Blooming resilience: transcriptomic insights into cotton flower responses to boll weevil infestation.

Key message: Cotton plants undergo a drastic transcriptional reprogramming after cotton boll weevil infestation, modulating several defense pathways to cope with the damage. The global demand for cotton fiber continues to rise, but pests and pathogens significantly hinder cotton production, causing substantial losses. Among these, the cotton boll weevil (Anthonomus grandis) is one of the most destructive pests. To investigate the molecular responses of cotton (Gossypium hirsutum) to boll weevil infestation, we evaluated the global gene expression of floral buds using mRNA-seq. Additionally, we analyzed the expression of non-coding RNAs, including microRNAs (miRNAs) and long intergenic non-coding RNAs (lincRNAs). Infestation by cotton boll weevil larvae triggered a rapid and drastic transcriptional reprogramming, with 1,656 and 1.698 genes modulated after two and twelve hours, respectively. Gene ontology enrichment analysis revealed significant regulation of defense-related and developmental processes, including photosynthesis, primary metabolism, and cell organization. Transcription factor families such as ERF, WRKY, GRAS, and NAC were strongly affected, highlighting their roles in coordinating defense responses. The jasmonate pathway showed intensive modulation, alongside secondary metabolite pathways like terpenoids and phenylpropanoids, which contribute to plant defense mechanisms. Non-coding RNAs also played a critical role in the response. We identified 921 unique known and novel miRNAs, with 36 modulated by the infestation, and predicted 98,850 putative lincRNAs, several of which were differentially expressed. Understanding the genetic and molecular mechanisms underlying cotton's defense against boll weevil, particularly during early infestation stages, is vital for developing biotechnological strategies to reduce pest damage. Our findings provide critical insights to enhance cotton resilience against herbivores.