Abstract
Agathis australis (Kauri) is a significant and iconic native tree of Aotearoa, New Zealand. A disease known as kauri-dieback is currently affecting kauri trees. The aetiology of the disease has been associated with Phytophthora agathidicida (PA) which poses severe threat to kauri at individual and population levels. Currently, the only treatment available is the injection of phosphite into the trees. We investigated the potential of fungal endophytes to influence the growth of PA. Seventeen previously isolated endophytic fungi from kauri roots were examined morphologically and the antagonistic effects against the plant pathogen. Five of the 17 fungal endophytes tested demonstrated growth suppression of the pathogen in dual culture. Pezicula sp. partly inhibited the growth of P. agathidicida whilst Coprinellus micaceus and Ilyonectria mors-panacis completely inhibited the growth of the pathogen. Oospores were not observed in the dual culture nor was the P. agathidicida viable when transferred into fresh culture media. This study illustrates that naturally occurring fungal species in kauri roots can suppress the growth of PA. This finding offers a possibility of a biological control for dieback disease in kauri which may contribute to the mitigation of natural disease management and biocontrol of plant diseases without compromising the natural ecosystem.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Submission of sequence data into NCBI is publicly available.
References
Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: The European situation. Eur J Plant Pathol. https://doi.org/10.1007/s10658-005-0233-0
Andres SE, Emery NJ, Rymer PD, Powell JR (2022) Soil chemistry and fungal communities are associated with dieback in an Endangered Australian shrub. Plant Soil. https://doi.org/10.1007/s11104-022-05724-7
Avcı E, Alp Avcı G, Ali Köse D (2014) Determination of antioxidant and antimicrobial activities of medically important mushrooms using different solvents and chemical composition via GC/MS analyses. J Food Nutri Res. https://doi.org/10.12691/jfnr-2-8-1
Azevedo JL, Maccheroni W, Pereira JO, De Araújo WL (2000) Endophytic microorganisms: A review on insect control and recent advances on tropical plants. Electron J Biotechnol. https://doi.org/10.2225/vol3-issue1-fulltext-4
Bacilio-Jiménez M, Aguilar-Flores S, Del Valle MV, Pérez A, Zepeda A, Zenteno E (2001) Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense. Soil Bio Biochem. https://doi.org/10.1016/S0038-0717(00)00126-7
Bassett IE, Horner IJ, Hough EG, Wolber FM, Egeter B, Stanley MC, Krull CR (2017) Ingestion of infected roots by feral pigs provides a minor vector pathway for kauri dieback disease Phytophthora agathidicida. Forestry. https://doi.org/10.1093/forestry/cpx019
Beever RE, Waipara NW, Ramsfield TD, Dick MA, Horner IJ (2007) Kauri (Agathis australis) under threat from Phytophthora? Phytophthoras in forests and natural ecosystems. Proceedings of the Fourth Meeting of the International Union of Forest Research Organizations (IUFRO), Monterey, California, pp 74–85
Berthelot C, Leyval C, Foulon J, Chalot M, Blaudez D (2016) Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiol Econ. https://doi.org/10.1093/femsec/fiw144
Byers AK, Condron L, O’Callaghan M, Waipara N, Black A (2021) Identification of Burkholderia and Penicillium isolates from kauri (Agathis australis) soils that inhibit the mycelial growth of Phytophthora agathidicida. N Z Plant Prot. https://doi.org/10.30843/nzpp.2021.74.11736
Cheeseman TF, Hemsley WB, Smith M (2011) Illustrations of the New Zealand flora. Wellington, John Mackay, Govt. Printer, 1914. https://doi.org/10.5962/bhl.title.12029
Chen J, Huang J (2011) Antimicrobial activity of edible mushroom culture filtrates on plant pathogens. Plant Pathol Bull 19(4):261–270
Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a herbaspirillum sp. isolated from wild rice species. App Environ Microbiol. https://doi.org/10.1128/aem.67.11.5285-5293.2001
Gage DJ, Bobo T, Long SR (1996) Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J Bacteriol. https://doi.org/10.1128/jb.178.24.7159-7166.1996
Goh J, Oh Y, Park YH, Mun HY, Park S, Cheon W (2022) Isolation and characterization of previously undescribed seventeen fungal species belonging to the order hypocreales in Korea. Kor J Mycol. https://doi.org/10.4489/KJM.20220001
Gopalaswamy G, Kannaiyan S, O’Callaghan KJ, Davey MR, Cocking EC (2000) The xylem of rice (Oryza sativa) is colonized by Azorhizobium caulinodans. Proc R Soc B: Biol Sci. https://doi.org/10.1098/rspb.2000.0973
Guiraud P, Steiman R, Ait-Laydi L, Seigle-Murandi F (1999) Degradation of phenolic and chloroaromatic compounds by coprinus spp. Chemosphere. https://doi.org/10.1016/S0045-6535(98)00479-2
Halkett J (1983) A basis for the management of New Zealand kauri (Agathis australis (D. Don) Lindl.) forest. N Z J For 28:15–23
Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol. https://doi.org/10.1139/m97-131
Harris J, Stöcker H (1998) Handbook of mathematics and computational science. pp 823–824
Hintikka V, Niemi K (1999) Nitrite tolerance of different ectomycorrhizal and wood- and litter-decomposing fungi. Karstenia. https://doi.org/10.29203/ka.1999.337
Hinton DM, Bacon CW (1995) Enterobacter cloacae is an endophytic symbiont of corn. Mycopathologia. https://doi.org/10.1007/BF01103471
Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O’Connell RJ, Schulze-Lefert P (2016) Root endophyte colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell. https://doi.org/10.1016/j.cell.2016.02.028
Horner IJ, Hough EG (2013) Forest trials testing phosphate for the control of kauri dieback. Agrichem P Protection 12:7–12
Horner IJ, Hough EG (2014) Pathogenicity of four phytophthora species on kauri: in vitro and glasshouse trials. N Z Plant Prot 67:54–59
Iwai S, Chai B, Sul WJ, Cole JR, Hashsham SA, Tiedje JM (2010) Gene-targeted-metagenomics reveals extensive diversity of aromatic dioxygenase genes in the environment. ISME J. https://doi.org/10.1038/ismej.2009.104
James EK (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crop Res. https://doi.org/10.1016/S0378-4290(99)00087-8
Jumpponen A, Trappe JM (1998) Dark septate endophytes: A review of facultative biotrophic root-colonizing fungi. New Phytol. https://doi.org/10.1046/j.1469-8137.1998.00265.x
Köhl J, Kolnaar R, Ravensberg WJ (2019) Mode of action of microbial biological control agents against plant diseases: Relevance beyond efficacy. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00845
Latha P, Anand T, Ragupathi N, Prakasam V, Samiyappan R (2009) Antimicrobial activity of plant extracts and induction of systemic resistance in tomato plants by mixtures of PGPR strains and Zimmu leaf extract against Alternaria solani. Biol Control. https://doi.org/10.1016/J.BIOCONTROL.2009.03.002
Likar M, Regvar M (2013) Isolates of dark septate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant Soil. https://doi.org/10.1007/s11104-013-1656-6
Lopez-Llorca LV, Duncan GH (1988) A study of fungal endoparasitism of the cereal cyst nematode (Hererodera avenae) by scannin electron microscopy. Can J Microbiol. https://doi.org/10.1139/m88-101
Marini-Macouzet C, Muñoz L, Gonzalez-Rubio A, Eguiarte LE, Souza V, Velez P (2020) Experimental analysis of interactions among saprotrophic fungi from a phosphorous-poor desert oasis in the chihuahuan desert. Mycobiology. https://doi.org/10.1080/12298093.2020.1788271
McInroy JA, Kloepper JW (2007) Studies on indigenous endophytic bacteria of sweet corn and cotton. Molecular ecology of rhizosphere microorganisms: biotechnology and the release of GMOs. Wiley. https://doi.org/10.1002/9783527615810.ch2
Pal KK, Gardener BMS (2006) Biological control of plant pathogens. Plant Health Instr. https://doi.org/10.1094/PHI-A-2006-1117-02
Rajkumar M, Lee WH, Lee KJ (2005) Screening of bacterial antagonists for biological control of Phytophthora blight of pepper. J Basic Microbiol 45:55–63
Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol. https://doi.org/10.1111/j.1469-8137.2009.02773.x
Schulz B, Boyle C, Draeger S, Römmert AK, Krohn K (2002) Endophytic fungi: A source of novel biologically active secondary metabolites. Mycol Res. https://doi.org/10.1017/S0953756202006342
Sessitsch A, Reiter B, Pfeifer U, Wilhelm E (2002) Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and Actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiol Econ. https://doi.org/10.1016/S0168-6496(01)00189-1
Shishido M, Breuil C, Chanway CP (1999) Endophytic colonization of spruce by plant growth-promoting rhizobacteria. FEMS Microbiol Econ. https://doi.org/10.1016/S0168-6496(99)00011-2
Soliman SSM, Greenwood JS, Bombarely A, Mueller LA, Tsao R, Mosser DD, Raizada MN (2015) An endophyte constructs fungicide-containing extracellular barriers for its host plant. Curr Biol. https://doi.org/10.1016/j.cub.2015.08.027
Spadaro D, Gullino ML (2005) Improving the efficacy of biocontrol agents against soilborne pathogens. Crop Prot. https://doi.org/10.1016/j.cropro.2004.11.003
Steward GA (2011) Growth and yield of New Zealand kauri. University of Canterbury, New Zealand (Master's thesis)
Stone JK, Bacon CW, White JF (2000) An overview of endophytic microbes: endophytism defined. Microbial Endophytes. https://doi.org/10.1163/_q3_SIM_00374
Sturz AV, Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. A Soil Eco. https://doi.org/10.1016/S0929-1393(00)00094-9
Tan RX, Zou WX (2001) Endophytes a rich source of fuctional metabolites. Nat Prod Rep 18:448–459
Tellenbach C, Sumarah MW, Grünig CR, Miller JD (2013) Inhibition of Phytophthora species by secondary metabolites produced by the dark septate endophyte Phialocephala europaea. Fungal Ecol. https://doi.org/10.1016/J.FUNECO.2012.10.003
Terhonen E, Sipari N, Asiegbu FO (2016) Inhibition of phytopathogens by fungal root endophytes of Norway spruce. Biol Control. https://doi.org/10.1016/j.biocontrol.2016.04.006
Tuite J (1969) Plant pathological methods: Fungi and bacteria. Burgess Pub. co., Minneapolis, Minn, p 239
Velez P, Espinosa-Asuar L, Figueroa M, Gasca-Pineda J, Aguirre-von-Wobeser E, Eguiarte LE, Hernandez-Monroy A, Souza V (2018) Nutrient dependent cross-kingdom interactions: Fungi and bacteria from an oligotrophic desert oasis. Front Microbiol. https://doi.org/10.3389/fmicb.2018.01755
Waipara NW, Hill S, Hill LMW, Hough EG, Horner IJ (2013) Surveillance methods to determine tree health, distribution of kauri dieback disease and associated pathogens. N Z Plant Prot 66:235–241
Weir BS, Paderes EP, Anand N, Uchida JY, Pennycook SR, Bellgard SE, Beever RE (2015) A taxonomic revision of Phytophthora Clade 5 including two new species, Phytophthora agathidicida and P. cocois. Phytotaxa. https://doi.org/10.11646/phytotaxa.205.1.2
Zahid S, Udenigwe CC, Ata A, Eze MO, Segstro EP, Holloway P (2006) New bioactive natural products from Coprinus micaceus. Nat Prod Res. https://doi.org/10.1080/14786410601101829
Zhan A, Schneider H, Lynch JP (2015) Reduced lateral root branching density improves drought tolerance in maize. Plant Physiol. https://doi.org/10.1104/pp.15.00187
Ziadi N, Zebarth BJ, Bélanger G, Cambouris AN, Xu G, Fan X, Miller AJ, Wang CC, Wang X, Van Nostrand JD, Deng Y, Xiaotao L, Zhou J, Han X, Deshwal VK, Singh SB, Kumar P, Chubey A, Vk D, Ryu CM (2016) Endophytic bacteria in microbial preparations that improve plant development (review). Front Microbiol. https://doi.org/10.1007/s11104-015-2778-9
Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. FEMS Microbiol Rev. https://doi.org/10.1111/j.1574-6976.2008.00123.x
Acknowledgements
The research team acknowledges Te Kawerau ā Maki and the support of Kauri Ora Community for our research on kauri, a taonga species in Aotearoa. The authors would like to thank Bella Burgess for assisting in the NCBI data submission, and Diana Lee for her technical help in culturing the endophyte isolates.
Funding
This work was supported by the School of Science, Faculty of Health and Environmental Science, Auckland University of Technology Doctor of Philosophy Research fund.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
All the authors of this manuscript have read and agree to the submission and the study has not been submitted elsewhere for publication.
Conflict of interest
The authors have no potential conflict of interest and have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lawrence, P., Jackson, L., Padamsee, M. et al. Screening of Agathis australis endophytes as biological control agents against kauri dieback pathogen Phytophthora agathidicida. J Plant Pathol (2024). https://doi.org/10.1007/s42161-023-01569-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s42161-023-01569-w