Involvement of a class III peroxidase and the mitochondrial protein TSPO in oxidative burst upon treatment of moss plants with a fungal elicitor

Molecular Plant-Microbe Interactions

Volumn 25, Issue 3, 2012, Pages 363-371

  Lehtonen, Mikko T ^a   Akita, Motomu ^a,b   Frank, Wolfgang ^c   Reski, Ralf ^c   Valkonen, Jari P T ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b KINKI UNIVERSITY   (Japan)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHITOSAN; MITOCHONDRIAL PROTEIN; PEROXIDASE; PLANT RNA; SUPEROXIDE; TETRAPYRROLE DERIVATIVE; VEGETABLE PROTEIN;

ARTICLE; BASIDIOMYCETES; BRYOPSIDA; ENZYMOLOGY; FUSARIUM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; PHENOTYPE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; PLANT IMMUNITY; RESPIRATORY BURST;

BASIDIOMYCOTA; BRYOPSIDA; CHITOSAN; FUSARIUM; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MITOCHONDRIAL PROTEINS; MUTATION; OXIDATION-REDUCTION; PEROXIDASES; PHENOTYPE; PLANT IMMUNITY; PLANT PROTEINS; RESPIRATORY BURST; RNA, PLANT; STRESS, PHYSIOLOGICAL; SUPEROXIDES; TETRAPYRROLES;

ARABIDOPSIS; BRYOPHYTA; PHYSCOMITRELLA; PHYSCOMITRELLA PATENS;

EID: 84857600224     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-10-11-0265     Document Type: Article

References (53)

1. Akita, M., Lehtonen, M. T., Koponen, H., Marttinen, E. M., and Valkonen, J. P. T. 2011. Infection of the Sunagoke moss panels with fungal pathogens hampers sustainable greening in urban environments. Sci. Total. Environ. 409:3166-3173.
2. Almagro, L., Gómez Ros, L. V., Belchi-Navarro, S., Bru, R., Ros Barceló, A., and Pedreño, M. A. 2009. Class III peroxidases in plant defence reactions. J. Exp. Bot. 60:377-390.
3. Andersson, R. A., Akita, M., Pirhonen, M., Gammelgård, E., and Valkonen, J. P. T. 2005. Moss-Erwinia pathosystem reveals possible similarities in pathogenesis and pathogen defense in vascular and nonvascular plants. J. Gen. Plant. Pathol. 71:23-28. (Pubitemid 40640881)
4. Angelova, M. B., Pashova, S. B., Spasova, B. K., Vassilev, S. V., and Slokoska, L. S. 2005. Oxidative stress response of filamentous fungi induced by hydrogen peroxide and paraquat. Mycol. Res. 109:150-158. (Pubitemid 40428303)
5. Anterola, A., Göbel, C., Hornung, E., Sellhorn, G., Feussner, I., and Grimes, H. 2009. Physcomitrella patens has lipoxygenases for both eicosanoid and octadecanoid pathways. Phytochemistry 70:40-52.
6. Apel, K., and Hirt, H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373-399. (Pubitemid 38940937)
7. Ashton, N. W., and Cove, D. J. 1977. The isolation and preliminary characterisation of auxotrophic and analogue resistant mutants of the moss, Physcomitrella patens. Mol. Gen. Genet. 154:87-95. (Pubitemid 8114661)
8. Audenaert, K., De Meyer, G. B., and Hofte, M. M. 2002. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128:491-501. (Pubitemid 34190864)
9. Balsemão-Pires, E., Jaillais, Y., Olson, B., Andrade, L., Umen, J., Chory, J., and Sachetto-Martins, G. 2011. The Arabidopsis translocator protein (AtTSPO) is regulated at multiple levels in response to salt stress and perturbations in tetrapyrrole metabolism. BMC Plant Biol. 11:108.
10. Beckett, R., Minibayeva, F., Luthje, S., and Bottger, M. 2004. Reactive oxygen species metabolism in desiccation-stressed thalli of the liverwort Dumortiera hirsuta. Physiol. Plant. 122:3-10. (Pubitemid 39246923)
11. Bindschedler, L., Dewdney, J., Blee, K., Stone, J., Asai, T., Plotnikov, J., Denoux, C., Hayes, T., Gerrish, C., Davies, D., Ausubel, F., and Bolwell, G. 2006. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47:851-863. (Pubitemid 44326435)
12. Brosché, M., Overmyer, K., Wrzaczek, M., Kangasjärvi, J., and Kangasjärvi, S. 2010. Stress signaling III: Reactive oxygen species. Pages 91-102 in: Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation. A. Pareek, S. K. Sopory, H. J. Bohnert, and Govindjee, eds. Springer, Dordrecht, The Netherlands.
13. Caldo, R. A., Nettleton, D., and Wise, R. P. 2004. Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. Plant Cell 16:2514-2528. (Pubitemid 39247088)
14. Cove, D. 2005. The moss Physcomitrella patens. Annu. Rev. Genet. 39:339-358. (Pubitemid 43011119)
15. Cuming, A. C. 2009. Plant-pathogen interactions: A view from the evolutionary basement. New Phytol. 183:237-239.
16. DiLeo, M. V., Pye, M. F., Roubtsova, T. V., Duniway, J. M., MacDonald, J. D., Rizzo, D. M., and Bostock, R. M. 2010. Abscisic acid in salt stress predisposition to Phytophthora root and crown rot in tomato and chrysanthemum. Phytopathology 100:871-879.
17. Frank, W., Baar, K., Qudeimat, E., Woriedh, M., Alawady, A., Ratnadewi, D., Gremillon, L., Grimm, B., and Reski, R. 2007. A mitochondrial protein homologous to the mammalian peripheral-type benzodiazepine receptor is essential for stress adaptation in plants. Plant J. 51:1004-1018. (Pubitemid 47373568)
18. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. 2006. Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9:436-442.
19. Govrin, E. M., and Levine, A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10:751-757. (Pubitemid 30466937)
20. Hano, C., Addi, M., Fliniaux, O., Bensaddek, L., Duverger, E., Mesnard, F., Lamblin, F., and Laine, E. 2008. Molecular characterization of cell death induced by a compatible interaction between Fusarium oxysporum f. sp. linii and flax (Linum usitatissimum) cells. Plant Physiol. Biochem. 46:590-600.
21. Hofius, D., Munch, D., Bressendorff, S., Mundy, J., and Petersen, M. 2011. Role of autophagy in disease resistance and hypersensitive response-associated cell death. Cell Death Differ. 18:1257-1262.
22. Kawano, T. 2003. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep. 21:829-837. (Pubitemid 36708495)
23. Keller, T., Damude, H., Werner, D., Doerner, P., Dixon, R., 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.
24. Knaul, J. Z., Hudson, S. M., and Creber, K. A. M. 1999. Improved mechanical properties of chitosan fibers. J. Appl. Polym. Sci. 72:1721-1732.
25. Krol, E., Mentzel, T., Chinchilla, D., Boller, T., Felix, G., Kemmerling, B., Postel, S., Arents, M., Jeworutzki, E., Al-Rasheid, K. A. S., Becker, D., and Hedrich, R. 2010. Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J. Biol. Chem. 285:13471-13479.
26. Lawton, M., and Saidasan, H. 2009. Pathogenesis in mosses. Annu. Plant Rev. 36:298-339.
27. Lehtonen, M. T., Akita, M., Kalkkinen, N., Ahola-Iivarinen, E., Rönnholm, G., Somervuo, P., Thelander, M., and Valkonen, J. P. T. 2009. Quicklyreleased peroxidase of moss in defense against fungal invaders. New Phytol. 183:432-443.
28. Lenz, H. D., Haller, E., Melzer, E., Gust, A. A., and Nuernberger, T. 2011. Autophagy controls plant basal immunity in a pathogenic lifestyledependent manner. Autophagy 7:773-774.
29. Li, J. L. Y., Sulaiman, M., Beckett, R. P., and Minibayeva, F. V. 2010. Cell wall peroxidases in the liverwort Dumortiera hirsuta are responsible for extracellular superoxide production, and can display tyrosinase activity. Physiol. Plant. 138:474-484.
30. Mayaba, N., Minibayeva, F., and Beckett, R. 2002. An oxidative burst of hydrogen peroxide during rehydration following desiccation in the moss Atrichum androgynum. New Phytol. 155:275-283. (Pubitemid 34838055)
31. Maxwell, D. P., Wang, Y., and McIntosh, L. 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. U.S.A. 96:8271-8276. (Pubitemid 29328444)
32. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M. A., Shulaev, V., Dangl, J. L., and Mittler R. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2:ra45.
33. Mochizuki, N., Tanaka, R., Grimm, B., Masuda, T., Moulin, M., Smith, A. G., Tanaka, A., and Terry, M. J. 2010. The cell biology of tetrapyrroles: A life and death struggle. Trends Plant Sci. 15:488-498.
34. Molina, A., Bueno, P., Marín, M. C., Rodríguez-Rosales, M. P., Belver, A., Venema, K., and Donaire, J. P. 2002. Involvement of endogenous salicylic acid content, lipoxygenase and antioxidant enzyme activities in the response of tomato cell suspension cultures to NaCl. New Phytol. 156:409-415. (Pubitemid 35456808)
35. Nanda, A. K., Andrio, E., Marino, D., Pauly, N., and Dunand, C. 2010. Reactive oxygen species during plant-microorganism early interactions. J. Integr. Plant Biol. 52:195-204.
36. Oliver, J. P., Castro, A., Gaggero, C., Cascón, T., Schmelz, E. A., Castresana, C., and Ponce de León I. 2009. Pythium infection activates conserved plant defense responses in mosses. Planta 230:569-579.
37. Noda, N. N., Ohsumi, Y., and Inagaki, F. 2010. Atg8-family interacting motif crucial for selective autophagy. FEBS (Fed. Eur. Biochem. Soc.) Lett. 584:1379-1385.
38. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45-e45.
39. Ponce de León, I., Oliver, J. P., Castro, A., Gaggero, C., Bentancor, M., and Vidal, S. 2007. Erwinia carotovora elicitors and Botrytis cinerea activate defense responses in Physcomitrella patens. BMC Plant Biol. 7:52.
40. Proctor, M. C. F., Ligrone, R., and Duckett, J. G. 2007. Desiccation tolerance in the moss Polytrichum formosum: Physiological and fine-structural changes during desiccation and recovery. Ann. Bot. 99:75-93. (Pubitemid 47355455)
41. Rensing, S. A., Lang, D., Zimmer, A. D., Terry, A., Salamov, A., Shapiro, H., Nishiyama, T., Perroud, P.-F., Lindquist, E., Kamisugi, Y., Tanahashi, T., Sakakibara, K., Fujita, T., Oishi, K., Shin-I, T., Kuroki, Y., Toyoda, A., Suzuki, Y, Hashimoto, S., Yamaguchi, K., Sugano, S., Kohara, Y., Fujiyama, A., Anterola, A., Aoki, S., Ashton, N., Barbazuk, W. B., Barker, E., Bennetzen, J., Blankenship, R., Cho, S. H., Dutcher, S. K., Estelle, M., Fawcett, J. A., Gundlach, H., Hanada, K., Hey, A., Hicks, K. A., Hughes, J., Lohr, M., Mayer, K., Melkozernov, A., Murata, T., Nelson, D., Pils, B., Prigge, M., Reiss, B., Renner, T., Rombauts, S., Rushton, P., Sanderfoot, A., Schween, G., Shiu, S.-H., Stueber, K., Theodoulou, F. L., Tu, H., de Peer, Y. V., Verrier, P. J., Waters, E., Wood, A., Yang, L., Cove, D., Cuming, A. C., Hasebe, M., Lucas, S., Mishler, B. D., Reski, R., Grigoriev, I. V., Quatrano, R. S., and Boore, J. L. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64-69.
42. Rodriguez-Rosales, M., Kerkeb, L., Bueno, P., and Donaire, J. 1999. Changes induced by NaCl in lipid content and composition, lipoxygenase, plasma membrane H+-ATPase and antioxidant enzyme activities of tomato (Lycopersicon esculentum. Mill) calli. Plant Sci. 143:143-150. (Pubitemid 29315129)
43. Schuller, D., Ban, N., Vanhuystee, R., McPherson, A., and Poulos, T. 1996. The crystal structure of peanut peroxidase. Structure 4:311-321.
44. Shibuya, N., and Minami, E. 2001. Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol. 59:223-233. (Pubitemid 34018124)
45. Strepp, R., Scholz, S., Kruse, S., Speth, V., and Reski, R. 1998. Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc. Natl. Acad. Sci. U.S.A. 95:4368-4373. (Pubitemid 28207918)
46. Tarpey, M. M., Wink, D. A., and Grisham, M. B. 2004. Methods for detection of reactive metabolites of oxygen and nitrogen: In vitro and in vivo considerations. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286:R431-R444. (Pubitemid 38252605)
47. Torres, M. 2010. ROS in biotic interactions. Physiol. Plant. 138:414-429.
48. Torres, M. A., Dangl, J. L., and Jones, J. D. G. 2002. 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. (Pubitemid 34060393)
49. Uehara, K., Maruyama, N., Huang, C.K., and Nakano, M. 1993. The first application of a chemiluminescence probe, 2-methyl-6-[p-methoxyphenyl]-3,7- dihydroimidazo[1,2-a]pyrazin-3-one (MCLA), for detecting O2-production, in vitro, from Kupffer cells stimulated by phorbol myristate acetate. FEBS (Fed. Eur. Biochem. Soc.) Lett. 335:167-170. (Pubitemid 23350400)
50. Van Aken, O., Zhang, B., Carrie, C., Uggalla, V., Paynter, E., Giraud, E., and Whelan, J. 2009. Defining the Mitochondrial Stress Response in Arabidopsis thaliana. Mol. Plant 2:1310-1324.
51. Vanhee, C., Zapotoczny, G., Masquelier, D., Ghislain, M., and Batoko, H. 2011. The Arabidopsis multistress regulator TSPO is a heme binding membrane protein and a potential scavenger of porphyrins via an autophagy-dependent degradation mechanism. Plant Cell 23:785-805.
52. Walley, J. W., Coughlan, S., Hudson, M. E., Covington, M. F., Kaspi, R., Banu, G., Harmer, S. L., and Dehesh, K. 2007. Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. PLoS Genet. 3:e172.
53. Wojtaszek, P. 1997. Oxidative burst: An early plant response to pathogen infection. Biochem. J. 322:681-692. (Pubitemid 27135612)