Skip to main content
Log in

Non-target impacts of the biocontrol agent Trichoderma atroviride on plant health and soil microbial communities in two native ecosystems in New Zealand

  • Published:
Australasian Plant Pathology Aims and scope Submit manuscript

Abstract

Eleven plant species representing two native ecosystems (1) podocarp forest (Dacrycarpus dacrydioides, Plagianthus regius, Pittosporum eugenioides, Cordyline australis, Melicytus ramiflorus, Coprosma robusta and Asplenium gracillimum) and (2) grassland (Poa cita, Chionochloa rubra, Chionochloa rigida and Festuca novae-zelandiae) and representatives of a wider beneficial microbe population (arbuscular mycorrhizae (AM) and Pseudomonas spp.) were studied to assess possible non-target effects of a commercial T. atroviride product. Comparison of several physical markers (plant height, basal diameter, total leaf number, total leaf area, and fresh and dry weight of leaves, shoots and roots) showed that this T. atroviride isolate had no negative effect on plant health. Although photosynthetic pigment analysis indicated significant differences in chlorophyll and carotene levels between the Trichoderma and control treatments for some plants, this variation was not supported by physical changes in plant health. Culture-dependent and -independent analysis of AM fungi and Pseudomonads demonstrated that T. atroviride had no effect on these potential plant beneficial taxa in either ecosystem. The findings from this study suggest using Pittosporum eugenioides and Pagianthus regius for assessing the impact of imported microbial biocontrol agents on the plant growth of established podocarp forest plants, and Cordyline australis and P. regius for assessing the impact of these agents on seedling establishment. In tussock grassland ecosystems, Festuca novae-zelandiae and Poa cita are suggested for growth impact assessments, and P. cita and Chionochloa rubra for seedling establishment trials. The use of a combination of basic culture-dependent and -independent techniques for assessing changes in soil microbial communities often associated with plant health is also suggested.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • Bailey BA, Lumsden RD (1998) Direct effects of Trichoderma and Gliocladium on plant growth and resistance to pathogens. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocaldium. Taylor & Francis Ltd, London

    Google Scholar 

  • Barratt BIP, Moeed A (2005) Environmental safety of biological control: policy and practice in New Zealand. Biol Contr 35:247–252

    Article  Google Scholar 

  • Barton J (2004) How good are we at predicting the field host-range of fungal pathogens used for classical biological control of weeds? Biol Contr 31:99–122

    Article  Google Scholar 

  • Barton J, Fowler SV, Gianotti AF, Winks CJ, Beurs M, Arnold GC, Forrester G (2007) Successful biological control of mist flower (Ageratina riparia) in New Zealand: agent establishment, impact and benefits to the native flora. Biol Contr 40:370–385

    Article  Google Scholar 

  • Baylis GTS, McNabb RFR, Morrison TM (1963) The mycorrhizal nodules of Podocarps. Trans Br Mycol Soc 46:378–384

    Article  Google Scholar 

  • Berg G, Grosch RK, Scherwinski K (2007) Risk assessment for microbial antagonists: are there effects on non-target organisms? Gesunde Pflanzen 59:107–117

    Article  CAS  Google Scholar 

  • Brimner TA, Boland GJ (2003) A review of the non-target effects of fungi used to biologically control plant diseases. Agric Ecosyst Environ 100:3–16

    Article  Google Scholar 

  • Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. Australian Centre for International Agricultural Research, Canberra

    Google Scholar 

  • Calvet C, Barea JM, Pera J (1992) In vitro interactions between the vesicular-arbuscular mycorrhizal fungus Glomus mosseae and some saprophytic fungi isolated from organic substrates. Soil Biol Biochem 24:775–780

    Article  Google Scholar 

  • Cooper KM (1976) A field survey of mycorrhizas in New Zealand ferns. New Zeal J Bot 14:169–181

    Article  Google Scholar 

  • Cordier C, Alabouvette C (2009) Effects of the introduction of a biocontrol strain of Trichoderma atroviride on non target soil micro-organisms. Eur J Soil Biol 45:267–274

    Article  Google Scholar 

  • Costa R, Gomes NCM, Krogerrecklenfort E, Opelt K, Berg G, Smalla K (2007) Pseudomonas community structure and antagonistic potential in the rhizosphere: insights gained by combining phylogenetic and functional gene-based analyses. Environ Microbiol 9:2260–2273

    Article  CAS  PubMed  Google Scholar 

  • Douglas GB, Dodd MB, Power IL (2007) Potential of direct seeding for establishing native plants into pastoral land in New Zealand. New Zeal J Ecol 31:143–153

    Google Scholar 

  • Finlay RD (2004) Mycorrhizal fungi and their multifunctional roles. Mycologist 18:91–96

    Article  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Green H, Larsen J, Axel Olsson P, Funck Jensen D, Jakobsen I (1999) Suppression of the biocontrol agent Trichoderma harzianum by mycelium of the arbuscular mycorrhizal fungus Glomus intraradices in root-free soil. Appl Environ Microbiol 65:1428–1434

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grosch RK, Scherwinski K, Lottmann J, Berg G (2006) Fungal antagonists of the plant pathogen Rhizoctonia solani: selection, control efficacy and influence on the indigenous microbial community. Mycol Res 110:1464–1474

    Article  CAS  PubMed  Google Scholar 

  • Harman GE, Bjorkman T (1998) Potential and existing uses of Trichoderma and Gliocladium for plant disease control and plant growth enhancement. In: Harman GE, Kubicek CP (eds) Trichoderma & Gliocladium. Taylor & Francis, London

    Google Scholar 

  • Harman GE, Petzoldt R, Comis A, Chen J (2004) Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology 94:147–153

    Article  PubMed  Google Scholar 

  • Hendry GAF, Price AH (1993) Stress indicators: chlorophylls and carotenoids. In: Hendry GAF, Grime JP (eds) Methods in comparative plant ecology. Chapman & Hall, London

    Chapter  Google Scholar 

  • Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25

    Article  CAS  PubMed  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    Article  CAS  Google Scholar 

  • Kichadi SN, Sreenivasa MN (1998) Interaction effects of Glomus fasciculatum and Trichoderma harzianum on Sclerotium rolfsii in the presence of spent slurry in tomato. Karnataka J Agr Sci 11:419–422

    Google Scholar 

  • Liang ZB, Drijber RA, Lee DJ, Dwiekat IM, Harris SD, Wedin DA (2008) A DGGE-cloning method to characterize arbuscular mycorrhizal community structure in soil. Soil Biol Biochem 40:956–966

    Article  CAS  Google Scholar 

  • Liu X, Ellsworth DS, Tyree MT (1997) Leaf nutrition and phyotosynthetic performance of sugar maple (Acer saccharum) in stands with contrasting health conditions. Tree Physiol 17:169–178

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting-rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  PubMed  Google Scholar 

  • McLaren RG, Cameron KC (1996) Soil-science - sustainable production and environmental protection. Oxford University Press, Auckland

    Google Scholar 

  • McLean KL, Swaminathan J, Frampton CM, Hunt JS, Ridgway HJ, Stewart A (2005) Effect of formulation on the rhizosphere competence and biocontrol ability of Trichoderma atroviride C52. Plant Pathol 54:212–218

    Article  Google Scholar 

  • Netto AT, Campostrini E, de Oliveira JG, Bressan-Smith RE (2005) Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves. Sci Hortic 104:199–209

    Article  Google Scholar 

  • Norton D (1995) Forest structure and processes. In: Molloy B (ed) Riccarton Bush: Putaringamotu. The Riccarton Bush Trust, Christchurch

    Google Scholar 

  • O’Sullivan DJ, O’Gara F (1992) Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiol Rev 56:662–676

    PubMed Central  PubMed  Google Scholar 

  • Pattern CL, Glick BR (1996) Bacterial biosynethsis of indole-3-acetic acid. Can J Microbiol 42:207–220

    Article  Google Scholar 

  • Paynter Q, Waipara N, Peterson P, Hona S, Fowler S, Gianotti A, Wilkie P (2006) The impact of two introduced biocontrol agents, Phytomyza vitalbae and Phoma clematidina, on Clematis vitalba in New Zealand. Biol Contr 36:350–357

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Penuelas J, Filella I (1998) Visible and near-infared reflectance techniques for diagnosing plant physiological status. Trends Plant Sci 3:151–156

    Article  Google Scholar 

  • Rabeendran N, Moot DJ, Jones EE & Stewart A (2000) Inconsistent growth promotion of cabbage and lettuce from Trichoderma isolates

  • Richardson AD, Duigan SP, Berlyn GP (2002) An evaluation of non-invasive methods to estimate foliar chlorophyll content. New Phytol 153:185–194

    Article  CAS  Google Scholar 

  • Sampson PH, Zarco-Tejada PJ, Mohammed GH, Miller JR, Noland TL (2003) Hyperspectral remote sensing of forest condition: estimating chlorophyll content in tolerant hardwoods. Forest Sci 49:381–391

    Google Scholar 

  • Sanguinetty CJ, Dais Neto E, Simpson AJG (1994) Rapid silver staining and recovery of PCR products on acrylamide gels. Biotechniques 17:915–919

    Google Scholar 

  • Savazzini F, Longa CMO, Pertot (2009) Impact of the biocontrol agent Trichoderma atroviride SC1 on soil microbial communities of a vineyard in northern Italy. Soil Biol Biochem 41:1457–1465

    Article  CAS  Google Scholar 

  • Scherwinski K, Wolf A, Berg G (2007) Assessing the risk of biological control agents on the indigenous microbial communities: Serratia plymuthica HRO-C48 and Streptomyces sp. HRO-71 as model bacteria. BioControl 52:87–112

    Article  CAS  Google Scholar 

  • Scherwinski K, Grosch R, Berg G (2008) Effect of bacterial antagonists on lettuce: active biocontrol of Rhizoctonia solani and negligible, short-term effects on nontarget microorganisms. FEMS Microbiol Ecol 64:106–116

    Article  CAS  PubMed  Google Scholar 

  • Shepherd LD, Holland BR, Perrie LR (2008) Conflict amongst chloroplast DNA sequences obscures the phylogeny of a group of Asplenium ferns. Mol Phylogenet Evol 48:176–187

    Article  CAS  PubMed  Google Scholar 

  • Siegel, S. & Castellan, N. J. (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill

  • Tait MA, Hik DS (2003) Is dimethylsulfoxide a reliable solvent for extracting chlorophyll under field conditions? Photosynth Res 78:87–91

    Article  CAS  PubMed  Google Scholar 

  • Walsh UF, Morrissey JP, O’Gara F (2001) Pseudomonas for biocontrol of phytopathogens: from functional genomics to commercial exploitation. Curr Opin Biotechnol 12:289–295

    Article  CAS  PubMed  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Whipps JM, Budge SP, Ebben MH (1989) Effect of Coniothyrium minitans and Trichoderma harzianum on Sclerotinia disease of celery and lettuce in the glasshouse at a range of humidities. In: Cavalloro R, Pelerents C (eds) Proceedings of the CEC/IOBC experts group meeting 27–29 May. Integrated Pest Management in Protected Vegetable Crops. A. A. Balkema, Rotterdam

    Google Scholar 

  • Wyss P, Boller TH, Wiemken A (1992) Testing the effect of biological control agents on the formation of vesicular arbuscular mycorrhiza. Plant Soil 147:159–162

    Article  Google Scholar 

Download references

Acknowledgments

This project was funded through New Zealand’s ‘Science Solutions for Better Border Biosecurity (B3)’ www.b3nz.org. The authors gratefully acknowledge the Riccarton Bush Trust and Richard and Anna Hill for enabling soil to be removed from Riccarton Bush and Flock Hill Station, respectively. The authors also thank Gary Houliston and Guy Forrester (Landcare Research) for their assistance in the statistical analysis of the DGGE data; Helen Harman and Olimpia Timudo (Landcare Research) for their technical assistance and Sarah Hunger for editorial assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. L. McLean.

Rights and permissions

Reprints and permissions

About this article

Cite this article

McLean, K.L., Dodd, S.L., Minchin, R.F. et al. Non-target impacts of the biocontrol agent Trichoderma atroviride on plant health and soil microbial communities in two native ecosystems in New Zealand. Australasian Plant Pathol. 43, 33–45 (2014). https://doi.org/10.1007/s13313-013-0229-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13313-013-0229-8

Keywords

Navigation