Comparative Analysis of HSF Genes From Secale cereale and its Triticeae Relatives Reveal Ancient and Recent Gene Expansions

Abstract

Plants have evolved sophisticated systems to cope with the environmental stresses, with the heat shock factor (HSF) family proteins composing an integral part of the transcriptional regulation system. Understanding the evolutionary history and functional diversity of HSFs will facilitate improving tolerance of crops to adverse environmental conditions. In this study, genome-wide analysis of Secale cereale identified 31 HSF genes. The total number of HSF genes in S. cereale is larger than that in barley and the three subgenomes of wheat, suggesting it is a valuable resource for mining functional HSFs. Chromosome analysis revealed an uneven distribution of HSF genes among the 7 S. cereale chromosomes, with no HSF gene was detected on chromosome 4. Further interspecies synteny analysis revealed that chromosome reorganization during species-speciation may lead to the escape of HSF genes from the S. cereale chromosome 4. Phylogenetic analysis revealed that S. cereale experienced more HSF gene duplications than barley and the three wheat subgenomes. Expression analysis demonstrated that S. cereale HSF genes showed diverse expression patterns across plant developmental stages and upon drought and freezing treatment, suggesting functional diversity of the gene family. Notably, we detected distinct expression patterns for a recently duplicated HSF gene pair, indicating functional divergence may have occurred between the two genes. The study presents the genome organization, evolutionary features and expression patterns of the S. cereale HSF genes. These results provide new insights into the evolution of HSF genes in Triticeae and may serve as a resource for Triticeae molecular breeding.

Keywords: HSF gene; S. cereale; evolution; functional diversity; stress tolerance.

FIGURE 1

Gene structure, domain composition and chromosome distribution of S. cereale HSF genes. (A). HSF genes in the S. cereale genome were ordered by the phylogeny. Gene structure and domain composition for each gene were shown following the gene name. (B). The number of HSF genes on each chromosome in S. cereale were shown and compared to those of T. aestivum and H. vulgare.

FIGURE 2

Class and subclass division of S. cereale HSF genes. (A). Classification of HSF genes in S. cereale based on protein sequence characteristics. (B). Proportion of different classes and subclasses of HSF genes in S. cereale, H. vulgare, T. aestivum (three subgenomes), O. sativa and A. thaliana respectively.

FIGURE 3

Phylogenetic analysis of HSF genes from S. cereale, H. vulgare, T. aestivum, O. sativa and A. thaliana. (A). A phylogeny of HSF genes from S. cereale, H. vulgare, T. aestivum (three subgenomes), O. sativa and A. thaliana based on the amino acid sequences of the HSF domain. Black brackets indicate a group of orthologous HSFs in Triticeae. The identification of class C Triticeae HSF orthologous group were based on an additional phylogeny provided in Supplementary Figure S2, which is constructed by using the full-length protein sequences encoded by HSFC genes. Black dots on the basal of several lineages indicate ancestral HSF lineages of monocots and dicots. (B). The number of HSF genes from different species in each Triticeae HSF orthologous group. A blue rectangle background indicates the HSF gene and HSF genes from at least one other species are in collinear blocks. A blue triangle indicates one of the HSFs in this orthologous group has a collinear relationship with HSF genes from at least one other species.

FIGURE 4

Expression analysis of HSF genes in S. cereale across different tissues, development stages and different stress treatments.