Deep evaluation of the evolutionary history of the Heat Shock Factor (HSF) gene family and its expansion pattern in seed plants

PeerJ. 2022 Aug 9:10:e13603. doi: 10.7717/peerj.13603. eCollection 2022.

Abstract

Heat shock factor (HSF) genes are essential in some of the basic developmental pathways in plants. Despite extensive studies on the structure, functional diversification, and evolution of HSF genes, their divergence history and gene duplication pattern remain unknown. To further illustrate the probable divergence patterns in these subfamilies, we analyzed the evolutionary history of HSF genes using phylogenetic reconstruction and genomic syntenic analyses, taking advantage of the increased sampling of genomic data from pteridophytes, gymnosperms and basal angiosperms. We identified a novel clade that includes HSFA2, HSFA6, HSFA7, and HSFA9 with a complex relationship, which is very likely due to orthologous or paralogous genes retained after frequent gene duplication events. We hypothesized that HSFA9 derives from HSFA2 through gene duplication in eudicots at the ancestral state, and then expanded in a lineage-specific way. Our findings indicate that HSFB3 and HSFB5 emerged before the divergence of ancestral angiosperms, but were lost in the most recent common ancestors of monocots. We also presumed that HSFC2 derives from HSFC1 in ancestral monocots. This work proposes that during the radiation of flowering plants, an era during which there was a differentiation of angiosperms, the size of the HSF gene family was also being adjusted with considerable sub- or neo-functionalization. The independent evolution of HSFs in eudicots and monocots, including lineage-specific gene duplication, gave rise to a new gene in ancestral eudicots and monocots, and lineage-specific gene loss in ancestral monocots. Our analyses provide essential insights for studying the evolutionary history of this multigene family.

Keywords: Diversification; Gene family evolution; Heat shock factor; Lineage-specific expansions; Whole genome duplication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Gene Duplication*
  • Heat-Shock Response
  • Magnoliopsida* / genetics
  • Phylogeny
  • Seeds

Grants and funding

This work was supported by National Natural Scientific Foundation of China (Grant No. 31870206, 31670369), the Innovation of Science and Technology Commission of Shenzhen Foundation (Grant No. JCYJ201206151530054), the Scientific Research Foundation of Fairy Lake Botanical Garden and the Scientific Research Program of Sino-Africa Joint Research Center (Grant No. SAJL201607). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.