Skip to main content
Log in

Effects of dark septate endophytes on tomato plant performance

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Non-mycorrhizal fungal root endophytes can be found in all natural and cultivated ecosystems, but little is known about their impact on plant performance. The impact of three mitosporic dark septate endophytes (DSE48, DSE49 and Leptodontidium orchidicola) on tomato plant characteristics was studied. Their effects on root and shoot growth, their influence on fruit yield and fruit quality parameters and their ability to diminish the impact of the pathogen Verticillium dahliae were investigated. While shoot biomass of young plants was enhanced between 10% and 20% by the endophytes DSE48 and L. orchidicola in one of two experiments and by DSE49 in both experiments, vegetative growth parameters of 24-week-old plants were not affected except a reproducible increase of root diameter by the isolate DSE49. Concerning fruit yield and quality, L. orchidicola could double the biomass of tomatoes and increased glucose content by 17%, but this was dependent on date of harvest and on root colonisation density. Additionally, the endophytes DSE49 and L. orchidicola decreased the negative effect of V. dahliae on tomato, but only at a low dosage of the pathogen. This indicates that the three dark septate endophytes can have a significant impact on tomato characters, but that the effects are only obvious at early stages of vegetative and generative development and currently too inconsistent to recommend the application of these DSEs in horticultural practice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Achatz B, von Rüden S, Andrade D, Neumann E, Pons-Kühnemann J, Kogel K-H, Franken P, Waller F (2010) Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil 333:59–70

    Article  CAS  Google Scholar 

  • 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 Phytol 184:529–544

    Article  CAS  PubMed  Google Scholar 

  • Alberton O, Kuyper TW, Summerbell RC (2010) Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 328:459–470

    Article  CAS  Google Scholar 

  • Andrade-Linares DR, Grosch R, Franken P (2011) Screening of tomato endophytic fungi for potential biological agents. IOBC/WPRS Bulletin

  • Anonymous (1992) Kleur-stadia tomaten. Central Bureau van de Tuibouwveilingen in Nederland, Gouda, The Netherlands

  • Barazani O, Von Dahl CC, Baldwin IT (2007) Sebacina vermifera promotes the growth and fitness of Nicotiana attenuata by inhibiting ethylene signaling. Plant Physiol 144:1223–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bütehorn B, Rhody D, Franken P (2000) Isolation and characterisation of Pitef1 encoding the translation elongation factor EF-1alpha of the root endophyte Piriformospora indica. Plant Biol 2:687–692

    Article  Google Scholar 

  • Conn VM, Franco CMM (2004) Effect of microbial inoculants on the indigenous actinobacterial endophyte population in the roots of wheat as determined by terminal restriction fragment length polymorphism. Appl Environ Microbiol 70:6407–6413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, 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-Microb Interact 19:1062–1071

    Article  CAS  Google Scholar 

  • Daie J, Campbell WF (1981) Response of tomato plants to stressful temperatures. Plant Physiol 67:26–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Kreij C, Voogt W, van den Bos AL, Baas R (1997) Voedingsoplossingen voor de teelt van tomaat in gesloten teeltsystemen. Brochure VG Tomaat, The Netherlands

    Google Scholar 

  • Deshmukh S, Hueckelhoven R, Schaefer 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Buttner C, Grosch R, Schwarz D, Franken P (2010) Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20:191–200

    Article  PubMed  Google Scholar 

  • Fernando AA, Currah RS (1996) A comparative study of the effects of the root endophytes Leptodontidium orchidicola and Phialocephala fortinii (Fungi Imperfecti) on the growth of some subalpine plants in culture. Can J Bot 74:1071–1078

    Article  Google Scholar 

  • Fradin EF, Thomma BPHJ (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Physiol 7:71–86

    CAS  Google Scholar 

  • Guil-Guerrero JL, Rebolloso-Fuentes MM (2009) Nutrient composition and antioxidant activity of eight tomato (Lycopersicon esculentum) varieties. J Food Compos Anal 22:123–129

    Article  CAS  Google Scholar 

  • Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant-Microb Interact 22:763–772

    Article  CAS  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  PubMed  Google Scholar 

  • Hoitink HAJ, Boehm MJ (1999) Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annu Rev Phytopathol 37:427–446

    Article  CAS  PubMed  Google Scholar 

  • Johnson C, Hall JL, Ho LC (1988) Pathways of uptake and accumulation of sugars in tomato fruit. Ann Bot 61:593–603

    Article  CAS  Google Scholar 

  • Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211

    Article  Google Scholar 

  • Jumpponen A, Trappe JM (1998) Performance of Pinus contorta inoculated with two strains of root endophytic fungus, Phialocephala fortinii: effects of synthesis system and glucose concentration. Can J Bot 76:1205–1213

    CAS  Google Scholar 

  • Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265

    Article  CAS  PubMed  Google Scholar 

  • Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite—what decides? Curr Opin Plant Biol 9:358–363

    Article  PubMed  Google Scholar 

  • Krumbein A, Peters P, Brückner B (2004) Flavour compounds and a quantitative descriptive analysis of tomatoes (Lycopersicon esculentum Mill.) of different cultivars in short-term storage. Postharvest Biol Technol 32:15–28

    Article  CAS  Google Scholar 

  • Krumbein A, Schwarz D, Kläring HP (2006) Effects of environmental factors on carotenoid content in tomato (Lycopersicon esculentum Mill.) grown in a greenhouse. J Appl Bot Food Qual 80:160–164

    CAS  Google Scholar 

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 56(1):173–189

    Article  Google Scholar 

  • Morgan DP, Epstein L, Ferguson L (1992) Verticillium wilt resistance in pistachio rootstock cultivars—assays and an assessment of 2 interspecific hybrids. Plant Dis 76:310–313

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–479

    Article  CAS  Google Scholar 

  • Narisawa K, Kawamata H, Currah RS, Hashiba T (2002) Suppression of Verticillium wilt in eggplant by some fungal root endophytes. Eur J Plant Pathol 108:103–109

    Article  Google Scholar 

  • Narisawa K, Usuki F, Hashiba T (2004) Control of Verticillium yellows in chinese cabbage by the dark septate endophytic fungus LtVB3. Phytopathology 94:412–418

    Article  CAS  PubMed  Google Scholar 

  • Ojiambo PS, Scherm H (2006) Biological and application-oriented factors influencing plant disease suppression by biological control: a meta-analytical review. Phytopathology 96:1168–1174

    Article  CAS  PubMed  Google Scholar 

  • Parlevliet JE (2002) Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica 124:147–156

    Article  CAS  Google Scholar 

  • Pegg G, Brady B (2002) Verticillium wilts. Cabi Publishing, Oxford

    Book  Google Scholar 

  • Pontecorvo G, Roper JA, Hemmons LM, Macdonald KD, Bufton AWJ (1953) The genetics of Aspergillus nidulans. Adv Genet 5:141–238

    CAS  PubMed  Google Scholar 

  • Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716

    Article  Google Scholar 

  • Rodriguez R, White J, Arnold A, Redman R (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  • Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54:513–524

    Article  CAS  PubMed  Google Scholar 

  • Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, Scholz U, Pons-Kuhnemann J, Sonnewald S, Sonnewald U, Kogel KH (2009) Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 59:461–474

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Shahollari B, Vadassery J, Varma A, Oelmuller R (2007) A leucine-rich repeat protein is required for growth promotion and enhanced seed production mediated by the endophytic fungus Piriformospora indica in Arabidopsis thaliana. Plant J 50:1–13

    Article  CAS  PubMed  Google Scholar 

  • Shivanna MB, Meera MS, Hyakumachi M (1994) Sterile fungi from Zoysiagrass rhizosphere as plant-growth promoters in spring wheat. Can J Microbiol 40:637–644

    Article  Google Scholar 

  • Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:1–23

    Article  Google Scholar 

  • Sinha AK, Wood RKS (1968) Resistance to vascular wilt parasites. Neth J Plant Pathol 74:149–156

    Article  Google Scholar 

  • Sirrenberg A, Goebel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K (2007) Piriformospora indica affects plant growth by auxin production. Physiol Plant 131:581–589

    Article  CAS  PubMed  Google Scholar 

  • Soares WL, Porto MFD (2009) Estimating the social cost of pesticide use: an assessment from acute poisoning in Brazil. Ecol Econ 68:2721–2728

    Article  Google Scholar 

  • Stammler G, Strobel D, Semar M, Klappach K (2006) Diagnostics of fungicide resistance and relevance of laboratory data for the field. Asp Appl Biol 78:29–36

    Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche des méthodes d'estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) The mycorrhizae: physiology and genetic. INRA Presse, Paris, pp 217–221

    Google Scholar 

  • Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20:1–11

    Article  PubMed  Google Scholar 

  • Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novak O, Strnad M, Ludwig-Muller J, Oelmuller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant-Microb Interact 21:1371–1383

    Article  CAS  Google Scholar 

  • Varma A, Verma S, Sudha SN, Butehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Venema JH, Posthumus F, van Hasselt PR (1999) Impact of suboptimal temperature on growth, photosynthesis, leaf pigments and carbohydrates of domestic and high-altitude wild Lycopersicon species. J Plant Physiol 155:711–718

    Article  CAS  Google Scholar 

  • Veronese P, Narasimhan ML, Stevenson RA, Zhu JK, Weller SC, Subbarao KV, Bressan RA (2003) Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. Plant J 35:574–587

    Article  CAS  PubMed  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M (2008) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86

    Article  CAS  Google Scholar 

  • Weiss M, Selosse MA, Rexer KH, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010

    Article  PubMed  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    Article  CAS  PubMed  Google Scholar 

  • Wilson D (1995) Endophyte—the evolution of a term, and clarification of its use and definition. Oikos 73:274–276

    Article  Google Scholar 

  • Wu LQ, Guo SX (2008) Interaction between an isolate of dark-septate fungi and its host plant Saussurea involucrata. Mycorrhiza 18:79–85

    Article  CAS  PubMed  Google Scholar 

  • Wu LQ, Lv YL, Meng ZX, Chen J, Guo SX (2010) The promoting role of an isolate of dark-septate fungus on its host plant Saussurea involucrata Kar. et Kir. Mycorrhiza 20:127–135

    Article  CAS  PubMed  Google Scholar 

  • Zhao YC, Hasenstein KH (2009) Primary root growth regulation: the role of auxin and ethylene antagonists. J Plant Growth Regul 28:309–320

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Ministries of Consumer Protection, Food and Agriculture of the Federal Republic of Germany, of the Land Brandenburg and of the Land Thüringen. DR Andrade-Linares was supported by the German Academic Exchange Service (DAAD). We are grateful for technical assistance to Mrs. Fandrey and Mrs. Widiger (pathosystem and climate chambers experiments), Mrs. Rathenow, Mrs. Hasse, Mrs. Stefanowski, Mrs. Marten (cultivation and harvest of plants) and Mrs. Jankowsky and Mrs. Platalla (quality analysis). The V. dahliae strain was kindly provided by Valerie Grimault (GEVES, Angers, France).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Philipp Franken.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andrade-Linares, D.R., Grosch, R., Restrepo, S. et al. Effects of dark septate endophytes on tomato plant performance. Mycorrhiza 21, 413–422 (2011). https://doi.org/10.1007/s00572-010-0351-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-010-0351-1

Keywords

Navigation