Regulating the Regulators: The Control of Transcription Factors in Plant Defense Signaling

Abstract

Being sessile, plants rely on intricate signaling pathways to mount an efficient defense against external threats while maintaining the cost balance for growth. Transcription factors (TFs) form a repertoire of master regulators in controlling various processes of plant development and responses against external stimuli. There are about 58 families of TFs in plants and among them, six major TF families (AP2/ERF (APETALA2/ethylene responsive factor), bHLH (basic helix-loop-helix), MYB (myeloblastosis related), NAC (no apical meristem (NAM), Arabidopsis transcription activation factor (ATAF1/2), and cup-shaped cotyledon (CUC2)), WRKY, and bZIP (basic leucine zipper)) are found to be involved in biotic and abiotic stress responses. As master regulators of plant defense, the expression and activities of these TFs are subjected to various transcriptional and post-transcriptional controls, as well as post-translational modifications. Many excellent reviews have discussed the importance of these TFs families in mediating their downstream target signaling pathways in plant defense. In this review, we summarize the molecular regulatory mechanisms determining the expression and activities of these master regulators themselves, providing insights for studying their variation and regulation in crop wild relatives (CWR). With the advance of genome sequencing and the growing collection of re-sequencing data of CWR, now is the time to re-examine and discover CWR for the lost or alternative alleles of TFs. Such approach will facilitate molecular breeding and genetic improvement of domesticated crops, especially in stress tolerance and defense responses, with the aim to address the growing concern of climate change and its impact on agriculture crop production.

Keywords: AP2/ERF; MYB; NAC; WRKY; bHLH; bZIP; defense; transcription factor regulations.

Figure 1

Schematic diagram of the representative domain of the six families of transcriptional regulators involved in plant defense. (a) AP2/ERF domain with three β-sheet strands for DNA binding and an α-helix motif. (b) bHLH domain with an N-terminal basic domain for DNA binding, followed by a helix-loop-helix motif that functions in protein-protein interactions or dimerization. (c) MYB domain formed by the presence of one-four helix-turn-helix repeat(s) involve in DNA binding. Different subclasses are characterized by having one-four copies of the repeat. The R2R3-MYB class is shown. (d) NAC domain consisting of 5 sub-domains, three highly conserved (A, C, D) and two diverse (B, E) sub-domains. (e) WRKY domain characterized by having a highly conserved WRKY motif followed by a zinc finger with either a C₂H₂- or C₂HC-type zinc finger. (f) bZIP domain containing an N-terminal basic domain for protein dimerization, which is followed by a leucine zipper region containing up to nine heptad repeats. The sequence of typical DNA target for each family of TFs are indicated in the boxes. aa: amino acids; ERF: ethylene responsive factor; RAV: related to abscisic acid insensitive3 (ABI3)/viviparous1 (VP1); DREB: dehydration-responsive element-binding protein; H1: helix 1; H2: helix 2; H3: helix 3; R2: repeat 2; R3: repeat 3; NAC-BS: NAC binding site; L: Leucine; X₆: any six amino acid residues.

Figure 2

The regulation of transcriptional regulators in defense. Diagram illustrates the regulation of defense transcription factor (TF) family members at different levels. At the transcriptional level, auto- and cross-regulation among members of the same TF family or between members of different TF families forms a regulatory node for their expression (1). Epigenetic changes, such as histone modification and DNA methylation can also direct the genetic regulation and priming of the TF gene expression in response to stress (2). At the post-transcriptional level, many defense regulators are targeted by small RNAs (e.g., miRNA) for precise control of the transcript accumulation (3). In addition, the presence of a characteristic DNA binding domain (Figure 1) and various conserved domains among the TFs mediate various post-translational controls of these regulators through different mechanisms, including protein localization in intracellular membranes (4), interaction and modification with other cellular proteins in the cytoplasm (5), or ubiquitination (6). Regulation and interactions among these TF families control expression of their downstream targets involved in primary and secondary metabolisms, as well as phytohormone production, thereby mediating growth and defense in plants. ER: endoplasmic reticulum.

Figure 3

Flow diagram illustrating a strategy for genetic improvement of domesticated crops through genetic engineering of transcriptional regulators in plant defense. Understanding the structural characteristics of TFs that are important in determining their expression at transcriptional (auto-/cross-regulations), post-transcriptional (miRNA, alternative splicing) and post-translational (protein-protein interactions, localization, modification, and stability) will allow the identification of candidate master regulators for genetic improvement (left). Climate change and domestication of crops will have negative impacts on food security due to limited adaptation and genetic diversity of agricultural crops against stresses. In parallel, with the advance of genome technologies and identification of crop wild relatives (CWR), genome sequencing of CWR will permit the exploration of alternative alleles of potential master regulators in the wild relatives (right). Integrating such information will facilitate the selection of transcriptional regulators for functional studies using various approaches and subsequent improvement of stress tolerance in domesticated crops through transgenic technologies and/or marker assisted breeding.