Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection

Abstract

Small RNA (sRNA)-induced RNA interference (RNAi) is an important conserved mechanism that modulates gene expression in almost all eukaryotes. Some sRNAs move short distances from cell to cell, while some travel long distances to spread systemically throughout the organism. Recent studies indicate that sRNAs can even move between organisms to induce gene silencing, a phenomenon called “cross-kingdom RNAi”. sRNA trafficking between a pathogen, pest, or symbiont and its respective host can have a significant impact on interaction compatibility. Certain sRNAs were found to travel from pathogens or pests into host cells and suppress host immunity to achieve successful infection in both plants and animals; while sRNAs generated from host cells also translocate into pathogen or parasite cells to inhibit their virulence. Such cross-kingdom RNAi mechanisms enable the development of efficient disease control methods using plant-derived RNAs that target essential genes of pathogens and pests. Moreover, uptake of exogenous RNAs from the environment was recently discovered in certain fungal pathogens, which makes it possible to suppress fungal diseases by directly applying pathogen–targeting RNAs on crops and post-harvested products to avoid extensive chemical treatment and circumvent generating genetically modified plants. This spray-induced gene silencing (SIGS) strategy is environmentally sustainable and friendly, and can be easily adapted to control multiple fungal diseases simultaneously.

Movement of small RNAs in and between plants and fungi

“…Based on studies of small RNA movement in plants and fungi described above, there are several pathways for cross‐kingdom small RNA transportation. Because naked small RNAs can move short and long distances in plants (Hyun et al , ) and can also be taken up by fungal cells (Wang, Thomas, and Jin, ), trafficking during plant–fungus interactions may involve naked small RNAs. For instance, when small RNAs targeting B. cinerea DCL1 and DCL2 genes were directly sprayed to Arabidopsis and tomato, treated plants gained resistance to grey mould disease, suggesting the naked exogenous small RNAs were assimilated into the pathogen and interfered with fungal virulence (Wang et al , ).…”

“…Based on studies of small RNA movement in plants and fungi described above, there are several pathways for cross-kingdom small RNA transportation. Because naked small RNAs can move short and long distances in plants (Hyun et al, 2011) and can also be taken up by fungal cells (Wang, Thomas, and Jin, 2017) .…”

Beyond insects: current status and achievements of RNA interference in mite pests and future perspectives

“…During evolution, a certain balance between herbivores, their plant hosts and pathogens/parasites has been reached. Using RNAi as a gene manipulator, key herbivore genes involved in maintaining this homeostasis could be targeted . We define such RNAi as ‘RNAi plus ’.…”

“…In addition, the RNAi plus approach could also be integrated in current dsRNA delivery strategies. Small RNAs could move within an organism (systemic RNAi), from the environment to the organism (environmental RNAi) and between interacting organisms (cross‐species RNAi), thereby inducing gene silencing in the target organism . This cross‐species RNAi offers interesting delivery possibilities, using for example transgenic plants and micro‐organisms.…”

Synthetic biology approach for plant protection using dsRNA

“…Consistent with the central role of dsRNA in triggering RNAi, numerous studies have shown that plants treated with virus‐specific dsRNA or single‐stranded RNA (ssRNA) molecules that fold into hairpin conformation showed antiviral resistance (Carbonell et al ., ; Gan et al ., ; Konakalla et al ., ; Tenllado and Diaz‐Ruiz, ; Tenllado et al ., ,b; Yin et al ., ). dsRNAs were also shown to be effective against fungi (Koch et al ., ; Wang et al ., , ) and insects (Baum et al ., ; Ghosh et al ., ; Li et al ., ; Luo et al ., ), thus providing important implications for dsRNA‐triggered RNAi as an emerging novel approach for crop protection. RNAi has been deployed for plant protection since it was discovered.…”