Effects of rust infection with Puccinia lagenophorae on pyrrolizidine alkaloids in Senecio vulgaris
Introduction
Puccinia lagenophorae is an obligate biotrophic fungal pathogen (rust). The pathogen is of Australian origin infecting Compositae plants. It was not known in Europe until 1960, when it was found to have been introduced accidentally and observed infecting Senecio vulgaris[1]. It is now commonly observed on S. vulgaris in Europe. It is autoecious and present on S. vulgaris from early summer to autumn. The rust appears as orange pustules on the stem and leaves, the pustules initially containing orange aeciospores, followed by teliospores. These teliospores are not known to infect a secondary host in this country. P. lagenophorae infection has been observed to significantly reduce the growth[2], reproductive capacity[3]and competitive ability[4]of S. vulgaris. It can also alter S. vulgaris transpiration rates[2]and chemistry5, 6.
S. vulgaris can be a problematic weed (e.g., in fruit orchards). Investigations are now looking into the possibility of biologically controlling the weed using P. lagenophorae[7].
Pyrrolizidine alkaloids (PAs) are the most characteristic secondary compounds produced by S. vulgaris[8]. They are exclusively synthesised in roots, translocated into shoots via the phloem path and allocated to the preferred sites of storage such as the flower heads and peripheral cell layers of stems and leaves, where they are stored in the cell vacuoles9, 10, 11. PAs are synthesised, translocated and stored in the form of their polar salt-like N-oxides. The function of PAs as powerful components of plant chemical defence against herbivores is well documented. PAs are strong feeding deterrents and most of them (i.e., 1,2-dehydropyrrolizidines) are easily bioactivated after ingestion by vertebrates by liver P-450 oxidases into reactive pyrroles which may cause cell damage and even initiate cancer12, 13, 14. The importance of PAs in chemical defence is most impressively shown by insect species of various unrelated taxa (e.g., Lepidoptera, Orthoptera, Coleoptera and Homoptera) which sequester plant derived PAs for their own benefit14, 15, 16, 17.
In contrast to the well documented function of PAs in plant chemical defence against herbivory and even more convincing as plant-acquired defence compounds in adapted insects against predators, their role in plant–pathogen interactions is still obscure. There are only few reports claiming antimicrobial activity of PAs. In these cases, however, only very weak antibacterial[11]or antifungal activities18, 19, 20were found in simple agar diffusion assays (i.e., EC50>0.5 mg ml−1). Due to these very low responses a significant role of PAs in plant–microbial defence remains doubtful. However, it is now clear that changes in host plant chemistry induced by pathogen infection can have significant effects on herbivores21, 22, 23, although pathogen effects on PAs have not been studied. Given the key role of PAs in anti-herbivore defences of S. vulgaris, we measured the effects of infection by P. lagenophorae on the total contents, tissue concentrations and structural compositions of PAs in the host.
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Results and discussion
At harvest the infected plants had a severe pathogen infection (with most leaves showing rust pustules). The older infected leaves had curled and deformed as a result of the presence of rust pustules. Some capitula were also covered in pustules, and in some cases the flowers appeared to be deformed. The vegetative shoot tissues (leaves plus stems) of infected plants appeared smaller in size than the uninfected plants, although their dry weights were not significantly different (Table 1). The
Plant material
Senecio vulgaris was grown from a seed of a single genotype (initially collected from the grounds of Lancaster University, GR: SD 4857) in John Innes Number 2 soil based compost (Keith Singleton, Egremont, UK). Seeds were germinated in trays and when the first leaf was visible, plants were potted on into 9 cm diameter pots. All plants were grown in a controlled environment (CE) room, with a 16 hr photoperiod and photosynthetically active radiation (PAR) of 500 μ mol m−2 sec−1 at bench height from 400
Acknowledgements
This study was supported by grants from the Deutsche Forschungsgemeinschaft and Fonds der Chemischen Industrie to T. Hartmann. G. Tinney's work in the U.K. was funded by a NERC studentship. We are grateful to D. Pennington and H. Williams for technical assistance.
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