Kinase Partner Zinc Finger Protein modulates pollen tube growth by influencing tip vesicle trafficking

Abstract The polar growth of pollen tubes requires the precise coordination of membrane trafficking processes, such as exocytosis and endocytosis, and the orderly deposition of cell wall materials at the growing tip. We previously identified two plasma membrane-localized receptor kinases, LePRK1 and LePRK2, which form a dynamic complex with the small GTPase-activating protein Kinase Partner Protein (KPP) and actin-binding proteins to regulate pollen tube growth. Here, we show that Kinase Partner Zinc-finger Protein (KPZP) in tomato (Solanum lycopersicum), whose N-terminus interacts with LePRK1 and LePRK2, negatively regulates the membrane targeting of both LePRK1 and LePRK2 and, thereby, the phenotype caused by LePRK1 or LePRK2 overexpression. A significant proportion of pollen tubes overexpressing KPZP exhibited cytoplasmic invagination at the tip while maintaining active cytoplasmic streaming in the shank. Furthermore, trans-Golgi network/early endosome -derived vesicles and recycling endosomes, which are typically found only in the inverted cone region, accumulated in large quantities in an expanded region in the front and shank of pollen tubes. This indicates that a significant proportion of vesicles failed to fuse with the cell membrane at the growing tip. KPZP overexpression led to an imbalance between exocytosis and endocytosis, resulting in the irregular deposition of cell wall polysaccharides at the pollen tube apex. Transgenic tomato pollen tubes overexpressing only the N-terminal portion of KPZP also showed the tip cytoplasm invagination phenotype. In conclusion, KPZP plays a crucial role in regulating vesicle trafficking at the pollen tube tip, limiting the distribution of LePRK1 and LePRK2 on the plasma membrane to maintain the expanding dome shape of pollen tubes.