Bioenergetics of pollen tube growth in Arabidopsis thaliana revealed by ratiometric genetically encoded biosensors

Abstract

Pollen tube is the fastest-growing plant cell. Its polarized growth process consumes a tremendous amount of energy, which involves coordinated energy fluxes between plastids, the cytosol, and mitochondria. However, how the pollen tube obtains energy and what the biological roles of pollen plastids are in this process remain obscure. To investigate this energy-demanding process, we developed second-generation ratiometric biosensors for pyridine nucleotides which are pH insensitive between pH 7.0 to pH 8.5. By monitoring dynamic changes in ATP and NADPH concentrations and the NADH/NAD+ ratio at the subcellular level in Arabidopsis (Arabidopsis thaliana) pollen tubes, we delineate the energy metabolism that underpins pollen tube growth and illustrate how pollen plastids obtain ATP, NADPH, NADH, and acetyl-CoA for fatty acid biosynthesis. We also show that fermentation and pyruvate dehydrogenase bypass are not essential for pollen tube growth in Arabidopsis, in contrast to other plant species like tobacco and lily.