miRNA Mediated Regulation and Interaction between Plants and Pathogens

Abstract

Plants have evolved diverse molecular mechanisms that enable them to respond to a wide range of pathogens. It has become clear that microRNAs, a class of short single-stranded RNA molecules that regulate gene expression at the transcriptional or post-translational level, play a crucial role in coordinating plant-pathogen interactions. Specifically, miRNAs have been shown to be involved in the regulation of phytohormone signals, reactive oxygen species, and NBS-LRR gene expression, thereby modulating the arms race between hosts and pathogens. Adding another level of complexity, it has recently been shown that specific lncRNAs (ceRNAs) can act as decoys that interact with and modulate the activity of miRNAs. Here we review recent findings regarding the roles of miRNA in plant defense, with a focus on the regulatory modes of miRNAs and their possible applications in breeding pathogen-resistance plants including crops and trees. Special emphasis is placed on discussing the role of miRNA in the arms race between hosts and pathogens, and the interaction between disease-related miRNAs and lncRNAs.

Keywords: arms race; interaction; miRNA; pathogen; plant.

Figure 1

The regulatory network of 22 nucleotides (nt)-long miRNAs and NBS-LRR mRNAs involved in production of phasiRNAs. The 22-nt miRNA guides AGO protein to cleave the target site on the NBS-LRR transcript, triggering dsRNA synthesis mediated by RDR6 (RNA-DEPENDENT RNA POLYMERASES 6) and SGS3 (SUPPRESSOR OF GENE SILENCING 3). dsRNA is subsequently processed by DCL4 (DICER-LIKE 4) and DRB4 (DOUBLE-STRANDED-RNA-BINDING PROTEIN 4) to generate a cluster of 21-nt phased siRNAs (phasiRNAs). These 21-nt phasiRNAs are loaded into AGO proteins, which in turn can lead to NBS-LRR mRNAs cleavage. On the other hand, these siRNAs will depress more new targets.

Figure 2

Hosts and pathogens are engaged in an arms race mediated by sRNAs. In plant–pathogen interactions, plants recognize PAMPs (pathogen-associated molecular pattern) with PRRs (pattern recognition receptor) to trigger innate immunity against most pathogen infections. Pathogens, in turn, secrete effectors including effector proteins and some sRNAs to facilitate infection. Some plant NB-LRR proteins are activated by effector proteins, triggering the second layer of immunity response, the so-called ETI. Additionally, hosts simultaneously export siRNAs and miRNAs to induce cross-kingdom gene silencing in the pathogen. Some plant miRNAs targeting disease resistance genes can be decoyed by certain specific lncRNAs, which attenuates the repression of miRNAs on their targets. EV: extracellular vesicles; TTSS: type Ⅲ secretion system. (Question symbols indicate predicted characteristics that need further mining).