Cross-kingdom small RNA communication between plants and fungal phytopathogens-recent updates and prospects for future agriculture

Abstract

Small RNAs (sRNAs) are short non-coding regulatory RNA sequences that silence the complementary expressive transcripts through an endogenous RNA mediated interference mechanism (RNAi). These sRNAs typically move through plasmodesmata and phloem in plants to support disease resistance, and also through septal pores and vesicles in fungi to act as effector of pathogenicity. Notably, recent reports have shown the occurrence of a bidirectional trafficking of these sRNAs between the host plants and the attacking fungal phytopathogen which have significant implication in the nature of the infection. While the trans-species sRNAs from the pathogen can silence the host mRNAs and inhibit the host immunity genes, the sRNA modules from the host plants can silence the mRNA in the pathogen by impeding the expression of the pathogenicity-related genes. In the present review, we discuss the current state of sRNA trafficking between the plant and the pathogen with special emphasis on the mechanism of cross-kingdom communication which could contribute to the development of pathogen and pest control in future agriculture.

The roles of small RNAs in rice-brown planthopper interactions

“…Host-induced gene silencing (HIGS) is a novel concept based on the cross-kingdom RNAi mechanism. HIGS involves overexpressing insect-targeted double-stranded RNAs (dsRNAs) or artificial miRNAs in host plants to specifically block the expression of feeding-and survival-related genes in target pests and pathogens (Huang et al, 2019;Jiang et al, 2023;Mahanty et al, 2023) (Figure 1A). A growing number of studies have demonstrated the successful application of HIGS in crop protection (Escobar et al, 2001;Seemanpillai et al, 2003;Zha et al, 2011;Van et al, 2014;Coleman et al, 2015;Shivakumara et al, 2017;Panwar et al, 2018).…”

“…Although allowing insects to feed on plants overexpressing exogenous dsRNA was not as effective as injecting insects directly, HIGS remains a promising pest control strategy. However, the implementation of HIGS depends on the generation of transgenic plants, which is both time-intensive and costly (Jiang et al, 2023;Mahanty et al, 2023). These limitations have so far hampered the application of HIGS to BPH control in rice.…”

“…Recently, a novel RNAi-based crop protection strategy called "spray-induced gene silencing (SIGS)" has been developed (Jiang et al, 2023;Mahanty et al, 2023). As the name implies, SIGS does not require genetic modification and instead involves simply spraying crop plants with synthesized exogenous dsRNA to selectively knock down insect or pathogen genes (Figure 1B).…”

Pseudocercospora fijiensis Conidial Germination Is Dominated by Pathogenicity Factors and Effectors

“…Gene silencing is a conserved eukaryotic homology-dependent post-transcriptional mechanism of gene expression regulation. In fungi, gene silencing controls growth, development, and virulence [125]. Gene ontology found an upregulation of gene silencing by miRNA.…”

A pipeline for validation of sRNA effectors suggests cross-kingdom communication in the symbiosis ofArabidopsiswithSerendipita indica

“…Plant sRNAs can also move intercellularly across plasmodesmata and systemically across the phloem, acting cell non-autonomously and can also translocate between interacting species (Zhan & Meyers, 2023). In the latter case, sRNAs are transferred bidirectionally between plant hosts and pathogenic microbes to modulate defence and virulence, a phenomenon called cross-kingdom RNAi (ckRNAi) (Göhre and Weiberg, 2023; Mahanty et al, 2023; Wang et al, 2017). ckRNAi in plant-pathogen interactions was discovered in 2013 when the necrotrophic fungus Botrytis cinerea was shown to induce silencing of host defence genes in Solanum lycopersicum and Arabidopsis thaliana ( At ) (Weiberg et al, 2013).…”