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

Abstract 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 two 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.