Breakthrough with the Californian Thistle Rust
For over a century the fungal rust pathogen, Puccinia punctiformis, of Californian thistle (Cirsium arvense) has been considered a promising biocontrol agent, but utilising this pathogen effectively has been hampered by an incomplete understanding of the disease cycle.
The rust is highly host specific, infecting only Californian thistle, and is present everywhere in the world where the thistle occurs, including New Zealand. The rust disease occurs in two forms, localised and systemic. Localised infections have minimal impact on the weed, whereas systemic infection results in severely distorted growth and eventual death of the shoot. Understanding the natural disease cycle of the fungus, particularly how systemic infection is initiated, is key to manipulating it for greater effect.
Recently an important breakthrough with this pathogen has been achieved through an international collaboration of scientists led by Dr Dana Berner (USDA, Maryland) and including AgResearch. Field experiments conducted in the United States, Russia, Greece and New Zealand, following the same simple protocol, have routinely generated systemic rust disease in populations of Californian thistle. “We believe this is a step in the right direction towards a greater understanding of the fungus, and therefore our ability to utilise it for biocontrol purposes,” explained Mike Cripps of AgResearch.
But before we get to the breakthrough here is a brief overview of the history of research, successes and setbacks that have brought us to this point. The life cycle of the rust is complex, involving all five possible spore types (spermatia, aeciospores, urediniospores, teliospores and basidiospores). The questions concerning the life cycle of this fungus that have persisted for decades are: which spore type causes systemic infection, and how and when does it encounter the host plant at a susceptible growth stage?
The teliospore stage of the fungus was always the likely candidate for causing systemic disease, but during early research in the 1950s the difficulties encountered in getting teliospores to germinate led some researchers to believe that that this spore type could not account for the amount of systemic disease observed in the field. They postulated that urediniospores might be responsible, but this explanation was unsatisfactory since it would have required an atypical genetic process. By the 1990s it had been discovered that stimulants from the host plant were required for teliospores to germinate. This explanation conformed to the known processes of rust spore development, and was generally accepted. However, the question of how and when the teliospores encountered a susceptible infection site on the plant still remained. The working hypothesis was that teliospores were dispersed on the soil surface and contacted adventitious shoot buds emerging from the roots of the thistle plant. However, the movement of teliospores through the soil and the haphazard contact with root buds was unlikely, and other explanations were sought. An idea that captured some attention was that stem-mining weevils (like Ceratapion onopordi) might vector the pathogen and inoculate the plant via egg deposition in the thistle shoot. To further muddle the story, the proponents of the weevil vector hypothesis also reinvoked urediniospores as the causal spore type of systemic infection, since these are the most common type encountered by the weevils in spring. But the importance of insect vectors in the disease cycle was called into question after surveys carried out in Europe and New Zealand showed equivalent frequencies of rust disease in both regions, with and without stem-mining weevils, respectively.
So the focus went back onto teliospores again. Teliospores are produced in summer, corresponding with the death of diseased shoots. In autumn there is always a flush of new thistle rosettes emerging after the summer growth has senesced. “We believed it was likely that debris bearing teliospores from old shoots landed on the autumn cohort of thistle shoots,” explained Mike. Infection could then take place with the fungus overwintering in the roots, followed by the expression of systemic disease appearing in spring. To test this hypothesis, researchers gathered diseased shoots in summer and inoculated rosettes in autumn with debris bearing teliospores.
In New Zealand, the autumn inoculations of rosettes resulted in systemic disease appearing in approximately 50% of the treated plots compared with 15% ambient disease in control plots. This result was highly significant, and similar successes were achieved at the other field trials around the world. This combined international study will be reported in a scientific journal later this year. “The study in New Zealand is ongoing and we will continue to monitor disease progress, and changes in the thistle population densities,” said Mike. There is still much to learn about the interactions of this pathogen with its host plant, but now we at least have a simple method of initiating systemic disease that we can build upon to improve the biological control of this important weed.