Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp.

Molecular Plant-Microbe Interactions

Volumn 19, Issue 5, 2006, Pages 502-511

  Miché, Lucie ^a   Battistoni, Federico ^a   Gemmer, Sabrina ^a   Belghazi, Maya ^b   Reinhold Hurek, Barbara ^a  

^a UNIVERSITY OF BREMEN   (Germany)

^b UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

glucuronidase; Proteome

Indexed keywords

CYCLOPENTANE DERIVATIVE; JASMONIC ACID; PROTEOME;

ARTICLE; AZOARCUS; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; MICROBIOLOGY; PHYSIOLOGY; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; SYMBIOSIS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION;

AZOARCUS; CYCLOPENTANES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, PLANT; ORYZA SATIVA; PLANT ROOTS; PROTEOME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYMBIOSIS; UP-REGULATION; VARIATION (GENETICS);

AZOARCUS; AZOARCUS SP.; BACTERIA (MICROORGANISMS); ORYZA SATIVA; POACEAE;

EID: 33646372447     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-19-0502     Document Type: Article

References (54)

1. Agrawal, G. K., Jwa, N. S., and Rakwal, R. 2000. A novel rice (Oryza sativa L.) acidic PR1 gene highly responsive to cut, phytohormones, and protein phosphatase inhibitors. Biochem. Biophys. Res. Comm. 274:157-165.
2. Bantignies, B., Seguin, J., Muzac, I., Dedaldechamp, F., Gulick, P., and Ibrahim, R. 2000. Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots. Plant Mol. Biol. 42:871-881.
3. Barraquio, W. L., Revilla, L., and Ladha, J. K. 1997. Isolation of endophytic diazotrophic bacteria from wetland rice. Plant Soil 194:15-24.
4. Berger, S. 2002. Jasmonate-related mutants of Arabidopsis as tools for studying stress signaling. Planta 214:497-504.
5. Claes, B., Dekeyser, R., Villarroel, R., Van den Bulcke, M., Bauw, G., Van Montagu, M., and Caplan, A. 1990. Characterization of a rice gene showing organ-specific expression in response to salt stress and drought. Plant Cell 2:19-27.
6. Czernic, P., Visser, B., Sun, W., Savoure, A., Deslandes, L., Marco, Y., Van Montagu, M., and Verbruggen, N. 1999. Characterization of an Arabidopsis thaliana receptor-like protein kinase gene activated by oxidative stress and pathogen attack. Plant J. 18:321-327.
7. de Souza Filho, G. A., Ferreira, B. S., Dias, J. M., Queiroz, K. S., Branco, A. T., Bressan-Smith, R. E., Oliveira, J. G., and Garcia, A. B. 2003. Accumulation of SALT protein in rice plants as a response to environmental stresses. Plant Sci. 164:623-628.
8. Egener, T., Hurek, T., and Reinhold-Hurek, B. 1999. Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots. Mol. Plant-Microbe Interact. 12:813-819.
9. Glazebrook, J. 1999. Genes controlling expression of defense responses in Arabidopsis. Curr. Opin. Plant Biol. 2:280-286.
10. Goff, S. A., Ricke, D., Lan, T. H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., Hadley, D., Hutchison, D., Martin, C., Katagiri, F., Lange, B. M., Moughamer, T., Xia, Y., Budworth, P., Zhong, J., Miguel, T., Paszkowski, U., Zhang, S., Colbert, M., Sun, W. L., Chen, L., Cooper, B., Park, S., Wood, T. C., Mao, L., Quail, P., Wing, R., Dean, R., Yu, Y., Zharkikh, A., Shen, R., Sahasrabudhe, S., Thomas, A., Cannings, R., Gutin, A., Pruss, D., Reid, J., Tavtigian, S., Mitchell, J., Eldredge, G., Scholl, T., Miller, R. M., Bhatnagar, S., Adey, N., Rubano, T., Tusneem, N., Robinson, R., Feldhaus, J., Macalma, T., Oliphant, A., and Briggs, S. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92-100.
11. Hashimoto, M., Kisseleva, L., Sawa, S., Furukawa, T., Komatsu, S., and Koshiba, T. 2004. A novel rice PR10 protein, RSOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signaling pathway. Plant Cell Physiol. 45:550-559.
12. Hause, B., Maier, W., Miersch, O., Kramell, R., and Strack, D. 2002. Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol. 130:1213-1220.
13. Hurek, T., and Reinhold-Hurek, B. 2003. Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J. Biotechnol. 106:169-178.
14. Hurek, T., Reinhold-Hurek, B., Van Montagu, M., and Kellenberger, E. 1994. Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J. Bacteriol. 176:1913-1923.
15. Hurek, T., Handley, L. L., Reinhold-Hurek, B., and Piché, Y. 2002. Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol. Plant-Microbe Interact. 15:233-242.
16. Iniguez, A. L., Dong, Y., and Triplett, E. W. 2004. Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol. Plant-Microbe Interact. 17:1078-1085.
17. Iniguez, A. L., Dong, Y., Carter, H. D., Ahmer, B. M. M., Stone, J. M., and Triplett, E. W. 2005. Regulation of enteric endophytic bacterial colonization by plant defense. Mol. Plant-Microbe Interact. 18:169-178.
18. James, E. K., and Olivares, F. L. 1998. Infection and colonization of sugar cane and other graminaceous plants by endophytic diazotrophs. Crit. Rev. Plant Sci. 17:77-119.
19. James, E. K., Reis, V. M., Olivares, F. L., Baldandi, J. I., and Döbereiner, J. 1994. Infection of sugar cane by the nitrogen-fixing bacterium Acetobacter diazotrophicus. J. Exp. Bot. 45:757-766.
20. James, E. K., Olivares, F. L., Baldani, J. I., and Döbereiner, J. 1997. Herbaspirillum, an endophytic diazotroph colonizing vascular tissue in leaves of Sorghum bicolor L. Moench. J. Exp. Bot. 48:785-797.
21. Kim, S. T., Cho, K. S., Yu, S., Kim, S. G., Hong, J. C., Han, C. D., Bae, D. W., Nam, M. H., and Kang, K. Y. 2003. Proteomic analysis of differentially expressed proteins induced by rice blast fungus and elicitor in suspension-cultured rice cells. Proteomics 3:2368-2378.
22. Konishi, H., Kitano, H., and Komatsu, S. 2005. Identification of rice root proteins regulated by gibberellin using proteome analysis. Plant Cell Environ. 28:328-339.
23. Kunkel, B. N., and Brooks, D. M. 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5:325-331.
24. Lane, B. G. 2002. Oxalate, germins, and higher-plant pathogens. IUBMB Life 53:67-75.
25. Lange, J., Xie, Y.-P., Broughton, W. J., Vögeli-Lange, R., and Boller, T. 1999. A gene encoding a receptor-like protein kinase in the roots of common bean is differentially regulated in response to pathogens, symbionts and nodulation factors. Plant Sci. 142:133-145.
26. Liu, J., Blaylock, L. A., Endre, G., Cho, J., Town, C. D., VandenBosch, K. A., and Harrison, M. J. 2003. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15:2106-2123.
27. Majoul, T., Chahed, K., Zamiti, E., Ouelhazi, L., and Ghrir, R. 2000. Analysis by two-dimensional electrophoresis of the effect of salt stress on the polypeptide patterns in roots of a salt-tolerant and a salt-sensitive cultivar of wheat. Electrophoresis 21:2562-2565.
28. McGee, J. D., Hamer, J. E., and Hodges, T. K. 2001. Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea. Mol. Plant-Microbe Interact. 14:877-886.
29. Montesano, M., Koiv, V., Mae, A., and Palva, E. T. 2001. Novel receptor-like protein kinases induced by Erwinia carotovora and short oligogalacturonides in potato. Mol. Plant Pathol. 2:339-346.
30. Moons, A., Prinsen, E., Bauw, G., and Van Montagu, M. 1997. Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243-2259.
31. Passardi, F., Penel, C., and Dunand, C. 2004. Performing the paradoxical: How plant peroxidases modify the cell wall. Treans Plant Sci. 9:534-540.
32. Qu, L. J., Chen, J., Liu, M., Pan, N., Okamoto, H., Lin, Z., Li, C., Li, D., Wang, J., Zhu, G., Zhao, X., Chen, X., Gu, H., and Chen, Z. 2003. Molecular cloning and functional analysis of a novel type of Bowman-Birk inhibitor gene family in rice. Plant Physiol. 133:560-570.
33. Rakwal, R., and Komatsu, S. 2000. Role of jasmonate in the rice (Oryza sativa L.) self-defense mechanism using proteome analysis. Electrophoresis 21:2492-2500.
34. Rakwal, R., Agrawal, G. K., and Yonekura, M. 1999. Separation of proteins from stressed rice (Oryza sativa L.) leaf tissues by two-dimensional polyacrylamide gel electrophoresis: Induction of pathogenesis-related and cellular protectant proteins by jasmonic acid, UV irradiation and copper chloride. Electrophoresis 20:3472-3478.
35. Rakwal, R., Agrawal, G. K., and Jwa, N. S. 2001. Characterization of a rice (Oryza sativa L.) Bowman-Birk proteinase inhibitor: Tightly light regulated induction in response to cut, jasmonic acid, ethylene and protein phosphatase 2A inhibitors. Gene 263:189-198.
36. Reinhold, B., Hurek, T., Niemann, E.-G., and Fendrik, J. 1986. Close association of Azospirillum and diazotrophic rods with different root zones of Kallar grass. Appl. Environ. Microbiol. 52:520-526.
37. Reinhold-Hurek, B., and Hurek, T. 1998a. Interactions of gramineous plants with Azoarcus spp. and other diazotrophs: Identification, localization and perspectives to study their function. Crit. Rev. Plant. Sci. 17:29-54.
38. Reinhold-Hurek, B., and Hurek, T. 1998b. Life in grasses: Diazotrophic endophytes. Trends Microbiol. 6:139-144.
39. Reinhold-Hurek, B., Hurek, T., Claeyssens, M., and Van Montagu, M. 1993. Cloning, expression in Escherichia coli, and characterization of cellulolytic enzymes of Azoarcus sp., a root-invading diazotroph. J. Bacteriol. 175:7056-7065.
40. Salekdeh, G. H., Siopongco, J., Wade, L. J., Ghareyazie, B., and Bennett, J. 2002. A proteomic approach to analyzing drought- and salt-responsiveness in rice. Field Crops Res. 76:199-219.
41. 2 incorporation following inoculation of sterile plants with Acetobacter diazotrophicus wild-type and nif mutant strains. Mol. Plant-Microbe Interact. 14:358-366.
42. Shen, S., Jing, Y., and Kuang, T. 2003. Proteomics approach to identify wound-response related proteins from rice leaf sheath. Proteomics 3:527-535.
43. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. 1996. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
44. Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Metraux, J. P., and Raskin, I. 1995. Salicylic acid in rice biosynthesis, conjugation, and possible role). Plant Physiol. 108:633-639.
45. Turner, J. G., Ellis, C., and Devoto, A. 2002. The jasmonate signal pathway. Plant Cell 14:S153-S164.
46. Van Damme, E. J., Zhang, W., and Peumans, W. J. 2004. Induction of cytoplasmic mannose-binding jacalin-related lectins is a common phenomenon in cereals treated with jasmonate methyl ester. Comm. Appl. Biol. Sci. 69:23-31.
47. van Loon, L. C., and van Strien, E. A. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55:85-97.
48. van Loon, L. C., Bakker, P. A., and Pieterse, C. M. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-483.
49. Vernoud, V., Horton, A. C., Yang, Z., and Nielsen, E. 2003. Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol. 131:1191-1208.
50. Wang, K. L., Li, H., and Ecker, J. R. 2002. Ethylene biosynthesis and signaling networks. Plant Cell 14 Suppl:S131-151.
51. Wang, Y., Ohara, Y., Nakayashiki, H., Tosa, Y., and Mayama, S. 2005. Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas flourescents FTP9601-T5 in Arabidopsis. Mol. Plant-Microbe Interact. 18:385-396.
52. Yamaguchi, T., Nakayama, K., Hayashi, T., Tanaka, Y., and Koike, S. 2002. Molecular cloning and characterization of a novel beta-1,3-glucanase gene from rice. Biosci. Biotech. Biochem. 66:1403-1406.
53. Yanni, Y. G., Rizk, R. Y., Corich, V., Squartini, A., Ninke, K., Philip-Hollingsworth, S., Orgambide, G., De Bruijn, F., Stoltzfus, J., Buckley, D., Schmidt, T. M., Mateos, P. F., Ladha, J. K., and Dazzo, F. B. 1997. Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99-114.
54. Yu, J., Hu, S., Wang, J., Wong, G. K., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X., Cao, M., Liu, J., Sun, J., Tang, J., Chen, Y., Huang, X., Lin, W., Ye, C., Tong, W., Cong, L., Geng, J., Han, Y., Li, L., Li, W., Hu, G., Li, J., Liu, Z., Qi, Q., Li, T., Wang, X., Lu, H., Wu, T., Zhu, M., Ni, P., Han, H., Dong, W., Ren, X., Feng, X., Cui, P., Li, X., Wang, H., Xu, X., Zhai, W., Xu, Z., Zhang, J., He, S., Xu, J., Zhang, K., Zheng, X., Dong, J., Zeng, W., Tao, L., Ye, J., Tan, J., Chen, X., He, J., Liu, D., Tian, W., Tian, C., Xia, H., Bao, Q., Li, G., Gao, H., Cao, T., Zhao, W., Li, P., Chen, W., Zhang, Y., Hu, J., Liu, S., Yang, J., Zhang, G., Xiong, Y., Li, Z., Mao, L., Zhou, C., Zhu, Z., Chen, R., Hao, B., Zheng, W., Chen, S., Guo, W., Tao, M., Zhu, L., Yuan, L., and Yang, H. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79-92.