Divergence and Conservative Evolution of XTNX Genes in Land Plants

Abstract

The Toll-interleukin-1 receptor (TIR) and Nucleotide-binding site (NBS) domains are two major components of the TIR-NBS-leucine-rich repeat family plant disease resistance genes. Extensive functional and evolutionary studies have been performed on these genes; however, the characterization of a small group of genes that are composed of atypical TIR and NBS domains, namely XTNX genes, is limited. The present study investigated this specific gene family by conducting genome-wide analyses of 59 green plant genomes. A total of 143 XTNX genes were identified in 51 of the 52 land plant genomes, whereas no XTNX gene was detected in any green algae genomes, which indicated that XTNX genes originated upon emergence of land plants. Phylogenetic analysis revealed that the ancestral XTNX gene underwent two rounds of ancient duplications in land plants, which resulted in the formation of clades I/II and clades IIa/IIb successively. Although clades I and IIb have evolved conservatively in angiosperms, the motif composition difference and sequence divergence at the amino acid level suggest that functional divergence may have occurred since the separation of the two clades. In contrast, several features of the clade IIa genes, including the absence in the majority of dicots, the long branches in the tree, the frequent loss of ancestral motifs, and the loss of expression in all detected tissues of Zea mays, all suggest that the genes in this lineage might have undergone pseudogenization. This study highlights that XTNX genes are a gene family originated anciently in land plants and underwent specific conservative pattern in evolution.

Keywords: XTNX genes; evolution; function divergence; land plants; plant disease resistance genes.

FIGURE 1

Identification and distribution of the XTNX genes across green plants. The phylogenetic relationship and WGD/WGT events were inferred from (Ruhfel et al., 2014; Panchy et al., 2016; Feng et al., 2017; Van de Peer et al., 2017; Xu et al., 2017). The total number of XTNX genes and their classifications in each species are shown.

FIGURE 2

Phylogenetic analysis of the XTNX genes from 51 land plants. An ML tree was constructed by taking the alignment of all coding sequences as input. The support values (SH-aLRT value) for basal nodes are indicated. Genes belonging to clades I, IIa, and IIb are shown in different colors.

FIGURE 3

The motif composition of the XTNX genes on the background of their phylogenetic relationship. The phylogenetic relationship of all XTNX genes are displayed as determined in Figure 2. A total of 50 motifs were identified from 143 full-length XTNX amino acid sequences. For each gene, the identified motifs were arranged according to the order they occur in the amino acid sequence, as indicated in the bottom of the panel. A colored box indicates presence of a motif, whereas a white box indicates its absence. Detailed information on the 50 motifs is provided in the Supplementary Table S5.

FIGURE 4

Syntenic analysis of the XTNX genes in Fabaceae and Brassicaceae species. (A) Two rounds of WGDs resulted in the XTNX genes in legume species. Collinearity between two Phaseolus vulgaris blocks containing two XTNX genes (02G158300 and 02G291100) resulted from the ancient WGD in the common ancestor of legume, whereas another collinearity block pair containing XTNX genes from soybean (chromosomes 01G versus 11G, and chromosomes 05G versus 08G) resulted from a soybean-specific WGD event. (B) Rapid loss of XTNX duplicons after the WGT in the Brassica rapa genome. Among the three chromosomal blocks that resulted from WGT in B. rapa, two of these have lost the XTNX genes within the blocks.

FIGURE 5

Expression of XTNX genes in different tissues of three angiosperms. The relative expression of XTNX genes in (A) Arabidopsis thaliana, (B) Zea mays, and (C) soybean.