Fungal plant pathogens use proteinaceous effectors as well as newly identified secondary metabolites (SMs) and small non-coding RNA (sRNA) effectors to manipulate the host plant’s defense system via diverse plant cell compartments, distinct organelles, and many host genes. However, most molecular studies of plant–fungal interactions have focused on secreted effector proteins without exploring the possibly equivalent functions performed by fungal (SMs) and sRNAs, which are collectively known as “non-proteinaceous effectors”. Fungal SMs have been shown to be generated throughout the plant colonization process, particularly in the early biotrophic stages of infection. The fungal repertoire of non-proteinaceous effectors has been broadened by the discovery of fungal sRNAs that specifically target plant genes involved in resistance and defense responses. Many RNAs, particularly sRNAs involved in gene silencing, have been shown to transmit bidirectionally between fungal pathogens and their hosts.
Plants have developed a broad spectrum of responses to counter pathogen invasion. Likewise, plant pathogens orchestrate a highly calibrated array of pathogenicity strategies in their quest to cause diseases [1]. The recent increased availability of fungal and plant genomes in the public domain has facilitated considerable progress in molecular plant–fungal interaction studies. During interaction with their hosts, fungal plant pathogens secrete many proteins known as effectors which manipulate the physiology of the host or suppress the host’s immunity to promote infection [2][3]. Most studies on effectors have focused almost exclusively on secreted proteins, without exploring the possibly equivalent functions performed by fungal secondary metabolites (SMs) (chemical effectors) and sRNAs (sRNA effectors) which are collectively referred to as non-proteinaceous effectors [2][4]. Accumulating evidence has indicated that, pathogens use sRNAs (such as siRNAs and microRNAs) and SMs to manipulate host cell functions [5][6]. Fungal SMs and sRNAs have been shown to manipulate host defense-related genes in the same was as proteinaceous effectors [7][8]. In general, SM and sRNA effectors are increasingly becoming important targets for studying the pathogenesis mechanisms of fungal pathogens [9].
Fungal SMs are not required for the growth and development of the fungus, but they have the potential to improve the pathogen’s fitness under certain conditions. Fungal SMs are often divided into polyketides, terpenes, non-ribosomal peptides and alkaloids on the basis of the primary enzymes and precursors that are involved in their biosynthesis [10][11]. The existence of fungal SMs, which have no discernible effect on the viability of the producer, raises issues about their potential influence on the environment [12]. SMs production by fungal pathogens and the presence of a host protein that is specifically susceptible to the corresponding toxin determines the ability of the pathogen to infect the host plant. Because host-specific toxin targets are encoded by plant genes, such genes can be referred to as dominant susceptibility genes [13]. Accumulating evidence indicates that fungal SMs serve as avirulence factors, host defense suppressors, and fungal cell wall hardening factors [8][14]. Fungal SMs are most effective during the early stage of infection (biotrophic phase), enhancing the fungus’ ability to penetrate and colonize its host without killing its host [2]. Fungal SMs can be host specific or non-host specific and generate necrosis in plant tissue. The majority of the fungal SMs have not been defined chemically, and the plants that they are intended to affect are still a mystery. The biological actions that have been reported to be caused by fungal SMs generated in-planta suggest that they have a broad range of plant cellular targets. The production and transport of proteins are targets of a wide range of fungal SMs [15][16].
sRNA | sRNA Origin | Target Origin | Target Genes | Function | Reference |
---|---|---|---|---|---|
miR408 | Puccinia striiformis f. sp. tritici (Pst) | T. aestivum | CLP1 | Negatively regulates host immune response by suppressing the expression of CLP1. | [22] |
Pst-milR1 | Pst | T. aestivum | PR2 | Represses plant innate immune response by suppressing the expression of PR2. | [7] |
Pst-milR1 | Pst | T. aestivum | SM638 | Innate immunity. | [7] |
pt-mil-RNA1 | Pt | T. aestivum | TCP14, CYB5R, and EF2 | Suppresses wheat defense response to Pt by targeting wheat TCP14, CYB5R and EF2. | [18] |
pt-mil-RNA2 | Pt | T. aestivum | TCP14, CYB5R and EF2 | Suppresses wheat defense response to Pt by targeting wheat TCP14, CYB5R and EF2. | [18] |
miR398 | Bgh | Barley | HvSOD1 | Negatively regulates host immunity by repressing HvSOD1 accumulation. | [23] |
miR9836 | Bgh | Barley | MLA1 | Dampens immune response signaling triggered by host MLA immune receptors. | [24] |
Fg-sRNA1 | F. graminearum | Chinese spring wheat | TaCEBiP | Suppresses wheat defense response by targeting and silencing TaCEBiP. | [25] |
Fol-milR1 | Fusarium oxysporum | Tomato | SlyFRG4 | Suppresses host immunity by silencing SylFRG4. | [26] |
Osa-miR167d | M. oryzae | Rice | ARF12, WRKY45 | Negatively regulates host immunity by downregulating AR12 expression. | [27] |
miR156 | M. oryzae | Rice | SPL14 | Enhances host susceptibility by suppressing the expression of SPL14 and WRKY45. | [28] |
Osa-miR164a | M. oryzae | Rice | OsNAC60 | Negatively regulates host immunity by suppressing OsNAC60 expression. | [29] |
miR168 | M. oryzae | Rice | AGO1 | Negatively regulates host immunity by suppressing AGO1 expression. | [30] |
Osa-miR169 | M. oryzae | Rice | NF-YAs | Enhances host susceptibility by suppressing the expression of nuclear factor N-Y (NF-YA) genes. | [31] |
miR319 | M. oryzae | Rice | TCP21 | Negatively regulates host immunity by suppressing TCP21 expression. | [32] |
miR396 | M. oryzae | Rice | OsGRFs | Negatively regulates host immunity by suppressing the expression of OsGRFs. | [33] |
Osa-miR439 | M. oryzae | Rice | Predicted target genes LOC_Os01g23940, LOC_Os01g36270, LOC_Os01g26340 and LOC_Os06g19250 | Enhances host susceptibility by suppressing the expression of predicted target genes LOC_Os01g23940, LOC_Os01g36270, LOC_Os01g26340 and LOC_Os06g19250. | [34][35] |
miR444b.2 | M. oryzae | Rice | MADS-box family genes | Negatively regulates host immunity by suppressing the expression of MADS-box family genes. | [36] |
siR109944 | Rhizoctonia solani | Rice | FBL55 | Suppresses host immunity to sheath blight. | [37] |
Bc-siR3.2 | Botrytis cinerea (B. cinerea) | A. thaliana | MPK1, MPK2 | Suppresses MPK1, MPK2 function in plant immunity. | [38] |
Bc-siR3.1 | B. cinerea | A. thaliana | PRXIIF | Suppresses PRXIIF genes. | [38] |
Bc-siR3.2 | B. cinerea | Solanum lycopersicum | MAPKKK4 | Suppresses MAPKKK4 function. | [38] |
Bc-siR5 | B. cinerea | A. thaliana | WAK | Suppression the function WAK genes. | [38] |
Bc-siR37 | B. cinerea | A. thaliana | WRKY7, PMR6 and FEI2 | Suppresses plant immunity by repressing the expression of WRKY7, PMR6 and FEI2. | [39] |