Evolutionary History and Functional Diversification of the JmjC Domain-Containing Histone Demethylase Gene Family in Plants

Abstract

Histone demethylases containing JumonjiC (JmjC) domains regulate gene transcription and chromatin structure by changing the methylation status of lysine residues and play an important role in plant growth and development. In this study, a total of 332 JmjC family genes were identified from 21 different plant species. The evolutionary analysis results showed that the JmjC gene was detected in each species, that is, the gene has already appeared in algae. The phylogenetic analysis showed that the KDM3/JHDM2 subfamily genes may have appeared when plants transitioned from water to land, but were lost in lycophytes (Selaginella moellendorffii). During the evolutionary process, some subfamily genes may have been lost in individual species. According to the analysis of the conserved domains, all of the plant JmjC genes contained a typical JmjC domain, which was highly conserved during plant evolution. The analysis of cis-acting elements showed that the promoter region of the JmjC gene was rich in phytohormones and biotic and abiotic stress-related elements. The transcriptome data analysis and protein interaction analyses showed that JmjC genes play an important role in plant growth and development. The results clarified the evolutionary history of JmjC family genes in plants and lay the foundation for the analysis of the biological functions of JmjC family genes.

Keywords: JmjC gene; growth and development; histone demethylation; phylogeny; stress response.

Figure 1

Phylogenetic relationships among 21 species. Different background colors in the phylogenetic tree show different pedigrees. The right side shows the number of JmjC genes in each species of the different subfamilies and the total number of JmjC genes found in the genome of each species.

Figure 2

Phylogenetic tree of JmjC proteins in 21 plant species. JmjCs are divided into five subfamilies, which are represented by arcs of different colors. The lines of different colors in the evolutionary tree represent the JmjCs of 10 different lineages. The color of the pie chart in the figure corresponds to the color of the JmjCs in the evolutionary tree.

Figure 3

Conserved amino acid residues of JmjC protein in plants. The height of each letter in the figure indicates the degree of conservation of amino acid residues. The number on the abscissa indicates the relative position of the amino acid in the motif. The three conserved catalytic residues of Fe (II) (His 188, Glu/Asp 190, and His 276) are marked with red triangles. The two conserved catalytic residues of α-KG (Ther/Phe 185 and Lys 206) are marked with black triangles.

Figure 4

Analysis of promoter cis-elements of JmjC genes in plants. The left side of the heatmap is the evolutionary history of 21 species. Green, red, and yellow boxes represent cis-elements related to phytohormone responses, biotic and abiotic stresses, and plant growth and development, respectively. The histogram indicates the number of cis-acting elements of different types in each species.

Figure 5

Expression profiles of the JmjC genes in different tissues and developmental stages of A. thaliana. On the left is the phylogenetic tree of Arabidopsis JmjCs.

Figure 6

Functional network assembly of the A. thaliana JmjC proteins. Red letters are the A. thaliana protein. Light blue and purple lines represent known interactions determined by the database and experiments, respectively. Green, red, and blue lines represent predicted interactions from gene proximity, fusion, and symbiosis, respectively. Light green, black, and gray lines indicate other interactions from text mining, co-expression, and protein homology, respectively. Empty nodes: proteins of unknown three-dimensional structure. Filled nodes: some three-dimensional structures are known or predicted.