Impaired Cellulose Synthase Guidance Leads to Stem Torsion and Twists Phyllotactic Patterns in Arabidopsis

The parallel alignment of stiff cellulose microfibrils in plant-cell walls mediates anisotropic growth. This is largely controlled by cortical microtubules, which drive the insertion and trajectory of the cellulose synthase (CESA) complex at the plasma membrane. The CESA interactive protein 1 (CSI1) acts as a physical linker between CESA and cortical microtubules. Here we show that the inflorescence stems of csi1 mutants exhibit subtle right-handed torsion. Because cellulose deposition is largely uncoupled from cortical microtubules in csi1, we hypothesize that strictly transverse deposition of microfibrils in the wild-type is replaced by a helical orientation of uniform handedness in the mutant and that the helical microfibril alignment generates torsion. Interestingly, both elastic and viscous models for an expanding cell predict that a net helical orientation of microfibrils gives rise to a torque. We indeed observed tilted microfibrils in csi1 cells, and the torsion was almost absent in a csi1 prc1 background with impaired cellulose synthesis. In addition, the stem torsion led to a novel bimodal and robust phyllotactic pattern in the csi1 mutant, illustrating how growth perturbations can replace one robust mathematical pattern with a different, equally robust pattern.