Identification of two glycerophosphodiester phosphodiesterase genes in maize leaf phosphorus remobilization

Phosphate deficiency is one of the leading causes of crop productivity loss. Phospholipid degradation liberates phosphate to cope with phosphate deficiency. Glycerophosphodiester phosphodiesterases (GPX-PDEs) hydrolyse the intermediate products of phospholipid catabolism glycerophosphodiesters into glycerol-3-phosphate, a precursor of phosphate. However, the function of GPX-PDEs in phosphate remobilization in maize remains unclear. In the present study, we characterized two phosphate deficiency-inducible GPX-PDE genes, ZmGPX-PDE1 and ZmGPX-PDE5, in maize leaves. ZmGPX-PDE1 and ZmGPX-PDE5 were transcriptionally regulated by ZmPHR1, a well-described phosphate starvation-responsive transcription factor of the MYB family. Complementation of the yeast GPX-PDE mutant gde1Δ indicated that ZmGPX-PDE1 and ZmGPX-PDE5 functioned as GPX-PDEs, suggesting their roles in phosphate recycling from glycerophosphodiesters. In vitro enzyme assays showed that ZmGPX-PDE1 and ZmGPX-PDE5 catalysed glycerophosphodiester degradation with different substrate preferences for glycerophosphoinositol and glycerophosphocholine, respectively. ZmGPX-PDE1 was upregulated during leaf senescence, and more remarkably, loss of ZmGPX-PDE1 in maize compromised the remobilization of phosphorus from senescing leaves to young leaves, resulting in a stay-green phenotype under phosphate starvation. These results suggest that ZmGPX-PDE1 catalyses the degradation of glycerophosphodiesters in maize, promoting phosphate recycling from senescing leaves to new leaves. This mechanism is crucial for improving phosphorus utilization efficiency in crops.