The mutualistic fungus piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen fusarium culmorum

Molecular Plant-Microbe Interactions

Volumn 26, Issue 5, 2013, Pages 599-605

  Harrach, Borbála D ^a   Baltruschat, Helmut ^b   Barna, Balázs ^a   Fodor, József ^a   Kogel, Karl Heinz ^c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b ANHALT UNIVERSITY OF APPLIED SCIENCES   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; ASCORBIC ACID; GLUTATHIONE; GLUTATHIONE DEHYDROGENASE (ASCORBATE); OXIDOREDUCTASE; SUPEROXIDE DISMUTASE;

ARTICLE; BASIDIOMYCETES; FUSARIUM; HORDEUM; LIPID PEROXIDATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT ROOT;

ANTIOXIDANTS; ASCORBIC ACID; BASIDIOMYCOTA; FUSARIUM; GLUTATHIONE; HORDEUM; LIPID PEROXIDATION; OXIDOREDUCTASES; PLANT ROOTS; SUPEROXIDE DISMUTASE;

FUNGI; FUSARIUM; FUSARIUM CULMORUM; HORDEUM; HORDEUM VULGARE; PIRIFORMOSPORA INDICA;

EID: 84876008947     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-09-12-0216-R     Document Type: Article

References (46)

1. Apel, K., and Hirt, H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Ann. Rev. Plant Biol. 55:373-399.
2. Baltruschat, H., Fodor, J., Harrach, B. D., Niemczyk, E., Barna, B., Gullner, G., Janeczko, A., Kogel, K.-H., Schäfer, P., Schwarczinger, I., Zuccaro, A., and Skoczowski, A. 2008. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol. 180:501-510.
3. Boddu, J., Cho, S., Kruger, W. M., and Muehlbauer, G. J. 2006. Transcriptome analysis of the barley-Fusarium graminearum interaction. Mol. Plant-Microbe Interact. 19:407-417.
4. Conklin, P. L., Williams, E. H., and Last, R. L. 1996. Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc. Natl. Acad. Sci. U.S.A. 93:9970-9974.
5. Cruz, C., Martins-Loucão, M. A., and Varma, A. 2010. The influence of plant co-culture of tomato plants with Piriformospora indica on biomass accumulation and stress tolerance. Acta Hortic. 868:123-128.
6. Cuzick, A., Maguire, K., and Hammond-Kosack, K. E. 2009. Lack of the plant signalling component SGT1b enhances disease resistance to Fusarium culmorum in Arabidopsis buds and flowers. New Phytol. 181:901-912.
7. DeLong, J. M., Prange, R. K., Hodges, D. M., Forney, C.F., Bishop, M.C., and Quilliam, M. 2002. Using a modified ferrous oxidation xylenol orange (FOX) assay for detection of lipid hydroperoxides in plant tissue. J. Agric. Food Chem. 50:248-254.
8. Deshmukh, S. D., and Kogel, K.-H. 2007. Piriformospora indica protects barley from root rot caused by Fusarium graminearum. J. Plant Dis. Prot. 114:263-268.
9. Desmond, O. J., Manners, J. M., Schenk, P. M., Maclean, D. J., and Kazan, K. 2008. Gene expression analysis of the wheat response to infection by Fusarium pseudograminearum. Physiol. Mol. Plant Pathol. 73:40-47.
10. Do, T. Q., Schultz, J. R., and Clarke, C. F. 1996. Enhanced sensitivity of ubiquinone-deficient mutants of Saccharomyces cerevisiae to products of autoxidized polyunsaturated fatty acids. Proc. Natl. Acad. Sci. U.S.A. 93:7534-7539.
11. Dolatabadi, H. K., Goltapeh, E. M., Mohammadi, N., Rabiey, M., Rohani, N., and Varma, A. 2012. Biocontrol potential of root endophytic fungi and Trichoderma species against Fusarium wilt of lentil under in vitro and greenhouse conditions. J. Agric. Sci. Technol. 14:407-420.
12. Eltayeb, A. E., Kawano, N., Badawi, G. H., Kaminaka, H., Sanekata, T., Shibahara, T., Inanaga, S., and Tanaka, K. 2007. Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225:1255-1264.
13. Fakhro, A., Andrade-Linares, D. R., von Bargen, S., Bandte, M., Buttner, C., Grosch, R., Schwarz, D., and Franken, P. 2010. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20:191-200.
14. Foyer, C. H., and Noctor, G. 2005. Oxidant and antioxidant signalling in plants: A re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28:1056-1071.
15. Franken, P. 2012. The plant strengthening root endophyte Piriformospora indica: Potential application and the biology behind. Appl. Microbiol. Biotechnol. 96:1455-1464.
16. Govrin, E. M., and Levine, A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10:751-757.
17. Halliwell, B., and Chirico, S. 1993. Lipid peroxidation: Its mechanism, measurement, and significance. Am. J. Clin. Nutr. 57(suppl.):715-725.
18. Hamilton, C. E., and Bauerle, T. L. 2012. A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Div. 54:39-49.
19. Harrach, B. D., Fodor, J., Pogány, M., Preuss, J., and Barna, B. 2008. Antioxidant, ethylene and membrane leakage responses to powdery mildew infection of near-isogenic barley lines with various types of resistance. Eur. J. Plant Pathol. 121:21-33.
20. Hogg, A. C., Johnston, R. H., and Dyer, A. T. 2007. Applying real-time quantitative PCR to Fusarium crown rot of wheat. Plant Dis. 91:1021- 1028.
21. Jansen, C., Wettstein, D., Schäfer, W., Kogel, K.-H., Felk, A., and Maier, F. J. 2005. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc. Natl. Acad. Sci. U.S.A. 102:16892-16897.
22. Khoshgoftarmanesh, A. H., Kabiri, S., Shariatmadari, H., Sharifnabi, B., and Schulin, R. 2010. Zinc nutrition effect on the tolerance of wheat genotypes to Fusarium root-rot disease in a solution culture experiment. Soil Sci. Plant Nutr. 56:234-243.
23. Kormanik, P. P., and McGraw, A. C. 1982. Quantification of vesiculararbuscular mycorrhizae in plant roots. Pages 37-45 in: Methods and Principles of Mycorrhizal Research. N. C. Schenck, ed. American Phytopathological Society, St. Paul, MN, U.S.A.
24. Kumar, M., Yadav, V., Tuteja, N., and Johri, A. K. 2009. Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780-790.
25. Li, Y. H., Yanagi, A., Miyawaki, Y., Okada, T., and Matsubara, Y. 2010. Disease tolerance and changes in antioxidative abilities in mycorrhizal strawberry plants. J. Jpn. Soc. Hortic. Sci. 79:174-178.
26. Lorenc-Kuku?a, K., Wrobel-Kwiatkowska, M., Starzycki, M., and Szopa, J. 2007. Engineering flax with increased flavonoid content and thus Fusarium resistance. Physiol. Mol. Plant Pathol. 70:38-48.
27. McGonigle, T. P., Miller, M. H., Evans, D. G., Fairchild, G. L., and Swan, J. A. 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol. 115:495-501.
28. Nicolaisen, M., Suproniene, S., Nielsen, L. K., Lazzaro, I., Spliid, N. H., and Justesen, A. F. 2009. Real time PCR for quantification of eleven individual Fusarium species in cereals. J. Microbiol. Methods 76:234- 240.
29. Nielsen, L. K. Jensen, J. D., Rodríguez, A., Jørgensen, L. N., and Justesen, A. F. 2012. TRI12 based quantitative real-time PCR assays reveal the distribution of trichothecene genotypes of F. graminearum and F. culmorum isolates in Danish small grain cereals. Int. J. Food Microbiol. 157:384-392.
30. PeŠkan-Berghöfer, T., Shahollari, B., Giong, P. H., Hehl, S., Markert, C., Blanke, V., Kost, G., Varma, A., and Oelmüller, R. 2004. Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol. Plant. 122:465-477.
31. Qiang, X., Weiss, M., Kogel, K.-H., and Schäfer, P. 2012. Piriformospora indica-A mutualistic basidiomycete with an exceptionally large plant host range. Mol. Plant Pathol. 13:508-518.
32. Richter, J., Baltruschat, H., Kabrodt, K., and Schellenberg, I. 2011. Impact of arbuscular mycorrhiza on the St. John's wort (Hypericum perforatum) wilt disease induced by Colletotrichum cf. gloeosporioides. J. Plant Dis. Prot. 118:109-118.
33. Rodriguez, R. J., Henson, J., Van Volkenburgh, E., Hoy, M., Wright, L., Beckwith, F., Kim, Y., and Redman, R. S. 2008. Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2:404-416.
34. Serfling, A., Wirsel, S. G. R., Lind, V., and Deising, H. B. 2007. Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523-531.
35. Sharma, M., Schmid, M., Rothballer, M., Hause, G., Zuccaro, A., Imani, J., Kampfer, P., Domann, E., Schäfer, P., Hartmann, A., and Kogel, K.- H. 2008. Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell. Microbiol. 10:2235-2246.
36. Sherameti, I., Tripathi, S., Varma, A., and Oelmüller, R. 2008. The rootcolonizing endophyte Piriformospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol. Plant-Microbe Interact. 21:799-807.
37. Strausbaugh, C. A., Overturf, K., and Koehn, A. C. 2005. Pathogenicity and real-time PCR detection of Fusarium spp. in wheat and barley roots. Can. J. Plant Pathol. 27:430-438.
38. Sun, C. A., Johnson, J., Cai, D. G., Sherameti, I., Oelmüller, R., and Lou, B. G. 2010. Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J. Plant Physiol. 167:1009-1017.
39. Vadassery, J., Tripathi, S., Prasad, R., Varma, A., and Oelmüller, R. 2009. Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J. Plant Physiol. 166:1263-1274.
40. Varma, A., Verma, S., Sudha, Sahay, N., Bütehorn, B., and Franken, P., 1999. Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl. Environ. Microbiol. 65:2741-2744.
41. Verma, S., Varma, A., Rexer, K. H., Hassel, A., Kost, G., Sarabhoy, A., Bisen, P., Bütehorn, B., and Franken, P. 1998. Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896-903.
42. Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., Heier, T., Hückelhoven, R., Neumann, C., Wettstein, D., Franken, P., and Kogel, K.-H. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. U.S.A. 102:13386-13391.
43. Weiss, M., Sykorova, Z., Garnica, S., Riess, K., Martos, F., Krause, C., Oberwinkler, F., Bauer, R., and Redecker, D. 2011. Sebacinales everywhere: Previously overlooked ubiquitous fungal endophytes. PloS One 6:e16793.
44. Published online. Yang, H., Zhao, X., Wu, J., Hu, M., and Xia, S. 2011. The benefits of exogenous NO: Enhancing Arabidopsis to resist Botrytis cinerea. Am. J. Plant Sci. 2:511-519.
45. Zarea, M. J., Hajinia, S., Karimi, N., Goltapeh, E. M., Rejali, F., and Varma, A. 2012. Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol. Biochem. 45:139-146.
46. Zhang, C. J., Liu, J. X., Zhang, Y. Y., Cai, X. F., Gong, P. J., Zhang, J. H., Wang, T. T., Li, H. X., and Ye, Z. B. 2011. Overexpression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Cell Rep. 30:389-398.