Remodelling of actin cytoskeleton in tomato cells in response to inoculation with a biocontrol strain of Fusarium oxysporum in comparison to a pathogenic strain

Plant Pathology

Volumn 64, Issue 6, 2015, Pages 1366-1374

  Humbert, C ^a   Aime S ^a   Alabouvette, C ^a   Steinberg, C ^a   Olivain, C ^a  

^a UNIV BOURGOGNE FRANCHE COMTÉ   (France)

Author keywords

Cell death; Cytochalasins; Fluorescence microscopy; Tomato cell suspension; TRITC phalloidin

Indexed keywords

APOPTOSIS; BIOCONTROL AGENT; CELLS AND CELL COMPONENTS; COMPARATIVE STUDY; DICOTYLEDON; FLUORESCENCE SPECTROSCOPY; FUNGUS; HOST-PATHOGEN INTERACTION; INHIBITION; INOCULATION; PHYSIOLOGICAL RESPONSE; PLANT DEFENSE; PROTEIN;

FUSARIUM OXYSPORUM; LYCOPERSICON ESCULENTUM;

EID: 84955213363     PISSN: 00320862     EISSN: 13653059     Source Type: Journal    
DOI: 10.1111/ppa.12375     Document Type: Article

References (41)

1. Aimé S, Alabouvette C, Steinberg C, Olivain C, 2013. The endophytic strain Fusarium oxysporum Fo47: a good candidate for priming the defense responses in tomato roots. Molecular Plant-Microbe Interactions 26, 918-26.
2. Alabouvette C, Olivain C, L'Haridon F, Aimé S, Steinberg C, 2007. Using strains of Fusarium oxysporum to control wilts: dream or reality? In: Vurro M, Gressel J, eds. Novel Biotechnologies for Bio-Control Agent Enhancement and Management. Dordrecht, Netherlands: Springer, 157-77.
3. Alabouvette C, Olivain C, Migheli Q, Steinberg C, 2009. Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. New Phytologist 184, 529-44.
4. Bao JR, Lazarovitz G, 2001. Differential colonization of tomato roots by nonpathogenic and pathogenic Fusarium oxysporum strains may influence Fusarium wilt control. Phytopathology 91, 449-56.
5. Benhamou N, Garrand C, 2001. Cytological analysis of defense-related mechanisms induced in pea root tissues in response to colonization by nonpathogenic Fusarium oxysporum Fo47. Phytopathology 91, 730-40.
6. Bolwerk A, Lagopodi AL, Lugtenberg BJJ, Bloemberg GV, 2005. Visualization of interactions between a pathogenic and a beneficial Fusarium strain during bio-control of tomato food and root rot. Molecular Plant-Microbe Interactions 18, 710-21.
7. Brown SS, Spudich JA, 1981. Mechanism of action by cytochalasin: evidence that it binds to actin filament ends. Journal of Cell Biology 88, 487-91.
8. Correll JC, Klittich CJR, Leslie JR, 1987. Nitrate nonutilizing mutants of Fusarium oxysporum and their use in vegetative compatibility tests. Phytopathology 77, 1640-6.
9. Davies DR, Bindschedler LV, Strickland TS, Bolwell GP, 2006. Production of reactive oxygen species in Arabidopsis thaliana cell suspension cultures in response to an elicitor from Fusarium oxysporum: implication for basal resistance. Journal of Experimental Botany 57, 1817-27.
10. De Almeida Engler J, Van Poucke K, Karimi M et al., 2004. Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. The Plant Journal 38, 12-26.
11. Dickman MB, Fluhr R, 2013. Centrality of host cell death in plant-microbe interactions. Annual Review of Phytopathology 51, 543-70.
12. Formela M, Samardakiewicz S, Marczak Ł et al., 2014. Effects of endogenous signals and Fusarium oxysporum on the mechanism regulating genistein synthesis and accumulation in yellow lupine and their impact on plant cell cytoskeleton. Molecules 19, 13392-421.
13. Gawehns F, Houterman PM, Ait Ichou F et al., 2014. The Fusarium oxysporum effector Six6 contributes to virulence and suppresses I-2-mediated cell death. Molecular Plant-Microbe Interactions 27, 336-48.
14. Guan X, Buchholtz G, Nick P, 2013. The cytoskeleton is disrupted by the bacterial effector HrpZ, but not by the bacterial PAMP flg22, in tobacco BY-2 cells. Journal of Experimental Botany 64, 1805-16.
15. Hano C, Addi M, Fliniaux O et al., 2008. Molecular characterization of cell death induced by a compatible interaction between Fusarium oxysporum f. sp. linii and flax (Linum usitatissimum) cells. Plant Physiology and Biochemistry 46, 590-600.
16. Henty-Ridilla JL, Shimono M, Li J, Chang JH, Day B, Staiger CJ, 2013. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathogens 9, e1003290.
17. Higaki T, Goh T, Hayashi T et al., 2007. Elicitor-induced cytoskeletal rearrangement relates to vacuolar dynamics and execution of cell death: in vivo imaging of hypersensitive cell death in tobacco BY-2 cells. Plant and Cell Physiology 48, 1414-25.
18. Higaki T, Kurusu T, Hasezawa S, Kutchitsu K, 2011. Dynamic intracellular reorganization of cytoskeletons and the vacuole in defense responses and hypersensitive cell death in plants. Journal of Plant Research 124, 315-24.
19. Jarosch B, Collins NC, Zellerhoff N, Schaffrath U, 2005. RAR1, ROR1, and the actin cytoskeleton contribute to basal resistance to Magnaporthe grisea in barley. Molecular Plant-Microbe Interactions 18, 397-404.
20. Kabbage M, Williams B, Dickman MB, 2013. Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathogens 9, e1003287.
21. Kobayashi Y, Kobayashi I, 2007. Depolymerization of the actin cytoskeleton induces defense responses in tobacco plants. Journal of General Plant Pathology 73, 360-4.
22. Kobayashi I, Kobayashi Y, Hardham AR, 1994. Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195, 237-47.
23. L'Haridon F, Aimé S, Duplessis S, Alabouvette C, Steinberg C, Olivain C, 2011. Isolation of differentially expressed genes during interactions between tomato cells and a protective or a non-protective strain of Fusarium oxysporum. Physiological and Molecular Plant Pathology 76, 9-19.
24. McLusky SR, Bennett MH, Beale MH, Lewis MJ, Gaskin P, Mansfield JW, 1999. Cell wall alterations and localized accumulation of feruloyl-3'methoxytyramine in onion epidermis at sites of attempted penetration by Botrytis allii are associated with actin polarization, peroxidase activity and suppression of flavonoid biosynthesis. The Plant Journal 17, 523-34.
25. Murashige T, Skoog F, 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 45, 473-97.
26. Olivain C, Alabouvette C, 1997. Colonization of tomato root by a non-pathogenic strain of Fusarium oxysporum. New Phytologist 137, 481-94.
27. Olivain C, Alabouvette C, 1999. Process of tomato root colonization by a pathogenic strain of Fusarium oxysporum f. sp. lycopersici in comparison with a non-pathogenic strain. New Phytologist 141, 497-510.
28. Olivain C, Trouvelot S, Binet MN, Cordier C, Pugin A, Alabouvette C, 2003. Colonization of flax roots and early physiological responses of flax cells inoculated with pathogenic and non-pathogenic strains of Fusarium oxysporum. Applied and Environmental Microbiology 69, 5453-62.
29. Opalski KS, Schultheiss H, Kogel KH, Hückelhoven R, 2005. The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f. sp. hordei. The Plant Journal 41, 291-303.
30. Rep M, van der Does HC, Meijer M et al., 2004. A small cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3 mediated resistance in tomato. Molecular Microbiology 53, 1373-83.
31. Schmidt SM, Panstruga R, 2007. Cytoskeleton functions in plant-microbe interactions. Physiological and Molecular Plant Pathology 71, 135-48.
32. Shan XC, Goodwin PH, 2005. Reorganization of filamentous actin in Nicotiana benthamiana leaf epidermal cells inoculated with Colletotrichum destructivum and Colletotrichum graminicola. International Journal of Plant Sciences 166, 31-9.
33. Shimada C, Lipka V, O'Connell R, Okuno T, Schulze-Lefert P, Takano Y, 2006. Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. Molecular Plant-Microbe Interactions 19, 270-9.
34. Škalamera D, Heath MC, 1998. Changes in the cytoskeleton accompanying infection-induced nuclear movements and the hypersensitive response in plant cells invaded by rust fungi. Planta 16, 191-200.
35. Smertenko A, Franklin-Tong VE, 2011. Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death and Differentiation 18, 1263-70.
36. Song X, Ma Q, Hao X, Li H, 2012. Roles of the actin cytoskeleton and an actin-binding protein in wheat resistance against Puccinia striiformis f. sp. tritici. Protoplasma 249, 99-106.
37. Takemoto D, Jones DA, Hardham AR, 2003. GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. The Plant Journal 33, 775-92.
38. Trouvelot S, Olivain C, Recorbet G, Migheli Q, Alabouvette C, 2002. Recovery of Fusarium oxysporum Fo47 mutants affected in their bio-control activity after transposition of the Fot1 element. Phytopathology 92, 936-45.
39. Yuan HY, Yao LL, Jia ZQ, Li Y, Li YZ, 2006. Verticillium dahliae toxin induced alterations of cytoskeletons and nucleoli in Arabidopsis thaliana suspension cells. Protoplasma 229, 75-82.
40. Yun BW, Atkinson HA, Gaborit C et al., 2003. Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. The Plant Journal 34, 768-77.
41. Zadworny M, Guzicka M, Łakomy P, Samardakiewicz S, Smoliński DJ, Much J, 2013. Analysis of microtubule and microfilament distribution in Pinus sylvestris roots following infection by Heterobasidion species. Forest Pathology 43, 222-31.