A fungal microRNA‐like RNA subverts host immunity and facilitates pathogen infection by silencing two host receptor‐like kinase genes

Abstract

Summary Small RNAs (sRNAs) play important roles in various biological processes by silencing their corresponding target genes in most eukaryotes. However, cross‐kingdom regulation mediated by fungal microRNA‐like RNAs (milRNAs) in plant–pathogen interactions is still largely unknown. Using molecular, genetic, histological, and biochemical approaches, we found that the apple tree Valsa canker pathogen Valsa mali milRNA Vm‐milR1 could suppress the host immunity by silencing two host receptor‐like kinase genes, MdRLKT1 and MdRLKT2. Vm‐milR1 was highly induced during V. mali infection. Deletion of Vm‐milR1 precursor abolished the generation of Vm‐milR1 and reduced the virulence of V. mali. Inoculation of Vm‐milR1 deletion mutants induced the host defence responses, including reactive oxygen species (ROS) accumulation, callose deposition, and high expression of defence‐related genes. Furthermore, Vm‐milR1 was confirmed to be able to suppress the expression of MdRLKT1 and MdRLKT2 in a sequence‐specific manner. Moreover, overexpression of either MdRLKT1 or MdRLKT2 enhanced apple resistance to V. mali by activating the host defence responses. Furthermore, knockdown of MdRLKT1 or MdRLKT2 compromised the host resistance to V. mali. Our study revealed that V. mali was equipped with Vm‐milR1 as an sRNA effector to silence host receptor‐like kinase genes, suppress the host defence responses, and facilitate pathogen infection.

Combatting Fusarium head blight: advances in molecular interactions between Fusarium graminearum and wheat

“…Fungal infection usually activates plant immune responses such as the influx of calcium ion (Ca 2+ ), ROS burst, transcriptional reprogramming, antimicrobial substance production, and callose deposition (Xu et al 2022b). Transcriptome and proteome profiling are efficient approaches for the identification of wheat genes that are associated with FHB resistance (Kazan and Gardiner 2018;Pan et al 2018;Liu et al, 2019).…”

Identification of microRNA and analysis of target genes in Panax ginseng

“…Rice osa-miR162a can enter the brown planthopper through feeding, silence the expression of NlTOR, a key gene for the growth and development of brown planthopper, and affect the expression of the downstream vitelline gene NlVg, thereby negatively regulating the egg production and hatchability of brown planthopper ( Shen et al, 2021 ). Vm-milR1, which is highly expressed during host infection, can positively regulate host disease resistance to apple tree decay bacteria by inhibiting the expression of the host-like receptor protein kinase genes MdRLKT1 and MdRLKT2 ( Xu et al, 2022 ). Therefore, we speculated that miRNA in P. ginseng may also play a certain regulatory role.…”

Comprehensive re-analysis of hairpin RNAs in fungi reveals ancestral links

“…Important questions still remain about how these loci may function, target, and affect the expression of target genes. These results are challenging to obtain and frequently require follow-up studies to confirm functionality and role of a proposed mi/milRNA [58]. Evidence of cleavage found in degradome and 5'-RACE experiments hints that fungal mi/milRNAs may function more similarly to plants [31,[59][60][61][62][63][64][65], as this evidence indicates directed cleavage of a target RNA.…”