Conversations between kingdoms: small RNAs

Abstract

Humans, animals, and plants are constantly under attack from pathogens and pests, resulting in severe consequences on global human health and crop production. Small RNA (sRNA)-mediated RNA interference (RNAi) is a conserved regulatory mechanism that is involved in almost all eukaryotic cellular processes, including host immunity and pathogen virulence. Recent evidence supports the significant contribution of sRNAs and RNAi to the communication between hosts and some eukaryotic pathogens, pests, parasites, or symbiotic microorganisms. Mobile silencing signals—most likely sRNAs—are capable of translocating from the host to its interacting organism, and vice versa. In this review, we will provide an overview of sRNA communications between different kingdoms, with a primary focus on the advances in plant-pathogen interaction systems.

Figure 1

Cross-kingdom gene silencing between animal cell and parasites. Animal cells produce host sRNAs, and selected host miRNAs translocate into intracellularly phagocytized parasites and target parasitic mRNAs. Some mammalian sRNAs are selectively sorted into vesicles for secretion via exocytosis (exosomes). Extracellular parasite cells likely internalize exosomal sRNAs and, in addition, take up extracellular long dsRNAs via cell membrane-associated RNA transporters, SID-1 and SID-2. Long dsRNAs are further processed into mature sRNAs by DCLs; both pathways may trigger gene silencing in the parasite. Parasites encapsulate and secrete parasitic sRNAs that circulate in body fluids of infected individual and are internalized by host cells, triggering parasitic-induced host gene silencing.

Figure 2. Cross-kingdom gene silencing between plants and interacting organisms. Host-induced gene silencing (HIGS) sRNAs are produced via transgenes in plants

(A)HIGS sRNAs translocate into pathogens and suppress virulence mRNAs in pathogenic fungi and oomycetes. We speculate that there are natural host sRNAs that target virulence mRNAs for host defense via similar pathways. Pathogen-derived sRNAs that mimic host sRNAs are translocated into host cells to hijack the host AGO/RISC machinery to suppress host immunity mRNAs. (B) HIGS sRNAs are effective against insect pests by translocating into insect pest cells and silence their virulence genes. Similarly, natural host sRNAs could also potentially target pest mRNAs for silencing. At the same time, pest sRNAs are also likely to be injected into host cells to suppress host immunity or manipulate other cellular pathways. (C) Parasitic plants, such as Cuscuta sp., form haustoria to acquire nutrients from the phloem source. Bi-directional exchange of a large array of mRNAs has been observed. It is likely sRNAs are also transported between hosts and parasitic plants as gene regulators. (D)HIGS sRNAs are effective against plant-parasitic nematodes. It is possible that natural host sRNAs may target nematode mRNAs for defense. On the other hand, nematode-induced gene silencing of host mRNAs is also likely, either via encapsulated or non-vesicular nematode sRNAs. (E) HIGS sRNAs are effective against mRNAs from symbiotic organisms, such as mycorrhiza. Similarly, natural host sRNAs, as well as symbiotic sRNAs, are also likely to be exchanged during the regulation of symbiosis.