Cell wall fucosylation in Arabidopsis influences control of leaf water loss and alters stomatal development and mechanical properties

We show that fucose-dependent pectin cross-linking is required for normal stomatal development and control of leaf water loss. Reduced guard cell wall stiffness in a fucosylation-defective mutant did not influence stomatal closure. The Arabidopsis sensitive-to-freezing8 (sfr8) mutant exhibits reduced cell wall (CW) fucose levels and compromised freezing tolerance. To examine whether CW fucosylation also affects the response to desiccation, we tested the effect of leaf excision in sfr8 and the allelic mutant mur1-1. Leaf water loss was strikingly higher than in the wild type in these, but not other, fucosylation mutants. We hypothesized that reduced fucosylation in guard cell (GC) walls might limit stomatal closure through altering mechanical properties. Multifrequency atomic force microscopy (AFM) measurements revealed a reduced elastic modulus (EMODIFIER LETTER PRIME), representing reduced stiffness, in sfr8 GC walls. Interestingly, however, we discovered a compensatory mechanism whereby a concomitant reduction in the storage modulus (EMODIFIER LETTER PRIMEMODIFIER LETTER PRIME) maintained a wild-type viscoelastic time response (tau) in sfr8. Stomata in intact leaf discs of sfr8 responded normally to a closure stimulus, abscisic acid, suggesting that the time response may relate more to closure properties than stiffness does. sfr8 stomatal pore complexes were larger than those of the wild type, and GCs lacked a fully developed cuticular ledge, both potential contributors to the greater leaf water loss in sfr8. We present data that indicate that fucosylation-dependent dimerization of the CW pectic domain rhamnogalacturonan-II may be essential for normal cuticular ledge development and leaf water retention.

Automated summary

We demonstrate the importance of fucose-dependent pectin cross-linking in stomatal development and leaf water loss control. The reduction of guard cell wall stiffness in a fucosylation-defective mutant does not affect stomatal closure. The fucosylation levels of cell walls and freezing tolerance of the Arabidopsis sensitive-to-freezing8 (sfr8) mutant are compromised. Leaf water loss is significantly higher in sfr8 and the allelic mutant mur1-1, indicating that CW fucosylation affects the response to desiccation.