The divergence and positive selection of the plant-specific BURP-containing protein family

Abstract

BURP domain-containing proteins belong to a plant-specific protein family and have diverse roles in plant development and stress responses. However, our understanding about the genetic divergence patterns and evolutionary rates of these proteins remain inadequate. In this study, 15 plant genomes were explored to elucidate the genetic origins, divergence, and functions of these proteins. One hundred and twenty-five BURP protein-encoding genes were identified from four main plant lineages, including 13 higher plant species. The absence of BURP family genes in unicellular and multicellular algae suggests that this family (1) appeared when plants shifted from relatively stable aquatic environments to land, where conditions are more variable and stressful, and (2) is critical in the adaptation of plants to adverse environments. Promoter analysis revealed that several responsive elements to plant hormones and external environment stresses are concentrated in the promoter region of BURP protein-encoding genes. This finding confirms that these genes influence plant stress responses. Several segmentally and tandem-duplicated gene pairs were identified from eight plant species. Thus, in general, BURP domain-containing genes have been subject to strong positive selection, even though these genes have conformed to different expansion models in different species. Our study also detected certain critical amino acid sites that may have contributed to functional divergence among groups or subgroups. Unexpectedly, all of the critical amino acid residues of functional divergence and positive selection were exclusively located in the C-terminal region of the BURP domain. In conclusion, our results contribute novel insights into the genetic divergence patterns and evolutionary rates of BURP proteins.

Keywords: BURP proteins; functional divergence; hormone response; phylogenetic tree; positive selection; promoter region; segmental duplication; stress response; tandem duplication.

Figure 1

Phylogenetic relationships, exon/intron structure, and motif structures of BURP domain‐containing genes. (A) The neighbor‐joining phylogenetic tree was constructed based on a complete protein sequence alignment of 125 BURP domain‐containing genes, which were identified using MUSCLE and MEGA6. Numbers at the nodes represent bootstrap support (1000 iterations). The color of subclades indicates the four corresponding gene subfamilies. Genes with similar functions clustered together are indicated by filled blue circles; (B) Exon/intron structures of the BURP domain‐containing genes. Yellow boxes: exons; blue boxes: 3ʹ untranslated region; lines: introns. Box and line lengths are scaled based on gene length; (C) MEME motif search results. Conserved motifs are indicated in numbered, colored boxes.

Figure 2

Multiple sequence alignment of several BURP domain‐containing protein sequences. The position of the BURP domain is indicated at the top of each sequence. The sites of two conserved cysteine (C) residues, and four repeats of the cysteine‐histidine motif, which are located in the C‐terminus BURP domain, are indicated by red frames. The critical amino acid sites of adaptive selection and functional divergence are marked by the red stars and blue circles, respectively.