Biogenesis, Trafficking, and Function of Small RNAs in Plants

Abstract

Small RNAs (sRNAs) encoded by plant genomes have received widespread attention because they can affect multiple biological processes. Different sRNAs that are synthesized in plant cells can move throughout the plants, transport to plant pathogens via extracellular vesicles (EVs), and transfer to mammals via food. Small RNAs function at the target sites through DNA methylation, RNA interference, and translational repression. In this article, we reviewed the systematic processes of sRNA biogenesis, trafficking, and the underlying mechanisms of its functions.

Keywords: DNA methylation; RNA interference; biogenesis; functions; small RNA; trafficking; translational repression.

Figure 1

Illustrations of siRNA biogenesis in plants (Ref Borges et al., 2018; Singh et al., 2021). (A) miRNA biogenesis model derived from MIR gene. (B) natsiRNA biogenesis model derived from Cis-antisense gene. (C) hcsiRNA biogenesis model derived from Heterochromatin. (D) vsiRNA biogenesis model derived from Viral/viroid genome. (E) Secondary siRNA biogenesis model derived from Normal gene. Pol: RNA Polymerase; DDL: Dawdle; DCL: RNase III enzyme DICER-LIKE; SE: SERRATE; HYL1: HYPONASTIC LEAVES1; HEN1: HUA ENHANCER 1; RDR: RNA-DEPENDENT RNA POLYMERASE.

Figure 2

Illustrations of siRNA trafficking in plants. (A) Movement between plant cells (Wang and Dean, 2020): Pathway 1, naked small RNAs, small RNAs bound to RNA binding protein (RBP) and small RNAs enclosed in vesicles can pass through plasmodesmata (PD) moves between cells; pathway 2, desmotubules (DM) connects the endoplasmic reticulum (ER) of two adjacent cells, and small RNA can be transported through DM; pathway 3, small RNA can be directly secreted from PM and spread in plants. Note: It is unknown whether vesicles can be transported via DM. (B) Long-distance movement in plants (Tamiru et al., 2018): I: Long-distance movement occurs through the repetitive mechanism of pathways 1 and 2 in the plasmodesmata; II: sRNA enters the phloem sieve tube through the plasmodesmata (PD), and transports it quickly from top to bottom with the phloem sap. (C) Cross-domain transport of sRNA by EV (Huang et al., 2019a): I: Free sRNA in plant cytoplasm can be packaged by Golgi and transported to the outside of the cell to be absorbed by Plant pathogen. At the same time, Plant pathogen also produces sRNA and delivers its own DNA or sRNA to plant cells; II: When vesicles are formed, sRNA needs to be combined with RBPs before it can be selectively loaded into EVs for cross-domain transport. Note: Plant pathogen here is only a type of organism that absorbs vesicles. Many organisms can absorb vesicles provided by plants or produce sRNA and transfer them to plant cells. “?” indicates whether plants can produce MV and whether other organisms can produce EVs is not yet clear; (D) Transfer of sRNA to animal cells: Plants deliver sRNA to the human body through decoction or raw food directly. After different forms of sRNA enter the gut, it is absorbed into the blood through the villi of the small intestine and circulates throughout the body with the blood. Human here refers to mammals. sRNA: small RNA; MVB: multivesicular bodies; sRNPC: sRNA ribonucleoprotein complex; DM: desmotubule; ER: endoplasmic reticulum; CW: cell wall; EV: extracellular vesicles; PM: plasma membrane; PD: plasmodesmata; SE: sieve tube elements; SP: sieve tube plates; MV: microvesicles.

Figure 3

Illustrations of sRNA function. (A) RNA-directed DNA methylation (RdDM) model (Tang, 2020). The scaffold RNAs are produced by Pol V, recruit their complementary sRNA to the RdDM target loci and guides DRM2 to catalyze DNA methylation. (B) sRNA-mediated target mRNA cleavage model. RISC is paired with target mRNAs according to the principle of base complementary pairing. The PIWI domain of AGO proteins has slicer endonuclease activity, and the paired regions are cleaved with the participation of AGO protein. (C) sRNA-mediated translational repression model (Simone et al., 2021): RISC competes with ribosomes for binding to the UTR region of mRNA, which affects the translation process and inhibits the formation of polypeptide chains. RISC: sRNAs carried by RNA-induced silencing complex; UTR: untranslational region; DRM2: DOMAINS REARRANGED METHYLTRANSFERASE 2.