Soil worms are among the most abundant and functionally diverse soil animals. However, they have been largely overlooked in studies on microplastic (MP) toxicity. MPs and plant secondary metabolites (PSMs) are ubiquitous in soil due to plant litter decomposition and heavy MP contamination, inevitably interacting and exerting combined toxicity on soil organisms. However, little research has been conducted on their joint effects. This study investigates the individual and combined toxic effects of polyethylene (PE) MPs and three PSMs (glycyrrhizic acid, tannic acid, and matrine) on the model organism Caenorhabditis elegans. Physiological and biochemical responses were assessed using fluorescence microscopy, image analysis, and statistical methods. After 42 h of exposure to PE MPs and/or PSMs, worm growth and development were negatively impacted. Under experimental conditions, matrine and PE MPs synergistically inhibited worm growth, exacerbated neurological damage, and induced oxidative stress. In contrast, glycyrrhizic acid and tannic acid alleviated PE MP-induced growth inhibition, mitigated oxidative stress, and demonstrated antioxidant properties that counteracted oxidative damage. This study offers new insights into the combined effects of MPs and PSMs in soil ecosystems, contributing to ecological risk assessments and pollution management strategies.

To assess the ecological risk of microplastics (MPs) in agricultural systems, it is critical to simultaneously focus on MP-mediated single-organism response and different trophic-level organism interaction. Herein, we placed earthworms in soils contaminated with different concentrations (0.02% and 0.2% w/w) of polyethylene (PE) and polypropylene (PP) MPs to investigate the effect of earthworms on tomato against Helicoverpa armigera (H. armigera) under MPs stress. We found that earthworms alleviated the inhibitory effects of MPs stress on tomato growth and disrupted H. armigera growth. Compared to individual MPs exposure, earthworm incorporation significantly increased the silicon and lignin content in herbivore-damaged tomato leaves by 19.1% and 57.6%, respectively. Metabolites involved in chemical defense (chlorogenic acid) and phytohormones (jasmonic acid) were also activated by earthworm incorporation. Furthermore, earthworms effectively reduced oxidative damage induced by H. armigera via promoting antioxidant metabolism. Overall, our results suggest that utilizing earthworms to regulate above- and below-ground interactions could be a promising strategy for promoting green agriculture.