The application of Arabidopsis thaliana in studying tripartite interactions among plants, beneficial fungal endophytes and biotrophic plant-parasitic nematodes
- 957 Downloads
The research demonstrated that Arabidopsis can be used as a model system for studying plant–nematode–endophyte tripartite interactions; thus, opening new possibilities for further characterizing the molecular mechanisms behind these interactions.
Arabidopsis has been established as an important model system for studying plant biology and plant–microbe interactions. We show that this plant can also be used for studying the tripartite interactions among plants, the root-knot nematode Meloidogyne incognita and a beneficial endophytic isolate of Fusarium oxysporum, strain Fo162. In various plant species, Fo162 can systemically reduce M. incognita infection development and fecundity. Here it is shown that Fo162 can also colonize A. thaliana roots without causing disease symptoms, thus behaving as a typical endophyte. As observed for other plants, this endophyte could not migrate from the roots into the shoots and leaves. Direct inoculation of the leaves also did not result in colonization of the plant. A significant increase in plant fresh weight, root length and average root diameter was observed, suggesting the promotion of plant growth by the endophyte. The inoculation of A. thaliana with F. oxysporum strain Fo162 also resulted in a significant reduction in the number of M. incognita juveniles infecting the roots and ultimately the number of galls produced. This was also observed in a split-root experiment, in which the endophyte and nematode were spatially separated. The usefulness of Arabidopsis opens new possibilities for further dissecting complex tripartite interactions at the molecular and biochemical level.
KeywordsBiotrophic plant-parasitic nematodes Endophyte Growth promotion Model system Tripartite interactions
Protein kinase of the AGC2 subfamily
Fusarium oxysporum strain Fo162
Infective second-stage juveniles of Meloidogyne incognita
3-Phosphoinositide-dependent protein kinase1
Oxidative signal-inducible1 protein kinase
We thank the German Academic Exchange Service (DAAD) for funding this research through a Ph.D. Scholarship. This research was part of a Ph.D. project to study the interrelationships between mutualistic endophytic microorganisms, root-knot nematodes and sap-sucking insects.
- Baldacci-Cresp F, Chang C, Maucourt M, Deborde C, Hopkins J, Lecomte P, Bernillon S, Brourquisse R, Moing A, Abad P, Hérouart D, Puppo A, Favery B, Frendo P (2012) (Homo)glutathione deficiency impairs root-knot nematode development in Medicago truncatula. PLoS Pathog 8:e1002471CrossRefPubMedCentralPubMedGoogle Scholar
- Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462CrossRefPubMedCentralPubMedGoogle Scholar
- Dababat AA (2006) Importance of the mutualistic endophyte Fusarium oxysporum 162 for enhancement of tomato transplants and the biological control of the root-knot nematode Meloidogyne incognita, with particular reference to mode-of-action. Dissertation, University of Bonn, GermanyGoogle Scholar
- Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci USA 103:18450–18457CrossRefPubMedCentralPubMedGoogle Scholar
- Ferris JM (1985) Crop loss prediction and modeling for management decisions. In: Zuckermann BM, Mai WF, Harrison MB (eds) Plant nematology-laboratory manual. The University of Massachusetts Agricultural Experimental Station, Amherst, pp 27–33Google Scholar
- Hallmann J, Sikora RA (1994) Influence of F. oxysporum, a mutualistic fungal endophyte, on M. incognita of tomato. J Plant Dis Prot 101:475–481Google Scholar
- Hussey RA, Barker KP (1973) A comparison of methods for collecting inocula for Meloidogyne sp, including a new technique. Plant Dis Rep 57:1025–1028Google Scholar
- Mendoza AR, Sikora RA (2009) Biological control of Radopholus similis in banana by combined application of the mutualistic endophyte Fusarium oxysporum strain 162, the egg pathogen Paecilomyces lilacinus strain 251 and the antagonistic bacteria Bacillus firmus. Biocontrol 54:263–272CrossRefGoogle Scholar
- Oostenbrink M (1960) Estimating nematode populations by some selected methods. In: Sasser JN, Jenkins WR (eds) Nematology. University of North Carolina, Chapel Hill, pp 85–102Google Scholar
- Peškan-Berghöfer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, 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 122:465–477CrossRefGoogle Scholar
- Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev 11:789–799Google Scholar
- Selim M (2010) Biological, chemical and molecular studies on the systemic induced resistance in tomato against Meloidogyne incognita caused by the endophytic Fusarium oxysporum, Fo162. Dissertation, University of Bonn, GermanyGoogle Scholar
- Veiga RSL, Faccio A, Genre A, Pieterse CMJ, Bonfante P, van Der Heijden MGA (2013) Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana. Plant, Cell Environ 36:1926–1937Google Scholar