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The application of Arabidopsis thaliana in studying tripartite interactions among plants, beneficial fungal endophytes and biotrophic plant-parasitic nematodes

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Abstract

Main conclusion

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.

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Abbreviations

AGC2-2:

Protein kinase of the AGC2 subfamily

Fo162:

Fusarium oxysporum strain Fo162

H2O2 :

Hydrogen peroxide

J2:

Infective second-stage juveniles of Meloidogyne incognita

NaOCl:

Sodium hypochloride

PA:

Phosphatidic acid

PDK1:

3-Phosphoinositide-dependent protein kinase1

OXI1:

Oxidative signal-inducible1 protein kinase

References

  • Abad P, Castagnone-Sereno P, Rosso MN, de Almeira EJ, Favery B (2009) Invasion, feeding and development. In: Perry RN, Moens M, Starr JL (eds) Root-knot nemadodes. CABI Publishing, Wallingford, pp 163–181

    Chapter  Google Scholar 

  • Aimé S, Cordier C, Alabouvette C, Olivain C (2008) Comparative analysis of PR gene expression in tomato inoculated with virulent Fusarium oxysporum f. sp. lycopersici and the biocontrol strain F. oxysporum Fo47. Physiol Mol Plant Pathol 73:9–15

    Article  Google Scholar 

  • Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C, Munnik T, Deák M, Koncz C, Bögre L (2004) A protein kinase target of a PDK1 signaling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Anthony RG, Khan S, Costa J, Pais MS, Bögre L (2006) The Arabidopsis protein kinase PTI1-2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J Biol Chem 281:37536–37546

    Article  CAS  PubMed  Google Scholar 

  • Bakker PAHM, Pieterse CMJ, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243

    Article  PubMed  Google Scholar 

  • 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:e1002471

    Article  PubMed Central  CAS  PubMed  Google 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 16:2448–2462

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barcala M, Garcia A, Cabrera J, Casson S, Lindsey K, Favery B, Garcia-Casado G, Solano R, Fenoll C, Escobar C (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J 61:698–712

    Article  CAS  PubMed  Google Scholar 

  • Bird AF (1962) The inducement of giant cells by Meloidogyne javanica. Nematologica 8:1–10

    Article  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    Article  CAS  PubMed  Google Scholar 

  • Caillaud MC, Dubreuil G, Quentin M, Perfus-Barbeoch L, Lecomte P, de Almeida EJ, Abad P, Rosso MN, Favery B (2008) Root-knot nematodes manipulate plant cell functions during a compatible interaction. J Plant Physiol 165:104–113

    Article  CAS  PubMed  Google Scholar 

  • Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmueller R (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7:e1002051

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7:210–216

    Article  CAS  PubMed  Google Scholar 

  • Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant–Microbe Interact 19:1062–1071

    Article  CAS  PubMed  Google 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, Germany

  • Dababat AA, Sikora RA (2007) Induced resistance by the mutualistic endophyte, Fusarium oxysporum strain 162, towards Meloidogyne incognita on tomato. Biocontrol Sci Technol 17:969–975

    Article  Google Scholar 

  • Daneshkhah R, Cabello S, Rozanska E, Sobczak M, Grundler FMW, Wieczorek K, Hofmann J (2013) Piriformospora indica antagonizes cyst nematode infection and development in Arabidopsis roots. J Exp Bot 64:3763–3774

    Article  PubMed Central  CAS  PubMed  Google 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 103:18450–18457

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Diedhiou PM, Hallmann J, Oerke EC, Dehne HW (2003) Effects of arbuscular mycorrhizal fungi and a non-pathogenic Fusarium oxysporum on Meloidogyne incognita infestation of tomato. Mycorrhiza 13:199–204

    Article  CAS  PubMed  Google Scholar 

  • Endo YB, Wergin WP (1973) Ultrastructural investigation of clover roots during early stages of infection by the root-knot nematode, Meloidogyne incognita. Protoplasma 78:365–379

    Article  Google Scholar 

  • Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol 109:813–820

    Article  PubMed Central  CAS  PubMed  Google 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 27–33

    Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:862–889

    Article  Google Scholar 

  • Frendo P, Harrison J, Norman C, Hernández Jiménez MJ, Van de Sype G, Gilabert A, Puppo A (2005) Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Mol Plant–Microbe Interact 18:254–259

    Article  CAS  PubMed  Google Scholar 

  • Gheysen G, Mitchum MG (2011) How nematodes manipulate plant development pathways for infection. Curr Opin Plant Biol 14:415–421

    Article  PubMed  Google Scholar 

  • Hallmann J, Sikora RA (1994) Influence of F. oxysporum, a mutualistic fungal endophyte, on M. incognita of tomato. J Plant Dis Prot 101:475–481

    Google Scholar 

  • Hallmann J, Sikora RA (1996) Toxicity of fungal endophyte secondary metabolites to plant parasitic nematodes and soil-borne plant pathogenic fungi. Eur J Plant Pathol 102:155–160

    Article  CAS  Google Scholar 

  • Hamamouch N, Li C, Seo PJ, Park CM, Davis EL (2011) Expression of Arabidopsis pathogenesis-related genes during nematode infection. Mol Plant Pathol 12:355–364

    Article  CAS  PubMed  Google Scholar 

  • Harrach BD, Baltruschat H, Barna B, Fodor J, Kogel KH (2013) The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Mol Plant–Microbe Interact 26:599–605

    Article  CAS  PubMed  Google Scholar 

  • Hofmann J, Szakasits D, Blöchl A, Sobczak M, Daxböck-Horvath S, Golinowski W, Bohlmann H, Grundler FM (2008) Starch serves as carbohydrate storage in nematode-induced syncytia. Plant Physiol 146:228–235

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hooper DJ, Llaman J, Subbotin SA (2005) Methods for extraction, processing and detection of plant and soil nematodes. In: Luc M, Sikora RA, Brige J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. CABI Publishing, Wallingford, pp 53–86

    Chapter  Google Scholar 

  • Hussey RA, Barker KP (1973) A comparison of methods for collecting inocula for Meloidogyne sp, including a new technique. Plant Dis Rep 57:1025–1028

    Google Scholar 

  • Katagiri F, Thilmony R, He SY (2002) The Arabidopsis thaliana-Pseudomonas syringae interaction. Arabidopsis Book. doi:10.1199/tab.0039

    PubMed Central  PubMed  Google Scholar 

  • Liberman LM, Sozzani R, Benfey PN (2012) Integrative systems biology: an attempt to describe a simple weed. Curr Opin Plant Biol 15:162–167

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martinuz A, Schouten A, Sikora RA (2012) Systemically induced resistance and microbial competitive exclusion: implications on biological control. Phytopathology 102:260–266

    Article  CAS  PubMed  Google Scholar 

  • Martinuz A, Schouten A, Sikora RA (2013) Post-infection development of Meloidogyne incognita on tomato treated with the endophytes Fusarium oxysporum strain Fo162 and Rhizobium etli strain G12. Biocontrol 58:95–105

    Article  Google 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 54:263–272

    Article  Google Scholar 

  • Menjivar R, Hagemann MH, Kranz J, Cabrera JA, Dababat AA, Sikora RA (2011) Biological control of Meloidogyne incognita on cucurbitaceous crops by the non-pathogenic endophytic fungus Fusarium oxysporum strain 162. Int J Pest Manag 57:249–253

    Article  Google Scholar 

  • Micali C, Göllner K, Humphry M, Consonni C, Panstruga R (2008) The powdery mildew disease of Arabidopsis: a paradigm for the interaction between plants and biotrophic fungi. Arabidopsis Book. doi:10.1199/tab.0115

    PubMed Central  PubMed  Google Scholar 

  • Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, Wubben M, Davis EL (2013) Nematode effector proteins: an emerging paradigm of parasitism. New Phytol 199:879–894

    Article  PubMed  Google Scholar 

  • Moens M, Perry RN, Starr JL (2009) Meloidogyne species: a diverse group of novel and important plant parasites. In: Perry RN, Moens M, Starr JL (eds) Root-knot nemadodes. CABI Publishing, Wallingford, pp 1–17

    Chapter  Google Scholar 

  • Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17

    Article  Google 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 85–102

    Google Scholar 

  • Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2006) Identification of PAD2 as a c-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172

    Article  PubMed  Google Scholar 

  • Peeters N, Guidot A, Vailleau F, Valls M (2013) Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol Plant Pathol 14:651–662

    Article  CAS  PubMed  Google 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 122:465–477

    Article  Google Scholar 

  • Petersen LN, Ingle RA, Knight MR, Denby KJ (2009) OXI1 protein kinase is required for plant immunity against Pseudomonas syringae in Arabidopsis. J Exp Bot 60:3727–3735

    Article  PubMed Central  CAS  PubMed  Google 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 11:789–799

    CAS  Google Scholar 

  • Qiang X, Zechmann B, Reitz MU, Kogel K-H, Schaefer P (2012) The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24:794–809

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L et al (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166

    Article  CAS  PubMed  Google Scholar 

  • Schlaeppi K, Bodenhausen N, Buchala A, Mauch F, Reymond P (2008) The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. Plant J 55:774–786

    Article  CAS  PubMed  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Schulz B, Rommert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 10:1275–1283

    Article  Google 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, Germany

  • Sijmons PC, Grundler FMW, von Mende N, Burrows P, Wyss U (1991) Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J 1:245–254

    Article  Google Scholar 

  • Sikora RA, Fernandez E (2005) Nematode parasites of vegetables. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture. CABI Publishing, Wallingford, pp 319–392

    Chapter  Google Scholar 

  • Sikora RA, Schäfer K, Dababat AA (2007) Modes of action associated with microbially induced in planta suppression of plant-parasitic nematodes. Australas Plant Pathol 36:124–134

    Article  Google Scholar 

  • Urban M, Daniels S, Mott E, Hammond-Kosack K (2002) Arabidopsis is susceptible to the cereal ear blight fungal pathogens Fusarium graminearum and Fusarium culmorum. Plant J 32:961–973

    Article  CAS  PubMed  Google 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 36:1926–1937

    Google Scholar 

  • Vu TT, Hauschild R, Sikora RA (2006) Fusarium oxysporum endophytes induced systemic resistance against Radopholus similis on banana. Nematology 8:847–852

    Article  Google Scholar 

  • Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiang C, Werner BL, E’Lise MC, Oliver D (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant–Microbe Interact 25:139–150

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

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.

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Martinuz, A., Zewdu, G., Ludwig, N. et al. The application of Arabidopsis thaliana in studying tripartite interactions among plants, beneficial fungal endophytes and biotrophic plant-parasitic nematodes. Planta 241, 1015–1025 (2015). https://doi.org/10.1007/s00425-014-2237-5

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