dahlia sRNAs with predicted plant targets have
been associated with plant AGO1, suggesting
that this fungus also employs sRNAs and
cross-kingdom RNAi for successful infection
(Wang et al. 2016). Moreover, sRNAs have
been found in extracellular vesicles secreted
by Malassezia sympodialis, Saccharomyces cerevisiae, Candida albicans, Paracoccidioides brasiliensis, and Cryptococcus neoformans (Peres
da Silva et al. 2015; Rayner et al. 2017). These
proofs suggest that an unknown cell-to-cell
transport mechanism must exist to translocate
sRNAs to the plant that could be used by other
pathogens to suppress host immune systems
(Weiberg et al. 2015).
In addition to sRNA translocation from
fungal pathogens into plants, plants can also
transfer sRNAs into fungi. This was initially
revealed when dsRNA targeting virulence
genes of fungal pathogens produced by engineered plants were able to trigger silencing in
the fungi and confer resistance to the infection
(Koch et al. 2013; Nowara et al. 2010; Panwar
et al. 2013; Tinoco et al. 2010). The use of this
strategy, name host-induced gene silencing
(HIGS), to control invading fungi has the
potential to become an important diseaseprotection method (Cai et al. 2018a; Nunes
and Dean 2012). Interestingly, the delivery of
own plant sRNAs was later confirmed by the
identification of specific plant sRNAs and miRNAs in fungal cells infecting plants (Cai et al.
2018b; Zhang et al. 2016). The delivery mechanism of sRNAs by the plant and taking up by
fungi is basically unknown, but exosome-like
vesicles have proven to play a critical role in the
secretion of sRNAs by A. thaliana infected with
B. cinerea. The fungus takes up these vesicles
resulting in the silencing of fungal virulencerelated genes, including genes involved in
vesicle-trafficking (Cai et al. 2018b). Together
these results suggest that cross-kingdom RNAi
might play an essential role in the arms race
between pathogens and host with bidirectional
translocation of sRNAs. Moreover, the ability of
the fungi to incorporate extracellular RNAs has
been devised as a strategy to control pathogens
by direct application of dsRNAs or sRNAs onto
host plants or post-harvest products to silence
target fungal genes and confers efficient disease
control (Cai et al. 2018a).
IV. Conclusions
The study of RNAi in the fungal kingdom has
revealed that it is a conserved mechanism present in most fungi with a primary function of
genome protection against foreign invaders
and TEs during vegetative and sexual cycles.
More impressively, recent studies have additionally unveiled a whole regulatory layer composed of different classes of regulatory esRNAs
that can control several target genes and
biological processes. In some fungi, illustrated
by Mucor circinelloides, the relevancy of the
RNAi-related regulation is huge controlling
physiological and developmental processes. In
contrast, milRNAs seems to fine-tune gene
expression, and more in-depth studies are
required to validate their functional roles in
particular biological processes experimentally.
The regulation of these processes by RNAirelated mechanisms is transient and reversible,
conferring substantial phenotypic plasticity for
rapid adaptation, as it has been demonstrated
for antifungal drug response. In addition to the
regulation of endogenous processes, plant fungal pathogens produce sRNAs to regulate the
expression of plant genes involved in plant
immunity. On the whole, all the different studies describing esRNAs in fungi have contributed to enlighten a heterogeneous world of new
regulatory mechanisms in Ascomycota, Basidiomycota, and Mucoromycota. The only common feature among all these fungi is the lack of
a unique or universal pathway for the production of esRNAs, showing a scenario where the
diversification of regulatory silencing mechanisms is the chosen strategy rather than the conserved pathways found in animals and plants.
References
Alexander WG, Raju NB, Xiao H, Hammond TM, Perdue TD, Metzenberg RL, Pukkila PJ, Shiu PKT
(2008) DCL-1 colocalizes with other components
of the MSUD machinery and is required for silencing. Fungal Genet Biol 45:719–727
Bartel DP (2004) MicroRNAs: genomics, biogenesis,
mechanism, and function. Cell 116:281–297
Bonath F, Domingo-Prim J, Tarbier M, Friedla ¨nder MR,
Visa N (2018) Next-generation sequencing reveals
two populations of damage-induced small RNAs at
5 Small RNAs in Fungi
117
been associated with plant AGO1, suggesting
that this fungus also employs sRNAs and
cross-kingdom RNAi for successful infection
(Wang et al. 2016). Moreover, sRNAs have
been found in extracellular vesicles secreted
by Malassezia sympodialis, Saccharomyces cerevisiae, Candida albicans, Paracoccidioides brasiliensis, and Cryptococcus neoformans (Peres
da Silva et al. 2015; Rayner et al. 2017). These
proofs suggest that an unknown cell-to-cell
transport mechanism must exist to translocate
sRNAs to the plant that could be used by other
pathogens to suppress host immune systems
(Weiberg et al. 2015).
In addition to sRNA translocation from
fungal pathogens into plants, plants can also
transfer sRNAs into fungi. This was initially
revealed when dsRNA targeting virulence
genes of fungal pathogens produced by engineered plants were able to trigger silencing in
the fungi and confer resistance to the infection
(Koch et al. 2013; Nowara et al. 2010; Panwar
et al. 2013; Tinoco et al. 2010). The use of this
strategy, name host-induced gene silencing
(HIGS), to control invading fungi has the
potential to become an important diseaseprotection method (Cai et al. 2018a; Nunes
and Dean 2012). Interestingly, the delivery of
own plant sRNAs was later confirmed by the
identification of specific plant sRNAs and miRNAs in fungal cells infecting plants (Cai et al.
2018b; Zhang et al. 2016). The delivery mechanism of sRNAs by the plant and taking up by
fungi is basically unknown, but exosome-like
vesicles have proven to play a critical role in the
secretion of sRNAs by A. thaliana infected with
B. cinerea. The fungus takes up these vesicles
resulting in the silencing of fungal virulencerelated genes, including genes involved in
vesicle-trafficking (Cai et al. 2018b). Together
these results suggest that cross-kingdom RNAi
might play an essential role in the arms race
between pathogens and host with bidirectional
translocation of sRNAs. Moreover, the ability of
the fungi to incorporate extracellular RNAs has
been devised as a strategy to control pathogens
by direct application of dsRNAs or sRNAs onto
host plants or post-harvest products to silence
target fungal genes and confers efficient disease
control (Cai et al. 2018a).
IV. Conclusions
The study of RNAi in the fungal kingdom has
revealed that it is a conserved mechanism present in most fungi with a primary function of
genome protection against foreign invaders
and TEs during vegetative and sexual cycles.
More impressively, recent studies have additionally unveiled a whole regulatory layer composed of different classes of regulatory esRNAs
that can control several target genes and
biological processes. In some fungi, illustrated
by Mucor circinelloides, the relevancy of the
RNAi-related regulation is huge controlling
physiological and developmental processes. In
contrast, milRNAs seems to fine-tune gene
expression, and more in-depth studies are
required to validate their functional roles in
particular biological processes experimentally.
The regulation of these processes by RNAirelated mechanisms is transient and reversible,
conferring substantial phenotypic plasticity for
rapid adaptation, as it has been demonstrated
for antifungal drug response. In addition to the
regulation of endogenous processes, plant fungal pathogens produce sRNAs to regulate the
expression of plant genes involved in plant
immunity. On the whole, all the different studies describing esRNAs in fungi have contributed to enlighten a heterogeneous world of new
regulatory mechanisms in Ascomycota, Basidiomycota, and Mucoromycota. The only common feature among all these fungi is the lack of
a unique or universal pathway for the production of esRNAs, showing a scenario where the
diversification of regulatory silencing mechanisms is the chosen strategy rather than the conserved pathways found in animals and plants.
References
Alexander WG, Raju NB, Xiao H, Hammond TM, Perdue TD, Metzenberg RL, Pukkila PJ, Shiu PKT
(2008) DCL-1 colocalizes with other components
of the MSUD machinery and is required for silencing. Fungal Genet Biol 45:719–727
Bartel DP (2004) MicroRNAs: genomics, biogenesis,
mechanism, and function. Cell 116:281–297
Bonath F, Domingo-Prim J, Tarbier M, Friedla ¨nder MR,
Visa N (2018) Next-generation sequencing reveals
two populations of damage-induced small RNAs at
5 Small RNAs in Fungi
117