Exchange of Small Regulatory RNAs between Plants and Their Pests

Abstract

Regulatory small RNAs are well known as antiviral agents, regulators of gene expression, and defenders of genome integrity in plants. Several studies over the last decade have also shown that some small RNAs are exchanged between plants and their pathogens and parasites. Naturally occurring trans-species small RNAs are used by host plants to silence mRNAs in pathogens. These gene-silencing events are thought to be detrimental to the pathogen and beneficial to the host. Conversely, trans-species small RNAs from pathogens and parasites are deployed to silence host mRNAs; these events are thought to be beneficial for the pests. The natural ability of plants to exchange small RNAs with invading eukaryotic organisms can be exploited to provide disease resistance. This review gives an overview of the current state of trans-species small RNA research in plants and discusses several outstanding questions for future research. SMALL REGULATORY RNA BACKGROUND Small regulatory RNAs (sRNAs) are numerous in plants. They usually range in size from 21 to 24 nucleotides and serve as key regulators of gene expression. sRNAs are involved in myriad processes, including development, cell type designation, responses to abiotic stress, and silencing of repetitive elements. sRNAs are processed from longer precursor RNAs (either the helical stem regions of self-complementary singlestranded RNAs or double-stranded RNAs [dsRNAs]) by endonucleases in the Dicer-like (DCL) protein family. DCL endonucleases produce an initial short duplex RNA. One of the two short RNA strands forms a complex with a protein in the Argonaute (AGO) family. The AGO-sRNA complex then identifies target RNAs based on complementarity between target and sRNA. sRNAs can be categorized based on differences in their biogenesis and differences in their modes of targeting (Fig. 1). MicroRNAs (miRNAs) in plants are processed from RNA polymerase II-transcribed primary RNAs. A region of the primary transcript forms an imperfect hairpin structure that is recognized by the DCL1 endonuclease. DCL1, along with several accessory proteins, liberates a miRNA/miRNA* duplex. The duplex is disassembled, with the mature miRNA becoming bound to an Argonaute (AGO) protein, most frequently AGO1. Once the mature miRNA is bound to an AGO protein, the miRNA* is typically separated from the complex and degraded (for a more detailed review of plant miRNA biogenesis, see Rogers and Chen, 2013). The resulting miRNA/AGO complex directs posttranscriptional regulation of mRNAs and long noncoding RNAs. Target selection is primarily based on complementarity between the miRNA and target RNA

Extracellular vesicles from Heligmosomoides bakeri and Trichuris muris contain distinct microRNA families and small RNAs that could underpin different functions in the host

“…S3 ). There is emerging data suggesting sRNAs from repetitive regions and transposable elements can in fact act as virulence factors in diverse parasite-host models including plant-parasite interactions ( Cai et al, 2019 , Dunker et al, 2020 , Hudzik et al, 2020 ). These classes of extracellular sRNAs that are found across diverse nematodes and other helminths therefore merit further attention.…”

Who Rules the Cell? An Epi-Tale of Histone, DNA, RNA, and the Metabolic Deep State

“…Along with the thinking of diets in humans being linked to epigenetics and diseases, one wonders whether plants metabolites, liberated after being ingested by the organism, can directly be used by the animal epi-genome as well. This hypothetical scenario is plausible; it would be analogous to horizontal gene transfer (bacteria taking up free DNA) or interspecific exchanges of small regulatory RNAs between pathogens and plants [for an example, see (Hudzik et al, 2020)].…”

The Dynamic Kaleidoscope of RNA Biology in Plants

“…These are synthesized by RNAPII and processed by Dicer-like (DCL) endonucleases to produce a miRNA/miRNA* duplex, which is further modified before assembly into an Argonaute (AGO) protein. This RNA-protein complex guides the posttranscriptional regulation of complementary transcripts, influencing transcript abundance through endonucleolytic cleavage and in some cases limiting translation (Rogers and Chen, 2013;Hudzik et al, 2020). The small-interfering RNA (siRNA) class of sRNAs can be powerful transcriptional gene silencers of viruses, inappropriately expressed transgenes, and transposable elements, through RNA-directed DNA methylation pathway amplification (Borges and Martienssen, 2015).…”

“…The topic of transspecies transfer of small regulatory RNAs is the focus of a valuable Update (Hudzik et al, 2020). Gene silencing by siRNAs is an essential component of plant defense from viruses, invasive fungi, and oomycetes.…”