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As a universal energy generation pathway utilizing carbon metabolism, glycolysis plays an important housekeeping role in all organisms. Pollen tubes expand rapidly via a mechanism of polarized growth, known as tip growth, to deliver sperm for fertilization. Here, we report a novel and surprising role of glycolysis in the regulation of growth polarity in Arabidopsis pollen tubes via impingement of Rho GTPase-dependent signaling. We identified a cytosolic phosphoglycerate kinase (pgkc-1) mutant with accelerated pollen germination and compromised pollen tube growth polarity. pgkc-1 mutation greatly diminished apical exocytic vesicular distribution of REN1 RopGAP (Rop GTPase activating protein), leading to ROP1 hyper-activation at the apical plasma membrane. Consequently, pgkc-1 pollen tubes contained higher amounts of exocytic vesicles and actin microfilaments in the apical region, and showed reduced sensitivity to Brefeldin A and Latrunculin B, respectively. While inhibition of mitochondrial respiration could not explain the pgkc-1 phenotype, the glycolytic activity is indeed required for PGKc function in pollen tubes. Moreover, the pgkc-1 pollen tube phenotype was mimicked by the inhibition of another glycolytic enzyme. These findings highlight an unconventional regulatory function for a housekeeping metabolic pathway in the spatial control of a fundamental cellular process., Author summary Glycolysis, which breaks down glucose to produce energy, has long been considered a “housekeeping” pathway in living cells, i.e., it helps maintain basic cellular functions. Here, we found that the glycolysis pathway plays an unconventional regulatory role in cell polarity, i.e., the intrinsic asymmetry in the shape, structure, and organization of cellular components. Mutation in the gene encoding the glycolytic enzyme cytosolic phosphoglycerate kinase (PGKc) leads to swollen and shorter pollen tubes in Arabidopsis thaliana, which is associated with the over-activation of Rho GTPase—a master regulator of cell polarity. Our results suggest that this phenomenon is caused by a specific regulatory role of cytosolic glycolysis rather than the global energy supply or moonlighting functions of glycolytic enzymes that modulate pollen tube growth polarity. Our findings shed light on the diverse biological roles of glycolysis in plants beyond simple “housekeeping” functions.