Metabolites with benzene ring from sugarcane leaf play important role in plant-Spodoptera frugiperda interaction

Secondary metabolism plays important role in plant growth and development, however, the relationship between secondary metabolism and adaptive plant-insect communication is largely unknown. The present study used sugarcane line highly susceptible to Spodoptera frugiperda and sister line with medium resistance to analyze the role of plant non-volatile organic compounds (NOCs) and volatile organic compounds (VOCs) in sugarcane-S. frugiperda interaction. A total of 46 plant NOCs and 15 plant VOCs significantly different between resistant and susceptible lines and were continuously up-regulated and down-regulated at different time points before/after S. frugiperda treatment were screened. Phenolic acids containing benzene ring accounted for the largest proportion of differential NOCs. Levels of 66.7% of these phenolic acids were higher in susceptible line. Feeding supplemented with NOCs showed that phenoxyacetic acid (phenolic acid) and 4-methoxybenzaldehyde (aromatic phenolic acid) both increased the male-to-female ratio of S. frugiperda. Aromatics containing benzene ring, accounted for the largest of differential VOCs in susceptible line. Two aromatics, p-cymene and benzene and 1-ethenyl-4-methoxy-, with higher level in susceptible line, were attractive to S. frugiperda. Terpenoids, aldehyde, and esters accounted for most of higher-in-resistant VOCs, with most tested to be repellent to S. frugiperda. Furthermore, transcriptome analysis of S. frugiperda feeding on susceptible and resistant lines combined with feeding assays revealed that tryptophan, as a precursor of aromatic compounds that also contains benzene ring, could promote the growth and development of S. frugiperda in nutritional deficiency condition. These findings together suggested that benzene-ring containing compounds play a critical role in plant-Spodoptera frugiperda interaction.