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Persistence of Phytophthora cinnamomi in nature: Biotrophic growth and presence of stromata, oospores and chlamydospores in annual and herbaceous perennial plant species

Crone, Michael (2012) Persistence of Phytophthora cinnamomi in nature: Biotrophic growth and presence of stromata, oospores and chlamydospores in annual and herbaceous perennial plant species. PhD thesis, Murdoch University.

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Phytophthora cinnamomi is a broad host range pathogen responsible for the degradation of many natural and cultivated ecosystems worldwide. For most biomes, numerous woody plant species are susceptible hosts and are killed after infection. Two unresolved phenomena with regards to the life-cycle of P. cinnamomi were addressed in this study. Firstly, an investigation was conducted to determine how this poorly saprophytic pathogen persists in the long-term in the absence of susceptible hosts. Secondly, it is not known how P. cinnamomi survives the long hot and dry summers of Mediterranean environments. Infested black gravel landscapes within the Eucalyptus marginata (jarrah) forest of South-West Western Australia were suitable areas to address both knowledge gaps.

Native annual and herbaceous perennial plant species common to severely infested black gravel sites were screened as possible hosts by controlled inoculation experiments and by sampling plants from the natural environment. Secondly, it was tested how long P. cinnamomi can survive on naturally infested black gravel sites in the absence of any living plant material. Vegetation was removed by herbicides, and pathogen survival monitored over 28 months.

Based on the sampling of plants from the natural environment and from controlled inoculation experiments, it was evident that the majority of annual and herbaceous perennial plant species screened were infected by P. cinnamomi but most were asymptomatic hosts. These species are clearly a reason why P. cinnamomi can survive indefinitely on infested sites in the absence of susceptible woody host species. Transmission electron microscopic examination demonstrated that haustoria were produced in some annual and herbaceous perennial species and indicated for the first time that P. cinnamomi can colonise plants as a biotroph, without becoming necrotrophic. This is the first time haustoria have been shown to be definitively produced by P. cinnamomi in continuously asymptomatic plants. Survival propagules, in the form of oospores, thick-walled chlamydospores and stromata were also observed in these naturally infected species. Mating tests showed that the oospores were selfed by the A2 mating type, and were produced in abundance with as many as 400 mm2 of plant tissue. Selfed oospores have not been observed previously in naturally infected plants. Thick-walled chlamydospores were also produced in abundance, and both propagules types were shown to survive the environmentally adverse summer months and germinate when conditions were conducive the following autumn. Finally, stromata were observed in the majority of asymptomatic hosts, and have never been observed previously for P. cinnamomi. These stromata were shown to provide the nutrients for the prolific oospores numbers observed.

28 months after vegetation was killed by the herbicide treatments no P. cinnamomi was recovered from the soil, indicating that the pathogen can be eradicated from a site, when no living host material is present.

This study has made major and significant contributions to our understanding of the life cycle of P. cinnamomi under natural conditions. The ability of the pathogen to grow as a necrotroph or endophytic biotroph indicates that the pathogen has evolved a range of growth modes allowing it to persist in an ecosystem regardless of whether susceptible hosts are present or not. It is likely, that similar studies in other natural ecosystems in Australia or elsewhere will provide similar results. The ability to eradicate the pathogen in a relatively short time period through the removal of host material provides many opportunities for the control of this pathogen in managed and natural ecosystems.

Item Type: Thesis (PhD)
Murdoch Affiliation(s): School of Biological Sciences and Biotechnology
Supervisor(s): Hardy, Giles, McComb, Jen and O'Brien, Philip
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