Abstract
Species of Phytophthora cause serious soilborne diseases of important crop plants and threaten natural ecosystems on a vast scale. Successful infection is usually initiated by motile, biflagellate zoospores that are chemotactically attracted to nearby roots. The zoospores home in at sites on the root surface that are favourable for subsequent penetration. There they encyst, secreting adhesive that glues them to the root surface. The germ tube that emerges from the cysts penetrates the root epidermis, usually growing intercellularly along the anticlinal cell walls. Intracellular growth also occurs and haustoria can develop in cortical cells. Within 2–3 days, the pathogen sporulates with the production of chlamydospores in cortical cells and multinucleate sporangia on the root surface. The sporangia undergo cytokinesis and release motile zoospores into the soil. A number of features of the infection cycle contribute to the rapid dissemination of infective propagules and successful disease establishment by Phytophthora pathogens. While basic aspects of the infection cycle were described 30–40 years ago, in the last decade immunocytochemical studies have helped uncover new details of cellular and molecular mechanisms involved in processes such as zoospore osmoregulation, motility and adhesion, and asexual sporulation. The increase in our understanding of Phytophthora pathogenesis that has resulted has already pointed to potential targets for novel inhibitors of Phytophthora diseases. Further investigations of the cell and molecular biology of Phytophthora pathogenicity promise to be an integral part of our development of highly specific and sustainable control measures in the future.
Similar content being viewed by others
References
Benhamou N, Coté F (1992) UItrastructure and cytochemistry of pectin and cellulose degradation in tobacco roots infected by Phytophthora parasitica var. nicotianae. Phytopathology 82, 468–478.
Bircher U, Hohl HR (1997) Environmental signalling during induction of appressorium formation in Phytophthora. Mycological Research 101, 395–402.
Cahill DM (1999) Detection, identification and disease diagnosis of soilborne pathogens. Australasian Plant Pathology 28, 34–44.
Cahill DM, Cope M, Hardham AR (1996) Thrust reversal by tubular mastigonemes: immunological evidence for a role of mastigonemes in forward motion of zoospores of Phytophthora cinnamomi. Protoplasma 194, 18–28.
Cahill DM, Hardham AR (1994a) A dipstick immunoassay for the specific detection of Phytophthora cinnamomi in soils. Phytopathology 84, 1284–1292.
Cahill DM, Hardham AR (1994b). Exploitation of zoospore taxis in the development of a novel dipstick immunoassay for the specific detection of Phytophthora cinnamomi. Phytopathology 84, 193–200.
Cahill DM, Legge N, Grant B, Weste G (1989) Cellular and histological changes induced by Phytophthora cinnamomi in a group of plant species ranging from fully susceptible to fully resistant. Phytopathology 79, 417–424.
Carlile MJ (1983) Motility, taxis, and tropism in Phytophthora. In ‘Phytophthora. Its biology, taxonomy, ecology, and pathology’. (Eds DC Erwin, S Bartnicki-Garcia and P Tsao) pp. 95–07. (American Phytopathological Society: St Paul)
Cho CW, Fuller MS (1989) Observations of the water expulsion vacuole of Phytophthora palmivora. Protoplasma 149, 47–55.
Coffey MD, Gees R (1991) The cytology of development. In ‘Advances in plant pathology Volume 7 Phytophthora infestans, the cause of late blight of potato’. (Eds DS Ingram and PH Williams) pp. 31–51. (Academic Press: London)
Coffey MD, Wilson UE (1983) An ultrastructural study of the lateblight fungus Phytophthora infestans and its interaction with the foliage of two potato cultivars possessing different levels of general (field) resistance. Canadian Journal of Botany 61, 2669–2685.
Cordier C, Gianinazzi S, Gianinazzi-Pearson V (1996) Colonisation patterns of root tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant and Soil 185, 223–232.
Crawford AR, Bassam BJ, Drenth A, Maclean DJ, Irwin JAG (1996) Evolutionary relationships among Phytophthora species deduced from rDNA sequence analysis. Mycological Research 100, 437–443.
Davidse LC (1986) Benzimidazole fungicides: mechanism of action and biological impact. Annual Review of Phytopathology 24, 43–65.
Dearnaley JDW, Hardham AR (1994) The Golgi apparatus of Phytophthora cinnamomi makes three types of secretory or storage vesicles concurrently. Protoplasma 182, 75–79.
Duniway JM (1976) Movement of zoospores of Phytophthora cryptogea in soils of various textures and matric potentials. Phytopathology 66, 877–882.
Duniway JM (1983) Role of physical factors in the development of Phytophthora diseases. In ‘Phytophthora. Its biology, taxonomy, ecology, and pathology’. (Eds DC Erwin, S Bartnicki-Garcia and P Tsao) pp. 175–187. (American Phytopathological Society: St Paul)
Ehrlich MA, Ehrlich HG (1966) Ultrastructure of the hyphae and haustoria of Phytophthora infestans and hyphae of P. parasitica. Canadian Journal of Botany 44, 1495–1508.
Emmett RW, Parbery DG (1975) Appressoria. Annual Review of Phytopathology 13, 147–163.
Enkerli K, Hahn MG, Mims CW (1997) Ultrastructure of compatible and incompatible interactions of soybean roots infected with the plant pathogenic oomycete Phytophthora sojae. Canadian Journal of Botany 75, 1493–1508.
Erwin DC, Ribeiro OK (1996) ‘Phytophthora diseases worldwide.’ (APS Press: St. Paul)
Fok AK, Aihara MS, Ishida M, Nolta KV, Steck TL, Allen RD (1995) The pegs on the decorated tubules of the contractile vacuole complex of Paramecium are proton pumps. Journal of Cell Science 108, 3163–3170.
Gautam Y, Cahill DM, Hardham AR (1999) Development of a quantitative immunodipstick assay for Phytophthora nicotianae. Food and Agricultural Immunology 11, 229–242.
Gees R, Hohl HR (1988) Cytological comparison of specific (R3) and general resistance to late blight in potato leaf tissue. Phytopathology 78, 350–357.
Gubler F, Hardham AR, Duniec J (1989) Characterising adhesiveness of Phytophthora cinnamomi zoospores during encystment. Protoplasma 149, 24–30.
Gunderson JH, Elwood H, Ingold A, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. Proceedings of the National Academy of Sciences of the United States of America 84, 5823–5827.
Hanchey P, Wheeler H (1971) Pathological changes in ultrastructure: tobacco roots infected with Phytophthora parasitica var. nicotianae. Phytopathology 61, 33–39.
Hardham AR (2001) Cell biology of fungal infection of plants. In ‘The Mycota Vol. VIII: Biology of the fungal cell’. (Eds RJ. Howard and NAR Gow.) (Springer-Verlag: Heidelberg) (In press)
Hardham AR, Gubler F (1990) Polarity of attachment of zoospores of a root pathogen and pre-alignment of the emerging germ tube. Cell Biology International Reports 14, 947–956.
Hardham AR, Mitchell HJ (1998) Use of molecular cytology to study the structure and biology of phytopathogenic and mycorrhizal fungi. Fungal Genetics and Biology 24, 252–284.
Hinch JM, Wetherbee R, Mallett JE, Clarke AE (1985) Response of Zea mays roots to infection with Phytophthora cinnamomi I. The epidermal layer. Protoplasma 126, 178–187.
Ho HH, Zentmyer GA (1977) Infection of avocado and other species of Persea by Phytophthora cinnamomi. Phytopathology 67, 1085–1089.
Hoch HC, Staples RC (1991) Signaling for infection structure formation in fungi. In ‘The fungal spore and disease initiation in plants and animals’. (Eds GT Cole and HC Hoch) pp. 25–46. (Plenum Press: New York)
Hoch HC, Staples RC, Whitehead B, Comeau J, Wolf ED (1987) Signaling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235, 1659–1662.
Hohl HR, Stössel P (1976) Host-parasite interfaces in a resistant and a susceptible cultivar of Solanum tuberosum inoculated with Phytophthora infestans: tuber tissue. Canadian Journal of Botany 54, 900–912.
Hohl HR, 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.
Howard RJ (1997) Breaching the outer barriers—cuticle and cell wall penetration. In ‘The Mycota V Part A Plant relationships’. (Eds G Carroll and P Tudzynski) pp. 43–60. (Springer-Verlag: Berlin)
Hyde GJ, Hardham AR (1992) Confocal microscopy of microtubule arrays in cryosectioned sporangia of Phytophthora cinnamomi. Experimental Mycology 16, 207–218.
Hyde GJ, Hardham AR (1993) Microtubules regulate the generation of polarity in zoospores of Phytophthora cinnamomi. European Journal of Cell Biology 62, 75–85.
Hyde GJ, Lancelle S, Hepler PK, Hardham AR (1991) Freeze substitution reveals a new model for sporangial cleavage in Phytophthora, a result with implications for cytokinesis in other eukaryotes. Journal of Cell Science 100, 735–746.
Jahn TL, Landman MD, Fonseca JR (1964) The mechanism of locomotion of flagellates. II. Function of the mastigonemes of Ochromonas. Journal of Protozoology 11, 291–296.
Jahnen W, Hahlbrock K (1988) Cellular localization of nonhost resistance reactions of parsley (Petroselinum crispum) to fungal infection. Planta 173, 197–204.
Kováts K, Binder A, Hohl HR (1991) Cytology of induced systemic resistance of tomato to Phytophthora infestans. Planta 183, 491–496.
Malajczuk N, McComb AJ, Parker CA (1977). Infection by Phytophthora cinnamomi Rands of roots of Eucalyptus calophylla R.Br. and Eucalyptus marginata Donn. ex Sm. Australian Journal of Botany 25, 483–500.
Margulis L, Schwartz KV (1988) ‘Five kingdoms. An illustrated guide to the phyla of life on Earth.’ (W.H. Freeman and Company: New York)
Marks GC, Mitchell JE (1971) Penetration and infection of alfalfa roots by Phytophthora megasperma and the pathological anatomy of infected roots. Canadian Journal of Botany 49, 63–67.
Marshall JS, Ashton AR, Govers F, Hardham AR. (2001a) Isolation and characterization of four genes encoding pyruvate, phosphate dikinase in the oomycete plant pathogen Phytophthora cinnamomi. Current Genetics (in press)
Marshall JS, Wilkinson JM, Moore T, Hardham AR (2001b) Structure and expression of the genes encoding proteins resident in large peripheral vesicles of Phytophthora cinnamomi zoospores. Protoplasma 215, 226–239.
Miller CR, Dowler WM, Petersen DH, Ashworth RP (1966) Observations on the mode of infection of Pythium ultimum and Phytophthora cactorum on young roots of peach. Phytopathology 56, 46–49.
Miller SA, Maxwell DP (1984) Light microscope observations of susceptible, host resistant, and nonhost resistant interactions of alfalfa with Phytophthora megasperma. Canadian Journal of Botany 62, 109–116.
Mitchell HJ, Hardham AR (1999) Characterisation of the water expulsion vacuole in Phytophthora nicotianae zoospores. Protoplasma 206, 118–130.
Mitchell RT, Deacon JW (1986) Chemotropism of germ-tubes from zoospore cysts of Pythium spp. Transactions of the British Mycological Society 86, 233–237.
Morris PF, Bone E, Tyler BM (1998) Chemotropic and contact responses of Phytophthora sojae hyphae to soybean isoflavonoids and artificial substrates. Plant Physiology 117, 1171–1178.
Morris PF, Ward EWB (1992) Chemoattraction of zoospores of the soybean pathogen, Phytophthora sojae, by isoflavones. Physiological and Molecular Plant Pathology 40, 17–22.
Paktitis S, Grant B, Lawrie A (1986) Surface changes in Phytophthora palmivora zoospores following induced differentiation. Protoplasma 135, 119–129.
Patterson DJ (1980) Contractile vacuoles and associated structures: their organization and function. Biological Review 55, 1–46.
Podger FD (1972) Phytophthora cinnamomi, a cause of lethal disease in indigenous plant communities in Western Australia. Phytopathology 62, 972–981.
Podger FD, Doepel RF, Zentmyer GA (1965) Association of Phytophthora cinnamomi with a disease of Eucalyptus marginata forest in Western Australia. Plant Disease Reports 49, 943–947.
Robold AV, Hardham AR (1998) Production of species-specific monoclonal antibodies that react with surface components on zoospores and cysts of Phytophthora nicotianae. Canadian Journal of Microbiology 44, 1161–1170.
Shimony C, Friend J (1975) Ultrastructure of the interaction between Phytophthora infestans and leaves of two cultivars of potato (Solanum tuberosum L.) Orion and Majestic. New Phytologist 74, 59–65.
Stössel P, Lazarovits G, Ward EWB (1980) Penetration and growth of compatible and incompatible races of Phytophthora megasperma var. sojae in soybean hypocotyl tissues differing in age. Canadian Journal of Botany 58, 2594–2601.
Temesvari LA, Rodriguez-Paris JM, Bush JM, Zhang L, Cardelli JA (1996) Involvement of the vacuolar proton-translocating ATPase in multiple steps of the endo-lysosomal system and in the contractile vacuole system of Dictyostelium discoideum. Journal of Cell Science 109, 1479–1495.
Tippett JT, Holland AA, Marks GC, O’Brien TP (1976) Penetration of Phytophthora cinnamomi into disease tolerant and susceptible eucalypts. Archives of Microbiology 108, 231–242.
Tippett J, Malajczuk N (1979) Interaction of Phytophthora cinnamomi and a resistant host, Acacia pulchella. Phytopathology 69, 764–772.
Waterhouse GM, Newhook FJ, Stamps DJ (1983) Present criteria for classification of Phytophthora. In ‘Phytophthora. Its biology, taxonomy, ecology, and pathology’. (Eds DC Erwin, S Bartnicki-Garcia and P Tsao) pp. 139–147. (American Phytopathological Society: St Paul)
Weerakoon ND, Roberts JK, Lehnen LP, Wilkinson JM, Marshall JS, Hardham AR (1998) Isolation and characterization of the single β-tubulin gene in Phytophthora cinnamomi. Mycologia 90, 85–95.
Widmer TL, Graham JH, Mitchell DJ (1998) Histological comparison of fibrous root infection of disease-tolerant and susceptible citrus hosts by Phytophthora nicotianae and P. palmivora. Phytopathology 88, 389–395.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hardham, A.R. The cell biology behind Phytophthora pathogenicity. Australasian Plant Pathology 30, 91–98 (2001). https://doi.org/10.1071/AP01006
Issue Date:
DOI: https://doi.org/10.1071/AP01006