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Simulated herbivory enhances Cd phytoextraction efficiency of sunflowers

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Abstract

Background

Metal hyperaccumulators are plant species that can uptake and store high concentrations of heavy metals in their aboveground tissues, while maintaining high vigor. Hyperaccumulation of metals was suggested to provide defense against natural enemies such as herbivores. However, heavy-metal uptake can incur physiological and ecological costs, suggesting that, like other anti-herbivore defenses, it might be induced by herbivore attack. Nevertheless, this idea has been scarcely studied.

Methods

We tested the hypothesis that herbivory could induce enhanced metal uptake in Helianthus annuus, which can accumulate high amounts of heavy metals in its aboveground tissues and is commonly used for phytoremediation of heavy-metal contaminated soils. In a greenhouse experiment, H. annuus plants were grown in low or high soil cadmium (Cd) concentration and subjected to control or herbivory treatments. Herbivory was simulated using both leaf damage and exogenous application of jasmonic acid, which activates anti-herbivore defenses in plants.

Results

Simulated herbivory increased Cd concentration in the leaves of H. annuus by 24 and 39% under low and high soil Cd availability, respectively. Moreover, while simulated herbivory decreased shoot biomass of H. annuus it resulted in increased total Cd uptake. These results demonstrate that hyperaccumulation of heavy metals might be a facultative trait, whose extent can be enhanced in response to herbivore damage.

Conclusions

This study provides first evidence that simulated herbivory can enhance total heavy metal uptake in plants that are used for remediation of contaminated soils, which can have important implications on the optimization of phytoremediation practices.

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Data availability

The data generated during the current study are available as Supplementary Information.

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Acknowledgements

We are grateful to Ruth Gottlieb, Inbal Eilon-First, Golan Zimmerman, and Snir Weintrob for their assistance with logistics and experimental setup, and to Zhanna Kats, Karina Gitin Heskiau, Ran Tal and Aviv Kaplan for their help with preparations and sample analysis. We would also like to thank the Laboratory of Environmental Bioengineering, the Hydrochemistry Laboratory and the Shenkar Laboratory at Tel Aviv University for allowing us to use their facilities. We are thankful to Yarok Organic Nursery for supplying us with sunflower seedlings.

Funding

This study was supported by a grant of the Israeli Science Foundation (ISF) to MG (grant 2904/19) and a fellowship of the Smaller-Winnikow Fund for Environmental Research to EG.

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Authors and Affiliations

  1. Porter School of the Environment and Earth Sciences, Tel Aviv University, Tel Aviv, Israel

    Eyal Grossman & Michal Gruntman

  2. School of Plant Sciences and Food Security, Tel Aviv University, Tel Aviv, Israel

    Michal Gruntman

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  1. Eyal Grossman
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  2. Michal Gruntman
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Contributions

EG and MG conceived the project and designed the experiment; EG performed the experiment and collected and analyzed the data; EG and MG wrote the manuscript.

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Correspondence to Michal Gruntman.

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Grossman, E., Gruntman, M. Simulated herbivory enhances Cd phytoextraction efficiency of sunflowers. Plant Soil 481, 385–394 (2022). https://doi.org/10.1007/s11104-022-05643-7

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