Recent CO2 levels promote increased production of the toxin parthenin in an invasive Parthenium hysterophorus biotype

Authors: Rice, Clifford; Wolf, Julie; Fleisher, David; Acosta, Savannah; BAJWA, ALI - University Of New South Wales; ADKINS, STEVE - University Of Queensland; ZISKA, LEWIS - Columbia University - New York

Submitted to: Nature Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/4/2021
Publication Date: 7/6/2021
Citation: Rice, C., Wolf, J.E., Fleisher, D.H., Acosta, S.M., Bajwa, A.A., Adkins, S.W., Ziska, L.H. 2021. Recent CO2 levels promote increased production of the toxin parthenin in an invasive Parthenium hysterophorus biotype. Nature Plants. 1-5. https://doi.org/10.1038/s41477-021-00938-6.
DOI: https://doi.org/10.1038/s41477-021-00938-6

Interpretive Summary: Atmospheric levels of carbon dioxide (CO2) increased by 45% over the last 200 years. Because CO2 is the substrate for photosynthesis, these higher levels often lead to increased quantities of plant carbon relative to plant mineral nutrients like nitrogen and phosphorus. Such an imbalance can change how plants allocate carbon among their various chemical components; for example, increased production of some carbon-based components that do not require any mineral atoms has been observed. A weed from the American tropics and subtropics, called Parthenium hysterophorus, has become a globally important invasive species, highly destructive particularly in disturbed ecosystems including cropland and pasture. This plant produces several carbon-based chemicals that act as plant defenses: by allelopathy (inhibiting seed germination and/or seedling growth of competing plants), and/or by toxicity to animals (severe asthma and contact dermatitis in humans, undigestible/unpalatable/toxic to grazing livestock). Two distinct types of this weed have been established in Australia; one is highly invasive and the other is not. Because this plants chemical defenses are carbon-based, we investigated whether recent increases in CO2 was associated with higher concentrations of a particularly noxious defense molecule, parthenin. This compound is a terpene, a class of aromatic, volatile plant compounds that often play a role in plant defenses. We grew the invasive and noninvasive types of P. hysterophorus from seed in growth chambers that could provide appropriate light and temperature for plant growth, at either pre-industrial or modern high levels of CO2, corresponding to 300 and 400 parts per million CO2, respectively. In plants harvested at the onset of flowering, we found that the invasive type plants were larger, and had twice the concentration of parthenin, than the noninvasive type. The invasive type plants grown at 400 ppm had 64% higher concentrations of parthenin than those grown at 300 ppm CO2. In contrast, the concentration of parthenin in noninvasive type plants did not increase at the higher CO2 levels. Our finding of higher levels of toxic parthenin in the invasive type of P. hysterophorus suggests that current levels of atmospheric CO2 are already contributing to changes in plant chemistry and ecology, and leading to decline in habitability in these areas. This information will be useful to scientists working with invasive plant species.

Technical Abstract: Atmospheric levels of carbon dioxide (CO2) have increased by 45% over the last 200 years. Elevated CO2 often increases plant carbon relative to mineral nutrients, and increased production of carbon-based metabolites has been observed. The neotropical Asteraceae Parthenium hysterophorus, a globally important invasive weed, produces several sesquiterpene lactones harmful to plants, microbes, and/or animals. Two biotypes of this weed, one highly invasive, the other non-invasive, have been introduced in Australia. We hypothesized that current CO2 contributes to the invasive biotype's success via increasing production of the defense molecule parthenin. We grew both biotypes from seed at pre-industrial (300 ppm) and modern (400 ppm) CO2 concentrations in growth chambers, and quantified parthenin at the onset of flowering using ultra performance liquid chromatography mass spectrometry. The invasive produced larger shoot biomass and higher parthenin concentration than the non-invasive biotype. At 400 ppm CO2, invasive shoot biomass was 76% larger relative to 300 ppm; while noninvasive was 57% larger. At 400 ppm CO2, invasive parthenin concentration was 64% higher relative to 300 ppm but was unchanged in the non-invasive biotype. These results suggest that current increases in atmospheric CO2 are altering the chemistry and ecology of this highly invasive weed.