ZmMS1/ZmLBD30-orchestrated transcriptional regulatory networks precisely control pollen exine development

Because of its significance for plant male fertility and,hence,direct impact on crop yield,pollen exine development has inspired decades of scientific inquiry.However,the molecularmechanismunderlying exine formation and thickness remains elusive.In this study,we identified that a previously unrecognized repressor,ZmMS1/ZmLBD30,controls proper pollen exine development in maize.Using an ms1 mutant with aberrantly thickened exine,we cloned a male-sterility gene,ZmMs1,which encodes a tapetum-specific lateral organ boundary domain transcription factor,ZmLBD30.Weshowed thatZmMs1/ZmLBD30 is initially turned on by a transcriptional activation cascade of ZmbHLH51-ZmMYB84-ZmMS7,and then it serves as a repressor to shut down this cascade via feedback repression to ensure timely tapetal degeneration and proper level of exine.This activation-feedback repression loop regulating male fertility is conserved in maize and sorghum,and similar regulatory mechanism may also exist in other flowering plants such as rice and Arabidopsis.Collectively,these findings reveal a novel regulatory mechanism of pollen exine development by which a long-sought master repressor of upstream activators prevents excessive exine formation.

ZmMs30 Encoding a Novel GDSL Lipase Is Essential for Male Fertility and Valuable for Hybrid Breeding in Maize

Genic male sterility (GMS) is very useful for hybrid vigor utilization and hybrid seed production. Although a large number of GMS genes have been identified in plants, little is known about the roles of GDSL lipase members in anther and pollen development. Here, we report a maize GMS gene, ZmMs30, which encodes a novel type of GDSL lipase with diverged catalytic residues. Enzyme kinetics and activity assays show that ZmMs30 has lipase activity and prefers to substrates with a short carbon chain. ZmMs30 is specifically expressed in maize anthers during stages 7-9. Loss of ZmMs30 function resulted in defective anther cuticle, irregular foot layer of pollen exine, and complete male sterility. Cytological and lipidomics analyses demonstrate that ZmMs30 is crucial for the aliphatic metabolic pathway required for pollen exine formation and anther cuticle development. Furthermore, we found that male sterility caused by loss of ZmMs30 function was stable in various inbred lines with different genetic background, and that it didn't show any negative effect on maize heterosis and production, suggesting that ZmMs30 is valuable for crossbreeding and hybrid seed production. We then developed a new multi-control sterility system using ZmMs30 and its mutant line, and demonstrated it is feasible for generating desirable GMS lines and valu. able for hybrid maize seed production. Taken together, our study sheds new light on the mechanisms of anther and pollen development, and provides a valuable male-sterility system for hybrid breeding maize.