ZmSMR4, a novel cyclin-dependent kinase inhibitor (CKI) gene in maize (Zea mays L.), functions as a key player in plant growth, development and tolerance to abiotic stress.

Endoreduplication is a key cell cycle variant in the developing maize endosperm and has been associated with cell enlargement and dry matter accumulation. Therefore, identification of the key genes associated with endosperm development and endoreduplication would not only lay the groundwork for understanding the biological process of endoreduplication but also be important for maize breeding. Here, we identified 12 putative endoreduplication-related candidate genes as members of the Zea mays L. SIAMESE-RELATED (ZmSMR) gene family and denoted them ZmSMR1-ZmSMR12. Sequence analysis indicated that all the ZmSMR protein sequences exhibited modest sequence similarity to the SIAMESE gene from Arabidopsis. Further analyses suggested that most ZmSMR genes might be associated with the transition from mitosis to endoreduplication because the expression levels of most ZmSMR genes were upregulated in endosperm cells during the phase of switching to an endoreduplication cell cycle. Additionally, the ZmSMRs responded to various abiotic stresses at the transcriptional level. One member of the ZmSMR gene family, the ZmSMR4 (KY946768) gene, was isolated as the first maize endoreduplication-related gene and has been used to develop transgenic Arabidopsis plants. ZmSMR4 was localized to the nucleus and could interact with ZmCDKA and ZmCDKB. Moreover, ZmSMR4 was able to rescue the multicellular trichome phenotype of Arabidopsis sim mutants and enhanced the endoreduplication levels of transgenic Arabidopsis plants. Arabidopsis plants overexpressing ZmSMR4 not only displayed enhanced leaf margin serrations but also showed several interesting breeding phenotypes, such as early blossoming and fuller seeds. Taken together, our data suggest that the ZmSMR4 gene is plant-specific and functions as a key player in the signalling network that controls plant growth, development and responses to abiotic stress by regulating the transition between the mitotic cycle and endoreduplication.