Host-pathogen interactions: Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection

Science Signaling

Volumn 7, Issue 320, 2014, Pages

  Siddique, Shahid ^a   Matera, Christiane ^a   Radakovic, Zoran S ^a   Hasan, M Shamim ^a,b   Gutbrod, Philipp ^a   Rozanska, Elzbieta ^c   Sobczak, Miroslaw ^c   Torres, Miguel Angel ^d   Grundler, Florian M W ^a  

^a UNIVERSITY OF BONN   (Germany)

^b HAJEE MOHAMMAD DANESH SCIENCE AND TECHNOLOGY UNIVERSITY   (Bangladesh)

^c WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^d UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; RBOHD PROTEIN; RBOHF PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SALICYLIC ACID; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; RBOHF PROTEIN, ARABIDOPSIS; RESPIRATORY BURST OXIDASE HOMOLOG D, ARABIDOPSIS;

ARABIDOPSIS THALIANA; ARTICLE; CELL DEATH; CELL MEMBRANE; CELL VIABILITY; ENZYME ACTIVITY; HELMINTH; HETERODERA SCHACHTII; NEMATODAL PLANT DISEASE; NEMATODE; NONHUMAN; PARASITOSIS; PLANT CELL; PLANT GROWTH; PLANT ROOT; PRIORITY JOURNAL; TRANSGENIC PLANT; ANIMAL; ARABIDOPSIS; ENZYMOLOGY; GENETICS; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DEATH; NADPH OXIDASE; NEMATODA; PLANT DISEASES; PLANT ROOTS; REACTIVE OXYGEN SPECIES;

EID: 84898858570     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004777     Document Type: Article

References (37)

1. B. H. Segal, M. J. Grimm, A. N. H. Khan, W. Han, T. S. Blackwell, Regulation of innate immunity by NADPH oxidase. Free Radic. Biol. Med. 53, 72-80 (2012)
2. J. D. Lambeth, NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189 (2004)
3. M. A. Torres, J. L. Dangl, J. D. G. Jones, Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. U. S. A. 99, 517-522 (2002)
4. Q. J. Groom, M. A. Torres, A. P. Fordham-Skelton, K. E. Hammond-Kosack, N. J. Robinson, J. D. G. Jones, rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J. 10, 515-522 (1996)
5. M. A. Torres, H. Onouchi, S. Hamada, C. Machida, K. E. Hammond-Kosack, J. D. G. Jones, Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J. 14, 365-370 (1998)
6. N. Doke, Involvement of superoxide anion generation in the hypersensitive response of potato-tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Pathol. 23, 345-357 (1983)
7. C. Lamb, R. A. Dixon, The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275 (1997)
8. H. Yoshioka, N. Numata, K. Nakajima, S. Katou, K. Kawakita, O. Rowland, J. D. G. Jones, N. Doke, Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15
9. D. Marino, C. Dunand, A. Puppo, N. Pauly, A burst of plant NADPH oxidases. Trends Plant Sci. 17, 9-15 (2012)
10. W. E. Durrant, X. Dong, Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185-209 (2004)
11. D. A. Dempsey, J. Shah, D. F. Klessig, Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18, 547-575 (1999)
12. J. Durner, J. Shah, D. F. Klessig, Salicylic acid and disease resistance in plants. Trends Plant Sci. 2, 266-274 (1997)
13. J. Draper, Salicylate, superoxide synthesis and cell suicide in plant defence. Trends Plant Sci. 2, 162-165 (1997)
14. K. Overmyer, M. Brosché, J. Kangasjärvi, Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 8, 335-342 (2003)
15. R. A. Dietrich, M. H. Richberg, R. Schmidt, C. Dean, J. L. Dangl, A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88, 685-694 (1997)
16. M. A. Torres, J. D. G. Jones, J. L. Dangl, Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37, 1130-1134 (2005)
17. U. Wyss, F. M. W. Grundler, Feeding behavior of sedentary plant parasitic nematodes. Netherlands J. Plant Pathol. 98, 165-173 (1992)
18. M. Sobczak, W. A. Golinowski, F. M. W. Grundler, Ultrastructure of feeding plugs and feeding tubes formed by Heterodera schachtii. Nematology 1, 363-374 (1999)
19. M. Sobczak, W. Golinowski, F. M. W. Grundler, Changes in the structure of Arabidopsis thaliana roots induced during development of males of the plant parasitic nematode Heterodera schachtii. Eur. J. Plant Pathol. 103, 113-124 (1997)
20. J. Muller, K. Rehbock, U. Wyss, Growth of Heterodera schachtii with remarks on amounts of food consumed. Revue Nematol. 4, 227-234 (1981)
21. S. Siddique, S. Endres, J. M. Atkins, D. Szakasits, K. Wieczorek, J. Hofmann, C. Blaukopf, P. E. Urwin, R. Tenhaken, F. M. W. Grundler, D. P. Kreil, H. Bohlmann, Myo-inositol oxygenase genes are involved in the development of syncytia induced by Heterodera schachtii in Arabidopsis roots. New Phytol. 184, 457-472 (2009)
22. D. L. Trudgill, Effect of environment on sex determination in Heterodera rostochiensis. Nematologica 13, 263-272 (1967)
23. G. Miller, K. Schlauch, R. Tam, D. Cortes, M. A. Torres, V. Shulaev, J. L. Dangl, R. Mittler, The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45 (2009)
24. C. K. Auh, T. M. Murphy, Plasma membrane redox enzyme is involved in the synthesis of O2 ? and H2O2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol. 107, 1241-1247 (1995)
25. G. H. Waetzig, M. Sobczak, F. M. W. Grundler, Localization of hydrogen peroxide during the defence response of Arabidopsis thaliana against the plant-parasitic nematode Heterodera glycines. Nematology 1, 681-686 (1999)
26. H. Thordal-Christensen, Z. G. Zhang, Y. D. Wei, D. B. Collinge, Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194 (1997)
27. K. A. Kristiansen, P. E. Jensen, I. M. Møller, A. Schulz, Monitoring reactive oxygen species formation and localisation in living cells by use of the fluorescent probe CM-H2DCFDA and confocal laser microscopy. Physiol. Plant 136, 369-383 (2009)
28. L. Dolan, K. Janmaat, V. Willemsen, P. Linstead, S. Poethig, K. Roberts, B. Scheres, Cellular organisation of the Arabidopsis thaliana root. Development 119, 71-84 (1993)
29. X. Y. Qiang, B. Zechmann, M. U. Reitz, K. H. Kogel, P. Schäfer, The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24, 794-809 (2012)
30. M. C. Wildermuth, J. Dewdney, G. Wu, F. M. Ausubel, Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562-565 (2001)
31. M. Pogány, U. von Rad, S. Grün, A. Dongó, A. Pintye, P. Simoneau, G. Bahnweg, L. Kiss, B. Barna, J. Durner, Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiol. 151, 1459-1475 (2009)
32. T. Hewezi, P. J. Howe, T. R. Maier,R. S. Hussey, M. G. Mitchum, E. L. Davis, T. J. Baum, Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol. 152, 968-984 (2010)
33. D. Szakasits, P. Heinen, K. Wieczorek, J. Hofmann, F. Wagner, D. P. Kreil, P. Sykacek, F. M. W. Grundler, H. Bohlmann, The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J. 57, 771-784 (2009)
34. J. Hofmann, A. El Ashry, S. Anwar, A. Erban, J. Kopka, F. Grundler, Metabolic profiling reveals local and systemic responses of host plants to nematode parasitism. Plant J. 62, 1058-1071 (2010)
35. P. C. Sijmons, F. M. W. Grundler, N. von Mende, P. R. Burrows, U. Wyss, Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J. 1, 245-254 (1991)
36. T. Stiernagle, Maintenance of C. elegans, in C. elegans: A Practical Approach, I. Hope, Ed. (Oxford University Press, Oxford, 2006)
37. K. J. Livak, T. D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2?DDCT method. Methods 25, 402-408 (2001).