Transcriptional regulation of plant innate immunity

Abstract

Transcriptional reprogramming is an integral part of plant immunity. Tight regulation of the immune transcriptome is essential for a proper response of plants to different types of pathogens. Consequently, transcriptional regulators are proven targets of pathogens to enhance their virulence. The plant immune transcriptome is regulated by many different, interconnected mechanisms that can determine the rate at which genes are transcribed. These include intracellular calcium signaling, modulation of the redox state, post-translational modifications of transcriptional regulators, histone modifications, DNA methylation, modulation of RNA polymerases, alternative transcription inititation, the Mediator complex and regulation by non-coding RNAs. In addition, on their journey from transcription to translation, mRNAs are further modulated through mechanisms such as nuclear RNA retention, storage of mRNA in stress granules and P-bodies, and post-transcriptional gene silencing. In this review, we highlight the latest insights into these mechanisms. Furthermore, we discuss some emerging technologies that promise to greatly enhance our understanding of the regulation of the plant immune transcriptome in the future.

Keywords: RNA; gene expression and regulation; plant immunity; transcription factors.

Figure 1. Mechanisms involved in the regulation of immune-related transcription

(A) Regulation of calcium (Ca²⁺) influx, which may lead to post-translational modifications of TFs (see also Figure 1E); (B) generation of ROS by RbohD, which may lead to post-translational modifications of TFs (see also Figure 1E); (C) co-factors that may contribute to regulation of transcription; (D) TFs regulate transcription by binding to a motif; (E) post-translational modifications of TFs, such as phosphorylation (P), sumoylation (SUMO), ubiquitination (Ub) and forming of oligomers through S-S bridges depending on the redox state; (F) modifications of histones (methylation [Me] or acetylation [Ac]) to regulate the chromatin state; (G) methylation of DNA; (H) phosphorylation of the C-terminal domain of RNA-polymerase II (PolII) promotes transcription; (I) PolII may initiate transcription at alternative transcription start sites; (J) the Mediator complex forms the bridge between specific TFs, general TFs (GTF) and PolII; (K) selective import of TFs or other proteins; (L) alternative splicing; (M) selective retention of mRNAs in the nucleus; (N) temporary storage of mRNAs in stress granules or P-bodies; (O) degradation of mRNAs from P-bodies; (P) release of mRNAs from stress granules or P-bodies into the cytosol, followed by translation; (Q) post-transcriptional gene silencing by small RNAs; (R) long non-coding RNAs can regulate transcription in different ways, depicted here is modulation of MED19a by ELENA1.

Figure 2. Next-generation toolkit for elucidating immune-responsive GRNs

Integration of data on TF DNA-binding, chromatin accessibility, and gene expression can be employed as a powerful tool to elucidate the highly interconnected gene regulatory networks (GRNs) that determine the plant immune transcriptome, even at single cell resolution. For instance, information related to TF-binding sites can be obtained from chromatin-immunoprecipitation followed by sequencing (ChIP-seq), and DNA affinity purification sequencing (DAP-seq). Information about chromatin status can be derived from methods such as Assay for Transposase-Accessible Chromatin using sequencing (ATAC-seq), micrococcal nuclease digestion with deep-sequencing (MNase-seq), or DNase-I hypersensitive sites sequencing (DNase-seq). Different variants of RNA (e.g. mRNA, miRNA, lncRNA) can be measured by RNA-seq. These data can be integrated to reveal GRNs that shape the plant immune transcriptome. The functionality of these GRNs can be tested and validated by mutant analysis under different conditions or in different tissues or cell types.