The trans-Golgi-localized protein BICAT3 regulates manganese allocation and matrix polysaccharide biosynthesis

Manganese (Mn(2+)) is essential for a diversity of processes, including photosynthetic water splitting and the transfer of glycosyl moieties. Various Golgi-localized glycosyltransferases that mediate cell wall matrix polysaccharide biosynthesis are Mn(2+) dependent, but the supply of these enzymes with Mn(2+) is not well understood. Here, we show that the BIVALENT CATION TRANSPORTER 3 (BICAT3) localizes specifically to trans-cisternae of the Golgi. In agreement with a role in Mn(2+) and Ca(2+) homeostasis, BICAT3 rescued yeast (Saccharomyces cerevisiae) mutants defective in their translocation. Arabidopsis (Arabidopsis thaliana) knockout mutants of BICAT3 were sensitive to low Mn(2+) and high Ca(2+) availability and showed altered accumulation of these cations. Despite reduced cell expansion and leaf size in Mn(2+)-deficient bicat3 mutants, their photosynthesis was improved, accompanied by an increased Mn content of chloroplasts. Growth defects of bicat3 corresponded with an impaired glycosidic composition of matrix polysaccharides synthesized in the trans-Golgi. In addition to the vegetative growth defects, pollen tube growth of bicat3 was heterogeneously aberrant. This was associated with a severely reduced and similarly heterogeneous pectin deposition and caused diminished seed set and silique length. Double mutant analyses demonstrated that the physiological relevance of BICAT3 is distinct from that of ER-TYPE CA(2+)-ATPASE 3, a Golgi-localized Mn(2+)/Ca(2+)-ATPase. Collectively, BICAT3 is a principal Mn(2+) transporter in the trans-Golgi whose activity is critical for specific glycosylation reactions in this organelle and for the allocation of Mn(2+) between Golgi apparatus and chloroplasts.