Genome-wide identification of HSP90 gene family in Rosa chinensis and its response to salt and drought stresses

Abstract

Heat shock protein 90 (HSP90) is important for many organisms, including plants. Based on the whole genome information, the gene number, gene structure, evolutionary relationship, protein structure, and active site of the HSP90 gene family in Rosa chinensis and Rubus idaeus were determined, and the expression of the HSP90 gene under salt, and drought stresses in two rose varieties Wangxifeng and Sweet Avalanche were analyzed. Six and eight HSP90 genes were identified from R. chinensis and Ru. idaeus, respectively. Phylogenetic analysis revealed that the analyzed genes were divided into two Groups and four subgroups (Classes 1a, 1b, 2a, and 2b). Although members within the same classes displayed highly similar gene structures, while the gene structures and conserved domains of Group 1 (Class 1a and 1b) and the Group 2 (Class 2a and 2b) are different. Tandem and segmental duplication genes were found in Ru. idaeus, but not in R. chinensis, perhaps explaining the difference in HSP90 gene quantity in the two analyzed species. Analysis of cis-acting elements revealed abundant abiotic stress, photolight-response, and hormone-response elements in R. chinensis HSP90s. qRT-PCR analysis suggested that RcHSP90-1-1, RcHSP90-5-1 and RcHSP90-6-1 in Sweet Avalanche and Wangxifeng varieties played important regulatory roles under salt and drought stress. The analysis of protein structure and active sites indicate that the potential different roles of RcHSP90-1-1, RcHSP90-5-1, and RcHSP90-6-1 in salt and drought stresses may come from the differences of corresponding protein structures and activation sites. These data will provide information for the breeding of rose varieties with high stress resistance.

Supplementary information: The online version contains supplementary material available at 10.1007/s13205-024-04052-0.

Keywords: Abiotic stress; HSP90 gene family; Protein active site; Relative expression; Rosa chinensis.

Fig. 1

Phylogenetic relationship analysis of 28 HSP90 proteins from Oryza sativa, Arabidopsis thaliana, Rosa chinensis, and Rubus idaeus. The diverse classes of HSP90 proteins are marked with different colors. The HSP90 proteins of Oryza sativa (Os), Arabidopsis thaliana (At), Rosa chinensis (Rc), and Rubus idaeus (Ri) were represented by green circles, blue checkmarks, red stars, and green checkmarks, respectively. Gene IDs of all the analyzed genes are presented in Table S2

Fig. 2

Location, homologous gene pairs, and tandem duplication of HSP90 genes in Rosa chinensis and Rubus idaeus. All HSP90 genes were mapped to their respective loci in Rosa chinensis (A) and Rubus idaeus (B). MCScanX software was used to analyze tandem duplication and homologous gene pairs. The genes in blue font indicate genes are generated through tandem repeats, while the genes at both ends of the red line are homologous gene pairs

Fig. 3

Macro-collinearity analysis of HSP90 genes between Oryza sativa, Arabidopsis thaliana, Rosa chinensis, and Rubus idaeus. Collinearity relationships are shown between two adjacent species. Gray lines in the background indicate the collinear blocks within different genomes and the red lines highlight the syntenic HSP90 gene pairs

Fig. 4

Conserved motifs and gene structure of HSP90 genes in different species. A Phylogenetic tree constructed using the neighbor-joining method with 1000 bootstrap replicates by MEGA X software. B Motif composition of HSP90 proteins. (C) Exon–intron structure of HSP90s. Yellow boxes indicate exons and black lines indicate introns

Fig. 5

Analysis of cis-acting elements

Fig. 6

Heatmap of expression profiling of rose HSP90 genes under different stress. The color scale bar represents the expression values (in log2-based tags per million values) of the genes. The values in square frames represent the tags per million values. T, Salt tolerant varieties; F, Salt sensitive varieties

Fig. 7

Expression analysis of RcHSP90s by qRT-PCR. Error bars indicate the standard error. Asterisks indicate significant differences (assessed using Duncan’s honestly significant difference test), **P < 0.01. All the raw data for qRT-PCR are listed in Table S3

Fig. 8

Protein structure and active sites of Class 1a. Purple amino acid markers represent protein active sites