Chenopodium ambrosioides originated from tropical America, and is a major malignant weed in the farmland ecosystems of corn (Zea mays), soybean (Glycine max), and buckwheat (Fagopyrum tataricum) in southwest China. Existing evidence shows that allelopathy is one of the main mechanisms for the successful invasion of C. ambrosioides, and the volatile pathway is the main way of its allelopathic effect. When receptor plants are allelopathically stressed by the invasive plant C. ambrosioides, they will increase the number of root border cells (RBCs) to alleviate the damage to the root system caused by the stress. To investigate the cellular and molecular mechanisms underlying this effect, maize, soybean and buckwheat were employed as receptor plants. Experimental groups were treated with volatile oil (V) and α-terpinene (T), with three treatment levels established for each group. The treatment concentrations for volatile oil were 6.25 μL/L, 12.50 μL/L, and 25.00 μL/L (denoted as V1, V2, and V3), while the concentrations for α-terpinene were set based on its relative content in V1, V2, and V3, being 3.125 μL/L, 6.255 μL/L, and 12.510 μL/L (denoted as T1, T2, T3), respectively. The impact of volatile oils and α-terpinene on the number, length, and curvature of receptor RBCs was investigated using the suspension air culture method. Additionally, the volatile sensitivity of the RBCs of receptor plants was analyzed. Transcriptomics techniques were employed to examine changes in the production and release of receptor RBCs and the expression levels of related genes. The effects of the treatments on their metabolic pathways were analyzed using KEGG and validated by qRT-PCR. Results indicated that the number of RBCs increased under the influence of volatile substances compared to the control, but the promoting effect diminished or even disappeared with prolonged treatment duration and increased treatment concentration. The curvature of RBCs initially increased and then decreased with rising volatile concentrations, while the mean length overall became shorter. The comprehensive allelopathic effect of α-terpinene was 0.76 times that of volatile oil, and the sensitivity of different receptor RBCs to the volatiles of C. ambrosioides was maize>buckwheat>soybean. Transcriptomics results revealed that the differentially expressed genes in buckwheat, soybean, and maize were 2506 (1524 down-regulated and 982 up-regulated), 461 (209 down-regulated and 252 up-regulated), and 4222 (1746 down-regulated and 2476 up-regulated), respectively, in the volatile oil treatment group, while 291 (145 down-regulated, 146 up-regulated), 1986 (757 down-regulated, 1229 up-regulated), and 3015 (1759 down-regulated, 1256 up-regulated), respectively, in the α-terpinene treatment group. KEGG analyses showed that genes related to lignin synthesis, pectin degradation/synthesis, and cell wall component remodeling associated with root border cell release were altered in receptor root tip cells when subjected to allelochemicals stress. The above outcomes suggest that under the allelopathic stress of low-intensity volatiles from C. ambrosioides, the stress signal pathways of corn, soybean, and buckwheat are activated. This leads to the remodeling of the cell wall in young roots, speeds up the degradation of the middle layer pectin, shortens the length of RBCs, enhances the curvature of RBCs, thereby reducing the adhesion between RBCs and the root cap, and further expedites the release of RBCs to deal with the allelopathic stress of C. ambrosioides. As the stress intensity rises, the generation and release of RBCs are hindered, and the defense function of the receptors against allelopathic stress deteriorates. The stress response of the exotic species corn to the allelopathic stress of C. ambrosioides is significantly faster than that of the native species soybean and buckwheat.