Transcriptomic analysis of tomato growth inhibition in response to an aqueous extract from soil continuously cropped with okra

A single-tillage system, monocropping, and the excessive pursuit of economic efficiency have exacerbated impediments to continuous cropping in greenhouse production systems. Crop rotation is an effective strategy to avoid the deleterious impacts of continuous cropping. However, in practice, the rotation of tomato (Solanum lycopersicum L.) and okra (Abelmoschus esculentus L.) inhibits the growth and fruiting of tomato. To explore the mechanism by which tomato growth is disrupted, tomato seedlings were grown for 9 days in nutrient solution supplemented with an aqueous extract (0, 250, or 500 mg/mL) from soil continuously planted with okra for 10 years. Transcriptome sequencing (RNA-seq) and physiological and biochemical analyses were conducted to characterize the response. In total, 4035 differentially expressed genes (DEGs) were identified in the leaves. Compared with the control, 3239 and 2990 DEGs were detected in the leaves of seedlings treated with 250 and 500 mg/mL extract, respectively. Bioinformatics analysis revealed that the DEGs participated in diverse biological processes, such as chlorophyll metabolism and lignin biosynthesis. The expression of chlorophyll synthesis-related genes was significantly inhibited, whereas chlorophyll decomposition-related gene expression and H2O2 content were promoted by the soil extract, which was not conducive to normal chlorophyll metabolism. The soil extract significantly increased phenylalanine ammonia-lyase activity and the transcript levels of lignin biosynthesis-related genes (PAL, HCT, CYP98A, CCoAMT1, CCoAMT2, CCR1, and CAD2), thereby promoting lignin biosynthesis and accumulation to enhance stress resistance, but the extract reduced 4CL1, CCR2, and CAD1 expression. The results from this study suggest that the soil aqueous extract is not conducive to normal chlorophyll metabolism in tomato leaves. Although tomato plants exposed to stress are capable of enhanced lignin synthesis through self-regulation to maintain higher water transport efficiency and stress resistance, long-term treatment is ultimately detrimental to lignin biosynthesis.