Structure, function and networks of transcription factors involved in abiotic stress responses

Abstract

Transcription factors (TFs) are master regulators of abiotic stress responses in plants. This review focuses on TFs from seven major TF families, known to play functional roles in response to abiotic stresses, including drought, high salinity, high osmolarity, temperature extremes and the phytohormone ABA. Although ectopic expression of several TFs has improved abiotic stress tolerance in plants, fine-tuning of TF expression and protein levels remains a challenge to avoid crop yield loss. To further our understanding of TFs in abiotic stress responses, emerging gene regulatory networks based on TFs and their direct targets genes are presented. These revealed components shared between ABA-dependent and independent signaling as well as abiotic and biotic stress signaling. Protein structure analysis suggested that TFs hubs of large interactomes have extended regions with protein intrinsic disorder (ID), referring to their lack of fixed tertiary structures. ID is now an emerging topic in plant science. Furthermore, the importance of the ubiquitin-proteasome protein degradation systems and modification by sumoylation is also apparent from the interactomes. Therefore; TF interaction partners such as E3 ubiquitin ligases and TF regions with ID represent future targets for engineering improved abiotic stress tolerance in crops.

Figure 1

Gene regulatory networks of plant transcription factors (TFs) in plant abiotic stress responses and abscisic acid-dependent gene expression. (A) Drought, salt, osmotic stress, temperature, and ABA stress factors modulating the level and activity of the TF (B) and their target genes (C). ABA-dependent signaling pathway can involve TF phosphorylation through the PYR/PYL/RCAR ABA receptor [15]. (B) The boxes represent TF proteins from the model plant Arabidopsis or from different crop plants. Red boxes and lines show that the TF is associated with ABA-signaling. For TF and target genes with several names only one of the names is shown. For references and abbreviations used see the main text. (C) The direct target genes are divided into regulatory genes including TF genes and stress-responsive genes encoding functional proteins. The Gene Ontology (GO) molecular function term is shown as a circle with color code below each Arabidopsis target gene. The GO molecular function annotation was obtained using the Gene Ontology search tool [16] at The Arabidopsis Information Resource. Green arrows and red bars denote TF activation and repression, respectively. Some target genes with no known GO-based molecular function were grouped (i.e., PR1 and PR5, Atrboh A and Atrboh E, SAUR20 and SAUR63, but also rice genes involved in ROS/H₂O₂ homeostasis, such as OsGSTU2).

Figure 2

Structure of well-studied members of the bZIP, AP2/ERF, NAC, WRKY, C2H2 ZF, HTH and bHLH TF families. (I) Tertiary structure of the TF family designating DBD in complex with DNA. (II) Schematic primary structure drawn to scale and disorder predictions for a selected TF. (III) Regions involved in protein-protein interactions and post-translational modifications. (A) X-ray structure of the bZIP DBD from mouse CREB (PDB accession code 1DH3) and schematic representation of the bZIP TF ABI5. (B) NMR structure of the ERF DBD from Arabidopsis ERF1 (1GCC) and schematic representation of the AP2/ERF TF DREB2A. (C) X-ray structure of the NAC DBD from Arabidopsis ANAC019 (3SWP) and schematic structure of ANAC019. (D) NMR structure of the WRKY DBD from Arabidopsis WRKY4 (2LEX) and schematic representation of WRKY40. (E) X-ray structure of the C2H2 ZF DBD from mouse Zif268 and schematic representation of Zat7. (F) NMR structure of the HTH domain, part of the MYB DBD, from human TRF2 and schematic representation of MYB15. (G) X-ray structure of the bHLH DBD from mouse MyoD and schematic representation of ICE1.

Figure 3

Arabidopsis interaction networks with different abiotic stress-related TFs as hub. The interactomes are visualized from the N-Browse viewer (http://www.arabidopsis.org/tools/nbrowse.jsp) [169] with manual modifications as indicated below (A) ABI5 interactome; (B) DREB2A interactome with addition of SRO1; (C) ANAC019 interactome; (D) WRKY40 interactome with addition of CHLH/ABAR; (E) Zat7 interactome; (F) MYB15 interactome; (G) ICE1 interactome.