Plastid-localized ZmENR1/ZmHAD1 complex ensures maize pollen and anther development through regulating lipid and ROS metabolism

Lipid metabolism is critical for male reproduction in plants. Many lipid-metabolic genic male-sterility (GMS) genes function in the anther tapetal endoplasmic reticulum, while little is known about GMS genes involved in de novo fatty acid biosynthesis in the anther tapetal plastid. In this study, we identify a maize male-sterile mutant, enr1, with early tapetal degradation, defective anther cuticle, and pollen exine. Using genetic mapping, we clone a key GMS gene, ZmENR1, which encodes a plastid-localized enoyl-acyl carrier protein (ACP) reductase. ZmENR1 interacts with β-hydroxyacyl-ACP dehydratase (ZmHAD1) to enhance the efficiency of de novo fatty acid biosynthesis. Furthermore, the ZmENR1/ZmHAD1 complex is regulated by a Maize Male Sterility 1 (ZmMS1)-mediated feedback repression loop to ensure anther cuticle and pollen exine formation by affecting the expression of cutin/wax- and sporopollenin-related genes. Intriguingly, homologous genes of ENR1 from rice and Arabidopsis also regulate male fertility, suggesting that the ENR1-mediated pathway likely represents a conserved regulatory mechanism underlying male reproduction in flowering plants.