Introduction: The brown planthopper (Nilaparvata lugens Stål, BPH) is one of the most economically significant pests of rice. The Bph30 gene has been successfully cloned and conferred rice with broad-spectrum resistance to BPH. However, the molecular mechanisms by which Bph30 enhances resistance to BPH remain poorly understood.

Methods: Here, we conducted a transcriptomic and metabolomic analysis of Bph30-transgenic (BPH30T) and BPH-susceptible Nipponbare plants to elucidate the response of Bph30 to BPH infestation.

Results: Transcriptomic analyses revealed that the pathway of plant hormone signal transduction enriched exclusively in Nipponbare, and the greatest number of differentially expressed genes (DEGs) were involved in indole 3-acetic acid (IAA) signal transduction. Analysis of differentially accumulated metabolites (DAMs) revealed that DAMs involved in the amino acids and derivatives category were down-regulated in BPH30T plants following BPH feeding, and the great majority of DAMs in flavonoids category displayed the trend of increasing in BPH30T plants; the opposite pattern was observed in Nipponbare plants. Combined transcriptomics and metabolomics analysis revealed that the pathways of amino acids biosynthesis, plant hormone signal transduction, phenylpropanoid biosynthesis and flavonoid biosynthesis were enriched. The content of IAA significantly decreased in BPH30T plants following BPH feeding, and the content of IAA remained unchanged in Nipponbare. The exogenous application of IAA weakened the BPH resistance conferred by Bph30.

Discussion: Our results indicated that Bph30 might coordinate the movement of primary and secondary metabolites and hormones in plants via the shikimate pathway to enhance the resistance of rice to BPH. Our results have important reference significance for the resistance mechanisms analysis and the efficient utilization of major BPH-resistance genes.

Diverse molecular processes regulate the interactions between insect herbivores and their host plants. When plants are exposed to insects, elicitors induce plant defenses, and complex physiological and biochemical processes are triggered, such as the activation of the jasmonic acid (JA) and salicylic acid (SA) pathways, Ca²⁺ flux, reactive oxygen species (ROS) burst, mitogen-activated protein kinase (MAPK) activation, and other responses. For better adaptation, insects secrete a large number of effectors to interfere with plant defenses on multiple levels. In plants, resistance (R) proteins have evolved to recognize effectors and trigger stronger defense responses. However, only a few effectors recognized by R proteins have been identified until now. Multi-omics approaches for high-throughput elicitor/effector identification and functional characterization have been developed. In this review, we mainly highlight the recent advances in the identification of the elicitors and effectors secreted by insects and their target proteins in plants and discuss their underlying molecular mechanisms, which will provide new inspiration for controlling these insect pests.