Abstract text: Arabidopsis GALACTURONOSYLTRANSFERASE1 (GAUT1) initiates pectic homogalacturonan (HG) biosynthesis and elongates HG acceptors in vitro. Its biological function and structure of the HG-containing polymer(s) it synthesizes remain unclear. Here we show that Arabidopsis gaut1 homozygous mutants grow as severely dwarfed seedlings that fail to yield mature plants due to defective cell expansion/elongation. Homozygous gaut1-1 mutant suspension cells are smaller than wild type (WT) with reduced HG:galacturonosyltransferase activity and wall galacturonic acid (GalA) content. Sequential extraction of gaut1-1 suspension cell walls with increasingly harsh solvents revealed a significant loss of GalA in the final 4M KOH post-chlorite extract. Digestion of this extract with endopolygalacturonase and high percentage polyacrylamide gel electrophoresis revealed doublet bands in WT extract downregulated in gaut1-1 and identified by NMR analysis as rhamnogalacturonan II (RG-II). The bulk of RG-II, generally extracted in early ammonium oxalate and sodium carbonate fractions, was not reduced in the gaut1-1 mutant. Super resolution microscopy revealed a decrease and disorganization of HG nanofilaments in hypocotyl and callus gaut1-1 walls compared to WT. The results support a model of GAUT1 synthesizing a unique HG held tightly in the cell wall, associated with a unique population of RG-II, and required for HG nanofilament organization and cell expansion/elongation.