Poison storage and maturation in serous cutaneous glands of anurans: an integrative ultrastructural outlook

The functional cycle of serous (poison) glands in anuran skin is divided into three phases: biosynthesis, accumulation (or storage), and secretory release. The intermediate phase of poison storage has peculiar traits: it occurs in the syncytial cytoplasm of the gland secretory unit, and may be long-lasting, if encounters with natural predators are infrequent, and serous product release is delayed. Intracytoplasmic secretory deposits have limiting membranes derived from the Golgi apparatus and are classified as vesicles or granules, according to the varying density of their contents. During storage, secretory deposits undergo marked rearrangements in their structures and composition, usually regarded as post-Golgian maturational processes. Serous maturation involves consistent events: vesicle-vesicle and granule-granule merging, as well as interaction between granules and syncytial cytoplasm. Merging processes tend to homogenize serous products by blending various molecular pools contained in secretory deposits. This maturational activity involves degradation of adhering plasma membranes, pertaining to contiguous vesicles/granules. Secretory granule-syncytium interactions allow exchange of molecules between the two compartments, and entail amplification of the surface of the membranes bounding the granules, in order to enhance molecular flow. Exchange surface increases through two main processes: enlargement of the halo between the secretory product and the limiting membrane of the granule, and/or formation of microvillous-like processes, jutting from the cytoplasm into this translucent compartment. Ultrastructural maturation features reveal marked variations of the aggregation of the poison, ranging from dilution to condensation. As observed in species from several genera, secretory granules may acquire similar ultrastructural traits through condensation, reflecting either maturational programs shared by phylogenetically related taxa or convergent evolution. In some families, condensation causes the secretory granules to have a recurrent substructure that results from a close associations of modular subunits (spheroidal or rod-like in shapes) with an average diameter of 90-100 nm. As a whole, ultrastructural findings collected from Old and New World anurans update concepts of serous maturation, which were originally developed by pioneering authors using light microscopy. Key activities in this fundamental phase of poison manufacturing are found in the syncytial cytoplasm that exchanges molecules with the serous product, and the secretory granules that contribute to maturation as active organelles, providing a finely tuned microenvironment.