J Plant Ecol ›› 2025, Vol. 18 ›› Issue (4): rtaf065.DOI: 10.1093/jpe/rtaf065

• Research Articles •    

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
  • Received:2025-02-26 Accepted:2025-05-17 Online:2025-05-17 Published:2025-08-01
  • 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).

土壤微生物诱导的植物挥发性物质对邻近植物重金属胁迫的预警作用

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.

摘要:
当前学术界在微生物产生的植物挥发性物质(microbe-induced plant volatiles, MIPVs)对生物胁迫的预警作用方面已经进行了广泛研究,但对非生物胁迫如何影响MIPVs的生态功能关注较少。为此,本研究以美洲商陆(Phytolacca americana)为研究对象,利用植物间通讯实验装置,研究了重金属胁迫诱导下美洲商陆个体释放的MIPVs是否有助于邻株植物对重金属的耐受作用。结果发现,高强度锰胁迫增加了未灭菌土壤中植株总MIPVs排放量,与之相反,在灭菌土壤中植株排放的总挥发性有机化合物并未显著变化。锰胁迫诱导下植株个体产生的MIPVs显著改变了邻株植物的激素水平,并导致土壤微生物组成的相似性增加和CSR策略的调整。因此,受体植株对后续锰胁迫的耐受性增强,表现为生长性能改善、抗氧化酶活性增加以及膜损伤减少。通过解析MIPVs介导的邻株植物重金属耐受性的启动机制,该研究揭示了土壤微生物在植物间信息交流中的关键信号作用。本研究初步尝试从MIPVs预警作用的角度揭示重金属胁迫下植物间的信息交流及其生态后果,可为将来研究提供重要启示。

关键词: 挥发物, 非生物胁迫, 预警效应, 重金属耐受, 美洲商陆(Phytolacca americana), CSR策略