Alternative splicing fine-tunes prey shift of Coccinellini lady beetles to non-target insect

可变剪接微调瓢虫的猎物转移,使其转向非目标昆虫

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Abstract

BACKGROUND: Coccinellini lady beetles have been applied as biological control agent of aphids, however, not all of these species are obligately aphidophagous. Thus, a comprehensive understanding of the molecular mechanisms behind predaceous specificity of Coccinellini lady beetles can provide important clues for evaluating their performance and ecological risk assessment in biological control. Post-transcriptional regulations act a key role in shaping organisms' rapid adaptation to changing environment, yet, little is known about their role in the acclimation of Coccinellini lady beetles to non-target preys. RESULTS: In this study, we conducted a genome-wide investigation to alternative splicing (AS) dynamics in three Coccinellini species Propylea japonica, Coccinella septempunctata and Harmonia axyridis in response to feeding shift from natural prey bean aphids (Megoura japonica) to non-target insect citrus mealybugs (Planococcus citri). Compared to aphid-feeding, all three lady beetles were subject to substantial splicing changes when preying on mealybugs. Most of these differentially spliced genes (DSGs) were not differentially expressed, and regulated different pathways from differentially expressed genes, indicating the functionally nonredundant role of AS. The DSGs were primarily associated with energy derivation, organ formation and development, chemosensation and immune responses, which may promote tolerance of lady beetles to nutrient deprivation and pathogen challenges induced by prey shift. The lady beetles feeding on mealybugs moreover downregulated the generation of splicing products containing premature termination codons (PTCs) for the genes involved in energy derivation and stimulus responses, to fine-tune their protein expression and rationalize energy allocation. CONCLUSION: These findings unraveled the functional significance of AS reprogramming in modulating acclimation of Coccinellini lady beetles to prey shift from aphids to non-target insects and provided new genetic clues for evaluating their ecological safety as biological control agents.

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