Morphological, functional, compositional and transcriptional constraints shape the distinct venom profiles of the assassin bug Sycanus croceovittatus

Predatory bugs employ a salivary venom apparatus to generate complex venoms for capturing and digesting prey. The venom apparatus consists of different glands for the production of distinct venom sets, but the underlying mechanisms behind this process remain poorly understood. Here we present a comprehensive analysis of the morphological, functional, compositional and transcriptional characteristics of venoms derived from posterior main gland (PMG), anterior main gland (AMG), and accessory gland (AG) of the assassin bug Sycanus croceovittatus. Structural observations revealed the intricate constructions of the venom apparatus, enabling the production and storage of three distinct venom sets in anatomically varied glands and allowing them to be modulated in a context-dependent manner upon utilization. There were remarkable differences in the biological activities exhibited by PMG, AMG, and AG venoms. Proteotranscriptomic analysis demonstrated that these venoms displayed compositional heterogeneity at both the quantity and variety levels of proteins. Transcriptional profiles of the identified venom proteins revealed gland-specific or biased expression patterns. These findings indicate that the divergence in venom profiles among different glands arises from morphological, functional, compositional and transcriptional constraints on the venom apparatus, reflecting remarkable morphogenesis and regulatory gene networks responsible for the compartmentalized production of venom proteins in different glands.