Genome-Wide Analysis of the Oat (Avena sativa) HSP90 Gene Family Reveals Its Identification, Evolution, and Response to Abiotic Stress

Abstract

Oats (Avena sativa) are an important cereal crop and cool-season forage worldwide. Heat shock protein 90 (HSP90) is a protein ubiquitously expressed in response to heat stress in almost all plants. To date, the HSP90 gene family has not been comprehensively reported in oats. Herein, we have identified twenty HSP90 genes in oats and elucidated their evolutionary pathways and responses to five abiotic stresses. The gene structure and motif analyses demonstrated consistency across the phylogenetic tree branches, and the groups exhibited relative structural conservation. Additionally, we identified ten pairs of segmentally duplicated genes in oats. Interspecies synteny analysis and orthologous gene identification indicated that oats share a significant number of orthologous genes with their ancestral species; this implies that the expansion of the oat HSP90 gene family may have occurred through oat polyploidization and large fragment duplication. The analysis of cis-acting elements revealed their influential role in the expression pattern of HSP90 genes under abiotic stresses. Analysis of oat gene expression under high-temperature, salt, cadmium (Cd), polyethylene glycol (PEG), and abscisic acid (ABA) stresses demonstrated that most AsHSP90 genes were significantly up-regulated by heat stress, particularly AsHSP90-7, AsHSP90-8, and AsHSP90-9. This study offers new insights into the amplification and evolutionary processes of the AsHSP90 protein, as well as its potential role in response to abiotic stresses. Furthermore, it lays the groundwork for understanding oat adaptation to abiotic stress, contributing to research and applications in plant breeding.

Keywords: HSP90; expression pattern; heat shock protein; oat; phylogenetic analysis.

Figure 1

Chromosomal localization of members of the oat HSP90 gene family. Blue to yellow colors within the chromosomes indicate increased gene density. Chromosome numbers are shown at the right of the vertical bar; gene locations are shown at the left of the vertical bar.

Figure 2

Phylogenetic tree analysis of the HSP90 proteins from A. sativa, A. insularis, A. longiglumis, Arabidopsis thaliana, Brachypodium disachyon, rice, and maize. The HSP90s were divided into six clades (Clades 1–6) based on the clustering of the protein sequence. The proteins from A. sativa, A. insularis, A. longiglumis, Arabidopsis thaliana, Brachypodium disachyon, rice, and maize are presented in brown, blue, dark orange, dark blue, green, gray, and dark green, respectively.

Figure 3

Phylogenetic tree, motif analysis, and gene structure of AsHSP90: (A) Phylogenetic tree analysis of the AsHSP90 protein. (B) Motif composition of AsHSP90. (C) Gene structure of the AsHSP90 genes in oats.

Figure 4

Gene duplications of the oat HSP90 gene family. Red lines indicate duplicated gene pairs in AsHSP90, and gray lines indicate co-linear gene pairs in the genome.

Figure 5

Synteny analysis of AsHSP90s in A. sativa and four representative plants. (A) All AsHSP90 synteny genes in oats and in Oryza sativa, A. longiglumis, Brachypodium distachyon, and A. insularis are indicated by red lines. The synteny blocks in the oats and the other species are shown in gray lines. (B) The nine AsHSP90 genes with covariance in the four species are shown as purple, blue, yellow, and green lines.

Figure 6

Distribution of cis-elements upstream of oat AsHSP90: (A) Distribution of types and numbers of cis-elements in the promoter of the oat AsHSP90 genes. (B) Classification and proportion of cis-elements in the AsHSP90 gene.

Figure 7

The relative expression of 20 AsHSP90 genes in oat leaves was detected with qRT-PCR after treatments of 0 h (CK), 3 h, 6 h, 12 h, and 48 h under different abiotic stresses. Error bars indicate the standard error (SE) between three replicates.