The Evolutionary Significance of RNAi in the Fungal Kingdom

Abstract

RNA interference (RNAi) was discovered at the end of last millennium, changing the way scientists understood regulation of gene expression. Within the following two decades, a variety of different RNAi mechanisms were found in eukaryotes, reflecting the evolutive diversity that RNAi entails. The essential silencing mechanism consists of an RNase III enzyme called Dicer that cleaves double-stranded RNA (dsRNA) generating small interfering RNAs (siRNAs), a hallmark of RNAi. These siRNAs are loaded into the RNA-induced silencing complex (RISC) triggering the cleavage of complementary messenger RNAs by the Argonaute protein, the main component of the complex. Consequently, the expression of target genes is silenced. This mechanism has been thoroughly studied in fungi due to their proximity to the animal phylum and the conservation of the RNAi mechanism from lower to higher eukaryotes. However, the role and even the presence of RNAi differ across the fungal kingdom, as it has evolved adapting to the particularities and needs of each species. Fungi have exploited RNAi to regulate a variety of cell activities as different as defense against exogenous and potentially harmful DNA, genome integrity, development, drug tolerance, or virulence. This pathway has offered versatility to fungi through evolution, favoring the enormous diversity this kingdom comprises.

Viral suppressors from members of the family Closteroviridae combating antiviral RNA silencing: a tale of a sophisticated arms race in host-pathogen interactions

“…Antiviral RNA silencing is a highly conserved regulatory mechanism of gene expression, which plays the most important role in different biological processes associated with host protection against viral infection. Plants recruit this mechanism as a shield against viruses by encoding abundant crucial components, such as RNA-dependent RNA polymerases (RdRps), Dicer ribonucleases (DCLs), Argonaute endonucleases (AGO), double-stranded RNA (dsRNA), and helicases (Lee and Carroll 2018;Muhammad et al 2019;Lax et al 2020). In response to this defense strategy, viruses have also evolved to produce various multifunctional proteins that act as VSRs to avoid being silenced and thus ensure successful infections (Daròs 2017;Gaffar and Koch 2019).…”

Fusarium graminearum DICER-like-dependent sRNAs are required for the suppression of host immune genes and full virulence

“…These results are consistent with our previous studies showing that knock-down or SIGS-mediated silencing of Fusarium DCLs and other components of the RNAi machinery reduced the virulence of the fungus on barley [ 8 , 44 ]. DCL enzymes are key components of the fungal RNAi machinery required for the biogenesis of sRNAs directing silencing of sequence-complementary endogenous and foreign genes [ 45 ]. The latter case involves DCL-dependent pathogen-derived sRNAs that target plant defense genes to increase virulence as shown for Botrytis cinerea [ 19 , 21 ], Puccinia striiformis [ 23 ] and Magnaporthe oryzae [ 46 ].…”

siRNA-Mediated Silencing of Antifungal Resistance Genes: A Research Protocol

“…This method presents several advantages. First, mFgDFV1 resistance is unlikely given the importance of siRNA silencing in fungi and the exploitation of the entire pathway as opposed to an individual protein [32]. Without siRNA, fungi are vulnerable to various sources of dangerous exogenous DNA such as viruses and transposons.…”