Abstract text: Post-transcriptional modifications are essential for regulating cellulose synthase (CESA) activity. However, the molecular mechanism by which nucleocytosolic O-glycosylation controls cellulose synthesis remains unclear. In this study, we demonstrate that the O-fucosyltransferase SPINDLY (SPY) modulates cellulose deposition in the mucilage of Arabidopsis thaliana. Seeds of spy mutants exhibited diminished cellulose rays and disorganized cellulose microfibrils within their compact mucilage capsules, likely resulting from disrupted microtubule organization. We identified TONNEAU1 RECRUITING MOTIF 4 (TRM4) as a previously unrecognized interacting partner of SPY in the cytoplasm and at the plasma membrane. TRM4 undergoes O-fucosylation by SPY in planta at serine residues 579 (Ser579) and Ser583, a modification that was abolished by a point mutation in the catalytic domain of SPY. In addition, the TRM4-CESA3 module plays a key role in regulating mucilage cellulose synthesis. Through O-fucosylation, SPY positively regulates TRM4 protein abundance by inhibiting its proteolysis, thereby enhancing the TRM4-CESA3 interaction and promoting cellulose synthesis. Furthermore, genetic evidence indicates that TRM4 functions downstream of SPY. Together, our findings provide new insights into the role of SPY-mediated protein O-fucosylation in the regulation of cellulose synthesis in plants.