Arabidopsis growth and reproduction require UDP-arabinofuranose import into the Golgi apparatus

The nucleotide sugar UDP-L-arabinofuranose is made in the cytosol through the interconversion of UDP-L-arabinopyranose by UDP-arabinomutases and subsequently transported into the Golgi lumen by nucleotide sugar transporters to provide substrate for arabinosyltransferases, a similar organization seen for many nucleotide sugars. The transport of nucleotide sugars is assumed to be a bottleneck in the biosynthesis of cell wall polysaccharides. Using a biochemical approach, we previously identified four nucleotide sugar transporters that specifically transport UDP-L-arabinofuranose in vitro. However, single loss-of-function mutants affecting these transporters did not show significant reductions in L-arabinose in cell wall extracts or obvious phenotypic differences compared to the wild type. Here we present physiological insights into the role of UDP-L-arabinofuranose transporters in planta through a detailed characterization of higher-order Arabidopsis thaliana mutants. Higher-order mutants contain reduced L-arabinose content, which correlates with developmental phenotypes including reduced plant growth, decreased hypocotyl elongation in the dark and defects in epidermal cells. Similar to the UDP-arabinomutase double mutant, a quadruple mutant of the UDP-L-arabinofuranose transporters is gametophytic male lethal and has collapsed pollen grains. Additionally, analysis of the nucleotide sugar pool in mutant leaves revealed that nucleotide sugar interconversion is affected. Together, our findings demonstrate that the transport of UDP-L-arabinofuranose from the cytosol into the Golgi lumen is a critical step in cell wall biosynthesis and is essential for plant growth, development and reproduction.