The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers

Abstract

In plants, oxidative stress and metabolic reprogramming frequently induce male sterility, however our knowledge of the underlying molecular mechanism is far from complete. Here, a maize genic male-sterility (GMS) mutant (ms33-6038) with a loss-of-function of the ZmMs33 gene encoding glycerol-3-phosphate acyltransferase 6 (GPAT6) displayed severe deficiencies in the development of a four-layer anther wall and microspores and excessive reactive oxygen species (ROS) content in anthers. In ms33-6038 anthers, transcriptome analysis identified thousands of differentially expressed genes that were functionally enriched in stress response and primary metabolism pathways. Further investigation revealed that 64 genes involved in ROS production, scavenging, and signaling were specifically changed in expression levels in ms33-6038 anthers compared to the other five investigated GMS lines. The severe oxidative stress triggered premature tapetal autophagy and metabolic reprogramming mediated mainly by the activated SnRK1-bZIP pathway, as well as the TOR and PP2AC pathways, proven by transcriptome analysis. Furthermore, 20 reported maize GMS genes were altered in expression levels in ms33-6038 anthers. The excessive oxidative stress and the metabolic reprogramming resulted in severe phenotypic deficiencies in ms33-6038 anthers. These findings enrich our understanding of the molecular mechanisms by which ROS and metabolic homeostasis impair anther and pollen development in plants.