Galactan mobilization during carbon starvation compromises cell wall-mediated fungal resistance in Arabidopsis

Polysaccharides are the main components present in plant cell walls. They form a network that is dynamically modified during growth and upon both abiotic and biotic stress. We investigated how the cell wall of Arabidopsis rosettes is remodeled during periods of dark-induced starvation in the wild type and in plastidic phosphoglucomutase (pgm) mutants, which suffer from periodic starvation due to starch deficiency. Time-course analysis demonstrated that up to one fifth of the galactose present in leaf cell walls is reversibly released upon starvation, while other cell wall monosaccharides were less affected. An investigation of BETA-GALACTOSIDASE (BGAL) expression and the analysis of bgal mutants indicated that BGAL1 and BGAL4 contribute to the release of cell wall galactose upon starvation. Increased transcript abundance of UDP-GLUCOSE 4-EPIMERASE (UGE) 1 and 3 under starvation proposed an increased flux through the galactose salvage pathway, however an analysis of the UDP- galactose pool in mutant plants indicated redundancy with other UGEs. Simultaneously to galactan degradation, GALACTAN SYNTHASE1 (GALS1) expression was reduced, attenuating the synthesis of new galactan chains. We show that overexpression of GALS1 prevents depletion of the recyclable cell wall galactose pool and is sufficient to rescue impaired penetration resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum upon dark-induced and periodic starvation. Our data suggest that pectic galactan in the plant cell wall serves as a sugar resource during starvation conditions. However, galactose release from the wall leads to impaired penetration resistance against a fungal pathogen, causing a tradeoff between sugar supply for plant metabolism and preformed defense. Significance statementPolysaccharides present in plant cell walls must be dynamically modified in response to external stimuli, but it is not well understood how cell wall remodeling is adjusted in response to metabolic cues and how this affects defense against pathogens. Here, we report that galactose is reversibly released from cell walls upon carbon starvation, which critically affects penetration resistance to a fungal pathogen.