Final Report Summary - DANDELION (Taraxacum officinale as a new plant-herbivore model to study fitness benefits of root secondary metabolites)
Publishable Summary
Plants invest much energy into synthesizing root secondary metabolites, many of which are assumed to improve plant fitness by protecting the plant against below ground herbivores. Testing this paradigm however has remained difficult due to the lack of suitable model plants. The key objective of DANDELION was the establishment of the common dandelion (Taraxacum officinale) as a powerful native chemo-molecular root-herbivore model to study the function and adaptive value of root secondary metabolites in nature.
To achieve this objective, we analyzed the chemical composition of dandelion latex, including the identification and quantification of major secondary metabolites. We then profiled these metabolites in a panel of dandelion genotypes and correlated their abundance with herbivore resistance and the evolutionary history of the different genotypes. Furthermore, we analyzed the latex and root transcriptome of one genotype to identify gene candidates that may be involved in the biosynthesis of the putative resistance factors.
We were able to document that dandelion produces three major classes of secondary metabolites: Sesquiterpene lactones (mainly taraxinic acid glucoside, TA-G), triterpene acetates and phenolic inositol esters. Correlative approaches showed that the abundance of TA-G is negatively associated with herbivore growth and positively associated with plant reproductive output under root herbivore attack. Furthermore, genotypes from regions that were under high pressure from the major dandelion root herbivore Melolontha melolontha produced higher levels of TA-G than genotypes from regions under low herbivore pressure. This trait was shown to be partially heritable. Transcriptome sequencing and homology analysis led to the identification of two germacrene A synthase homologues, one of which was highly expressed in the latex. This gene, called ToGAS1, was silenced through RNAi. This approach allowed us to document that ToGAS1 is required for TA-G biosynthesis and that plants that are silenced in ToGAS1 are more attractive for M. melolontha. Taken together, these experiments show that TA-G acts as a key metabolite that protects dandelions against root herbivores, improves plant performance and is under positive selection by M. melolontha.
The results of DANDELION advance our fundamental understanding of the role of root secondary metabolites as defenses against root herbivores. Our work illustrates how dandelion plants resist a major root-feeding enemy by producing high concentrations of repellent toxins in their root latex. This work is relevant for current efforts to use dandelion in agriculture, as it identifies a major resistance factor of the plant that will need to be maintained during breeding and selection to preserve the plant’s capacity to withstand root pests. It furthermore illustrates how root secondary metabolites may be used to repell root pests. As M. melolontha can be a major pest in orchards, our work can serve as a basis to develop approaches which may protect sensitive plants, for instance through appropriate companion cropping. Finally, this work may help to improve the public perception of plants as fascinating organisms by illustrating a defense strategy of dandelion as an iconic grassland species of Europe.
Matthias Erb, Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland, matthias.erb@ips.unibe.ch
http://www.ips.unibe.ch/research/interactions/
Plants invest much energy into synthesizing root secondary metabolites, many of which are assumed to improve plant fitness by protecting the plant against below ground herbivores. Testing this paradigm however has remained difficult due to the lack of suitable model plants. The key objective of DANDELION was the establishment of the common dandelion (Taraxacum officinale) as a powerful native chemo-molecular root-herbivore model to study the function and adaptive value of root secondary metabolites in nature.
To achieve this objective, we analyzed the chemical composition of dandelion latex, including the identification and quantification of major secondary metabolites. We then profiled these metabolites in a panel of dandelion genotypes and correlated their abundance with herbivore resistance and the evolutionary history of the different genotypes. Furthermore, we analyzed the latex and root transcriptome of one genotype to identify gene candidates that may be involved in the biosynthesis of the putative resistance factors.
We were able to document that dandelion produces three major classes of secondary metabolites: Sesquiterpene lactones (mainly taraxinic acid glucoside, TA-G), triterpene acetates and phenolic inositol esters. Correlative approaches showed that the abundance of TA-G is negatively associated with herbivore growth and positively associated with plant reproductive output under root herbivore attack. Furthermore, genotypes from regions that were under high pressure from the major dandelion root herbivore Melolontha melolontha produced higher levels of TA-G than genotypes from regions under low herbivore pressure. This trait was shown to be partially heritable. Transcriptome sequencing and homology analysis led to the identification of two germacrene A synthase homologues, one of which was highly expressed in the latex. This gene, called ToGAS1, was silenced through RNAi. This approach allowed us to document that ToGAS1 is required for TA-G biosynthesis and that plants that are silenced in ToGAS1 are more attractive for M. melolontha. Taken together, these experiments show that TA-G acts as a key metabolite that protects dandelions against root herbivores, improves plant performance and is under positive selection by M. melolontha.
The results of DANDELION advance our fundamental understanding of the role of root secondary metabolites as defenses against root herbivores. Our work illustrates how dandelion plants resist a major root-feeding enemy by producing high concentrations of repellent toxins in their root latex. This work is relevant for current efforts to use dandelion in agriculture, as it identifies a major resistance factor of the plant that will need to be maintained during breeding and selection to preserve the plant’s capacity to withstand root pests. It furthermore illustrates how root secondary metabolites may be used to repell root pests. As M. melolontha can be a major pest in orchards, our work can serve as a basis to develop approaches which may protect sensitive plants, for instance through appropriate companion cropping. Finally, this work may help to improve the public perception of plants as fascinating organisms by illustrating a defense strategy of dandelion as an iconic grassland species of Europe.
Matthias Erb, Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland, matthias.erb@ips.unibe.ch
http://www.ips.unibe.ch/research/interactions/