Functional diversification of tomato HsfA1 factors is based on DNA binding domain properties

Gene. 2019 Sep 25;714:143985. doi: 10.1016/j.gene.2019.143985. Epub 2019 Jul 19.

Abstract

In all eukaryotes, the response to heat stress (HS) is dependent on the activity of HS transcription factors (Hsfs). Plants contain a large number of Hsfs, however, only members of the HsfA1 subfamily are considered as master regulators of stress response and thermotolerance. In Solanum lycopersicum, among the four HsfA1 members, only HsfA1a has been proposed to possess a master regulator function. We performed a comparative analysis of HsfA1a, HsfA1b, HsfA1c and HsfA1e at different levels of regulation and function. HsfA1a is constitutively expressed under control and stress conditions, while the other members are induced in specific tissues and stages of HS response. Despite that all members are localized in the nucleus when expressed in protoplasts, only HsfA1a shows a wide range of basal activity on several HS-induced genes. In contrast, HsfA1b, HsfA1c, and HsfA1e show only high activity for specific subsets of genes. Domain swapping mutants between HsfA1a and HsfA1c revealed that the variation in that transcriptional transactivation activity is due to differences in the DNA binding domain (DBD). Specifically, we identified a conserved arginine (R107) residue in the turn of β3 and β4 sheet in the C-terminus of the DBD of HsfA1a that is highly conserved in plant HsfA1 proteins, but is replaced by leucine and cysteine in tomato HsfA1c and HsfA1e, respectively. Although not directly involved in DNA interaction, R107 contributes to DNA binding and consequently the activity of HsfA1a. Thus, we demonstrate that this variation in DBD in part explains the functional diversification of tomato HsfA1 members.

Keywords: Co-activator; DNA binding; Heat shock protein; High temperature; Solanum lycopersicum; Transcription.

MeSH terms

  • Arabidopsis Proteins / genetics*
  • DNA-Binding Proteins / genetics*
  • Gene Expression Regulation, Plant / genetics
  • Heat Shock Transcription Factors / genetics*
  • Heat-Shock Proteins / genetics
  • Heat-Shock Response / genetics
  • Hot Temperature
  • Lycopersicon esculentum / genetics*
  • Plant Proteins / genetics*
  • Protein Domains / genetics
  • Protoplasts / physiology
  • Temperature
  • Thermotolerance / genetics
  • Transcription, Genetic / genetics
  • Transcriptional Activation / genetics

Substances

  • Arabidopsis Proteins
  • DNA-Binding Proteins
  • Heat Shock Transcription Factors
  • Heat-Shock Proteins
  • HsfA1a protein, Arabidopsis
  • Plant Proteins