Alanine metabolism mediates energy allocation of the brown planthopper to adapt to resistant rice.

ABSTRACT

INTRODUCTION: During the adaptation to host plant resistance, herbivorous insects faced the challenge of overcoming plant defenses while ensuring their own development and reproductive success. To achieve this, a strategic allocation of energy resources for detoxification and ecological fitness maintenance became essential. OBJECTIVE: This study aimed to elucidate the intricate energy allocation mechanisms involved in herbivore adaptation that are currently poorly understood. METHODS: The rice Oryza sativa and its monophagous pest, the brown planthopper (BPH), Nilaparvata lugens were used as a model system. An integrated analysis of metabolomes and transcriptomes from different BPH populations were conducted to identify the biomarkers. RNA interference of key genes and exogenous injection of key metabolites were performed to validate the function of biomarkers. RESULTS: We found that alanine was one of the key biomarkers of BPH adaptation to resistant rice variety IR36. We also found that alanine flow determined the adaptation of BPH to IR36 rice. The alanine aminotransferase (ALT)-mediated alanine transfer to pyruvate was necessary and sufficient for the adaptation. This pathway may be conserved, at least to some extent, in BPH adaptation to multiple rice cultivars with different resistance genes. More importantly, ALT-mediated alanine metabolism is the foundation of downstream energy resource allocation for the adaptation. The adapted BPH population exhibited a significantly higher level of energy reserves in the fat body and ovary when fed with IR36 rice, compared to the unadapted population. This rendered the elevated detoxification in the adapted BPH and their ecological fitness recovery. CONCLUSION: Overall, our findings demonstrated the crucial role of ALT-mediated alanine metabolism in energy allocation during the adaptation to resistant rice in BPH. This will provide novel knowledge regarding the co-evolutionary mechanisms between herbivores and their host plants.