J Plant Ecol ›› Advance articles     DOI:10.1093/jpe/rtaf065

   

Soil microbe-induced plant volatiles can alert neighboring plants to heavy metal stress

Jie-Ren Jin1, Tian-Tian Lin2,*, Chao-Nan Wang1, Xiao Xu2, Dan-Feng Liu2, Yi Wang2, Yu-Peng Geng2, Rui-Ting Ju1, Ming Nie1,*, Bo Li1,2,*   

  1. 1Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, National Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Institute of Biodiversity Science and Institute of Eco-Chongming, School of Life Sciences, Fudan University, Shanghai, China
    2Ministry of Education Key Laboratory for Transboundary Ecosecurity of Southwest China, Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology and Centre for Invasion Biology, Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming 650504, Yunnan, China

    *Correspondence: Bo Li
    Email: bool@fudan.edu.cn
    Tian-Tian Lin
    Email: tlin@ynu.edu.cn
    Ming Nie
    Email: mnie@fudan.edu.cn
  • Online:2025-05-17 Published:2025-05-17
  • Supported by:
    This work was financially supported by the National Key Research and Development Program of China (2022YFC2601100), the National Natural Science Foundation of China (Grant No.: U2102218, 31901228, 32001204), the Science and Technology Department of Shanghai (Grant No.: 23015810100), and the Department of Science and Technology of Yunnan Province (Grant No.: 202405AS350011).

Abstract: While the alerting effects of microbe-induced plant volatiles (MIPVs) to biotic stressors have been extensively studied, the ecological functions of MIPVs responding to abiotic stressors have received less attention. Using an interplant communication assay setup, we employed Phytolacca americana as a study species to investigate whether heavy metal-induced MIPVs released by the emitter plants contribute to metal tolerance in neighboring receiver plants. We found that high levels of manganese (Mn) stress increased the total MIPV emissions of plants cultivated in non-sterilized soil, in contrast to VOCs emitted by plants in sterilized soil. MIPVs produced by the Mn-stressed plants notably altered the hormonal profiles of the receiver plants, leading to increased similarity in soil microbial assembles and modification of CSR strategies. Consequently, the receiver plants exhibited enhanced tolerance to subsequent Mn stress, as evidenced by improved growth performance, increased antioxidant enzyme activities, and reduced membrane damage. By unraveling the mechanism underlying MIPV-mediated tolerance priming for neighboring plants, we reveal a key signal role of soil microorganisms involved in plant-plant communication. This study represents one of the initial efforts to elucidate the alerting effects of MIPVs induced by heavy metal stress on neighboring plants and its ecological consequences.

Key words: volatile organic compounds, abiotic stress, alerting effect, heavy metal tolerance, Phytolacca americana, CSR strategies.