Skip to main content
Log in

Globalisation, the founder effect, hybrid Phytophthora species and rapid evolution: new headaches for biosecurity

  • Original Paper
  • Published:
Australasian Plant Pathology Aims and scope Submit manuscript

Abstract

The oomycete genus Phytophthora contains a large number of plant pathogens that cause significant damage to natural and agricultural systems. Until recently species have been distinguished using a limited set of morphological characters. The development of DNA-based technologies has revealed much broader and more complex diversity than previously recognised, and has led to the recent description of many new species. This review looks at the underlying mechanisms for the generation of diversity within the genus. The intercontinental movement and transplantation of infected plant material partially explains the appearance of new species in unexpected places. However, it is also likely that novel species arise as a result of the hybridisation and rapid evolution of introduced species under episodic selection pressures. Hybrid progeny may possess equal or greater virulence than parent species, thereby posing an increasing risk to our natural environment and agricultural production systems. These discoveries amplify the threats posed by the introduction of plant pathogens into new environments, and expose a crucial weakness in current evidence-based biosecurity regimes. Further work is required to identify hybrids, anticipate and understand the occurrence of hybridisation, and to implement appropriate quarantine and risk management measures.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmed S, de Labrouhe DT, Delmotte F (2012) Emerging virulence arising from hybridisation facilitated by multiple introductions of the sunflower downy mildew pathogen Plasmopara halstedii. Fungal Genet Biol 49(10):847–855

    Article  CAS  PubMed  Google Scholar 

  • Arneson PA (2011) Coffee rust. Plant Health Instr. doi:10.1094/PHI-I-2000-0718-02

    Google Scholar 

  • Bertier L, Leus L, D’hondt L, de Cock AWAM, Hofte M (2013) Host adaptation and speciation through hybridisation and polyploidy in Phytophthora. PLoS 8(12):e85385

    Article  Google Scholar 

  • Blair JE, Coffey MD, Park S-Y, Geiser DM, Kang S (2008) A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet Biol 45:266–277

    Article  CAS  PubMed  Google Scholar 

  • Bonants PJM, Hagenaar-de Weerdt M, Man in’t Veld WA, Baayen RP (2000) Molecular characterization of natural hybrids of Phytophthora nicotianae and P. cactorum. Phytopathology 90:867–874

    Article  CAS  PubMed  Google Scholar 

  • Brasier CM (1991) Current questions in Phytophthora systematics: the role of the population approach. In: Phytophthora. Ed. by Lucas, JA, Shattock RC, Shaw DS and Cooke LR. Cambridge University Press, Cambridge. pp. 104–128

  • Brasier CM (1995) Episodic selection as a force in fungal microevolution, with special reference to clonal speciation and hybrid introgression. Can J Bot 73(1):1213–1221

    Article  Google Scholar 

  • Brasier CM (2000) The rise of the hybrid fungi. Nature 405:134–135

    Article  CAS  PubMed  Google Scholar 

  • Brasier CM (2001) Rapid evolution of introduced plant pathogens via interspecific hybridization. Bioscience 51:123–133

    Article  Google Scholar 

  • Brasier CM (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol 57:792–808

    Article  Google Scholar 

  • Brasier CM (2009) Phytophthora biodiversity: How many Phytophthora species are there? In (Goheen, E.M. and Frankel, S.J. Eds).Phytophthoras in Forests and Natural Ecosystems. Proceedings of the Fourth International Union of Forest Research Organisations (IUFRO) Working Party 7.02.09. General Technical Report PSW-GTR-221. Albany, CA: USDA Forest Service, Pacific Southwest Research Station, pp. 101–115

  • Brasier CM, Kirk SA (2001) Comparative aggressiveness of standard and variant hybrid alder phytophthoras, Phytophthora cambivora and other Phytophthora species on bark of Alnus, Quercus and other woody hosts. Plant Pathol 50:218–229

    Article  Google Scholar 

  • Brasier CM, Kirk SA, Pipe N, Buck KW (1998) Rare hybrids in natural populations of the Dutch elm disease pathogens Ophiostoma ulmi and O. novo-ulmi. Mycol Res 102:45–57

    Article  Google Scholar 

  • Brasier CM, Cooke D, Duncan JM (1999) Origin of a new Phytophthora pathogen through interspecific hybridization. Proc Natl Acad Sci 96:5878–5883

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brasier CM, Sanchez-Hernandez E, Kirk SA (2003) Phytophthora inundata sp. nov., a part heterothallic pathogen on trees and shrubs in wet or flooded soils. Mycol Res 107:477–484

    Article  PubMed  Google Scholar 

  • Brasier CM, Kirk SA, Delcan J, Cooke DEL, Jung T, Man in’t Veld WA (2004) Phytophthora alni sp. nov. and its variants: designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycol Res 108:1172–1184

    Article  CAS  PubMed  Google Scholar 

  • Burgess TI, Webster JL, Ciampini JA, White D, Hardy GESJ, Stukely MJC (2009) Re-evaluation of Phytophthora species isolated during 30 years of vegetation health surveys in Western Australia using molecular techniques. Plant Dis 93(3):215–223

    Article  CAS  Google Scholar 

  • Clay K, Kover PX (1996) The red queen hypothesis and plant/pathogen interactions. Annu Rev Phytopathol 34:29–50

    Article  CAS  PubMed  Google Scholar 

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    Article  CAS  PubMed  Google Scholar 

  • Cooke DEL and Andersson B (2013) Phytophthora infestans and potato blight in Europe. Phytophthora: a global perspective Ed. Lamour, K. CABI Plant Protection Series, No.2. pp. 59–64

  • Cooke DEL, Duncan JM (1997) Phylogenetic analysis of Phytophthora species based on ITS1 and ITS2 sequences of the ribosomal RNA gene repeat. Mycol Res 101:667–677

    Article  CAS  Google Scholar 

  • Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol 30:17–32

    Article  CAS  PubMed  Google Scholar 

  • Davison EM, Drenth A, Kumar S, Mack S, Mackie AE, McKirdy S (2006) Pathogens associated with nursery plants imported into Western Australia. Aust Plant Pathol 35:473–475

    Article  Google Scholar 

  • de Cock AWAM, Lévesque CA (2004) New species of Pythium and Phytophthora. Stud Mycol 50:481–487

    Google Scholar 

  • Dobrowolski M, Tommerup I, Shearer B, O’Brien P (2003) Three clonal lineages of Phytophthora cinnamomi in Australia revealed by microsatellites. Phytopathology 93:695–704

    Article  CAS  PubMed  Google Scholar 

  • Donahoo RS, Lamour KH (2008) Interspecific hybridization and apomixis between Phytophthora capsici and Phytophthora tropicalis. Mycologia 100:911–920

    Article  CAS  PubMed  Google Scholar 

  • Drenth A, Goodwin SB (1999) Population structure: Oomycetes. In: Worral JJ (ed) Structure and Dynamics of Fungal Populations. Kluwer Academic Publishers, The Netherlands, pp. 195–224

    Chapter  Google Scholar 

  • Drenth A, Guest D (2013) Phytophthora palmivora in tropical tree crops. In: Lamour, K (ed) Phytophthora: a global perspective. CABI Plant Protection Series, No.2 pp. 187–196

  • Drenth A, Tas ICQ, Govers F (1994) DNA fingerprinting uncovers a new sexually reproducing population of Phytophthora infestans in The Netherlands. Eur J Plant Pathol 100:97–107

    Article  Google Scholar 

  • Érsek T, Man in’t Veld WA (2013) Phytophthora species hybrids: a novel threat to crops and natural ecosystems. In: Lamour, K (ed) Phytophthora: a global perspective. CABI Plant Protection Series, No.2. pp. 37–47

  • Érsek T, Ribeiro OK (2010) An annotated list of new Phytophthora species described post-1996. Acta Phytopathol Entomol Hung 45:251–266

    Article  Google Scholar 

  • Érsek T, English JT, Schoelz JE (1995) Creation of species hybrids of Phytophthora with modified host ranges by zoospore fusion. Phytopathology 85:1343–1347

    Article  Google Scholar 

  • Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135

    Article  PubMed  Google Scholar 

  • Förster H, Cummings MP, Coffey MD (2000) Phylogenetic relationships of Phytophthora species based on ribosomal ITS I DNA sequence analysis with emphasis on Waterhouse groups V and VI. Mycol Res 104:1055–1061

    Article  Google Scholar 

  • Fry WE, Goodwin SB, Dyer AT, Matuszak JM, Drenth A, Tooley PW, Sujkowski LS, Koh YJ, Cohen BA, Spielman LJ, Deahl KL, Inglis DA, Sandlan KP (1993) Historical and recent migrations of Phytophthora infestans: chronology, pathways and implications. Plant Dis 77:653–661

    Article  Google Scholar 

  • Gaeta RT, Chris Pires J (2010) Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol 186:18–28

    Article  CAS  PubMed  Google Scholar 

  • Gavino PD, Smart CD, Sandrock RW, Miller JS, Hamm PB, Lee TY, Davis RM, Fry WE (2000) Implications of sexual reproduction for Phytophthora infestans in the United States: generation of an aggressive lineage. Plant Dis 84:731–735

    Article  Google Scholar 

  • Goodwin SB, Fry WE (1994) Genetic analysis of interspecific hybrids between Phytophthora infestans and Phytophthora mirabilis. Exp Mycol 18:20–32

    Article  Google Scholar 

  • Goodwin SB, Smart CD, Sandrock RW, Deahl KL, Punja ZK, Fry WE (1998) Genetic change within populations of Phytophthora infestans in the United States and Canada during 1994 to 1996: role of migration and recombination. Phytopathology 88:939–949

    Article  CAS  PubMed  Google Scholar 

  • Goss EM, Cardenas ME, Myers K, Forbes GA, Fry WE, Restrepo S, Grünwald NJ (2011) The plant pathogen Phytophthora andina emerged via hybridization of an unknown Phytophthora species and the Irish potato famine pathogen, P infestans. PLoS One 6:e24543

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grunwald NJ, Werres S, Goss EM, Taylor CR, Fieland VJ (2012) Phytophthora obscura sp. nov., a new species of the novel Phytophthora subclade 8d. Plant Pathol 61:610–622

    Article  CAS  Google Scholar 

  • Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398

    Article  CAS  PubMed  Google Scholar 

  • Halterman D, Gevens AJ (2013) Phytophthora infestans in the US. In: Lamour, K (ed) Phytophthora: a global perspective. CABI Plant Protection Series, No.2. pp. 68–78

  • Heybroek HM (1993) The Dutch Elm Breeding Program. In: Sticklen & Sherald (Eds.) Dutch Elm Disease Research, Chapter 3. Springer Verlag, New York

  • Huberli D, Hardy GESJ, White D, Williams N, Burgess TI (2013) Fishing for Phytophthora from western Australia waterways: a distribution and diversity survey. Australas Plant Pathol 42:251–260

    Article  Google Scholar 

  • Ioos R, Andrieux A, Marçais B, Frey P (2006) Genetic characterization of the natural hybrid species Phytophthora alni as inferred from nuclear and mitochondrial DNA analyses. Fungal Genet Biol 43:511–529

    Article  CAS  PubMed  Google Scholar 

  • Jung T, Burgess TI (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jung T, Stukely MJC, Hardy GESJ, White D, Paap T, Dunstan WA, Burgess TI (2011) Multiple new Phytophthora species from ITS Clade 6 associated with natural ecosystems in Australia: evolutionary and ecological implications. Persoonia 26:13–39

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaschani F, Van der Hoorn RAL (2011) A model of the C14-EPIC complex indicates hotspots for a protease-inhibitor arms race in the oomycete-potato interaction. Plant Signal Behav 6(1):109–112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Linde C, Drenth A, Kemp GHJ, Wingfield MJ, Von Broembsen S (1997) Population structure of Phytophthora cinnamomi in South Africa. Phytopathology 87:822–827

    Article  CAS  PubMed  Google Scholar 

  • Linderman RG, Davis EA (2006) Evaluation of chemical and biological agents for control of Phytophthora species on intact plants or detached leaves of rhododendron and lilac. In: Frankel, S.J., Shea, P.J. and Haverty, M.I. (eds) Proceedings of the Sudden Oak Death Second Science Symposium: The State of Our Knowledge. General Technical Report PSW-GTR-196. United States Department of Agriculture (USDA) Forest Service, Pacific Southwest Research Station, Albany, California, pp. 265– 268

  • Man in’t Veld WA, Venbaas-Rijks WJ, Ilieva E, de Cock AWAM, Bonants PJM, Pieters R (1998) Natural hybrids of Phytophthora nicotianae and Phytophthora cactorum demonstrated by isozyme analysis and random amplified polymorphic DNA. Phytopathology 88:922–929

    Article  Google Scholar 

  • Man in’t Veld WA, de Cock WAM, Summerbell RC (2007) Natural hybrids of resident and introduced Phytophthora species proliferating on multiple new hosts. Eur J Plant Pathol 117:25–33

    Article  Google Scholar 

  • Man in’t Veld WA, Rosendahl KCHM, Hong C (2012) Phytophthora serendipita sp. nov. and P. pelgrandis, two destructive pathogens generated by natural hybridization. Mycologia 104:1390–1396

    Article  Google Scholar 

  • Martens C, Van de Peer Y (2010) The hidden duplication past of the plant pathogen Phytophthora and its consequences for infection. BMC Genomics 11:353

    Article  PubMed Central  PubMed  Google Scholar 

  • May KJ, Drenth A, Irwin JAG (2003) Interspecific hybrids between the homothallic Phytophthora sojae and Phytophthora vignae. Australas J Plant Pathol 32:353–359

    Article  CAS  Google Scholar 

  • Mayr E (1942) Systematics and the Origin of Species, from the Viewpoint of a Zoologist. Harvard University Press, Cambridge

    Google Scholar 

  • Newcombe G, Stirling B, McDonald S, Bradshaw JR (2000) Melampsora x columbiana, a natural hybrid of M. medusae and M. occidentalis. Mycol Res 104:261–274

    Article  Google Scholar 

  • Nirenberg HI, Gerlach WF, Gräfenhan T (2009) Phytophthora x pelgrandis, a new natural hybrid pathogenic to Pelargonium grandiflorum hort. Mycologia 101:220–231

    Article  CAS  PubMed  Google Scholar 

  • Parkunan V, Johnson CS, Bowman BC, Hong CX (2010) Population structure, mating type, and mefenoxam sensitivity of Phytophthora nicotianae in Virginia tobacco fields. Plant Dis 94:1361–1365

    Article  Google Scholar 

  • Paun O, Fay MF, Soltis DE, Chase MW (2007) Genetic and epigenetic alterations after hybridization and genome doubling. Taxon 56:649–656

    Article  PubMed Central  PubMed  Google Scholar 

  • Peters RD, Al-Mughrabi KI, Kalischuk ML, Dobinson KF, Conn KL, Alkher H, Islam MR, Daayf F, Lynn J, Bizimungu B, De Koeyer D, Lévesque CA, Kawchuk LM (2014) Characterization of Phytophthora infestans population diversity in Canada reveals increased migration and genotype recombination. Can J Plant Pathol 36:73–82

    Article  Google Scholar 

  • Podger FD (1968) Aetiology of jarrah dieback and disease of dry sclerophyll Eucalyptus marginata Sm. forests in Western Australia. MSc Thesis, University of Western Australia

  • Rea A, Jung T, Burgess TI, Stukely MJC, Hardy GESJ (2010) Phytophthora elongata sp. nov. a novel pathogen from the Eucalyptus marginata forest of Western Australia. Australas Plant Pathol 39:477–491

    Article  Google Scholar 

  • Ristaino JB (2002) Tracking historic migrations of the Irish potato famine pathogen, Phytophthora infestans. Microbes Infect 4:1369–1377

    Article  PubMed  Google Scholar 

  • Runge F, Telle S, Ploch S, Savory E, Day B, Sharma R, 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 Glob Mycol J 2:163–171

    Article  Google Scholar 

  • Sansome E (1977) Polyploidy and induced gametangial formation in British isolates of Phytophthora infestans. J Genet Microbiol 99:311–316

    Article  Google Scholar 

  • Sansome E, Brasier CM (1974) Polyploidy associated with varietal differentiation in the megasperma complex of Phytophthora. Trans Br Mycol Soc 63:461–467

    Article  Google Scholar 

  • Sansome E, Brasier CM, Hamm PB (1991) Phytophthora meadii may be a species hybrid. Mycol Res 95:273–277

    Article  Google Scholar 

  • Scott PM, Burgess TI, Barber PA, Shearer BL, Stukely MJ, Hardy GE, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scott P, Burgess T, Hardy G (2013) Globalisation and Phytophthora. In Lamour, K (ed) Phytophthora: a global perspective. CABI Plant Protection Series, No.2. pp. 37–47

  • Sujkowski LS (1994) Increased genotypic diversity via migration and possible occurrence of sexual reproduction of Phytophthora infestans in Poland. Phytopathology 84:201–207

    Article  Google Scholar 

  • Truong NV, Liew EC, Burgess LW (2010) Characterisation of Phytophthora capsici isolates from black pepper in Vietnam. Fungal Biol 114:160–170

    Article  CAS  PubMed  Google Scholar 

  • Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313(5791):1261–1266

    Article  CAS  PubMed  Google Scholar 

  • Vercauteren A, Boutet X, D’hondt L, Van Bockstaele E, Maes M, Leus L, Chandelier A, Heungens K (2011) Aberrant genome size and instability of Phytophthora ramorum oospore progenies. Fungal Genet Biol 48(5):537–543

    Article  CAS  PubMed  Google Scholar 

  • Villa NO, Kageyama K, Asano T, Suga H (2006) Phylogenetic relationships of Pythium and Phytophthora species based on ITS rDNA, cytochrome oxidase II and beta-tubulin gene sequences. Mycologia 98:410–422

    Article  CAS  PubMed  Google Scholar 

  • Wellings CR, McIntosh RA (1990) Puccinia striiformis f.sp. tritici in Australasia: pathogenic changes during the first ten years. Plant Pathol 39:316–325

    Article  Google Scholar 

  • Whisson SC, Drenth A, Maclean DJ, Irwin JAG (1994) Evidence for outcrossing in Phytophthora sojae and linkage of a DNA marker to two avirulence genes. Curr Genet 27:77–82

    Article  CAS  PubMed  Google Scholar 

  • Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PR (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115–118

    Article  CAS  PubMed  Google Scholar 

  • Whittaker SL, Shattock RC, Shaw DS (1991) Inheritance of DNA contents in sexual progenies of Phytophthora infestans. Mycol Res 95:1094–1100

    Article  Google Scholar 

  • Win-Tin, Dick MW (1975) Cytology of Oomycetes. Arch Microbiol 105:283–293

  • Wuethrich B (1998) Why sex? Putting theory to the test. Science 281:1980–1982

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Copes WE, Hong CX (2014) Two novel species representing a new clade and cluster of Phytophthora. Fungal Biol 118:72–82

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Professor André Drenth for his insightful and constructive discussions and comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Guest.

Additional information

Novel pathogenic Phytophthora species are emerging as the result of the rapid evolution of introduced species, and pose an increasing biosecurity risk.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Callaghan, S., Guest, D. Globalisation, the founder effect, hybrid Phytophthora species and rapid evolution: new headaches for biosecurity. Australasian Plant Pathol. 44, 255–262 (2015). https://doi.org/10.1007/s13313-015-0348-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13313-015-0348-5

Keywords

Navigation