Role of environment and genetics in production of secondary metabolites in the invasive Australian weed Echium plantagineum L.

Dominik Skoneczny

Research output: ThesisDoctoral Thesis

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The study of plant-plant interactions and invasion is a challenging task that requires a holistic approach towards developing a critical understanding of why some plant species are successful invaders while others are not. This research studied weed invasion in light of key biosynthetic pathways in roots and shoots, and has progressed from simplistic studies previously focused on one major metabolite of interest that have not taken into account plant stress, genetics and environment simultaneously. Echium plantagineum L. (Boraginaceae) commonly known as Paterson’s curse or Salvation Jane, is an exotic and invasive weed in Australia that was introduced from the Iberian Peninsula in the 19th century. It has spread across 30 M ha in southeastern Australia and exhibits potential for further invasion. It is a toxic herb that frequently establishes as monocultures and consequently has resulted in AUD $250 M in annual losses to the Australian farming, meat and fibre industries. Echium plantagineum accumulates toxic pyrrolizidine alkaloids (PAs) in its foliage and antimicrobial and phytotoxic shikonins or naphthoquinones (NQs) in its root periderm. The chemical diversity, ecochemical function and metabolic relation between PAs and NQs has not been explored previously in light of plant invasion and plant-plant interactions. Production of bioactive secondary metabolites and population genetics are key factors contributing to plant invasion. The production of secondary metabolites in exotics can be altered as a result of escape from natural enemies, evolutionary adaptation towards increased competitive traits, or environmental pressures. A metabolic profiling platform was developed to identify and profile PAs and NQs using UHPLC/Q-ToF MS (ultra-high pressure liquid chromatography coupled to quadrupole time of flight mass spectrometry) in both positive and negative mode respectively. This platform was utilized to identify secondary metabolites and investigate the impacts of invasion on the biodiversity of ecosystems and the regulation of defence metabolism in the context of changing climate and plant stress. Methanolic foliar and ethanolic periderm and soil extracts were analysed using semi-quantitative targeted and untargeted metabolic profiling approaches. Seventeen PAs and nine NQs were identified in the foliage and root periderm, respectively. Periderm extracts contained predominantly dimethylacrylshikonin, β-hydroxyisovalerylshikonin and isovalerylshikonin while acetylshikonin was the key metabolite detected in soil samples. Shoot extracts were dominated by echimidine, echiumine and lycopsamine-N-oxides. A total of 22 Australian and 13 European geographically distinct populations were evaluated in the study. The regulation of secondary metabolite production was studied in phenological and time-course experiments in four Australian populations of E. plantagineum in controlled glasshouse conditions. These results were compared to the metabolic profiles of a non-invasive exotic congener E. vulgare. Secondary metabolites were also analysed over time in response to simulated drought, herbivory, temperature stress and intraspecific competition in controlled phytotron conditions. Additionally, key genes involved in the NQ biosynthetic pathway were identified using sequence-specific primers based on Genebank accessions from related species. Production of PAs and NQs was initiated < 24 h from germination and increased over time until flowering. Echium vulgare accumulated lower concentrations of PAs but up to three-fold higher levels of NQs than E. plantagineum. NQs were potentially acting as carbon substrates in the root periderm for future conversion to additional bioactive forms or different metabolites under environmental stressors. Upregulation of NQ biosynthesis was observed in response to imposed stress including elevated temperature, moderate drought, mechanical damage and intraspecific competition. Biosynthesis of PAs, in contrast, was less variable and frequently declined during exposure to stress possibly due to trade-offs between secondary products production and primary metabolism. The most rapid response in accumulation of secondary metabolites was observed within 6 h after simulated herbivory and 72 h after exposure to drought. Australian field populations of E. plantagineum produced up to six-fold greater concentrations of NQs and up to three-fold lower concentrations of PAs, in comparison to plants collected from native ranges. Echium plantagineum stands tended to be botanically more diverse but at a lower density in the Iberian Peninsula. Populational differences in chemistry were limited in Australian populations of E. plantagineum. A greater inter-populational diversity was noted in the endemic range. This thesis is a comprehensive and detailed report on the role of bioactive secondary plant products in plant invasion and stress response. In particular, I conclude that the success of E. plantagineum in Australia is likely a result of numerous factors including the synergistic effect of biological traits, high rates of seed production, flexible regulation of defence metabolism both above and belowground, greater levels of genetic diversity and escape from natural enemies.
Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • Charles Sturt University
  • Weston, Leslie, Principal Supervisor
  • Weston, Paul, Principal Supervisor
  • Gurr, Geoff M., Principal Supervisor, External person
Award date01 Oct 2017
Publication statusPublished - 2017


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