Phytophthora

Stephen C Whisson, Scottish Crop Research Institute, Invergowrie, Dundee, United Kingdom

Published online: April 2010

DOI: 10.1002/9780470015902.a0021265

Diseases of plants caused by species of the genus Phytophthora represent some of the most devastating diseases of crops worldwide. All known species of Phytophthora are plant pathogens. Although superficially similar to filamentous fungi, the Phytophthora species belong to the class oomycetes, and are more closely related to brown algae. Phytophthora-incited disease may be controlled by genetically encoded resistance in the host plants. In cases where no host plant resistance to Phytophthora disease is available, application of control chemicals may be successful in controlling disease, although intensive chemical control is potentially environmentally damaging. Much recent research into Phytophthora biology has utilised modern molecular biology techniques. DNA (deoxyribonucleic acid) sequencing of three Phytophthora genomes has revealed an extraordinary repertoire of genes encoding proteins secreted by Phytophthora for the purpose of overcoming and subverting host plant innate and active defence responses, indicating pathogenicity in this genus to be a highly complex process.

Key Concepts

  • Species of Phytophthora cause some of the most destructive plant diseases known.
  • Phytophthora species resemble fungi, but are phylogenetically distinct.
  • Some Phytophthora species have coevolved with their hosts, leading to a gene-for-gene system of matching plant resistance and Phytophthora avirulence gene products.
  • Some, but not all, Phytophthora diseases may be controlled by resistance in the host plant, or through the application of control chemicals.
  • Phytophthora species secrete a complex array of proteins, including effectors, during invasion of plant tissues, some of which act to suppress plant defence responses.
  • Some effectors may be recognised by host plants, leading to resistance.
  • Other effectors may be required for pathogen growth and development during infection.
  • Numerous secreted Phytophthora proteins exhibit evidence of selection pressure from their plant hosts.

Keywords: Phytophthora; oomycete; avirulence; effector; fungicide; plant pathology

Figure 1. Major lifecycle stages of Phytophthora, with Ph. infestans used as example. Asexually formed sporangia (a) are multinucleate and their cytoplasm may cleave to form motile zoospores (b). Encystment occurs next (c), followed by cyst germination and formation of the appressorium (d) for infection of the host plant. Following penetration into the host plant, intercellular hyphae are formed with occasional formation of haustoria ((e); trypan blue staining). After plant tissue is fully colonised, hyphae emerge from host surfaces to form sporangiophores bearing more sporangia ((f); trypan blue staining). The formation of sporangia is most conspicuous when it occurs as a mass of white aerial hyphae and sporangiophores (g) on aerial parts of the plant. Oospores (h) are sexually derived spores formed when opposite mating types (for heterothallic species) meet in the same diseased plant. Homothallic species form oospores continually without the requirement for presence of another mating type. Zo, zoospore; cy, cyst; gc, germinated cyst; ap, appressorium; ih, intercellular hyphae; ha, haustorium; oo, oogonium and at, antheridium. Scale bars represent 50 m (a), 20 m (b, c, f), 10 m (d), 30 m (e) and 40 m (h).
Figure 2. Examples of plant disease caused by species of Phytophthora. (a) Disease lesion caused by Ph. infestans on a potato leaf. (b) Leaf and stem infection of Rhododendron caused by Ph. kernoviae. (c) Root infection of raspberry caused by Ph. fragariae var rubi. Note stunting of infected plant at right and corresponding darkened and reduced root mass. (d) Canker (with bark removed) of Macadamia tree caused by Ph. cinnamomi. (e) ‘Bleeding’ trunk lesion of alder caused by Ph. alni. (f) Dieback of durian trees caused by Ph. palmivora. (g) Black pod disease of cocoa caused by Ph. palmivora. Images shown in (b), (c) and (e) were supplied by David Cooke, Scottish Crop Research Institute, UK. Images shown in (d), (f) and (g) were supplied by Andre Drenth, University of Queensland, Australia.
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 References
    Avrova A, Boevink P, Young V et al. (2008) A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. Cellular Microbiology 10: 2271–2284.
    Baldauf SL (2003) The deep roots of eukaryotes. Science 300: 1703–1706.
    Bhattacharjee S, Hiller NL, Liolios K et al. (2006) The malarial host targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathogens 2: e50.
    Blum M, Boehler M, Randall E et al. (2010) Mandipropamid targets the cellulose synthase-like PiCesA3 to inhibit cell wall biosynthesis in the oomycete plant pathogen, Phytophthora infestans. Molecular Plant Pathology 11: 227–243.
    book Bourke A (1991) "Potato late blight in Europe in 1845: the scientific controversy". In: Lucas JA, Shattock RC, Shaw DS and Cooke LR (eds) Phytophthora, pp. 12–24. Cambridge, UK: Cambridge University Press.
    Brasier CM, Cooke DE and Duncan JM (1999) Origin of a new Phytophthora pathogen through interspecific hybridization. Proceedings of the National Academy of Sciences of the USA 96: 5878–5883.
    Brunner F, Rosahl S, Lee J et al. (2002) Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO Journal 21: 6681–6688.
    Burki F, Shalchian-Tabrizi K, Minge M et al. (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 2: e790 doi:10.1371/journal.pone.0000790.
    Carter GA, Smith RM and Brent KJ (1981) Sensitivity to metalaxyl of Phytophthora infestans populations in potato crops in south-west England in 1980 and 1981. Annals of Applied Biology 100: 433–441.
    Chisholm ST, Coaker G, Day B and Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803–814.
    Clement D, Risterucci AM, Motamayor JC, N'Goran J and Lanaud C (2003) Mapping QTL for yield components, vigor, and resistance to Phytophthora palmivora in Theobroma cacao L. Genome 46: 204–212.
    Cooke DE, Drenth A, Duncan JM, Wagels G and Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology 30: 17–32.
    Davidse LC, Looijen D, Turkensteen LJ and van der Wal D (1981) Occurrence of metalaxyl-resistant strains of Phytophthora infestans in Dutch potato fields. The Netherlands Journal of Plant Pathology 87: 65–68.
    Dick MA, Dobbie K, Cooke DE and Brasier CM (2006) Phytophthora captiosa sp. nov. and P. fallax sp. nov. causing crown dieback of Eucalyptus in New Zealand. Mycological Research 110: 393–404.
    Dou D, Kale SD, Wang X et al. (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20: 1930–1947.
    Duncan JM (1999) Phytophthora: an abiding threat to our crops. Microbiology Today 26: 114–116.
    book Erwin DC and Ribeiro OK (1996) Phytophthora Diseases Worldwide. St. Paul, MN: APS Press.
    Fry W (2008) Phytophthora infestans: the plant (and R gene) destroyer. Molecular Plant Pathology 9: 385–402.
    Gaulin E, Dramé N, Lafitte C et al. (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18: 1766–1777.
    Grenville-Briggs LJ, Anderson VL, Fugelstad J et al. (2008) Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. Plant Cell 20: 720–738.
    Grouffaud S, van West P, Avrova A, Birch PRJ and Whisson SC (2008) Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology 154: 3743–3751.
    Guest D (2007) Black pod: diverse pathogens with a global impact on cocoa yield. Phytopathology 97: 1650–1653.
    Haas BJ, Kamoun S, Zody MC et al. (2009) Genome sequence and comparative analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393–398.
    Hardham AR (2006) Cell biology of plant-oomycete interactions. Cellular Microbiology 9: 31–39.
    Haverkort AJ, Boonekamp PM, Hutten R et al. (2008) Societal costs of late blight in potato and prospects of durable resistance through cisgenic modification. Potato Research 51: 47–57.
    Hohl HR and Suter E (1976) Host–parasite interfaces in a resistant and a susceptible cultivar of Solanum tuberosum inoculated with Phytophthora infestans: leaf tissue. Canadian Journal of Botany 54: 1956–1970.
    Hua C, Wang Y, Zheng X et al. (2008) A Phytophthora sojae G-protein alpha subunit is involved in chemotaxis to soybean isoflavones. Eukaryotic Cell 7: 2133–2140.
    Irwin JAG, Maxwell DP and Bingham ET (1981) Inheritance of resistance to Phytophthora megasperma in diploid alfalfa. Crop Science 21: 271–276.
    Jones JD and Dangl JL (2006) The plant immune system. Nature 444: 323–329.
    Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology 44: 41–60.
    de Koning-Ward TF, Gilson PR, Boddey JA et al. (2009) A newly discovered protein export machine in malaria parasites. Nature 459: 945–949.
    Lokossou AA, Park T, van Arkel G et al. (2009) Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV. Molecular Plant–Microbe Interactions 22: 630–641.
    Phillips AJ, Anderson VL, Robertson EJ, Secombes CJ and van West P (2007) New insights into animal pathogenic oomycetes. Trends in Microbiology 16: 13–19.
    Purss GS (1972) Pathogenic specialization in Phytophthora vignae. Australian Journal of Agricultural Research 23: 453–456.
    Purwantara A, Flett SP and Keane PJ (1996) Resistance of nineteen cultivars of subterranean clover to four races of Phytophthora clandestina. Euphytica 91: 351–358.
    Qi J, Asano T, Jinno M et al. (2005) Characterization of a Phytophthora mating hormone. Science 309: 1828.
    Richards TA, Dacks JB, Jenkinson JM, Thornton CR and Talbot NJ (2006) Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Current Biology 16: 1857–1864.
    Rubin A, Gotlieb D, Gisi U and Cohen Y (2008) Mutagenesis of Phytophthora infestans for resistance against carboxylic acid amide and phenylamide fungicides. Plant Disease 92: 675–683.
    Schmitthenner AF (1985) Problems and progress in control of Phytophthora root rot of soybean. Plant Disease 69: 362–368.
    Schornack S, Huitema E, Cano LM et al. (2009) Ten things to know about oomycete effectors. Molecular Plant Pathology 10: 795–803.
    book Schwinn FJ and Margot P (1991) "Control with chemicals". In: Ingram DS and Williams PH (eds) Phytophthora infestans, Cause of Late Blight of Potato. Advances in Plant Pathology, vol. 7, pp. 225–265. London, UK: Academic Press.
    Stiller JW, Huang J, Ding Q, Tian J and Goodwillie C (2009) Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses? BMC Genomics 10: 484.
    Turkensteen LJ, Flier WG, Wanningen R and Mulder A (2000) Production, survival and infectivity of oospores of Phytophthora infestans. Plant Pathology 49: 688–696.
    Tyler BM, Tripathy S, Zhang X et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261–1266.
    Van der Biezen EA and Jones JD (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends in Biochemical Science 23: 454–456.
    Vleeshouwers VGAA, Driesprong JD, Kamphuis LG et al. (2006) Agroinfection-based high-throughput screening reveals specific recognition of INF elicitins in Solanum. Molecular Plant Pathology 7: 499–510.
    van West P, Morris BM, Reid B et al. (2002) Oomycete plant pathogens use electric fields to target roots. Molecular Plant–Microbe Interactions 15: 790–798.
    Whisson SC, Boevink P, Moleleki LN et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115–118.
    Win J, Morgan W, Bos J et al. (2007) Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 19: 2349–2369.
    Wollgiehn R, Brautigam E, Schumann B and Erge D (1984) Action of metalaxyl on nucleic acid and protein syntheses in Phytophthora nicotianae. Zeitschrift fur Allgemeine Mikrobiologie 24: 269–279.
 Further Reading
    book Drenth A and Guest DI (2004) Diversity and Management of Phytophthora in Southeast Asia. Canberra, Australia: Australian Centre for International Agricultural Research (ACIAR).
    book Erwin DC, Bartnicki-Garcia S and Tsao PH (1983) Phytophthora: Its Biology, Taxonomy, Ecology and Pathology. St. Paul, MN: APS Press.
    Judelson HS and Blanco FA (2005) The spores of Phytophthora: weapons of the plant destroyer. Nature Reviews Microbiology 3: 47–58.
    book Lamour K and Kamoun S (2009) Oomycete genetics and genomics: diversity, interactions and research tools. Hoboken, NJ: Wiley-Blackwell.
    book Ribeiro OK (1978) A Source Book of the Genus Phytophthora. Liechtenstein, Vaduz: Cramer.

Related Sub-Topics:

Crops and Plant Breeding | Microbial Evolution and Taxonomy | Algae | Fungi | Plant Disease
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Article Title: Phytophthora
 
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Whisson, Stephen C(Apr 2010) Phytophthora. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021265]