The Elaboration of miRNA Regulation and Gene Regulatory Networks in Plant⁻Microbe Interactions

Abstract

: Plants are exposed to diverse abiotic and biotic stimuli. These require fast and specific integrated responses. Such responses are coordinated at the protein and transcript levels and are incorporated into larger regulatory networks. Here, we focus on the evolution of transcriptional regulatory networks involved in plant-pathogen interactions. We discuss the evolution of regulatory networks and their role in fine-tuning plant defense responses. Based on the observation that many of the cornerstones of immune signaling in angiosperms are also present in streptophyte algae, it is likely that some regulatory components also predate the origin of land plants. The degree of functional conservation of many of these ancient components has not been elucidated. However, ongoing functional analyses in bryophytes show that some components are conserved. Hence, some of these regulatory components and how they are wired may also trace back to the last common ancestor of land plants or earlier. Of course, an understanding of the similarities and differences during the evolution of plant defense networks cannot ignore the lineage-specific coevolution between plants and their pathogens. In this review, we specifically focus on the small RNA regulatory networks involved in fine-tuning of the strength and timing of defense responses and highlight examples of pathogen exploitation of the host RNA silencing system. These examples illustrate well how pathogens frequently target gene regulation and thereby alter immune responses on a larger scale. That this is effective is demonstrated by the diversity of pathogens from distinct kingdoms capable of manipulating the same gene regulatory networks, such as the RNA silencing machinery.

Keywords: co-evolution; gene expression; molecular plant pathology; plant evolution; plant immunity; plant pathogens; plant–microbe interaction.

Figure 1

A simplified cladogram of the green lineage; The cladogram is based on a phylogeny recovered by Puttick et al. [23].

Figure 2

The suppression of the RNA silencing machinery of plants by pathogen-encoded RNA Silencing Suppressors: (a) The known effectors that affect host RNA silencing in P. syringae. AvrPto inhibits the association of BRASSINOSTEROID INSENSITIVE 1-associated receptor kinase 1 (BAK1) and FLAGELLIN-SENSITIVE 2 (FLS2), which results in the stabilization of pre-miRNAs and reduces miRNA abundance [10]. HopT1-1 interferes directly with the RNA silencing machinery by inhibiting the function of AGO1 [10]. Nucleotide-binding site-leucine-rich repeats (NBS-LRRs), TRANSPORT INHIBITOR RESPONSE 1 (TIR1) and COP1-interacting protein 4 (CIP4) are known targets of miRNAs that are affected by RNA silencing suppressors of P. syringae. (b) The known RNA silencing suppressors of Phytophthora sp. PSR1, a P. sojae-specific RNA silencing suppressor, interacts with PIP1. PIP1 is required for the correct assembly of the Dicing-bodies, which are the protein complexes that include DCL1. The destabilization of the Dicing-body results in reduced miRNA accumulation. PSR2 is conserved in several Phytophthora species. [94,95]. It binds and inhibits DRB4. DRB4 acts in the phasiRNA pathway, and PSR2 specifically reduces phasiRNAs that are secreted—likely via extracellular vesicles. These phasiRNAs have a target in Phytophthora and targeting impacts the virulence and sporulation of the pathogen [98]. (c) The function of the recently identified RNA silencing suppressor of Puccinia graminis f. sp. tritici (Pgt). PgtSR1 (SR1) negatively regulates siRNA biosynthesis and affects miRNA biogenesis. The miRNAs that were affected had targets that are associated with plant defense signalling, including several defense-associated transcription factors [12].