Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum

Plant Cell

Volumn 16, Issue 3, 2004, Pages 616-628

  Sagi, Moshe ^a   Davydov, Olga ^b   Orazova, Saltanat ^a   Yesbergenova, Zhazira ^a   Ophir, Ron ^b   Stratmann, Johannes W ^c   Fluhr, Robert ^b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; ENZYMES; GENES; REDOX REACTIONS;

PATHOGENS; PHENOTYPE;

PLANTS (BOTANY);

LYCOPERSICON; LYCOPERSICON ESCULENTUM;

EID: 1542437689     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.019398     Document Type: Article

References (47)

1. Ahmad, K., and Henikoff, S. (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9, 1191-1200.
2. Allan, A.C., and Fluhr, R. (1997). Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9, 1559-1572.
3. Baker, C.J., and Orlandi, E.W. (1995). Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33, 299-321.
4. Banfi, B., Molnar, G., Maturana, A., Steger, K., Hegedus, B., Demaurex, N., and Krause, K.H. (2001). A Ca2+-activated NADPH oxidase in testis, spleen, and lymph nodes. J. Biol. Chem. 276, 37594-37601.
5. Bokoch, G.M., Bohl, B.P., and Chuang, T.H. (1994). Guanine-nucleotide exchange regulates membrane translocation of Rac/Rho GTP-binding proteins. J. Biol. Chem. 269, 31674-31679.
6. Brandstadter, J., Rossbach, C., and Theres, K. (1996). Expression of genes for a defensin and a proteinase inhibitor in specific areas of the shoot apex and the developing flower in tomato. Mol. Gen. Genet. 252, 146-154.
7. Cheong, Y.H., Chang, H.S., Gupta, R., Wang, X., Zhu, T., and Luan, S. (2002). Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129, 661-677.
8. Coelho, S.M., Taylor, A.R., Ryan, K.P., Sousa-Pinto, I., Brown, M.T., and Brownlee, C. (2002). Spatiotemporal patterning of reactive oxygen production and Ca2+ wave propagation in fucus rhizoid cells. Plant Cell 14, 2369-2381.
9. Cross, A.R., and Jones, O.T. (1986). The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase. Blochem. J. 237, 111-116.
10. Denu, J.M. (2003). Linking chromatin function with metabolic networks: Sir2 family of NAD(+)-dependent deacetylases. Trends Biochem. Sci. 28, 41-48.
11. Desikan, R., Mackerness, S.A.H., Hancock, J.T., and Neill, S.J. (2001). Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127, 159-172.
12. Doke, N., and Ohashi, Y. (1988). Involvement of an O2-generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus. Physiol. Mol. Plant Pathol. 32, 163-175.
13. Donald, S.P., Sun, X.Y., Hu, C.A.A., Yu, J., Mei, J.M., Valle, D., and Phang, J.M. (2001). Proline oxidase, encoded by p53-induced gene-6, catalyzes the generation of proline-dependent reactive oxygen species. Cancer Res. 61, 1810-1815.
14. Foreman, J., Demidchik, V., Bothwell, J.H., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., Jones, J.D., Davies, J.M., and Dolan, L. (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442-446.
15. Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E.M., and Coupland, G. (1997). A polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386, 44-51.
16. Graan, T., and Ort, D.R. (1984). Quantitation of the rapid electron donors to P700, the functional plastoquinone pool, and the ratio of the photosystems in spinach chloroplasts. J. Biol. Chem. 259, 14003-14010.
17. Ho, L.C., Belda, R., Brown, M., Andrews, J., and Adams, P. (1993). Uptake and transport of calcium and the possible causes of blossom-end rot in tomato. J. Exp. Bot. 44, 509-518.
18. Immink, R.G.H., Ferrario, S., Busscher-Lange, J., Kooiker, M., Busscher, M., and Angenent, G.C. (2003). Analysis of the petunia MADS-box transcription factor family. Mol. Genet. Genomics 268, 598-606.
19. Jiang, M., and Zhang, J. (2003). Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defence in leaves of maize seedlings. Plant Cell Environ. 26, 929-939.
20. Joo, J.H., Bae, Y.S., and Lee, U.S. (2001). Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126, 1055-1060.
21. Keller, T., Damude, H.G., Werner, D., Doerner, P., Dixon, R.A., and Lamb, C. (1998). A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10, 255-266.
22. Krizek, B.A., and Meyerowitz, E.M. (1996). The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122, 11-22.
23. Kwak, J.M., Mori, I.C., Pei, Z.M., Leonhardt, N., Torres, M.A., Dangl, J.L., Bloom, R.E., Bodde, S., Jones, J.D.G., and Schroeder, J.I. (2003). NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623-2633.
24. Lee, G.I., and Howe, G.A. (2003). The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J. 33, 567-576.
25. Liscum, E., and Reed, J.W. (2002). Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol. Biol. 49, 387-400.
26. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410.
27. Mou, Z., Fan, W., and Dong, X. (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-944.
28. Narvaez-Vasquez, J., and Ryan, C.A. (2002). The systemin precursor gene regulates both defensive and developmental genes in Solanum tuberosum. Proc. Natl. Acad. Sci. USA 99, 15818-15821.
29. Neill, S., Desikan, R., and Hancock, J. (2002a). Hydrogen peroxide signalling. Curr. Opin. Plant Biol. 5, 388-395.
30. Neill, S.J., Desikan, R., Clarke, A., Hurst, R.D., and Hancock, J.T. (2002b). Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53, 1237-1247.
31. Oleksiak, M.F., Churchill, G.A., and Crawford, D.L. (2002). Variation in gene expression within and among natural populations. Nat. Genet. 32, 261-266.
32. Ori, N., Eshed, Y., Paran, I., Presting, G., Aviv, D., Tanksley, S., Zamir, D., and Fluhr, R. (1997). The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell 9, 521-532.
33. Orozco-Cardenas, M., and Ryan, C.A. (1999). Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 96, 6553-6557.
34. Orozco-Cardenas, M.L., Narvaez-Vasquez, J., and Ryan, C.A. (2001). Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13, 179-191.
35. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E., and Schroeder, J.I. (2000). Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731-734.
36. Pnueli, L., Carmel-Goren, L., Hareven, D., Gutfinger, T., Alvarez, J., Ganal, M., Zamir, D., and Lifschitz, E. (1998). The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125, 1979-1989.
37. Ryan, C.A. (2000). The systemin signaling pathway: Differential activation of plant defensive genes. Biochim. Biophys. Acta 1477, 112-121.
38. Sagi, M., and Fluhr, R. (2001). Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126, 1281-1290.
39. Savaldi-Goldstein, S., Aviv, D., Davydov, O., and Fluhr, R. (2003). Alternative splicing modulation by a LAMMER kinase impinges on developmental and transcriptome expression. Plant Cell 15, 926-938.
40. Simon-Plas, F., Elmayan, T., and Blein, J.P. (2002). The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J. 31, 137-147.
41. Strassner, J., Schaller, F., Frick, U.B., Howe, G.A., Weiler, E.W., Amrhein, N., Macheroux, P., and Schaller, A. (2002). Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound response. Plant J. 32, 585-601.
42. Thordal-Christensen, H., Zhang, Z.G., Wei, Y.D., and Collinge, D.B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
43. Tian, Q., and Reed, J.W. (1999). Control of auxin-regulated root development by the Arabidopsis thallana SHY2/IAA3 gene. Development 126, 711-721,
44. Torres, M.A., Dangl, J.L., and Jones, J.D.G. (2002). Arabidopsis gp91(phox) homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99, 517-522.
45. Torres, M.A., Onouchi, H., Hamada, S., Machida, C., Hammond-Kosack, K.E., and Jones, J.D.G. (1998). Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J. 14, 365-370.
46. Vranova, E., Atichartpongkul, S., Villarroel, R., Van Montagu, M., Inze, D., and Van Camp, W. (2002). Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc. Natl. Acad. Sci. USA 99, 10870-10875.
47. Yoshioka, H., Numata, N., Nakajima, K., Katou, S., Kawakita, K., Rowland, O., Jones, J.D., and Doke, N. (2003). Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15, 706-718.