Diversity of woody-host infecting Phytophthora species in public parks and botanic gardens as revealed by metabarcoding, and opportunities for mitigation through best practice

  • Sarah Green Forest Research
  • Carolyn E. Riddell Forest Research
  • Debbie Frederickson-Matika Forest Research
  • April Armstrong Forest Research
  • Matt Elliot Forest Research
  • Jack Forster Forest Research
  • Pete E. Hedley The James Hutton Institute
  • Jenny Morris The James Hutton Institute
  • Peter Thorpe The James Hutton Institute
  • David E.L. Cooke The James Hutton Institute
  • Paul M. Sharp Institute of Evolutionary Biology at the University of Edinburgh
  • Leighton Pritchard The James Hutton Institute

Abstract

The diversity of Phytophthora species in soils collected from 14 highly disturbed sites in northern Britain, including botanic gardens, arboreta, public parks and other amenity woodland sites, was analysed using a molecular technique known as DNA metabarcoding. This technique enables the identification of multiple species present in a single environmental sample based on a DNA ‘barcode’ unique to each species. The genus Phytophthora was targeted in this study due to its increasing impact on Britain’s forests and woodlands over the
last 20 years. The introduction and spread of new Phytophthora species into Britain has been strongly associated with the movement of traded containerised plants, with a number of Phytophthora outbreaks reported on host trees located in public gardens and parks that had recently undergone planting or landscape regeneration schemes. This study was undertaken to assess the extent to which these highly disturbed sites with extensive planting regimes act as harbours for woody-host infecting Phytophthora species. A total of 23 Phytophthora species, the majority of which are known to be pathogens of woody hosts, were detected across the 14 sites sampled. These included four quarantine-regulated pathogens and four species not
previously recorded in Britain. Also detected were three as-yet undescribed Phytophthora species and nine oomycete sequences with no clear match to any known genus. There was no effect of geographical location, elevation, underlying soil type, host family or host health status on the Phytophthora assemblages at each site, suggesting that the Phytophthora communities detected are likely to comprise introduced species associated with planting programmes. P. austrocedri and P. pseudosyringae were two of the most abundant Phytophthora
species detected, both of which cause serious damage to trees and are regarded as fairly recent introductions to Britain. The practical implications of the findings in terms of mitigating Phytophthora introduction, spread and impact at botanic gardens, arboreta and urban parks are discussed.

Author Biographies

Sarah Green, Forest Research

Sarah Green is Forest Pathologist

Carolyn E. Riddell, Forest Research

Forest Pathology Technician

Debbie Frederickson-Matika, Forest Research

Forest Pathology Technician

April Armstrong, Forest Research

Forest Pathology Technician

Matt Elliot, Forest Research

Forest Pathology Technician

Jack Forster, Forest Research

Statistician

Pete E. Hedley, The James Hutton Institute

Genome Technology Group Leader

Jenny Morris, The James Hutton Institute

Sequencing Centre Technician

Peter Thorpe, The James Hutton Institute

Postdoctoral Researcher

David E.L. Cooke, The James Hutton Institute

Research Leader & Pathologist

Paul M. Sharp, Institute of Evolutionary Biology at the University of Edinburgh

Professor of Genetics

Leighton Pritchard, The James Hutton Institute

Computational Biologist

References

BARSOUM, N., A’HARA, S., COTTRELL, J. & GREEN, S. (2018). Using developments in molecular techniques to improve forest biodiversity monitoring. Forestry Commission Research Note 32, Forestry Commission, Edinburgh.

BEALES, P.A., GILTRAP, P.M., WEBB, K.M. & OZOLINA, A. (2009). A further threat to UK heathland bilberry (Vaccinium myrtillus) by Phytophthora pseudosyringae. New Disease Reports, 19: 56.

BRASIER, C.M. (2008). The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology, 57: 792–808.

BRASIER, C.M., COOKE, D.E.L., DUNCAN, J.M. & HANSEN, E.M. (2003). Multiple new phenotypic taxa from trees and riparian ecosystems in Phytophthora gonapodyides- P. megasperma ITS clade 6, which tend to be high temperature tolerant and either inbreeding or sterile. Mycological Research, 107: 277–290.

BURGESS, T.I., WHITE, D., MCDOUGALL, K.M., GARNAS, J., DUNSTAN, W.A., CATALÀ, S., CARNEGIE, A.J., WORBOYS, S., CAHILL, D., VETTRAINO, A.-M., STUKELY, M.J.C., LIEW, E.C.Y. ET AL. (2017). Distribution and diversity of Phytophthora across Australia. Pacific Conservation Biology, 23(2): 150–162.

CATALÀ, S., BERBEGA, M., PÉREZ-SIERRA, A. & ABAD-CAMPOS, P. (2017). Metabarcoding and development of new real-time specific assays reveal Phytophthora species diversity in holm oak forests in eastern Spain. Plant Pathology, 66: 115–123.

CATALÀ, S., PÉREZ-SIERRA, A. & ABAD-CAMPOS, P. (2015). The use of genus-specific amplicon pyrosequencing to assess Phytophthora species diversity using eDNA from soil and water in northern Spain. PLoS ONE, 10, e0119311.

COOKE, D.E.L. (2015). Threats posed by Phytophthora to Scottish plant health; a review of previous findings, pathways of entry and further spread and the status of diagnostic techniques. RESAS Phytophthora Risk Review.

Report Commissioned by the Scottish Government.

CRONE, M., MCCOMB, J.A., O’BRIEN, P.A. & HARDY, G.E.S. (2013a). Annual and herbaceous perennial native Australian plant species are symptomless hosts of Phytophthora cinnamomi in the Eucalyptus marginata (jarrah) forest of Western Australia. Plant Pathology, 62: 1057–1062.

CRONE, M., MCCOMB, J.A., O’BRIEN, P.A. & HARDY, G.E.S. (2013b). Survival of Phytophthora cinnamomi as oospores, stromata, and thick-walled chlamydospores in roots of symptomatic and asymptomatic annual and herbaceous perennial plant species. Fungal Biology, 117: 112–123.

GREEN, S., BRASIER, C.M., SCHLENZIG, A., MCCRACKEN, A., MACASKILL, G.A., WILSON, M. & WEBBER, J.F. (2013). The destructive invasive pathogen Phytophthora lateralis found on Chamaecyparis lawsoniana across the UK. Forest Pathology, 43: 19–28.

GREEN, S., ELLIOT, M., ARMSTRONG, A. & HENDRY, S.J. (2015). Phytophthora austrocedrae emerges as a serious threat to juniper (Juniperus communis) in Britain. Plant Pathology, 64: 456–466.

GREEN, S., MACASKILL, G.A., DUN, H., ARMSTRONG, A.C. & HENRICOT, B. (2016). First report of Phytophthora austrocedri infecting Nootka cypress in Britain. New Disease Reports, 33:21.

GREEN, S. & WEBBER, J.F. (2012). The emerging threat from Phytophthora to trees in Scotland. Scottish Forestry, 66: 9–16.

HANSEN, E.M., GOHEEN, D.J., JULES, E.S. & ULLIAN, B. (2000). Managing Port-Orford-Cedar and the introduced pathogen Phytophthora lateralis. Plant Disease, 84: 4–14.

HENRICOT, B., PÉREZ-SIERRA, A., ARMSTRONG, A.C., SHARP, P.M. & GREEN, S. (2017). Morphological and genetic analyses of the invasive forest pathogen Phytophthora austrocedri reveal two clonal lineages colonised Britain and Argentina from a common ancestral population. Phytopathology, 107: 1532–1540.

HONG, C., GALLEGLY, M.E., RICHARDSON, P.A. & KONG, P. (2011). Phytophthora pini Leonian resurrected to distinct species status. Mycologia, 103: 351–360.

HULBERT, J.M., AGNE, M.C., BURGESS, T.I., ROETS, F. & WINGFIELD, M.J. (2017). Urban environments provide opportunities for early detections of Phytophthora invasions. Biological Invasions, 19: 3629–3644.

ILLUMINA (2013). 16S Metagenomic sequencing library preparation. Available online: http://support.illumina.com/content/dam/illumina-support/documents/documentation/chemistry_documentation/16s/16s-metagenomiclibrary-prep-guide-15044223-b.pdf (accessed August 2019).

JUNG, T., HANSEN, E.M., WINTON, L., OBWALD, W. & DELATOUR, C. (2002). Three new species of Phytophthora from European oak forests. Mycological Research, 106: 397–411.

JUNG, T., JUNG, M.H., CACCIOLA, S.O., CECH, T., BAKONYI, J., SERESS, D., MOSCA, S., SCHENA, L., SEDDAIU, S., PANE, A., MAGNANO DI SAN LIO, A., MAIA, C. ET AL. (2017a). Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA Fungus, 8:219–244.

JUNG, T., JUNG, M.H., SCANU, B., SERESS, D., KOVÁCS, D.M., MAIA, C., PÉREZ-SIERRA, A., CHANG, T.T., CHANDELIER, A., HEUNGENS, K., VAN POUCKE, K., ABAD-CAMPOS, P. ET AL. (2017b). Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia, 38: 100–135.

JUNG, T., ORLIKOWSKI, L., HENRICOT, B., ABAD-CAMPOS, P., ADAY, A.G., AGUÍN CASAL, O., BAKONYI, J., CACCIOLA, S.O., CECH, T., CHAVARRIAGA, D., CORCOBADO, T., CRAVADOR, A. ET AL. (2016). Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology, 46: 134–163.

MENDOZA, M.L.Z., SICHERITZ-PONTÉN, T. & GILBERT, M.T.P. (2015). Environmental genes and genomes: understanding the differences and challenges in the approaches and software for their analyses. Briefings in Bioinformatics, 16: 745–758.

PAAP, T., BURGESS, T.I. & WINGFIELD, M.J. (2017). Urban trees: bridge-heads for forest pest invasions and sentinels for early detection. Biological Invasions, 19: 3515–3526.

PAWLUCZYK, M., WEISS, J., LINKS, M.G., ARANGUREN, M.E., WILKINSON, M.D. & EGEA-CORTINES, M. (2015). Quantitative evaluation of bias in PCR amplification and next-generation sequencing derived from metabarcoding samples. Analytical and Bioanalytical Chemistry, 407: 1841–1848.

PRIGIGALLO, M.I., MOSCA, S., CACCIOLA, S.O., COOKE, D.E.L. & SCHENA, L. (2015). Molecular analysis of Phytophthora diversity in nursery-grown ornamental and fruit plants. Plant Pathology, 64: 1308–1319.

REDONDO, M.Á., BOBERG, J., STENLID, J. & OLIVA, J. (2016). First report of Phytophthora pseudosyringae causing basal cankers on horse chestnut in Sweden. Plant Disease, 100: 1024.

REDONDO, M.Á., BOBERG, J., STENLID, J. & OLIVA, J. (2018). Functional traits associated with the establishment of introduced Phytophthora spp. in Swedish forests. Journal of Applied Ecology, 55: 1538–1552.

RIDDELL, C.E., FREDERICKSON-MATIKA, D., ARMSTRONG, A.C., ELLIOT, M., FORSTER, J.,

HEDLEY, P.E., MORRIS, J., THORPE, P., COOKE, D.E.L., PRITCHARD, L., SHARP, P.M. & GREEN, S. (2019). Metabarcoding reveals a high diversity of woody host-associated Phytophthora spp. in soils at public gardens and amenity woodlands in Britain. PeerJ. doi:10.7717/peerj.6931.

SCANU, B., JONES, B. & WEBBER, J.F. (2012). A new disease of Nothofagus in Britain caused by Phytophthora pseudosyringae. New Disease Reports, 25: 27.

SCANU, B. & WEBBER, J.F. (2016). Dieback and mortality of Nothofagus in Britain: ecology, pathogenicity and sporulation potential of the causal agent Phytophthora pseudosyringae. Plant Pathology, 65: 26–36.

SCIBETTA, S., SCHENA, L., CHIMENTO, A., CACCIOLA, S.O. & COOKE, D.E.L. (2012). A molecular method to assess Phytophthora diversity in environmental samples. Journal of Microbiological Methods, 88: 356–368.

VANNINI, A., BRUNI, N., TOMASSINI, A., FRANCESCHINI, S. & VETTRAINO, A.M. (2013). Pyrosequencing of environmental soil samples reveals biodiversity of the Phytophthora resident community in chestnut forests. FEMS Microbiology Ecology, 85: 433–442.

VÉLEZ, M.L., COETZEE, M.P.A., WINGFIELD, M.J., RAJCHENBERG, M. & GRESLEBIN, A.G. (2013). Evidence of low levels of genetic diversity for the Phytophthora austrocedrae population in Patagonia, Argentina. Plant Pathology, 63: 212–220.

WALLACE, S. (2015). Diversity of Phytophthora species in Costa Rica’s tropical forests. MSc thesis, University of Maryland.

YANG, X., TYLER, B.M. & HONG, C. (2017). An expanded phylogeny for the genus Phytophthora. IMA Fungus, 8: 355–384.

Published
2020-02-21
How to Cite
Green, S., Riddell, C. E., Frederickson-Matika, D., Armstrong, A., Elliot, M., Forster, J., Hedley, P. E., Morris, J., Thorpe, P., Cooke, D. E., Sharp, P. M., & Pritchard, L. (2020). Diversity of woody-host infecting Phytophthora species in public parks and botanic gardens as revealed by metabarcoding, and opportunities for mitigation through best practice. Sibbaldia: The International Journal of Botanic Garden Horticulture, (18), 67-88. https://doi.org/10.23823/Sibbaldia/2020.289
Section
Articles