Phospholipid homeostasis and gametophyte development require the glycerophosphodiester phosphodiesterases GDPD5 and GDPD6

Glycerophosphodiester phosphodiesterases (GDPDs) hydrolyze glycerophosphodiesters, phospholipid metabolites generated by acyl hydrolases. We analyzed the function of the two related proteins GDPD5 and GDPD6 from Arabidopsis (Arabidopsis thaliana), which are expressed during phosphate starvation and in flower organs. Heterologously expressed GDPD5 and GDPD6 hydrolyzed glycerophosphocholine and other glycerophosphodiesters, indicating that they are involved in the turnover of phosphatidylcholine (PC). The membrane lipid composition in leaves and roots of single gdpd5 or gdpd6 mutants was not altered during growth under normal conditions and phosphate starvation, suggesting that GDPD5 and GDPD6 are not involved in phospholipid turnover under phosphate starvation. After crossing gdpd5 and gdpd6 null mutants, no double homozygous (g5g5 g6g6) plants were obtained. Genetic analyses of the F1 progeny after selfing, or reciprocal crosses of G5g5 G6g6 with WT plants, revealed that the double heterozygous plants cannot produce viable female or male gametes with the haplotypes G5G6 or g5g6. About 50% of the seeds of G5g5 G6g6 plants were aborted. The development of microspores was affected, and ∼50% of pollen grains were distorted and lacked organelles. The anthers of G5g5 G6g6 plants showed decreased PC content, indicating that GDPD5 and GDPD6 are essential for PC homeostasis. Therefore, compromised PC homeostasis affects membrane biogenesis during sporogenesis and gametogenesis, compromising ovule and pollen viability in G5g5 G6g6 plants.