in

From the ground up: Belowground herbivory and phytoplasma infection influence aboveground herbivore performance


Abstract

In cranberry (Vaccinium macrocarpon), phytoplasma infection increases plant susceptibility to herbivores; however, its role in shaping interactions between belowground and aboveground herbivores remains unclear. Here, we examined how phytoplasma infection and belowground herbivory by Japanese beetle (Popillia japonica) grubs jointly influence plant traits and performance of aboveground herbivores. Greenhouse experiments were conducted using a wild and a modern cranberry variety in a factorial design with infection status (uninfected vs. infected) and belowground herbivory (absence vs. presence). We measured nutrient (carbon and nitrogen) content, defence compounds (total phenolics and proanthocyanidins), and phytohormones (jasmonic acid [JA] and salicylic acid [SA]), along with performance of two foliar-feeding caterpillars, Sparganothis sulfureana and Lymantria dispar. Phytoplasma infection enhanced aboveground herbivore performance and was associated with higher nitrogen content, reduced phenolic compounds, lower JA levels, and elevated SA levels. In contrast, belowground herbivory induced plant defences, as evidenced by increased phenolics and JA, and reduced aboveground herbivore performance. Although the strength of these effects varied between varieties, the two factors produced opposing effects consistent with contrasting defence-related responses. Our findings show that phytoplasma infection and root herbivory exert contrasting influences on plant-mediated herbivore resistance, highlighting the importance of considering multiple stressors in plant-herbivore interactions within agroecosystems.

Subjects

  • Ecology
  • Plant sciences

Acknowledgements

We thank Robert Holdcraft, Yahel Ben-Zvi, and Vera Kyryczenko-Roth for their assistance with plant propagation, greenhouse experiments, and Japanese beetle collection. We are also grateful to Kristia Adams for her help with molecular studies, and Lindsay Lindhult for illustrating Fig. 6. This research was supported by the New Jersey Blueberry/Cranberry Research Council, the Yunnan International Joint Laboratory of Fruit-Vegetable-Flower Invasive Insect Pest Management (Yunnan FVF-IPM International Joint Lab; No. 202303AP140018), the College of Agricultural Sciences at Penn State, USDA ARS Agreement No. 58-8042-3-049, and USDA’s National Institute of Food and Agriculture and Hatch Appropriations under Projects #PEN04600, #PEN04606 and Accession #1009362.

Funding

This research was supported by the New Jersey Blueberry/Cranberry Research Council, the Yunnan International Joint Laboratory of Fruit-Vegetable-Flower Invasive Insect Pest Management (Yunnan FVF-IPM International Joint Lab; No. 202303AP140018), the College of Agricultural Sciences at Penn State, USDA ARS Agreement No. 58-8042-3-049, and USDA’s National Institute of Food and Agriculture and Hatch Appropriations under Projects #PEN04600, #PEN04606 and Accession #1009362.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to
Cesar Rodriguez-Saona.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Material 1 (download DOCX )

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Cite this article

Liu, Ht., Han, P., Tooker, J.F. et al. From the ground up: Belowground herbivory and phytoplasma infection influence aboveground herbivore performance.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-64596-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-026-64596-4

Keywords

  • Defence induction hypothesis
  • Plant-herbivore interactions
  • Cranberry false blossom disease
  • C/N
  • Phenolics
  • Phytohormones


Source: Ecology - nature.com

Fires in Europe are breaking records: here’s what the future holds

Connecting research to policy on Capitol Hill

Back to Top