32, 299-315.
27. Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T. and Jones, J.D. (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135, 1113-1128.
28. Pedley, K.F. and Martin, G.B. (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu. Rev. Phytopathol. 41, 215-243.
29. Peng, J., Carol, P., Richards, D.E., King, K.E., Cowling, R.J., Murphy, G.P. and Harberd, N.P. (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11, 3194-3205.
30. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
31. Pysh, L.D., Wysocka-Diller, J.W., Camilleri, C., Bouchez, D. and Benfey, P.N. (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 18, 111-119.
32. Ron, M. and Avni, A. (2004) The receptor for the fungal elicitor ethyleneinducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell, 16, 1604-1615.
33. Ronald, P.C., Salmeron, J.M., Carland, F.M. and Staskawicz, B.J. (1992) The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J. Bacteriol. 174, 1604-1611.
34. Rushton, P.J. and Somssich, I.E. (1998) Transcriptional control of plant genes responsive to pathogens. Curr. Opin. Plant Biol. 1, 311-315.
35. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
36. Salmeron, J.M., Oldroyd, G.E., Rommens, C.M., Scofield, S.R., Kim, H.S., Lavelle, D.T., Dahlbeck, D. and Staskawicz, B.J. (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell, 86, 123-133.
37. Schenk, P.M., Kazan, K., Wilson, I., Anderson, J.P., Richmond, T., Somerville, S.C. and Manners, J.M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl Acad. Sci. USA, 97, 11655-11660.
38. Schmidt, D.D., Voelckel, C., Hartl, M., Schmidt, S. and Baldwin, I.T. (2005) Specificity in ecological interactions: attack from the same lepidopteran herbivore results in species-specific transcriptional responses in two solanaceous host plants. Plant Physiol. 138, 1763-1773.
39. Schumacher, K., Schmitt, T., Rossberg, M., Schmitz, G. and Theres, K. (1999) The Lateral suppressor ( Ls) gene of tomato encodes a new member of the VHIID protein family. Proc. Natl Acad. Sci. USA, 96, 290-295.
40. Scott, J.W., Jones, J.B., Somodi, G.C. and Stall, R.E. (1995) Screening tomato accessions for resistance to Xanthomonas campestris pv. vesicatoria, race T3. Hortscience, 30, 579-581.
41. Silverstone, A.L., Ciampaglio, C.N. and Sun, T. (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell, 10, 155-169.
42. Smit, P., Raedts, J., Portyanko, V., Debelle, F., Gough, C., Bisseling, T. and Geurts, R. (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science, 308, 1789-1791.
43. Tao, Y., Xie, Z., Chen, W., Glazebrook, J., Chang, H.S., Han, B., Zhu, T., Zou, G. and Katagiri, F. (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell, 15, 317-330.
44. Thomas, C.L., Jones, L., Baulcombe, D.C. and Maule, A.J. (2001) Size constraints for targeting post-transcriptional gene silencing and for using RNA-directed methylation in Nicotiana benthamiana using a potato virus X vector. Plant J. 25, 417-425.
45. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
46. Tian, C., Wan, P., Sun, S., Li, J. and Chen, M. (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol. Biol. 54, 519-532.
47. Vandenabeele, S., Van Der Kelen, K., Dat, J., Gadjev, I., Boonefaes, T., Morsa, S., Rottiers, P., Slooten, L., Van Montagu, M., Zabeau, M., Inze, D. and Van Breusegem, F. (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc. Natl Acad. Sci. USA, 100, 16113-16118.
48. Wasternack, C., Stenzel, I., Hause, B., Hause, G., Kutter, C., Maucher, H., Neumerkel, J., Feussner, I. and Miersch, O. (2006) The wound response in tomato - Role of jasmonic acid. J. Plant Physiol. 163, 297-306.
49. Yu, Z.H., Wang, J.F., Stall, R.E. and Vallejos, C.E. (1995) Genomic localization of tomato genes that control a hypersensitive reaction to Xanthomonas campestris pv. vesicatoria (Doidge) Dye. Genetics, 141, 675-682.