Evolutionary history of histone demethylase families: distinct evolutionary patterns suggest functional divergence

Background: Histone methylation can dramatically affect chromatin structure and gene expression and was considered irreversible until recent discoveries of two families of histone demethylases, the KDMI (previously LSDI) and JmjC domain-containing proteins. These two types of proteins have different functional domains and distinct substrate specificities. Although more and more KDMI and JmjC proteins have been shown to have histone demethylase activity, our knowledge about their evolution history is limited. Results: We performed systematic phylogenetic analysis of these histone demethylase families and uncovered different evolutionary patterns. The KDMI genes have been maintained with a stable low copy number in most organisms except for a few duplication events in flowering plants. In contrast, multiple genes for JmjC proteins with distinct domain architectures were present before the split of major eukaryotic groups, and experienced subsequent birth-and-death evolution. In addition, distinct evolutionary patterns can also be observed between animal and plant histone demethylases in both families. Furthermore, our results showed that some JmjC subfamilies contain only animal genes with specific demethylase activities, but do not have plant members. Conclusion: Our study improves the understanding about the evolutionary history of KDMI and JmjC genes and provides valuable insights into their functions. Based on the phylogenetic relationship, we discussed possible histone demethylase activities for several plant JmjC proteins. Finally, we proposed that the observed differences in evolutionary pattern imply functional divergence between animal and plant histone demethylases.