Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Pacific Conservation Biology Pacific Conservation Biology Society
A journal dedicated to conservation and wildlife management in the Pacific region.
RESEARCH ARTICLE

Distribution and diversity of Phytophthora across Australia

Treena I. Burgess A M , Diane White A , Keith M. McDougall B , Jeff Garnas C , William A. Dunstan A , Santiago Català D , Angus J. Carnegie E , Stuart Worboys F , David Cahill G , Anna-Maria Vettraino H , Michael J. C. Stukely I , Edward C. Y. Liew J , Trudy Paap A C , Tanay Bose C , Duccio Migliorini C , Briony Williams A , Frances Brigg K , Colin Crane I , Timothy Rudman L and Giles E. St. J. Hardy A
+ Author Affiliations
- Author Affiliations

A Centre for Phytophthora Science and Management, School of Veterinary and Life Sciences, Murdoch University, WA 6150, Australia.

B Department of Ecology, Environment and Evolution, La Trobe University, PO Box 821, Wodonga, Vic. 3689, Australia.

C Forestry and Agriculture Biotechnology Institute, University of Pretoria, Pretoria, 0002, South Africa.

D Instituto Agroforestal Mediterráneo, Universitat Politècnica de València, Valencia, 46100, Spain.

E NSW Forest Science, NSW Department of Primary Industries, Parramatta, NSW 2150, Australia.

F Australian Tropical Herbarium, James Cook University Cairns Campus, Macgregor Road, Smithfield, Qld 4870 Australia.

G Faculty of Science, Engineering and Built Environment Research, Deakin University, Locked Bag 20000, Geelong, Vic. 3220, Australia.

H Department of Innovation in Biological Systems, Food and Forestry (DIBAF), University of Tuscia, 01100 Viterbo, Italy.

I Forest and Ecosystem Management, Parks and Wildlife, 17 Dick Perry Avenue, Kensington, WA 6151, Australia.

J Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney, NSW 2000, Australia.

K State Agriculture and Biotechnology Institute, School of Veterinary and Life Sciences, Murdoch University, WA 6150, Australia.

L Department of Primary Industries, Parks, Water and Environment, Hobart, Tas. 7000, Australia.

M Corresponding author. Email: tburgess@murdoch.edu.au

Pacific Conservation Biology 23(2) 150-162 https://doi.org/10.1071/PC16032
Submitted: 19 August 2016  Accepted: 12 December 2016   Published: 13 January 2017

Abstract

The introduction and subsequent impact of Phytophthora cinnamomi within native vegetation is one of the major conservation issues for biodiversity in Australia. Recently, many new Phytophthora species have been described from Australia’s native ecosystems; however, their distribution, origin, and potential impact remain unknown. Historical bias in Phytophthora detection has been towards sites showing symptoms of disease, and traditional isolation methods show variable effectiveness of detecting different Phytophthora species. However, we now have at our disposal new techniques based on the sampling of environmental DNA and metabarcoding through the use of high-throughput sequencing. Here, we report on the diversity and distribution of Phytophthora in Australia using metabarcoding of 640 soil samples and we compare the diversity detected using this technique with that available in curated databases. Phytophthora was detected in 65% of sites, and phylogenetic analysis revealed 68 distinct Phytophthora phylotypes. Of these, 21 were identified as potentially unique taxa and 25 were new detections in natural areas and/or new introductions to Australia. There are 66 Phytophthora taxa listed in Australian databases, 43 of which were also detected in this metabarcoding study. This study revealed high Phytophthora richness within native vegetation and the additional records provide a valuable baseline resource for future studies. Many of the Phytophthora species now uncovered in Australia’s native ecosystems are newly described and until more is known we need to be cautious with regard to the spread and conservation management of these new species in Australia’s unique ecosystems.

Additional Keywords: amplicon pyrosequencing, eDNA, high-throughput sequencing, invasive species.


References

Aghighi, S., Hardy, G. E. S., Scott, J. K., and Burgess, T. I. (2012). Phytophthora bilorbang sp. nov., a new species associated with the decline of Rubus anglocandicans (European blackberry) in Western Australia. European Journal of Forest Pathology 133, 841–855.
Phytophthora bilorbang sp. nov., a new species associated with the decline of Rubus anglocandicans (European blackberry) in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Brasier, C. M. (1996). Phytophthora cinnamomi and oak decline in southern Europe. Environmental constraints including climate change. Annales des Sciences Forestieres 53, 347–358.
Phytophthora cinnamomi and oak decline in southern Europe. Environmental constraints including climate change.Crossref | GoogleScholarGoogle Scholar |

Brasier, C. M. (2008). The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology 57, 792–808.
The biosecurity threat to the UK and global environment from international trade in plants.Crossref | GoogleScholarGoogle Scholar |

Brasier, C. M., and Webber, J. (2010). Plant pathology: sudden larch death. Nature 466, 824–825.
Plant pathology: sudden larch death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVSmurnF&md5=e691bd5dcbe2f5b1f83057364db64eb5CAS |

Brasier, C. M., Cooke, D. E. L., Duncan, J. M., and 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.
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.Crossref | GoogleScholarGoogle Scholar |

Brasier, C. M., Kirk, S. A., Delcan, J., Cooke, D. E. L., Jung, T., and Man In’t Veld, W. A. (2004). Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycological Research 108, 1172–1184.
Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1Clu7k%3D&md5=0be67ca671ff1969c927590f0770ec1fCAS |

Bunce, M., Oskam, C. L., and Allentoft, M. E. (2012). The use of quantitative real-time PCR in ancient DNA research. In ‘Methods in Molecular Biology – Ancient DNA’. (Eds B. Shapiro, and M. Hofreiter.) pp. 121–132. (Humana Press: New York.)

Burgess, T. I. (2015). Molecular characterization of natural hybrids formed between five related indigenous clade 6 Phytophthora species. PLoS One 10, e0134225.
Molecular characterization of natural hybrids formed between five related indigenous clade 6 Phytophthora species.Crossref | GoogleScholarGoogle Scholar |

Burgess, T. I., Webster, J. L., Ciampini, J. A., White, D., Hardy, G. E. S., and Stukely, M. J. C. (2009). Re-evaluation of Phytophthora species isolated during 30 years of vegetation health surveys in Western Australia using molecular techniques. Plant Disease 93, 215–223.
Re-evaluation of Phytophthora species isolated during 30 years of vegetation health surveys in Western Australia using molecular techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjs1Kntb4%3D&md5=befa4902432880714c6f6c1388752ef6CAS |

Burgess, T. I., Scott, J. K., Mcdougall, K. L., Stukely, M. J. C., Crane, C., Dunstan, W. A., Brigg, F., Andjic, V., White, D., Rudman, T., Arentz, F. A., Ota, N., and Hardy, G. E. S. (2016). Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens. Global Change Biology , .
Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens.Crossref | GoogleScholarGoogle Scholar |

Cahill, D. M., Rookes, J. E., Wilson, B. A., Gibson, L., and Mcdougall, K. L. (2008). Phytophthora cinnamomi and Australia’s biodiversity: impacts, predictions and progress towards control. Australian Journal of Botany 56, 279–310.
Phytophthora cinnamomi and Australia’s biodiversity: impacts, predictions and progress towards control.Crossref | GoogleScholarGoogle Scholar |

Callaghan, S., and Guest, D. (2015). Globalisation, the founder effect, hybrid Phytophthora species and rapid evolution: new headaches for biosecurity. Australasian Plant Pathology 44, 255–262.
Globalisation, the founder effect, hybrid Phytophthora species and rapid evolution: new headaches for biosecurity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjvVCmsbw%3D&md5=07a86f4ae3a57caf48e58f806928c1baCAS |

Català, S., Pérez-Sierra, A., and 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.
The use of genus-specific amplicon pyrosequencing to assess Phytophthora species diversity using eDNA from soil and water in northern Spain.Crossref | GoogleScholarGoogle Scholar |

Català, S., Berbegal, M., Pérez‐Sierra, A., and Abad‐Campos, P. (2016). Metabarcoding and development of new real‐time specific assays reveal Phytophthora species diversity in holm oak forests in eastern Spain. Plant Pathology , .
Metabarcoding and development of new real‐time specific assays reveal Phytophthora species diversity in holm oak forests in eastern Spain.Crossref | GoogleScholarGoogle Scholar |

Crone, M., Mccomb, J. A., O’brien, P. A., and Hardy, G. E. S. (2013). 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.
Survival of Phytophthora cinnamomi as oospores, stromata, and thick-walled chlamydospores in roots of symptomatic and asymptomatic annual and herbaceous perennial plant species.Crossref | GoogleScholarGoogle Scholar |

Crous, P. W., Groenewald, J. Z., Shivas, R. G., Edwards, J., Seifert, K. A., Alfenas, A. C., Alfenas, R. F., Burgess, T. I., Carnegie, A. J., Hardy, G. E. S., Hiscock, N., Hüberli, D., Jung, T., Louis-Seize, G., Okada, G., Pereira, O. L., Stukely, M. J. C., Wang, W., White, G. P., Young, A. J., Mctaggart, A. R., Pascoe, I. G., Porter, I. J., and Quaedvlieg, W. (2011). Fungal Planet description sheets: 69–91. Persoonia 26, 108–156.
Fungal Planet description sheets: 69–91.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbjvVWhsw%3D%3D&md5=9733bcce9088993667f680f2d6b03776CAS |

Crous, P. W., Summerell, B. A., Shivas, R. G., Burgess, T. I., Decock, C. A., Dreyer, L. L., Granke, L. L., Guest, D. I., Hardy, G. E. S., Hausbeck, M. K., Hüberli, D., Jung, T., Koukol, O., Lennox, C. L., Liew, E. C. Y., Lombard, L., Mctaggart, A. R., Pryke, J. S., Roets, F., Saude, C., Shuttleworth, L. A., Stukely, M. J. C., Vánky, K., Webster, B. J., Windstam, S. T., and Groenewald, J. Z. (2012). Fungal Planet description sheets: 107–127. Persoonia 28, 138–182.
Fungal Planet description sheets: 107–127.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s%2FoslOjtw%3D%3D&md5=2f31bd53606a0802264bba96a1e56cd8CAS |

Crous, P. W., Wingfield, M. J., Schumacher, R. K., Summerell, B. A., Giraldo, A., Gené, J., Guarro, J., Wanasinghe, D. N., Hyde, K. D., Camporesi, E., Gareth Jones, E. B., Thambugala, K. M., Malysheva, E. F., Malysheva, V. F., Acharya, K., Álvarez, J., Alvarado, P., Assefa, A., Barnes, C. W., Bartlett, J. S., Blanchette, R. A., Burgess, T. I., Carlavilla, J. R., Coetzee, M. P. A., Damm, U., Decock, C. A., Den Breeÿen, A., De Vries, B., Dutta, A. K., Holdom, D. G., Latham, S. R., Manjón, J. L., Marincowitz, S., Mirabolfathy, M., Moreno, G., Nakashima, C., Papizadeh, M., Romberg, M. K., Shivas, R. G., Stalpers, J. A., Stielow, B., Stukely, M. J. C., Swart, W. J., Tan, Y. P., Van Der Bank, M., Wood, A. R., Zhang, Y., and Groenewald, J. W. (2014). Fungal Planet description sheets: 281–319. Persoonia 33, 212–289.
Fungal Planet description sheets: 281–319.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MngvFyjuw%3D%3D&md5=5cfe76b1591966efa92cfc9d31400f92CAS |

Dick, M. A., Dobbie, K., Cooke, D. E. L., and Brasier, C. M. (2006). Phytophthora captiosa sp. nov. and P. fallax sp. nov. causing crown dieback of Eucalyptus in New Zealand. Mycological Research 110, 393–404.
Phytophthora captiosa sp. nov. and P. fallax sp. nov. causing crown dieback of Eucalyptus in New Zealand.Crossref | GoogleScholarGoogle Scholar |

Dick, M. A., Williams, N. M., Bader, M. K. F., Gardner, J. F., and Bulman, L. S. (2014). Pathogenicity of Phytophthora pluvialis to Pinus radiata and its relation with red needle cast disease in New Zealand. New Zealand Journal of Forestry Science 44, 6.
Pathogenicity of Phytophthora pluvialis to Pinus radiata and its relation with red needle cast disease in New Zealand.Crossref | GoogleScholarGoogle Scholar |

Dunstan, W. A., Howard, K., Hardy, G. E. S., and Burgess, T. I. (2016). A overview of Australia’s Phytophthora species assemblage in natural ecosystems recovered from a survey in Victoria. IMA Fungus 7, 47–58.
A overview of Australia’s Phytophthora species assemblage in natural ecosystems recovered from a survey in Victoria.Crossref | GoogleScholarGoogle Scholar |

Durán, A., Gryzenhout, M., Slippers, B., Ahumada, R., Rotella, A., Flores, F., Wingfield, B. D., and Wingfield, M. J. (2008). Phytophthora pinifolia sp. nov. associated with a serious needle disease of Pinus radiata in Chile. Plant Pathology 57, 715–727.
Phytophthora pinifolia sp. nov. associated with a serious needle disease of Pinus radiata in Chile.Crossref | GoogleScholarGoogle Scholar |

Erwin, D. C., and Ribeiro, O. K. (1996). ‘Phytophthora Diseases Worldwide.’ (APS Press: St Paul, MN).

Garkaklis, M. J., Calver, M. C., Wilson, B. A., and Hardy, G. E. S. (2004). Habitat alteration caused by introduced plant disease: a significant threat to the conservation of Australian forest fauna. In ‘Conservation of Australia’s Forest Fauna’. (Ed. D. Lunney.) pp. 899–913. (Royal Zoological Society of New South Wales: Sydney.)

Ginetti, B., Moricca, S., Squires, J. N., Cooke, D. E. L., Ragazzi, A., and Jung, T. (2014). Phytophthora acerina sp. nov., a new species causing bleeding cankers and dieback of Acer pseudoplatanus trees in planted forests in northern Italy. Plant Pathology 63, 858–876.
Phytophthora acerina sp. nov., a new species causing bleeding cankers and dieback of Acer pseudoplatanus trees in planted forests in northern Italy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFOltbfP&md5=cc37d963f87709d85cda5d7b3b014f14CAS |

Green, S., Hendry, S. J., Macaskill, G. A., Laue, B. E., and Steele, H. (2012). Dieback and mortality of Juniperus communis in Britain associated with Phytophthora austrocedrae. New Disease Reports 26, .
Dieback and mortality of Juniperus communis in Britain associated with Phytophthora austrocedrae.Crossref | GoogleScholarGoogle Scholar |

Greslebin, A. G., Hansen, E. M., Winton, L. M., and Rajchenberg, M. (2005). Phytophthora species from declining Austrocedrus chilensis forests in Patagonia, Argentina. Mycologia 97, 218–228.
Phytophthora species from declining Austrocedrus chilensis forests in Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |

Greslebin, A. G., Hansen, E. M., and Sutton, W. (2007). Phytophthora austrocedrae sp. nov., a new species associated with Austrocedrus chilensis mortality in Patagonia (Argentina). Mycological Research 111, 308–316.
Phytophthora austrocedrae sp. nov., a new species associated with Austrocedrus chilensis mortality in Patagonia (Argentina).Crossref | GoogleScholarGoogle Scholar |

Hansen, E. M. (2012). Phythophthora alni. Forest Phytophthoras 2, .
Phythophthora alni.Crossref | GoogleScholarGoogle Scholar |

Hansen, E. M., Streito, J.-C., and Delatour, C. (1999). First confirmation of Phytophthora lateralis in Europe. Plant Disease 83, 587–587.
First confirmation of Phytophthora lateralis in Europe.Crossref | GoogleScholarGoogle Scholar |

Hansen, E. M., Goheen, D. J., Jules, E. S., and Ullian, B. (2000). Managing Port-Orford-cedar and the introduced pathogen Phytophthora lateralis. Plant Disease 84, 4–14.
Managing Port-Orford-cedar and the introduced pathogen Phytophthora lateralis.Crossref | GoogleScholarGoogle Scholar |

Hansen, E. M., Reeser, P. W., and Sutton, W. (2012). Phytophthora beyond agriculture. Annual Review of Phytopathology 50, 359–378.
Phytophthora beyond agriculture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWht73K&md5=687d857e5b66aae66e0ec7ff2e29c9feCAS |

Harris, R., Cassis, G., Auld, T., and Hutton, I. (2005). Floristics and structure of the mossy cloud forest of Mt Gower summit, Lord Howe Island. Pacific Conservation Biology 11, 246–256.
Floristics and structure of the mossy cloud forest of Mt Gower summit, Lord Howe Island.Crossref | GoogleScholarGoogle Scholar |

Hong, C., Gallegly, M. E., Richardson, P. A., and Kong, P. (2011). Phytophthora pini Leonian resurrected to distinct species status. Mycologia 103, 351–360.
Phytophthora pini Leonian resurrected to distinct species status.Crossref | GoogleScholarGoogle Scholar |

Hong, C., Richardson, P. A., Hao, W., Ghimire, S. R., Kong, P., Moorman, G. W., Lea-Cox, J. D., and Ross, D. S. (2012). Phytophthora aquimorbida sp. nov. and Phytophthora taxon ‘aquatilis’ recovered from irrigation reservoirs and a stream in Virginia, USA. Mycologia 104, 1097–1108.
Phytophthora aquimorbida sp. nov. and Phytophthora taxon ‘aquatilis’ recovered from irrigation reservoirs and a stream in Virginia, USA.Crossref | GoogleScholarGoogle Scholar |

Hüberli, D., Tommerup, I. C., and Hardy, G. E. S. (2000). False-negative isolations or absence of lesions may cause mis-diagnosis of diseased plants infected with Phytophthora cinnamomi. Australasian Plant Pathology 29, 164–169.
False-negative isolations or absence of lesions may cause mis-diagnosis of diseased plants infected with Phytophthora cinnamomi.Crossref | GoogleScholarGoogle Scholar |

Hüberli, D., Hardy, G. E. S., White, D., Williams, N., and Burgess, T. I. (2013). Fishing for Phytophthora from Western Australia’s waterways: a distribution and diversity survey. Australasian Plant Pathology 42, 251–260.
Fishing for Phytophthora from Western Australia’s waterways: a distribution and diversity survey.Crossref | GoogleScholarGoogle Scholar |

Ireland, K. B., Hardy, G. E. S., and Kriticos, D. J. (2013). Combining inferential and deductive approaches to estimate the potential geographical range of the invasive plant pathogen, Phytophthora ramorum. PLoS One 8, e63508.
Combining inferential and deductive approaches to estimate the potential geographical range of the invasive plant pathogen, Phytophthora ramorum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnslGhtrc%3D&md5=af5fdc0315fe8a8015930277c53a38c2CAS |

Irwin, J. G., Cahill, D. M., and Drenth, A. (1995). Phytophthora in Australia. Australian Journal of Agricultural Research 46, 1311–1337.
Phytophthora in Australia.Crossref | GoogleScholarGoogle Scholar |

Jung, T., and Burgess, T. I. (2009). Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia 22, 95–110.
Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7ltlCnsA%3D%3D&md5=56ce451baf83b2331cca34a4e6cec1eaCAS |

Jung, T., Stukely, M. J. C., Hardy, G. E. S., White, D., Paap, T., Dunstan, W. A., and Burgess, T. I. (2011). Multiple new Phytophthora species from ITS clade 6 associated with natural ecosystems in Australia: evolutionary and ecological implications. Persoonia 26, 13–39.
Multiple new Phytophthora species from ITS clade 6 associated with natural ecosystems in Australia: evolutionary and ecological implications.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbjvVWitw%3D%3D&md5=a4108759b2ff54cbcc73c91a0c267775CAS |

Kingsford, R. T., Watson, J. E., Lundquist, C. J., Venter, O., Hughes, L., Johnston, E. L., Atherton, J., Gawel, M., Keith, D. A., Mackey, B. G., and Morley, C. (2009). Major conservation policy issues for biodiversity in Oceania. Conservation Biology 23, 834–840.
Major conservation policy issues for biodiversity in Oceania.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MrgsVersQ%3D%3D&md5=1b64a26fd2c7ea3ec9ea2f05e7755e98CAS |

Martin, F. N., Blair, J. E., and Coffey, M. D. (2014). A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora. Fungal Genetics and Biology 66, 19–32.
A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXksFWrsLs%3D&md5=ae071142c8cbfce46fd3d9ec29a2816aCAS |

Migliorini, D., Ghelardini, L., Tondini, E., Luchi, N., and Santini, A. (2015). The potential of symptomless potted plants for carrying invasive soilborne plant pathogens. Diversity & Distributions 21, 1218–1229.
The potential of symptomless potted plants for carrying invasive soilborne plant pathogens.Crossref | GoogleScholarGoogle Scholar |

Nagel, J. H., Gryzenhout, M., Slippers, B., Wingfield, M. J., Hardy, G. E. S., Stukely, M. J. C., and Burgess, T. I. (2013). Characterization of Phytophthora hybrids from ITS clade 6 associated with riparian ecosystems in South Africa and Australia. Fungal Biology 117, 329–347.
Characterization of Phytophthora hybrids from ITS clade 6 associated with riparian ecosystems in South Africa and Australia.Crossref | GoogleScholarGoogle Scholar |

Oh, E., Gryzenhout, M., Wingfield, B. D., Wingfield, M. J., and Burgess, T. I. (2013). Surveys of soil and water reveal a goldmine of Phytophthora diversity in South African natural ecosystems. IMA Fungus 4, 123–131.
Surveys of soil and water reveal a goldmine of Phytophthora diversity in South African natural ecosystems.Crossref | GoogleScholarGoogle Scholar |

Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., Mcglinn, D., Minchin, P. R., O’hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E., and Wagner, H. (2016). vegan: Community Ecology Package. Available at: https://cran.r-project.org, https://github.com/vegandevs/vegan.

Parke, J. L., and Rizzo, D. M. (2011). Phytophthora ramorum. Forest Phytophthoras 1, .
Phytophthora ramorum.Crossref | GoogleScholarGoogle Scholar |

Prigigallo, M. I., Abdelfattah, A., Cacciola, S. O., Faedda, R., Sanzani, S. M., Cooke, D. E., and Schena, L. (2016). Metabarcoding analysis of Phytophthora diversity using genus-specific primers and 454 pyrosequencing. Phytopathology 106, 305–313.
Metabarcoding analysis of Phytophthora diversity using genus-specific primers and 454 pyrosequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXls1SrtA%3D%3D&md5=c0106c708440aec0c4379f348ed5aeccCAS |

Rea, A., Jung, T., Burgess, T. I., Stukely, M. J. C., and Hardy, G. E. S. (2010). Phytophthora elongata sp. nov. a novel pathogen from the Eucalyptus marginata forest of Western Australia. Australasian Plant Pathology 39, 477–491.
Phytophthora elongata sp. nov. a novel pathogen from the Eucalyptus marginata forest of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Rea, A., Burgess, T. I., Hardy, G. E. S., Stukely, M. J. C., and Jung, T. (2011). Two novel species of Phytophthora associated with episodic dieback of kwongan vegetation of south-west Western Australia. Plant Pathology 60, 1055–1068.
Two novel species of Phytophthora associated with episodic dieback of kwongan vegetation of south-west Western Australia.Crossref | GoogleScholarGoogle Scholar |

Reeser, P., Sutton, W., and Hansen, E. M. (2013). Phytophthora pluvialis, a new species from mixed tanoak–Douglas-fir forests of western Oregon, USA. North American Fungi 8, 1–8.
Phytophthora pluvialis, a new species from mixed tanoak–Douglas-fir forests of western Oregon, USA.Crossref | GoogleScholarGoogle Scholar |

Runge, F., Telle, S., Ploch, S., Savory, E., Day, B., Sharma, R., and Thines, M. (2011). The inclusion of downy mildews in a multi-locus-dataset and its reanalysis reveals a high degree of paraphyly in Phytophthora. IMA Fungus 2, 163–171.
The inclusion of downy mildews in a multi-locus-dataset and its reanalysis reveals a high degree of paraphyly in Phytophthora.Crossref | GoogleScholarGoogle Scholar |

Safaiefarahani, B., Mostowfizadeh-Ghalamfarsa, R., Hardy, G. E. S., and Burgess, T. I. (2015). Re-evaluation of the Phytophthora cryptogea species complex and the description of a new species, Phytophthora pseudocryptogea sp. nov. Mycological Progress 14, 108.
Re-evaluation of the Phytophthora cryptogea species complex and the description of a new species, Phytophthora pseudocryptogea sp. nov.Crossref | GoogleScholarGoogle Scholar |

Scarlett, K., Daniel, R., Shuttleworth, L. A., Roy, B., Bishop, T. F. A., and Guest, D. I. (2015). Phytophthora in the Gondwana rainforests of Australia World Heritage Area. Australasian Plant Pathology 44, 335–348.
Phytophthora in the Gondwana rainforests of Australia World Heritage Area.Crossref | GoogleScholarGoogle Scholar |

Schoebel, C. N., Stewart, J., Gruenwald, N. J., Rigling, D., and Prospero, S. (2014). Population history and pathways of spread of the plant pathogen Phytophthora plurivora. PLoS One 9, e85368.
Population history and pathways of spread of the plant pathogen Phytophthora plurivora.Crossref | GoogleScholarGoogle Scholar |

Scibetta, S., Schena, L., Chimento, A., Cacciola, S. O., and Cooke, D. E. L. (2012). A molecular method to assess Phytophthora diversity in environmental samples. Journal of Microbiological Methods 88, 356–368.
A molecular method to assess Phytophthora diversity in environmental samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFOisb8%3D&md5=a67b55c1dc4c9931da2a53ee37f65445CAS |

Scott, P. M., Burgess, T. I., Barber, P. A., Shearer, B. L., Stukely, M. J. C., Hardy, G. E. S., and Jung, T. (2009). Phytophthora multivora sp. nov., a new species recovered from declining Eucalyptus, Banksia, Agonis and other plant species in Western Australia. Persoonia 22, 1–13.
Phytophthora multivora sp. nov., a new species recovered from declining Eucalyptus, Banksia, Agonis and other plant species in Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7ltlCgsQ%3D%3D&md5=a7cf265ad107664041606b73a237f4a3CAS |

Scott, P., Burgess, T. I., and Hardy, G. E. S. (2013). Globalization and Phytophthora. In ‘Phytophthora, A Global Perspective’. (Ed. K. Lamour.) pp. 226–233. (CAB International: Boston, MA.)

Shearer, B. L., Crane, C. E., Barrett, S., and Cochrane, A. (2007). Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Australian Journal of Botany 55, 225–238.
Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Shivas, R. G. (1989). Fungal and bacterial diseases of plants in Western Australia. Journal of the Royal Society of Western Australia 72, 1–62.

Simamora, A., Stukely, M. J. C., Hardy, G. E. S., and Burgess, T. I. (2015). Phytophthora boodjera sp. nov., a damping-off pathogen in production nurseries and from urban and natural landscapes, with an update on the status of P. alticola. IMA Fungus 6, 319–335.
Phytophthora boodjera sp. nov., a damping-off pathogen in production nurseries and from urban and natural landscapes, with an update on the status of P. alticola.Crossref | GoogleScholarGoogle Scholar |

Taberlet, P., Coissac, E., Hajibabaei, M., and Rieseberg, L. H. (2012). Environmental DNA. Molecular Ecology 21, 1789–1793.
Environmental DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVGksLw%3D&md5=84a99e4e5df8f2ae85c2b614697f7c60CAS |

Vannini, A., Bruni, N., Tomassini, A., Franceschini, S., and 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.
Pyrosequencing of environmental soil samples reveals biodiversity of the Phytophthora resident community in chestnut forests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVemsr3E&md5=a1be19d528f47189f70f7112f44ddb98CAS |

Von Broembsen, S. L., and Kruger, F. J. (1985). Phytophthora cinnamomi associated with mortality of native vegetation in South Africa. Plant Disease 69, 715–717.
Phytophthora cinnamomi associated with mortality of native vegetation in South Africa.Crossref | GoogleScholarGoogle Scholar |

Weir, B. S., Paderes, E. P., Anand, N., Uchida, J. Y., Pennycook, S. R., Bellgard, S. E., and Beever, R. E. (2015). A taxonomic revision of Phytophthora Clade 5 including two new species, Phytophthora agathidicida and P. cocois. Phytotaxa 205, 21–38.
A taxonomic revision of Phytophthora Clade 5 including two new species, Phytophthora agathidicida and P. cocois.Crossref | GoogleScholarGoogle Scholar |