Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis

The vacuole occupies most of the volume of plant cells; thus, the tonoplast marker delta-tonoplast intrinsic protein-green fluorescent protein delineates cell shape, for example, in epidermis. This permits rapid identification of mutants. Using this strategy, we identified the cell shape phenotype-1 (csp-1) mutant in Arabidopsis thaliana. Beyond an absence of lobes in pavement cells, phenotypes included reduced trichome branching, altered leaf serration and stem branching, and increased stomatal density. This result from a point mutation in AtTPS6 encoding a conserved amino-terminal domain, thought to catalyze trehalose-6-phosphate synthesis and a carboxy-terminal phosphatase domain, is catalyzing a two-step conversion to trehalose. Expression of AtTPS6 in the Saccharomyces cerevisiae mutants tps1 (encoding a synthase domain) and tps2 (encoding synthase and phosphatase domains) indicates that AtTPS6 is an active trehalose synthase. AtTPS6 fully complemented defects in csp-1. Mutations in class I genes (AtTPS1-AtTPS4) indicate a role in regulating starch storage, resistance to drought, and inflorescence architecture. Class II genes (AtTPS5-AtTPS11) encode multifunctional enzymes having synthase and phosphatase activity. We show that class II AtTPS6 regulates plant architecture, shape of epidermal pavement cells, and branching of trichomes. Thus, beyond a role in development, we demonstrate that the class II gene AtTPS6 is important for controlling cellular morphogenesis.