Natural variation in the ZmPIMT1 promoter enhances seed aging tolerance by regulating PABP2 repair in maize

PROTEIN L-ISOASPARTYL O-METHYLTRANSFERASE (PIMT) promotes seed vigor by repairing damaged proteins. However, whether PIMT variants have arisen during maize (Zea mays) domestication remains unknown. Here, we found 2 variants in the ZmPIMT1 promoter. The ZmPIMT1 Hap C7-2 promoter exhibited stronger activity than the ZmPIMT1 Hap Z58 promoter. Maize inbred lines carrying the ZmPIMT1 Hap C7-2 promoter had greater seed vigor than ZmPIMT1 Hap Z58 lines in a population of Zhengdan 958 recombinant inbred lines (RILs) and a maize inbred population. By characterizing the maize zmpimt1 knockdown mutant, ZmPIMT1-overexpressing maize and Arabidopsis thaliana heterologous ZmPIMT1 overexpression lines, we demonstrated that ZmPIMT1 positively regulates seed vigor. Co-IP and LC-MS/MS assays showed that ZmPIMT1 interacts with and repairs damaged POLY(A) BINDING PROTEIN2 (PABP2). ZmPIMT1 stabilizes PABP2 RNA-binding activity and regulates the stability and translation efficiency of the mRNA during maize seed germination. Disruption of PABP2 decreases seed vigor in Arabidopsis thaliana. Furthermore, the F-statistics (Fixation index; FST) and nucleotide diversity (θπ) ratio between teosinte and maize lines showed that ZmPIMT1 likely has not undergone selection during maize domestication. Our findings unveil a molecular mechanism in which ZmPIMT1 regulates seed vigor in maize and highlight a potential application of the advantageous ZmPIMT1 haplotype for breeding new varieties with increased seed vigor.