A biphasic molecular program orchestrates ontogenetic transitions and ecological specialization in invasive whitefly, Bemisia tabaci

The sweet potato whitefly, Bemisia tabaci, is a globally important pest that poses serious challenges to agriculture because of its remarkable ability to adapt and thrive in various environments. Despite its widespread presence, its development and growth remain poorly understood. In this study, we used a comprehensive multiomics approach, including small RNA (microRNA (miRNA)) sequencing, messenger RNA (mRNA) transcriptomics, and quantitative proteomics, to decipher the molecular developmental dynamics of B. tabaci at different life stages, such as eggs, nymphs, puparia (pupae), and adults. The findings revealed two principal ontogenetic stages in the life cycle of B. tabaci. The initial phase encompasses ontogenetic metamorphosis from the ovum to the inaugural nymphal instar, characterized by a decrease in matrilineal influence and an increase in metabolic activity. The subsequent phases occur as the organism advances its transition from the fourth-instar nymph stage to sexual maturity, resulting in profound metamorphic transformations and ecological adaptations. We revealed that specific miRNAs, especially Btab-miR-34 and Btab-miR-2944b, play critical roles in regulating these stages by repressing processes such as DNA replication and cuticle formation. Furthermore, novel miRNAs such as bta-miR-307a, bta-miR-352a, and bta-miR-107a have emerged as key regulators that direct pathways involved in detoxification and environmental sensing. Our analysis of transcriptional dynamics revealed that each life stage has a unique molecular blueprint. Eggs focus mainly on replication, whereas adults produce proteins related to detoxification and sensory functions. Proteomic data further confirmed that these molecular programs are functionally active during development. This network suggests that established miRNAs are crucial for maintaining developmental stability, whereas newer regulators support lineage-specific adaptations that improve survival. This research highlights the complex and finely tuned molecular mechanisms that regulate the growth and development of B. tabaci. These insights also offer valuable information that can help improve pest management strategies in agriculture.

烟粉虱（Bemisia tabaci）是一种全球重要的农业害虫，因其卓越的环境适应与种群繁衍能力，给农业生产带来了严峻挑战。尽管该虫分布范围极广，但学界对其生长发育的分子机制仍知之甚少。本研究采用涵盖小RNA（microRNA，miRNA）测序、信使RNA（messenger RNA，mRNA）转录组学以及定量蛋白质组学在内的整合多组学策略，解析了烟粉虱在卵、若虫、伪蛹（蛹）以及成虫等不同生命阶段的分子发育动态。研究结果揭示了烟粉虱生命周期中的两个核心发育阶段：第一阶段为从卵到初龄若虫的个体发育变态过程，该阶段的显著特征为母源调控影响逐渐减弱，代谢活性逐步升高；第二阶段则为四龄若虫向性成熟过渡的后续发育进程，伴随剧烈的变态重塑与生态适应性演化。本研究发现，特定miRNA——尤其是Btab-miR-34与Btab-miR-2944b——通过抑制DNA复制、表皮形成等生物学过程，在调控上述发育阶段中发挥关键作用。此外，bta-miR-307a、bta-miR-352a与bta-miR-107a等新型miRNA，作为调控解毒与环境感知通路的核心调控因子，在发育过程中扮演重要角色。转录组动态分析表明，烟粉虱的每个生命阶段均拥有独特的分子表达谱：卵期主要聚焦于DNA复制过程，而成虫则大量表达与解毒及感官功能相关的蛋白质。蛋白质组学数据进一步证实，这些分子程序在发育进程中具备显著的功能活性。该调控网络表明，保守miRNA对于维持发育稳定性至关重要，而新型调控因子则助力物种特异性的适应性进化，以提升种群生存能力。本研究阐明了调控烟粉虱生长发育的复杂且精密的分子机制，相关研究结果可为优化农业害虫防治策略提供重要参考价值。