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Review

Roles of Small RNAs in Virus-Plant Interactions

by
Baogang Zhang
†,
Wenji Li
†,
Jialin Zhang
,
Lu Wang
and
Jianguo Wu
*
Vector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou 350002, China
*
Author to whom correspondence should be addressed.
†
These authors contribute equally to this work.
Viruses 2019, 11(9), 827; https://doi.org/10.3390/v11090827
Submission received: 28 July 2019 / Revised: 27 August 2019 / Accepted: 28 August 2019 / Published: 5 September 2019
(This article belongs to the Special Issue Plant Immunity to Virus Infections)
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Abstract

:
Small RNAs (sRNAs), including microRNAs (miRNAs) and short interfering RNAs (siRNAs), are non-coding but powerful RNA molecules of 20–30 nucleotides in length. sRNAs play crucial regulatory roles in diverse plant biological processes. Recently, many studies on sRNAs have been reported. We summarize new findings of sRNAs in virus-plant interactions to accelerate the function analysis of sRNAs. The main content of this review article includes three parts: virus-responsive sRNAs, function analysis of sRNAs in virus pathogenicity or host resistance, and some sRNAs-mediated underlying mechanisms in virus-plant interactions. New findings of sRNAs deepen our understanding about sRNAs’ roles, which might contribute to the design of novel control measures against plant viruses.

1. Introduction

Small RNAs (sRNAs), which are a group of non-coding small RNA molecules of approximately 20–30 nucleotides (nt) in length, are mainly divided into two subgroups: microRNAs (miRNAs) and small interfering RNAs (siRNAs). The first miRNA, lin-4, which regulated lin-14 transcript via RNA-RNA interaction, was identified in 1993 [1]. After that, the discovery and functional studies on sRNAs have become one hotspot in the past 30 years. Several new species and families of sRNAs have been discovered. Some sRNAs are responsive to abiotic and biotic factors, and they exist in all tissues during the whole life, playing crucial regulatory roles in plant growth and development [2,3,4]. sRNAs play inactive regulatory roles in most plant species during the entire life cycle by sequence-specific regulation of genes, transposons, parasites. Virus diseases caused serious crop losses. In Asia, rice viruses, such as rice stripe virus (RSV), rice dwarf virus (RDV), rice grassy stunt virus (RGSV), rice black streaked dwarf virus (RBSDV), and southern rice black streaked dwarf virus (SRBSDV) have huge economic impacts [5]. Virus infection differentially regulates the accumulation levels of sRNAs, which alters virus pathogenicity or host resistance [6]. Here, we summarize some new findings on roles of sRNAs in virus-plant interactions.

2. The Biogenesis and Action Modes of sRNAs

Many sRNAs are identified by cloning and genetic methods. High throughput sequencing technology greatly accelerated this process. The latest released miRBase (v22) data registered 48,860 mature miRNAs in 271 organisms (http://www.mirbase.org, release 22) [7]. miRNAs are from miRNA genes (MIRs), the vast majority of which are located in intergenic regions [2]. MIRs are transcripted by DNA directed RNA polymerase producing pri-miRNAs with imperfect complementary fold-back secondary structures [2]. Subsequently, pri-miRNAs are processed by a processing complex to produce mature miRNAs. The processing complex contains a set of core proteins, including Dicer-like RNase III (DCL), Double strand RNA binding protein (DRB)/Hyponastic leaves (HYL), Serrate (SE), and RNA methytransferase Hua enhancer (HEN) [8]. Among them, DRB/HYL protein is responsible for binding double strand RNAs, and DCL cuts double strand RNAs, and HEN is responsible for the methylation of duplex molecules to stabilize miRNAs [9]. In Arabidopsis thaliana, there are ten DCLs, four DRBs, one SE, and one HEN. Components in the same family played redundant or specific functions. For example, mature miRNAs of 21-, 22-, or 24-nt in length are responsible for DCL1/4, DCL2, and DCL3, respectively. siRNAs are divided into endogenous siRNAs and exogenous siRNAs. Endogenous siRNAs consist of five subcategories: trans-acting siRNAs (ta-siRNAs), natural sense-antisense transcript siRNAs (nat-siRNAs), repeat-associated siRNAs (ra-siRNAs), long siRNAs (lsiRNAs), and heterochromatic siRNAs (hc-siRNA). The biogenesis of ta-siRNAs is directed by miRNAs. In Arabidopsis thaliana, miR173, miR390, and miR828 direct the cleavage of TAS1/TAS2, TAS3, and TAS4, respectively. The precursor of nat-siRNA is from overlapping regions of natural sense-antisense transcript pairs [10]. They can be induced by environmental clues. DCL1/3, SGS3 (suppressor of genesilencing), and RDR2/6 (RNA-dependent RNA polymerase) are required for double-strand RNAs processing [10,11]. lsiRNAs are 30-40 nt in length, whose biogenesis requires DCL1/4, HYL1, HEN1, RDR6, and Polymerase IV [12]. hc-siRNAs are derived from transposons or repeated sequences, and they can be transcripted by Polymerase IV; hc-siRNAs play roles in DNA and H3K9 methylation at homologous chromatin to maintain genome integrity [13]. The biogenesis of hc-siRNAs also requires processing complex, including RDR2, DCL3, and HEN1 proteins [2]. In addition to these endogenous siRNAs, plants may contain exogenous siRNAs derived from virus, bacteria, fungi, oomycetes, or other parasites in parasite-plant interactions. The biogenesis of virus-derived siRNAs (vsiRNAs) is analogous to endogenous sRNAs and also requires DCL and RDR proteins [14]. Six RDR proteins have been predicted in Arabidopsis thaliana [15,16], but only one or two RDR proteins have been predicted in rice and maize (Zea mays L.) [17,18]. Phylogenetic analysis suggests that three RDR gene copies are present in the eukaryotic ancestor, with RDRα clade members RDR1, RDR2, and RDR3 involved in antiviral immunity [19]. Recently, aminophospholipid transporting ATPase (ALA1 and ALA2) have been demonstrated to be necessary for the biogenesis of vsiRNAs or endogenous siRNAs, which is the down-stream of RDRs in Arabidopsis thaliana [20].
The produced mature sRNA is selectively sorted into RISC complex with Argonaute (AGO) protein for the following modification of targets by mRNA degradation, translational inhibition, DNA and/or histone methylation [2,21,22]. sRNAs often regulate gene expression through DNA/histone methylation, mRNA translational inhibition or mRNA cleavage at either transcriptional gene silencing (TGS) or the posttranscriptional gene silencing (PTGS) level. For example, AGO proteins mainly mediated RNA interfering by mRNA cleavage. Ten AGOs are encoded in Arabidopsis thaliana. AGO1, AGO2, AGO5, AGO7, and AGO10 proteins are mostly assembled with 21-22-nt sRNAs, whereas the AGO4, AGO6, and AGO9 proteins are mainly assembled with 24-nt sRNAs. 21-nt miRNAs are incorporated into the AGO1 protein to cleave target mRNAs, while long miRNAs direct DNA methylation of their own loci by AGO4 in Arabidopsis thaliana [23]. According to 5′ end rules, AGO1, AGO2, AGO5, and AGO7 preferentially interact with 5′ uridine, 5′ adenosine, 5′ cytosine, and 5′ uridine miRNAs, respectively. However, on occasion, AGO1 and AGO2 act redundantly in miR408-mediated plantacyanin regulation [24]. In addition, AGO1 has diverse functions, such as chromatin remodeling, co-transcriptional splicing regulation, as well as RNA maturation [25]. The majority of 21-nt siRNAs direct mRNA cleavage, while 24-nt siRNAs mediate DNA or histone methylation. For example, target mRNA cleavage or DNA methylation mediated by 21-nt ta-siRNA requires DCL4, AGO1 for cleavage, or DCL1, AGO4/6 for DNA methylation [26]. In Arabidopsis thaliana, DCL1 is responsive for miRNAs’ biogenesis, DCL3 is responsive for endogenous siRNAs’ biogenesis, and DCL2 is responsive for viral siRNAs’ biogenesis [3]. In Figure 1 we can take a glance on the biogenesis and action modes of sRNAs.

3. Virus-Responsive sRNAs in Virus-Plant Interactions

Virus infection alters the accumulation levels of sRNAs in host plants. Firstly, the ratio of different size of sRNAs changed after virus infection. When virus infected hosts, 21- and 22-nt sRNAs of plants increased, while 24-nt sRNAs decreased. For example, sRNAs changed in the potato virus Y (PVY)-tobacco (Nicotiana tabacum) and Beta macrocarpa, mungbean yellow mosaic india virus (MYMIV)-blackgram (Vigna mungo) interactions [27,28]. In the interactions between cucumber green mottle mosaic virus-Lagenaria siceraria, RBSDV-maize (Zea mays), the size distribution of vsiRNAs showed similar phenomena [29,30]. However, size distribution of vsiRNAs of distinct viruses is not the same. 22-nt siRNAs of cotton leafroll dwarf polerovirus (CLRDV) are predominant in virus infected cotton (Gossypium hirsutum) leaves, and 21–24 nt long viral sRNAs have higher frequencies matching in the 3′ region of the viral genome [31]. Accordingly, the metabolism of sRNAs is changed in response to virus invasion.
The profiles of sRNAs responsive to virus invasion are explored to gain insights into metabolism of sRNAs in virus infection. The expression of miR162 increases in response to infection of CLRDV in cotton [31]. miR444, a monocot-specific miRNA that is ubiquitously expressed in rice, wheat, barley, sorghum, and sugarcane, is induced by RSV, while miR528 and miR396 are down-regulated by RSV [32,33]. RSV invasion also alters the accumulation levels of other miRNAs, for example, RSV increases the accumulation levels of miR159a/b/e/f, 168, 394, 395, 398, 399, 160*, 171*, and 1425*, and decreases the accumulation levels of miR156, 166, 167, and 171 [34,35,36]. miR168 is induced by CymRSV, tobacco mosaic virus (TMV), potato virus X (PVX), tobacco etch virus (TEV), and other viruses [37]. In addition to miRNAs, siRNAs are affected by viral infection. siRNAs, called P5_3′ or P10_3′, are induced by RSV [34]. Different from vsiRNAs in virus-host interactions, a distinct class of viral activated siRNA (vasiRNA) is activated by RNA viruses. Most vasiRNAs are mapped to the exon region of host genes and rRNA, requiring DCL4/RDR1/AGO2 proteins for their biogenesis and action in Arabidopsis thaliana [38]. Infected by viruses in plants, the accumulation levels of miRNAs, endogenous siRNAs, and vsiRNAs changed in host plants. Accordingly, how does virus affect sRNAs’ accumulation in hosts? Some researches revealed that some viral proteins have been found to alter sRNAs’ accumulation when expressed alone in host plants. In virus-rice interactions, RDV infection induced OsRDRs, whereas RSV elevated expression of some specific DCLs and AGOs. Correspondingly, RDV-regulated miRNA*s and miRNAs are less than RSV [34]. Viral protein was identified to act as scaffold between host plant and pri-miRNAs. RSV-encoded NS3 was firstly identified as a RNA silencing suppressor reducing levels of siRNAs in tobacco, and it binds to siRNAs, short duplexes, and long ssRNAs [39]. However, in RSV-rice interactions, RSV-encoded nonstructural protein NS3 interacts with DRB1 protein to aid pri-miRNA processing in vivo accelerating miRNAs’ biogenesis [36]. Table 1 summarizes sRNAs that altered by virus infection.

4. sRNAs-Mediated Viral Disease Symptoms

Viral infection normally causes developmental defects in vegetable or reproductive stages. These virus-caused abnormities can also be called disease symptoms, for example, virus infection changes stem height or number [30,35,42,47], leaf shape or color [29,35,36,42,47,48,49,50], size of root crowns [47], plant fertility rates [35], plant fruit [35], and even seriously causing the plant death [51]. Cucumber mosaic virus (CMV) 2b protein interacts with host catalase, CAT3, causing necrosis spots in Arabidopsis thaliana [49]. OsIAA10 causes dwarf phenotype and increases tillers by negatively regulating auxin signaling pathway, and it is degraded by TIR1-mediated protein degradation pathway. RDV-encoded capsid protein P2 causes viral symptoms by targeting OsIAA10 [47]. What the underlying forming mechanisms of viral symptoms is one longstanding and interesting scientific question. As reviewed by Pallas in 2011, hypersensitive response, R resistance genes, RNA silencing, plant hormones, and other unknown mechanisms contributed to pathological phenotypes [52]. Secondary siRNAs’ biogenesis is blocked by a suppressor, such as viral βC1 encoded by TYLCCNV satellite, which requires Nbrgs-CaM expression to decrease RDR6-mediated sRNAs’ production, and alters viral symptoms [53]. This indirectly revealed the crucial roles of sRNAs in the forming of viral symptoms. Increasing evidences indicated that sRNAs played pivotally regulatory roles in the induction of virus-induced disease symptoms.
The accumulation levels of sRNAs alter plant leaf morphology. It was observed that a correlation between symptom severity and the accumulation levels of miR156, 160, 166, 169, and 171 [54]. miR156, miR160, miR164, miR319, miR390, and miR396 are involved in leaf morphogenesis, and miR160 interacted with miR165/166 to control leaf development [55]. It is known that miRNAs and ta-siRNAs play roles in regulating leaf development by a comprehensive network [56]. Virus can alter miRNAs’ accumulation, contributing to construct disease symptoms. Double mutant of miR159 (mir159ab) presents severe stunting and up-curled rosette leaves in Arabidopsis thaliana [42]. When infected by a mild subgroup II strain CMV-LS, Arabidopsis thaliana silencing of miR165 and miR166 shows viral symptoms that resemble those infected by the severe strain [42]. Hence, miR165/166 are involved in the viral symptoms. miR159 was proved to negatively regulate this viral symptom by targeting MYB33 and MYB65 [42]. The inhibition of osa-miR171b causes stunting and leaf yellowing symptoms, and there are less chlorophyll in rice [35]. Rice that was infected by RSV for 30 days displayed less osa-miR171b accumulation level, presenting the viral symptoms [35]. Further research reveals that osa-miR171b-mediated viral symptoms are dependent on its targets, OsSCL6-IIabc [35]. In addition to miRNAs, siRNAs also alter viral disease symptoms. The first identified case is a siRNA derived from the CMV Y-satellite (Y-sat) RNA. It targets tobacco chlorophyll biosynthetic gene (Chll), causing Chll mRNA silencing, which is solely responsive for the yellowing symptom in tobacco [57]. Additionally, Y-sat mediated target mRNA cleavage is specifically dependent on the 22-nt long siRNA sequence by using the RNA silencing machinery [44]. sRNAs alter the seeds filling rate and vigor. The suppression of miR1432 increases the grain filling rate and grain weight [58]. miR1432 targets Acyl-CoA thioesterase (OsACOT) regulating the metabolism pathway of fatty acid, auxin, and abscisic acid [58]. Under the same aging condition, the accumulation of osa-miR164c and osa-miR168 are related with the seed germination rates. The accumulation of miR168 is positively related with seed germination rates, while the accumulation of miR164c is negatively related with seed germination rates [4].

5. sRNAs-Mediated Pathogenic or Resistant Mechanisms

Plants displayed resistant or susceptible phenotypes based on the strength and effect of antiviral defenses against viruses. The resistant or susceptible phenotype is compared with the phenotype of control. We judge the pathogenic or resistant phenotypes according to the viral disease severity, which is assessed by viral symptoms and/or viral accumulation. Plant immunity to some pathogens is often referred to high resistance to some pathogens, presenting no obvious disease symptoms after being infected by these pathogens. Plant resistance to some pathogens is referred to slight damage or losses after infected by pathogens. Growth and development losses are not serious in crop plants with pathogen resistance. However, the susceptible phenotype of plant is referred to be sensitive to pathogens, which presents serious damage in plant growth and development, even host death. In virus-plant interactions, the severity of disease symptoms and viral particles’ accumulation are often used to assess the host compatibility to viruses, although they are not always completely relevant. Increasing evidence reveals that sRNAs play roles in pathogenic or resistant mechanisms. Firstly, according to bioinformatics prediction, miRNAs have strong potential for antiviral activity through the formation of miRNA–viral genome pairings [59]. The tumor protein (TCTP) is required for potato virus Y (PVY) successful infection in tobacco; however, vsiRNAs target TCTP gene triggering plant viral resistance in PVY-tobacco interactions [27]. miRNAs involved in immunity to various pathogens, including bacteria, fungus, virus and parasites [60,61,62,63,64,65,66,67,68,69]. Here, we focus on sRNAs-mediated viral pathogenic or resistant mechanisms. In 2014, Du et al. provided direct evidence revealing that the accumulation level of miR159ab was correctly associated with severity of viral disease symptoms after various virulence group of the same virus infection [42]. Viruses can enhance their toxicity via sRNAs. As for siRNAs, vsiR3114 of cotton leaf curl Multan virus (CLCuMuV) target cotton contig28334 to increase plant viral susceptibility [46].
Nicaise et al. (2014) have proposed four antiviral mechanisms: dominant resistance, recessive resistance, and RNAi- or hormone-mediated resistance [70]. As the RNA silencing pathway interacts with other antiviral mechanisms, it is hard to clearly distinguish RNA silencing-dependent or-independent antiviral mechanisms. The RNA silencing is still the most effective approach to suppress viral proliferation. For example, RISC targets viral nucleocapsid or movement proteins to block viral amplication [71]. RNA silencing is triggered by either endogenous or exogenous dsRNAs, and it requires DCLs, AGOs, DRBs, and RDRs [72]. RNA silencing that is directed by vsiRNAs requires some of DCLs, AGOs, DRBs, RDRs, and other components. At least four distinct RNA silencing pathways were discovered since 2008, and they were separately by DCL1-4 [72]. Knock-out or knock-down of RDRs enhances viral toxicity on Arabidopsis thaliana, tobacco, tomato, pepper, rice, and maize; conversely, the overexpression of RDRs protects tomato, tobacco, and pepper against viruses [15,16,17,18,73,74,75]. AGO1 is the key factor of RISC, and the hypomorphicago1 mutant exhibits increased susceptibility to various viruses [72,76]. In Arabidopsis thaliana, four DCLs, two AGOs, one DRB, and one RDR were identified. In virus-plant interactions, the plants take advantage of distant vsiRNAs to down-regulate viral RNAs/DNAs by RNA silencing [14]. As a counter defense, viruses use various suppressors to overcome RNA-silencing-mediated antiviral defense [14]. Viral suppressors could perturb sRNAs’ biogenesis to indirectly alter viral disease symptoms. Suppressors are classified into viral suppressors of RNA silencing (VSRs) and endogenous suppressors of RNA silencing (ESRs), according to their sources. Previously identified VSRs include Pns10, P6, NS3, 2b, and so on [36,39,77,78,79], and ESRs include Nbrgs-CaM [53,80]. Although the structural flexibility of miRNAs increases the versatility and regulatory potential, P19 has usurped this process by changing affinity between AGO10 and 22-nt miR168 [81]. RDV-encoded Pns10 down-regulates the expression level of RDR6 in Arabidopsis thaliana and tobacco [77]. The P6 protein is the suppressor of rice yellow stunt rhabdovirus (RYSV), blocking RDR6-mediated secondary siRNAs’ biosynthesis [78]. A DNA satellite that is associated with the geminivirus tomato yellow leaf curl China virus (TYLCCNV) encodes the βC1 protein, which induces the calmodulin-like protein Nbrgs-CaM in tobacco and Arabidopsis thaliana to suppress RDR6 expression, so Nbrgs-CaM was identified as an endogenous suppressor of RNA silencing [53,80]. Vice versa, these silencing components are regulated by sRNAs. AGO1 is the target of miR168, negatively regulated by miR168-directed mRNA cleavage. Though CymRSV infection induces the expression of miR168 and mRNA of AGO1 at the same time, the AGO1 protein significantly decreases in Arabidopsis thaliana [37]. In Arabidopsis thaliana, DCL1 mRNA is negatively regulated by miR162, which indicates the existence of a feedback loop in the biogenesis of miRNAs by miRNAs-mediated RNA silencing [43]. Figure 2 shows some recently identified cases about sRNAs that are involved in virus-plant interactions. To protect AGO1-mediated antiviral resistance, plants have evolved a decoy protein AGO18. AGO18 is induced by RSV and competes with AGO1 for miR168 to alleviate the degradation of AGO1a; it is dependent on the PAZ domain, but not the PIWI domain, which indicates that the protection relies on sRNAs’ binding function, but not silencing function [41]. In addition, AGO18 functions as a core regulator in different viral resistance pathways. In Arabidopsis thaliana, 22-nt isomiR168 could bind to AGO10, the homolog protein of AGO1, to keep AGO1’s homeostasis [81]. Accordingly, AGO10 can function as a miRNA locker to suppress the degradation of class III HOMEDOMAIN-LEUCINE ZIPPER (HD-ZIP III), which is crucial for SAM development, by sequestering miR166/165 in Arabidopsis thaliana [82,83]. Osa-miR444 enhances antiviral resistance by regulating RDR1-mediated RNA silencing pathway in rice. RDR1 positively regulates plant antiviral immunity, but its expression is repressed by MADS box proteins that directly bind to RDR1 promoter regions. OsMADS23/27a/57 are targets of osa-miR444, thus osa-miR444 indirectly regulates RDR1’s homeostasis in plants [32]. In cotton, viral resistance against cotton leaf curl Burewala virus (CLCuBV) is also enhanced by miRNAs-mediated RNA silencing. Among them, Ghr-miR168 was predicted to be perfectly complementary to the C1, C3, C4, V1, and V2 of CLCuBV genome [45]. Hence, the miRNAs-mediated antiviral resistance is well studied; however, other sRNAs are less studied.
sRNAs regulate R gene-mediated viral resistance. During the process of TMV infection of tobacco, 22-nt miR6019 directs the biogenesis of 21-nt secondary miR6020 with the help of RDR6 and DCL4; these two miRNAs function as a guide strand to cleave Toll and Interlecukin-1 receptor-NB-LRR receptor N genes, thereby negatively regulating TMV resistance [84]. Antiviral RNAi-defective2 (AVI2), a multispan transmembrane protein, was identified to be necessary for DCL2-mediated vsiRNAs’ biogenesis, and it plays a partially redundant role with AVI2H in RDR1-medaited the biogenesis of vsiRNAs and vasiRNAs [85]. CMV induces it and it is required for antiviral RNAi, the underlying mechanism needs further research [85]. The molecular mechanism is conserved in three Solanaceae species-tobacco, tomato, and potato, such as nta-miR482/N, nta-miR6019/N, nta-miR6020/N, sly-miR6022/Cf9 (6-10), sly-miR6023/Cf9 (6-10), sly-miR6024/Tm22, sly-miR6026/Tm22, stu–miR482b/NL25, stu–miR482b/Ry, stu–miR482c/RB4 (4), stu–miR482d/R2(10+), stu-miR6024/RX2, stu-miR6024/Rpn1-vnt1, and stu-miR6026/Rpn1-vnt1.
There are other sRNAs-mediated antiviral mechanisms. Reactive oxygen species (ROS), generated during virus invasion, especially hydrogen peroxide, hydroxyl radicals, and superoxide peroxide, positively regulate antiviral immunity in plants [33,86]. Additionally, ROS burst is one the plant antiviral defense, enhancing rice viral resistance. Research in rice reveals that AGO18 competitively binds to miR528 to protect its target gene, L-ascorbate oxidase (AO) mRNA, boosting ROS-mediated resistance [33]. Although miR528 negatively regulates the ROS levels by targeting its target genes, such as AO and SPL9, it is suppressed by RSV. SPL9 is a squamosa promoter binding protein-like family member, which directly binds to miR528 promoter to active expression [33,87]. Antiviral immunity mediated by plasmodesmata and hydrogen peroxide may be correlated with the spread of RNA silencing signals [88]. Successful viral infection depends on various susceptibility factors, while within-host viral replication requires numerous host proteins; consequently, a functional deficiency in these factories may block or prevent viral invasion [89]. The function defect of P58IPK leads to enhanced viral pathogenicity, therefore it functions as a susceptibility factor [51]. Several such factors were identified, including eukaryotic translation elongation factor 1A (eEF1A), the SUMO-conjugating enzyme (SCE1), heat shock protein 70 (Hsp70), and essential for poteXvirus accumulation 1 (EXA1) [90,91,92,93]. Bendahmane et al. (2002) reported that a viral coat protein from potato virus X was recognized by the Rx protein in potato and triggered hypersensitive response in leaves [94]. Many avr-R protein pairs have been identified. The viral CP proteins from PVX, TCV, and CMV are recognized by Rx, HRT (HR to turnip crinkle virus), and RCY1 (Resistance to CMV (Y)) [95,96,97]. In addition, other viral components could be recognized by R proteins, such as cylindrical inclusion protein (CI)-TuRB01, cytoplasmic inclusion cistron-Rsv3, P3-TuMV, and so on [98,99,100]. Viral invasion differentially regulates phytohormones homeostasis, for example, RBSDV invasion increases the concentration of abscisic acid (ABA), cytokinins (CTKs), whereas decreases the concentration of indole-3-acetic acid (IAA), gibberellins (Gas), jasmonic acid (JA), and salicylic acid (SA) in rice [47,101,102]. Accordingly, hosts and viruses competitively regulate plant hormones. Growing evidence revealed that sRNAs-mediated hormones homeostasis played crucial functions in virus-plant interactions. Osa-miR319 is induced by rice ragged stunt virus (RRSV), which reduces OsTCP21 expression and JA concentrations, and rice with low JA levels is more susceptible to viruses [40]. Recently, osa-miR393 overexpressed in rice presents more susceptibility to RBSDV by suppressing auxin recognization, in which JA content is decreased when infected by virus [103]. sRNAs-mediated methylation of viral DNA or RNA genomes or other fragments is a common defense strategy against DNA viruses [6]. Methylation is one of the viral defense responses. In CMV-tobacco interactions, the DNA methylation plays important roles in modulating viral clearance and resistance signaling [104]. RNA silencing suppressor 2b encoded by CMV did not change sRNAs production or transcription, but it reduced the plant methylation levels, and then increased viral pathogenicity [105]. In addition, genome editing that based on the CRISPR/Cas system can be used to protect hosts from viruses; this approach has been demonstrated to be effective antiviral strategy against DNA and RNA viruses in dicot and monocot plants [106,107].

6. Conclusions and Perspectives

Some viral diseases cause serious production and quality losses [5,30,108]. Viruses, which obligate intracellular pathogens, require fatty acids, carbon, energy, and other materials and cellular structures for replication in host cells, leading to the second largest crop losses [47,50,109,110]. However, viral diseases are rarely curable due to the lack of effective control measures. Different viruses may have variant pathogenic mechanisms, which require various management strategies [101]. Antiviral materials screened by genetic method for artificial breeding is an effective viral management strategy, and revealing antiviral mechanisms will accelerate the genetic breeding. With the development of sequencing technology, more and more sRNAs were identified [111]. Their crucial regulatory roles are gradually recognized. This review highlighted the functional roles and the underling mechanisms of miRNAs and siRNAs in virus-plant interactions, which may aid in the development of virus-resistant varieties.
sRNAs-mediated RNA silencing and gene expression modification can be used to manipulate plant immunity. Researches on sRNAs provide inspiration for crop breeding that is based on their own attributes and advantages. Firstly, plant miRNAs’ regulatory specificity provides a basis for artificial miRNA usage in agriculture [112]. sRNAs perform their specific functions at designated positions in accordance with complementary base pairing rules by cleavage, translation inhibition, and methylation, so they often act as precision-guide weapons. They play crucial regulatory functions in plant antiviral resistance by many different mechanisms, which enlarged the usage scale in technology. Secondly, sRNAs are short in length. It is a natural advantage in regulating plant development and immunity, because their small size made them flexible and diffusible. They can easily transfer from cell to cell, tissue to tissue, and even species to species. sRNAs shuttle between different species. sRNAs in plants are not only derived from the host itself, but also from its interacting species [113]. The fungal pathogen Botrytis cinerea was previously reported to transfer sRNAs into host plant cells to silence host immunity genes by hijacking the AGO1-mediated silencing mechanism [114]. A similar phenomenon was observed in the interactions between cotton and Verticillium dahliae. When Verticillium dahliae infects cotton plants, plants exported both miR166 and miR159 into the fungus to inhibit virulence gene expression [115]. Although vsiRNAs are detected in host plants, we think viruses could be targeted by plant sRNAs. Hence, we should further dig their potential functions by focusing on the different sRNAs interaction networks. Plant miR2911 encoded by honeysuckle directly targets virus in mammals, and plant miR168 can specifically target mammals low-density lipoprotein receptor adapter protein 1 [116,117]. Recently, the accumulation of specific virus gene is silenced by feeding with siR471 and siR519 transgenic lettuce of artificial interfering miRNAs in mice [118]. Accordingly, the shuttle of miRNAs in different species has given us inspiration that regulatory function of miRNAs are more powerful and they have potential application in the aspect of RNAi-mediated genetic therapy [118]. Thirdly, sRNAs-mediated regulation is fine-tuning of gene expression otherwise an on-off regulation. In plant breeding, a desirable trait is often balanced by some other unexpected characteristics. As superior fine-tuners of complex crop traits, miRNAs have intrinsic, unmatched advantages for the balancing of sharply conflicting features that are useful for crop improvement [119]. Plant fitness and stresses resistance are two main opposite traits in the crop breeding work, so how to take care of both sides is an important question for the breeders taking into consideration. The common way to solve the problem is to sacrifice some fitness penalty to enhance their resistance to various stresses. However, some researchers have solved the problem in a different way. IPA1 and OsSPL7, the target of miR156, enhances the rice resistance against bacterial blight, Xanthomonas oryzae pv. oryzae (Xoo), but decreases the grain yield in rice. However, induced the expression of IPA1 driven by the OsHEN1 promoter increases both Xoo resistance and grain yield [69]. This study provides a new approach for us to take stresses resistance and yield into consideration, which also can be used for antiviral breeding. Feedback regulation to alleviate an over-accumulated defense response is important for plant development because a fitness cost is associated with response to pathogen infection. It is possible that sRNAs are involved in this feedback regulation [84]. Based on these data, to reduce the fitness and production costs, the sRNAs-mediated underlying mechanisms need to be further investigated. Additionally, we think that sRNAs’ expression levels can be manipulated to the suitable, valuable agronomic traits in food and economic crops.

Author Contributions

All authors planned the content of the manuscript. B.Z. wrote the initial manuscript. J.W. revised the manuscript.

Funding

This work is supported by grants from the National Natural Science Foundation of China (No.31722045, 31871934, and 31772128), Fok Ying-Tong Education Foundation of China (No.161024), Education and Research Projects for Young Teachers in Fujian Provincial Department of Education (No.JT180112), Outstanding Youth Research Program of Fujian Agriculture and Forestry University (No.XJQ201804), Excellent Talent Plan in the New Century of Fujian Province (No.2014J06011), and China Postdoctoral Science Foundation (No.2019M652236). Apologize to colleagues whose work could not be discussed due to space limitations.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Lee, R.C.; Feinbaum, R.L.; Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75, 843–854. [Google Scholar] [CrossRef]
  2. Chen, X. Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 2009, 25, 21–44. [Google Scholar] [CrossRef]
  3. Xie, Z.; Johansen, L.K.; Gustafson, A.M.; Kasschau, K.D.; Lellis, A.D.; Zilberman, D.; Jacobsen, S.E.; Carrington, J.C. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2004, 2, e104. [Google Scholar] [CrossRef]
  4. Zhou, Y.; Zhou, S.; Wang, L.; Wu, D.; Cheng, H.; Du, X.; Mao, D.; Zhang, C.; Jiang, X. miR164c and miR168a regulate seed vigor in rice. J. Integr. Plant Biol. 2019. [Google Scholar] [CrossRef]
  5. Zhou, G.; Xu, D.; Xu, D.; Zhang, M. Southern rice black-streaked dwarf virus: A white-backed planthopper-transmitted fijivirus threatening rice production in Asia. Front. Microbiol. 2013, 4, 270. [Google Scholar] [CrossRef]
  6. Prasad, A.; Sharma, N.; Muthamilarasan, M.; Rana, S.; Prasad, M. Recent advances in small RNA mediated plant-virus interactions. Crit. Rev. Biotechnol. 2019. [Google Scholar] [CrossRef]
  7. Kozomara, A.; Birgaoanu, M.; Griffiths-Jones, S. miRBase: From microRNA sequences to function. Nucleic Acids Res. 2019, 47, D155–D162. [Google Scholar] [CrossRef]
  8. Jones-Rhoades, M.W.; Bartel, D.P.; Bartel, B. MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 2006, 57, 19–53. [Google Scholar] [CrossRef]
  9. Park, W.; Li, J.; Song, R.; Messing, J.; Chen, X. Carpel factory, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 2002, 12, 1484–1495. [Google Scholar] [CrossRef]
  10. Borsani, O.; Zhu, J.; Verslues, P.E.; Sunkar, R.; Zhu, J.K. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 2005, 123, 1279–1291. [Google Scholar] [CrossRef]
  11. Zhang, X.; Xia, J.; Lii, Y.E.; Barrera-Figueroa, B.E.; Zhou, X.; Gao, S.; Lu, L.; Niu, D.; Chen, Z.; Leung, C.; et al. Genome-wide analysis of plant nat-siRNAs reveals insights into their distribution, biogenesis and function. Genome Biol. 2012, 13, R20. [Google Scholar] [CrossRef]
  12. Katiyar-Agarwal, S.; Gao, S.; Vivian-Smith, A.; Jin, H. A novel class of bacteria-induced small RNAs in Arabidopsis. Gene Dev. 2007, 21, 3123–3134. [Google Scholar] [CrossRef]
  13. Reinhart, B.J.; Bartel, D.P. Small RNAs correspond to centromere heterochromatic repeats. Science 2002, 297, 1831. [Google Scholar] [CrossRef]
  14. Zhang, C.; Wu, Z.; Li, Y.; Wu, J. Biogenesis, function, and applications of virus-derived small RNAs in plants. Front. Microbiol. 2015, 6, 1237. [Google Scholar] [CrossRef]
  15. Liao, Y.W.; Liu, Y.R.; Liang, J.Y.; Wang, W.P.; Zhou, J.; Xia, X.J.; Zhou, Y.H.; Yu, J.Q.; Shi, K. The relationship between the plant-encoded RNA-dependent RNA polymerase 1 and alternative oxidase in tomato basal defense against Tobacco mosaic virus. Planta 2015, 241, 641–650. [Google Scholar] [CrossRef]
  16. Yu, D.; Fan, B.; MacFarlane, S.A.; Chen, Z. Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol. Plant-Microbe Interact. MPMI 2003, 16, 206–216. [Google Scholar] [CrossRef]
  17. He, J.; Dong, Z.; Jia, Z.; Wang, J.; Wang, G. Isolation, expression and functional analysis of a putative RNA-dependent RNA polymerase gene from maize (Zea mays L.). Mol. Biol. Rep. 2010, 37, 865–874. [Google Scholar] [CrossRef]
  18. Chen, H.; Tamai, A.; Mori, M.; Ugaki, M.; Tanaka, Y.; Samadder, P.P.; Miyao, A.; Hirochika, H.; Yamaoka, N.; Nishiguchi, M. Analysis of rice RNA-dependent RNA polymerase 1 (OsRDR1) in virus-mediated RNA silencing after particle bombardment. J. Gen. Plant Pathol. 2010, 76, 152–160. [Google Scholar] [CrossRef]
  19. Zong, J.; Yao, X.; Yin, J.; Zhang, D.; Ma, H. Evolution of the RNA-dependent RNA polymerase (RdRP) genes: Duplications and possible losses before and after the divergence of major eukaryotic groups. Gene 2009, 447, 29–39. [Google Scholar] [CrossRef]
  20. Guo, Z.; Lu, J.; Wang, X.; Zhan, B.; Li, W.; Ding, S.W. Lipid flippases promote antiviral silencing and the biogenesis of viral and host siRNAs in Arabidopsis. Proc. Natl. Acad. Sci. USA 2017, 114, 1377–1382. [Google Scholar] [CrossRef]
  21. Montgomery, T.A.; Howell, M.D.; Cuperus, J.T.; Li, D.; Hansen, J.E.; Alexander, A.L.; Chapman, E.J.; Fahlgren, N.; Allen, E.; Carrington, J.C. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 2008, 133, 128–141. [Google Scholar] [CrossRef]
  22. Poulsen, C.; Vaucheret, H.; Brodersen, P. Lessons on RNA silencing mechanisms in plants from eukaryotic Argonaute structures. Plant Cell 2013, 25, 22–37. [Google Scholar] [CrossRef]
  23. Wu, L.; Zhou, H.; Zhang, Q.; Zhang, J.; Ni, F.; Liu, C.; Qi, Y. DNA methylation mediated by a microRNA pathway. Mol. Cell 2010, 38, 465–475. [Google Scholar] [CrossRef]
  24. Maunoury, N.; Vaucheret, H. AGO1 and AGO2 act redundantly in miR408-mediated Plantacyanin regulation. PLoS ONE 2011, 6, e28729. [Google Scholar] [CrossRef]
  25. Bajczyk, M.; Bhat, S.S.; Szewc, L.; Szweykowska-Kulinska, Z.; Jarmolowski, A.; Dolata, J. Novel nuclear functions of Arabidopsis ARGONAUTE1: Beyond RNA interference. Plant Physiol. 2019, 179, 1030–1039. [Google Scholar] [CrossRef]
  26. Wu, L.; Mao, L.; Qi, Y. Roles of dicer-like and argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol. 2012, 160, 990–999. [Google Scholar] [CrossRef]
  27. Guo, Y.; Jia, M.A.; Yang, Y.; Zhan, L.; Cheng, X.; Cai, J.; Zhang, J.; Yang, J.; Liu, T.; Fu, Q.; et al. Integrated analysis of tobacco miRNA and mRNA expression profiles under PVY infection provids insight into tobacco-PVY interactions. Sci. Rep. 2017, 7, 4895. [Google Scholar] [CrossRef]
  28. Liu, J.Y.; Fan, H.Y.; Wang, Y.; Zhang, Y.L.; Li, D.W.; Yu, J.L.; Han, C.G. Characterization of microRNAs of Beta macrocarpa and their responses to Beet necrotic yellow vein virus infection. PLoS ONE 2017, 12, e0186500. [Google Scholar] [CrossRef]
  29. Li, J.; Zheng, H.; Zhang, C.; Han, K.; Wang, S.; Peng, J.; Lu, Y.; Zhao, J.; Xu, P.; Wu, X.; et al. Different virus-derived siRNAs profiles between leaves and fruits in cucumber green mottle mosaic virus-infected Lagenaria siceraria plants. Front. Microbiol. 2016, 7, 1797. [Google Scholar] [CrossRef]
  30. Li, M.; Li, Y.; Xia, Z.; Di, D.; Zhang, A.; Miao, H.; Zhou, T.; Fan, Z. Characterization of small interfering RNAs derived from Rice black streaked dwarf virus in infected maize plants by deep sequencing. Virus Res. 2017, 228, 66–74. [Google Scholar] [CrossRef]
  31. Silva, T.F.; Romanel, E.A.; Andrade, R.R.; Farinelli, L.; Østerås, M.; Deluen, C.; Corrêa, R.L.; Schrago, C.E.; Vaslin, M.F. Profile of small interfering RNAs from cotton plants infected with the polerovirus Cotton leafroll dwarf virus. BMC Mol. Biol. 2011, 12, 40. [Google Scholar] [CrossRef]
  32. Wang, H.; Jiao, X.; Kong, X.; Hamera, S.; Wu, Y.; Chen, X.; Fang, R.; Yan, Y. A signaling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol. 2016, 170, 2365–2377. [Google Scholar] [CrossRef]
  33. Wu, J.; Yang, R.; Yang, Z.; Yao, S.; Zhao, S.; Wang, Y.; Li, P.; Song, X.; Jin, L.; Zhou, T.; et al. ROS accumulation and antiviral defence control by microRNA528 in rice. Nat. Plants 2017, 3, 16203. [Google Scholar] [CrossRef]
  34. Du, P.; Wu, J.; Zhang, J.; Zhao, S.; Zheng, H.; Gao, G.; Wei, L.; Li, Y. Viral infection induces expression of novel phased microRNAs from conserved cellular microRNA precursors. PLoS Pathog. 2011, 7, e1002176. [Google Scholar] [CrossRef]
  35. Tong, A.; Yuan, Q.; Wang, S.; Peng, J.; Lu, Y.; Zheng, H.; Lin, L.; Chen, H.; Gong, Y.; Chen, J.; et al. Altered accumulation of osa-miR171b contributes to rice stripe virus infection by regulating disease symptoms. J. Exp. Bot. 2017, 68, 4357–4367. [Google Scholar] [CrossRef]
  36. Zheng, L.; Zhang, C.; Shi, C.; Yang, Z.; Wang, Y.; Zhou, T.; Sun, F.; Wang, H.; Zhao, S.; Qin, Q.; et al. Rice stripe virus NS3 protein regulates primary miRNA processing through association with the miRNA biogenesis factor OsDRB1 and facilitates virus infection in rice. PLoS Pathog. 2017, 13, e1006662. [Google Scholar] [CrossRef]
  37. Varallyay, E.; Valoczi, A.; Agyi, A.; Burgyan, J.; Havelda, Z. Plant virus-mediated induction of miR168 is associated with repression of Argonaute1 accumulation. EMBO J. 2010, 29, 3507–3519. [Google Scholar] [CrossRef]
  38. Cao, M.; Du, P.; Wang, X.; Yu, Y.Q.; Qiu, Y.H.; Li, W.; Gal-On, A.; Zhou, C.; Li, Y.; Ding, S.W. Virus infection triggers widespread silencing of host genes by a distinct class of endogenous siRNAs in Arabidopsis. Proc. Natl. Acad. Sci. USA 2014, 111, 14613–14618. [Google Scholar] [CrossRef]
  39. Xiong, R.; Wu, J.; Zhou, Y.; Zhou, X. Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe tenuivirus. Virology 2009, 387, 29–40. [Google Scholar] [CrossRef]
  40. Zhang, C.; Ding, Z.; Wu, K.; Yang, L.; Li, Y.; Yang, Z.; Shi, S.; Liu, X.; Zhao, S.; Yang, Z.; et al. Suppression of jasmonic acid-mediated defense by viral-inducible microRNA319 facilitates virus infection in rice. Mol. Plant 2016, 9, 1302–1314. [Google Scholar] [CrossRef]
  41. Wu, J.; Yang, Z.; Wang, Y.; Zheng, L.; Ye, R.; Ji, Y.; Zhao, S.; Ji, S.; Liu, R.; Xu, L.; et al. Viral-inducible Argonaute18 confers broad-spectrum virus resistance in rice by sequestering a host microRNA. Elife 2015, 4, E05733. [Google Scholar] [CrossRef]
  42. Du, Z.; Chen, A.; Chen, W.; Westwood, J.H.; Baulcombe, D.C.; Carr, J.P. Using a viral vector to reveal the role of microRNA159 in disease symptom induction by a severe strain of Cucumber mosaic virus. Plant Physiol. 2014, 164, 1378–1388. [Google Scholar] [CrossRef]
  43. Xie, Z.; Kasschau, K.D.; Carrington, J.C. Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr. Biol. 2003, 13, 784–789. [Google Scholar] [CrossRef]
  44. Shimura, H.; Pantaleo, V.; Ishihara, T.; Myojo, N.; Inaba, J.; Sueda, K.; Burgyan, J.; Masuta, C. A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog. 2011, 7, e1002021. [Google Scholar] [CrossRef]
  45. Akhter, Y.; Khan, J.A. Genome wide identification of cotton (Gossypium hirsutum)-encoded microRNA targets against Cotton leaf curl Burewala virus. Gene 2018, 638, 60–65. [Google Scholar] [CrossRef]
  46. Wang, J.; Tang, Y.; Yang, Y.; Ma, N.; Ling, X.; Kan, J.; He, Z.; Zhang, B. Cotton leaf curl multan virus-derived viral small RNAs can target cotton genes to promote viral infection. Front. Plant Sci. 2016, 7, 1162. [Google Scholar] [CrossRef]
  47. Jin, L.; Qin, Q.; Wang, Y.; Pu, Y.; Liu, L.; Wen, X.; Ji, S.; Wu, J.; Wei, C.; Ding, B.; et al. Rice dwarf virus P2 protein hijacks auxin signaling by directly targeting the rice OsIAA10 protein, enhancing viral infection and disease development. PLoS Pathog. 2016, 12, e1005847. [Google Scholar] [CrossRef]
  48. Kundu, A.; Paul, S.; Dey, A.; Pal, A. High throughput sequencing reveals modulation of microRNAs in Vigna mungo upon Mungbean Yellow Mosaic India Virus inoculation highlighting stress regulation. Plant Sci. 2017, 257, 96–105. [Google Scholar] [CrossRef]
  49. Inaba, J.; Kim, B.M.; Shimura, H.; Masuta, C. Virus-induced necrosis is a consequence of direct protein-protein interaction between a viral RNA-silencing suppressor and a host catalase. Plant Physiol. 2011, 156, 2026–2036. [Google Scholar] [CrossRef]
  50. Mei, Y.; Wang, Y.; Hu, T.; Yang, X.; Lozano-Duran, R.; Sunter, G.; Zhou, X. Nucleocytoplasmic shuttling of the geminivirus C4 potein mediated by phosphorylation and myristoylation is critical for viral pathogenicity. Mol. Plant 2018, 11, 1466–1481. [Google Scholar] [CrossRef]
  51. Bilgin, D.D.; Liu, Y.; Schiff, M.; Dinesh-Kumar, S.P. P58IPK, a plant ortholog of double-stranded RNA-dependent protein kinase PKR inhibitor, functions in viral pathogenesis. Dev. cell 2003, 4, 651–661. [Google Scholar] [CrossRef]
  52. Pallas, V.; Garcia, J.A. How do plant viruses induce disease? Interactions and interference with host components. J. Gen. Virol. 2011, 92, 2691–2705. [Google Scholar] [CrossRef]
  53. Li, F.; Huang, C.; Li, Z.; Zhou, X. Suppression of RNA silencing by a plant DNA virus satellite requires a host calmodulin-like protein to repress RDR6 expression. PLoS Pathog. 2014, 10, e1003921. [Google Scholar] [CrossRef]
  54. Bazzini, A.A.; Hopp, H.E.; Beachy, R.N.; Asurmendi, S. Infection and coaccumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proc. Natl. Acad. Sci. USA 2007, 104, 12157–12162. [Google Scholar] [CrossRef] [Green Version]
  55. Yang, T.; Wang, Y.; Teotia, S.; Wang, Z.; Shi, C.; Sun, H.; Gu, Y.; Zhang, Z.; Tang, G. The interaction between miR160 and miR165/166 in the control of leaf development and drought tolerance in Arabidopsis. Sci. Rep. 2019, 9, 2832. [Google Scholar] [CrossRef]
  56. Yang, T.; Wang, Y.; Teotia, S.; Zhang, Z.; Tang, G. The making of leaves: How small RNA networks modulate leaf development. Front. Plant Sci. 2018, 9, 824. [Google Scholar] [CrossRef]
  57. Smith, N.A.; Eamens, A.L.; Wang, M.B. Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS Pathog. 2011, 7, e1002022. [Google Scholar] [CrossRef]
  58. Zhao, Y.F.; Peng, T.; Sun, H.Z.; Teotia, S.; Wen, H.L.; Du, Y.X.; Zhang, J.; Li, J.Z.; Tang, G.L.; Xue, H.W.; et al. miR1432-OsACOT (Acyl-CoA thioesterase) module determines grain yield via enhancing grain filling rate in rice. Plant Biotechnol. J. 2019, 17, 712–723. [Google Scholar] [CrossRef]
  59. Perez-Quintero, A.L.; Neme, R.; Zapata, A.; Lopez, C. Plant microRNAs and their role in defense against viruses: A bioinformatics approach. BMC Plant Biol. 2010, 10, 138. [Google Scholar] [CrossRef]
  60. Feng, H.; Wang, X.; Zhang, Q.; Fu, Y.; Feng, C.; Wang, B.; Huang, L.; Kang, Z. Monodehydroascorbate reductase gene, regulated by the wheat PN-2013 miRNA, contributes to adult wheat plant resistance to stripe rust through ROS metabolism. Biochim. Biophys. Acta 2014, 1839, 1–12. [Google Scholar] [CrossRef]
  61. Feng, H.; Duan, X.; Zhang, Q.; Li, X.; Wang, B.; Huang, L.; Wang, X.; Kang, Z. The target gene of tae-miR164, a novel NAC transcription factor from the NAM subfamily, negatively regulates resistance of wheat to stripe rust. Mol. Plant Pathol. 2014, 15, 284–296. [Google Scholar] [CrossRef]
  62. Xu, W.; Meng, Y.; Wise, R.P. Mla- and Rom1-mediated control of microRNA398 and chloroplast copper/zinc superoxide dismutase regulates cell death in response to the barley powdery mildew fungus. New Phytol. 2014, 201, 1396–1412. [Google Scholar] [CrossRef]
  63. Liu, J.; Cheng, X.; Liu, D.; Xu, W.; Wise, R.; Shen, Q.-H. The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling. PLoS Genet. 2014, 10, e1004755. [Google Scholar] [CrossRef]
  64. Yang, L.; Mu, X.; Liu, C.; Cai, J.; Shi, K.; Zhu, W.; Yang, Q. Overexpression of potato miR482e enhanced plant sensitivity to Verticillium dahliae infection. J. Integr. Plant Biol. 2015, 57, 1078–1088. [Google Scholar] [CrossRef]
  65. Zhao, W.; Li, Z.; Fan, J.; Hu, C.; Yang, R.; Qi, X.; Chen, H.; Zhao, F.; Wang, S. Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. J. Exp. Bot. 2015, 66, 4653–4667. [Google Scholar] [CrossRef]
  66. Ouyang, S.; Park, G.; Atamian, H.S.; Han, C.S.; Stajich, J.E.; Kaloshian, I.; Borkovich, K.A. MicroRNAs suppress NB domain genes in tomato that confer resistance to Fusarium oxysporum. PLoS Pathog. 2014, 10, e1004464. [Google Scholar] [CrossRef]
  67. Wei, C.; Kuang, H.; Li, F.; Chen, J. The I2 resistance gene homologues in Solanum have complex evolutionary patterns and are targeted by miRNAs. BMC Genom. 2014, 15, 743. [Google Scholar] [CrossRef]
  68. Zhu, Q.H.; Fan, L.; Liu, Y.; Xu, H.; Llewellyn, D.; Wilson, I. miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLoS ONE 2013, 8, e84390. [Google Scholar] [CrossRef]
  69. Liu, M.; Shi, Z.; Zhang, X.; Wang, M.; Zhang, L.; Zheng, K.; Liu, J.; Hu, X.; Di, C.; Qian, Q.; et al. Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat. Plants 2019. [Google Scholar] [CrossRef]
  70. Nicaise, V. Crop immunity against viruses: Outcomes and future challenges. Front. Plant Sci. 2014, 5, 660. [Google Scholar] [CrossRef]
  71. Takumi Shimizu, T.O.; Hiraguri, A.; Nakazono-Nagaoka, E.; Uehara-Ichiki, T.; Nakajima, M.; Akutsu, K.; Omura, T.; Sasaya, T. Strong resistance against rice grassy stunt virus is induced in transgenic rice plants expressing double-stranded RNA of the viral genes for nucleocapsid or movement proteins as targets for RNA interference. Phytopathology 2013, 103, 513–519. [Google Scholar] [CrossRef]
  72. Qu, F.; Ye, X.; Morris, T.J. Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc. Natl. Acad. Sci. USA 2008, 105, 14732–14737. [Google Scholar] [CrossRef]
  73. Qin, L.; Mo, N.; Zhang, Y.; Muhammad, T.; Zhao, G.; Zhang, Y.; Liang, Y. CaRDR1, an RNA-Dependent RNA polymerase plays a positive role in pepper resistance against TMV. Front. Plant Sci. 2017, 8, 1068. [Google Scholar] [CrossRef]
  74. Yang, S.J.; Carter, S.A.; Cole, A.B.; Cheng, N.H.; Nelson, R.S. A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc. Natl. Acad. Sci. USA 2004, 101, 6297–6302. [Google Scholar] [CrossRef]
  75. Hong, W.; Qian, D.; Sun, R.; Jiang, L.; Wang, Y.; Wei, C.; Zhang, Z.; Li, Y. OsRDR6 plays role in host defense against double-stranded RNA virus, Rice Dwarf Phytoreovirus. Sci. Rep. 2015, 5, 11324. [Google Scholar] [CrossRef]
  76. Morel, J.B.; Godon, C.; Mourrain, P.; Beclin, C.; Boutet, S.; Feuerbach, F.; Proux, F.; Vaucheret, H. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 2002, 14, 629–639. [Google Scholar] [CrossRef]
  77. Ren, B.; Guo, Y.; Gao, F.; Zhou, P.; Wu, F.; Meng, Z.; Wei, C.; Li, Y. Multiple functions of Rice dwarf phytoreovirus Pns10 in suppressing systemic RNA silencing. J. Virol. 2010, 84, 12914–12923. [Google Scholar] [CrossRef]
  78. Guo, H.; Song, X.; Xie, C.; Huo, Y.; Zhang, F.; Chen, X.; Geng, Y.; Fang, R. Rice yellow stunt rhabdovirus protein 6 suppresses systemic RNA silencing by blocking RDR6-mediated secondary siRNA synthesis. Mol. Plant Microbe Interact. MPMI 2013, 26, 927–936. [Google Scholar] [CrossRef]
  79. Zhang, X.; Yuan, Y.R.; Pei, Y.; Lin, S.S.; Tuschl, T.; Patel, D.J.; Chua, N.H. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006, 20, 3255–3268. [Google Scholar] [CrossRef]
  80. Anandalakshmi, R.; Marathe, R.; Ge, X.; Herr, J.M., Jr.; Mau, C.; Mallory, A.; Pruss, G.; Bowman, L.; Vance, V.B. A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 2000, 290, 142–144. [Google Scholar] [CrossRef]
  81. Iki, T.; Clery, A.; Bologna, N.G.; Sarazin, A.; Brosnan, C.A.; Pumplin, N.; Allain, F.H.T.; Voinnet, O. Structural flexibility enables alternative maturation, ARGONAUTE sorting and activities of miR168, a global gene silencing regulator in plants. Mol. Plant 2018, 11, 1008–1023. [Google Scholar] [CrossRef]
  82. Zhu, H.; Hu, F.; Wang, R.; Zhou, X.; Sze, S.H.; Liou, L.W.; Barefoot, A.; Dickman, M.; Zhang, X. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 2011, 145, 242–256. [Google Scholar] [CrossRef]
  83. Manavella, P.A.; Weigel, D.; Wu, L. Argonaute10 as a miRNA locker. Cell 2011, 145, 173–174. [Google Scholar] [CrossRef]
  84. Li, F.; Pignatta, D.; Bendix, C.; Brunkard, J.O.; Cohn, M.M.; Tung, J.; Sun, H.; Kumar, P.; Baker, B. MicroRNA regulation of plant innate immune receptors. Proc. Natl. Acad. Sci. USA 2012, 109, 1790–1795. [Google Scholar] [CrossRef] [Green Version]
  85. Guo, Z.; Wang, X.B.; Wang, Y.; Li, W.X.; Gal-On, A.; Ding, S.W. Identification of a new host factor required for antiviral RNAi and amplification of viral siRNAs. Plant Physiol. 2018, 176, 1587–1597. [Google Scholar] [CrossRef]
  86. Li, T.; Huang, Y.; Xu, Z.S.; Wang, F.; Xiong, A.S. Salicylic acid-induced differential resistance to the Tomato yellow leaf curl virus among resistant and susceptible tomato cultivars. BMC Plant Biol. 2019, 19, 173. [Google Scholar] [CrossRef]
  87. Yao, S.; Yang, Z.; Yang, R.; Huang, Y.; Guo, G.; Kong, X.; Lan, Y.; Zhou, T.; Wang, H.; Wang, W.; et al. Transcriptional regulation of miR528 by OsSPL9 orchestrates antiviral response in rice. Mol. Plant 2019. [Google Scholar] [CrossRef]
  88. Zhang, X.; Lai, T.; Zhang, P.; Zhang, X.; Yuan, C.; Jin, Z.; Li, H.; Yu, Z.; Qin, C.; Tor, M.; et al. Mini review: Revisiting mobile RNA silencing in plants. Plant Sci. 2019, 278, 113–117. [Google Scholar] [CrossRef]
  89. Hyodo, K.; Okuno, T. Host factors used by positive-strand RNA plant viruses for genome replication. J. Gen. Plant Pathol. 2014, 80, 123–135. [Google Scholar] [CrossRef]
  90. Yusa, A.; Neriya, Y.; Hashimoto, M.; Yoshida, T.; Fujimoto, Y.; Hosoe, N.; Keima, T.; Tokumaru, K.; Maejima, K.; Netsu, O.; et al. Functional conservation of EXA1 among diverse plant species for the infection by a family of plant viruses. Sci. Rep. 2019, 9, 5958. [Google Scholar] [CrossRef]
  91. Yamaji, Y.; Sakurai, K.; Hamada, K.; Komatsu, K.; Ozeki, J.; Yoshida, A.; Yoshii, A.; Shimizu, T.; Namba, S.; Hibi, T. Significance of eukaryotic translation elongation factor 1A in tobacco mosaic virus infection. Arch. Virol. 2010, 155, 263–268. [Google Scholar] [CrossRef]
  92. Xiong, R.; Wang, A. SCE1, the SUMO-conjugating enzyme in plants that interacts with NIb, the RNA-dependent RNA polymerase of Turnip mosaic virus, is required for viral infection. J. Virol. 2013, 87, 4704–4715. [Google Scholar] [CrossRef]
  93. Chen, Z.; Zhou, T.; Wu, X.; Hong, Y.; Fan, Z.; Li, H. Influence of cytoplasmic heat shock protein 70 on viral infection of Nicotiana benthamiana. Mol. Plant Pathol. 2008, 9, 809–817. [Google Scholar] [CrossRef]
  94. Bendahmane, A.; Farnham, G.; Moffett, P.; Baulcombe, D.C. Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J. 2002, 32, 195–204. [Google Scholar] [CrossRef]
  95. Bendahmane, A.; Kanyuka, K.; Baulcombe, D.C. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 1999, 11, 781–792. [Google Scholar] [CrossRef]
  96. Kachroo, P.; Yoshioka, K.; Shah, J.; Dooner, H.K.; Klessig, D.F. Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. Plant Cell 2000, 12, 677–690. [Google Scholar] [CrossRef]
  97. Sekine, K.T.; Ishihara, T.; Hase, S.; Kusano, T.; Shah, J.; Takahashi, H. Single amino acid alterations in Arabidopsis thaliana RCY1 compromise resistance to Cucumber mosaic virus, but differentially suppress hypersensitive response-like cell death. Plant Mol. Biol. 2006, 62, 669–682. [Google Scholar] [CrossRef]
  98. Zhang, C.; Hajimorad, M.R.; Eggenberger, A.L.; Tsang, S.; Whitham, S.A.; Hill, J.H. Cytoplasmic inclusion cistron of Soybean mosaic virus serves as a virulence determinant on Rsv3-genotype soybean and a symptom determinant. Virology 2009, 391, 240–248. [Google Scholar] [CrossRef]
  99. Kim, B.M.; Suehiro, N.; Natsuaki, T.; Inukai, T.; Masuta, C. The P3 protein of turnip mosaic virus can alone induce hypersensitive response-like cell death in Arabidopsis thaliana carrying TuNI. Mol. Plant Microbe Interact. MPMI 2010, 23, 144–152. [Google Scholar] [CrossRef]
  100. Jenner, C.E.; Sanchez, F.; Nettleship, S.B.; Foster, G.D.; Ponz, F.; Walsh, J.A. The cylindrical inclusion gene of Turnip mosaic virus encodes a pathogenic determinant to the Brassica resistance gene TuRB01. Mol. Plant Microbe Interact. MPMI 2000, 13, 1102–1108. [Google Scholar] [CrossRef]
  101. Zhang, H.; Tan, X.; He, Y.; Xie, K.; Li, L.; Wang, R.; Hong, G.; Li, J.; Li, J.; Taliansky, M.; et al. Rice black-streaked dwarf virus P10 acts as either a synergistic or antagonistic determinant during superinfection with related or unrelated virus. Mol. Plant Pathol. 2019. [Google Scholar] [CrossRef]
  102. Huang, R.; Li, Y.; Tang, G.; Hui, S.; Yang, Z.; Zhao, J.; Liu, H.; Cao, J.; Yuan, M. Dynamic phytohormone profiling of rice upon rice black-streaked dwarf virus invasion. J. Plant Physiol. 2018, 228, 92–100. [Google Scholar] [CrossRef]
  103. Zhang, H.; Tan, X.; Li, L.; He, Y.; Hong, G.; Li, J.; Lin, L.; Cheng, Y.; Yan, F.; Chen, J.; et al. Suppression of auxin signalling promotes rice susceptibility to Rice black streaked dwarf virus infection. Mol. Plant Pathol. 2019, 20. [Google Scholar] [CrossRef]
  104. Wang, C.; Wang, C.; Xu, W.; Zou, J.; Qiu, Y.; Kong, J.; Yang, Y.; Zhang, B.; Zhu, S. Epigenetic changes in the regulation of Nicotiana tabacum response to cucumber mosaic virus infection and symptom recovery through single-base resolution methylomes. Viruses 2018, 10, 402. [Google Scholar] [CrossRef]
  105. Zhao, J.H.; Fang, Y.Y.; Duan, C.G.; Fang, R.X.; Ding, S.W.; Guo, H.S. Genome-wide identification of endogenous RNA-directed DNA methylation loci associated with abundant 21-nucleotide siRNAs in Arabidopsis. Sci. Rep. 2016, 6, 36247. [Google Scholar] [CrossRef]
  106. Zhang, T.; Zhao, Y.; Ye, J.; Cao, X.; Xu, C.; Chen, B.; An, H.; Jiao, Y.; Zhang, F.; Yang, X.; et al. Establishing CRISPR/Cas13a immune system conferring RNA virus resistance in both dicot and monocot plants. Plant Biotechnol. J. 2019. [Google Scholar] [CrossRef]
  107. Ali, Z.; Abulfaraj, A.; Idris, A.; Ali, S.; Tashkandi, M.; Mahfouz, M.M. CRISPR/Cas9-mediated viral interference in plants. Genome Biol. 2015, 16, 238. [Google Scholar] [CrossRef] [Green Version]
  108. Zhou, Y.; Xu, Z.; Duan, C.; Chen, Y.; Meng, Q.; Wu, J.; Hao, Z.; Wang, Z.; Li, M.; Yong, H.; et al. Dual transcriptome analysis reveals insights into the response to Rice black-streaked dwarf virus in maize. J. Exp. Bot. 2016, 67, 4593–4609. [Google Scholar] [CrossRef]
  109. Munger, J.; Bennett, B.D.; Parikh, A.; Feng, X.-J.; McArdle, J.; Rabitz, H.A.; Shenk, T.; Rabinowitz, J.D. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 2008, 26, 1179. [Google Scholar] [CrossRef]
  110. Bi, J.; Yang, Y.; Chen, B.; Zhao, J.; Chen, Z.; Song, B.; Chen, J.; Yan, F. Retardation of the calvin cycle contributes to the reduced CO2 assimilation ability of rice stripe virus-infected N. benthamiana and suppresses viral infection. Front. Microbiol. 2019, 10, 568. [Google Scholar] [CrossRef]
  111. Massart, S.; Chiumenti, M.; De Jonghe, K.; Glover, R.; Haegeman, A.; Koloniuk, I.; Kominek, P.; Kreuze, J.; Kutnjak, D.; Lotos, L.; et al. Virus detection by high-throughput sequencing of small RNAs: Large-scale performance testing of sequence analysis strategies. Phytopathology 2019, 109, 488–497. [Google Scholar] [CrossRef]
  112. Schwab, R.; Ossowski, S.; Riester, M.; Warthmann, N.; Weigel, D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 2006, 18, 1121–1133. [Google Scholar] [CrossRef]
  113. Weiberg, A.; Jin, H. Small RNAs—The secret agents in the plant-pathogen interactions. Curr. Opin. Plant Biol. 2015, 26, 87–94. [Google Scholar] [CrossRef]
  114. Weiberg, A.; Wang, M.; Lin, F.M.; Zhao, H.; Zhang, Z.; Kaloshian, I.; Huang, H.D.; Jin, H. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 2013, 342, 118–123. [Google Scholar] [CrossRef]
  115. Zhang, T.; Zhao, Y.L.; Zhao, J.H.; Wang, S.; Jin, Y.; Chen, Z.Q.; Fang, Y.Y.; Hua, C.L.; Ding, S.W.; Guo, H.S. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2016, 2, 16153. [Google Scholar] [CrossRef]
  116. Zhou, Z.; Li, X.; Liu, J.; Dong, L.; Chen, Q.; Liu, J.; Kong, H.; Zhang, Q.; Qi, X.; Hou, D.; et al. Honeysuckle-encoded atypical microRNA2911 directly targets influenza A viruses. Cell Res. 2015, 25, 39–49. [Google Scholar] [CrossRef]
  117. Zhang, L.; Hou, D.; Chen, X.; Li, D.; Zhu, L.; Zhang, Y.; Li, J.; Bian, Z.; Liang, X.; Cai, X.; et al. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: Evidence of cross-kingdom regulation by microRNA. Cell Res. 2012, 22, 107–126. [Google Scholar] [CrossRef]
  118. Zhang, S.; Sang, X.; Hou, D.; Chen, J.; Gu, H.; Zhang, Y.; Li, J.; Yang, D.; Zhu, H.; Yang, X.; et al. Plant-derived RNAi therapeutics: A strategic inhibitor of HBsAg. Biomaterials 2019, 210, 83–93. [Google Scholar] [CrossRef]
  119. Tang, J.; Chu, C. MicroRNAs in crop improvement: Fine-tuners for complex traits. Nat. Plants 2017, 3, 17077. [Google Scholar] [CrossRef]
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Figure 1. The schematic diagram of biogenesis and action modes of small RNAs (sRNAs). MIR are transcripted by RNA polymerase II producing pri-miRNAs with hairpin structure. Mature miRNAs are produced by processing complex including Dicer-like RNase III (DCL), Hyponastic leaves/Double strand RNA binding protein (HYL/DRB), Serrate (SE), and Hua enhancer (HEN) proteins. Mature miRNA is incorporated into action mode complex to direct the target silencing by cleavage or methylation. Based on the difference in origin, siRNAs are divided into endogenous or exogenous siRNAs. Viral genome or replication intermediates all can form hairpin structure. Additionally, host native or viral siRNA-directed double strand RNAs are the origin of sRNAs’ biogenesis. Double strand RNAs are processed by processing complex, which mainly include DCL, Argonaut (AGO), Suppressor of genesilencing (SGS), and RDR (RNA-dependent RNA polymerase) proteins to produce siRNAs. Mature siRNA is incorporated into action mode complex to direct the target silencing by cleavage or methylation at transcriptional or post transcriptional level.
Figure 1. The schematic diagram of biogenesis and action modes of small RNAs (sRNAs). MIR are transcripted by RNA polymerase II producing pri-miRNAs with hairpin structure. Mature miRNAs are produced by processing complex including Dicer-like RNase III (DCL), Hyponastic leaves/Double strand RNA binding protein (HYL/DRB), Serrate (SE), and Hua enhancer (HEN) proteins. Mature miRNA is incorporated into action mode complex to direct the target silencing by cleavage or methylation. Based on the difference in origin, siRNAs are divided into endogenous or exogenous siRNAs. Viral genome or replication intermediates all can form hairpin structure. Additionally, host native or viral siRNA-directed double strand RNAs are the origin of sRNAs’ biogenesis. Double strand RNAs are processed by processing complex, which mainly include DCL, Argonaut (AGO), Suppressor of genesilencing (SGS), and RDR (RNA-dependent RNA polymerase) proteins to produce siRNAs. Mature siRNA is incorporated into action mode complex to direct the target silencing by cleavage or methylation at transcriptional or post transcriptional level.
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Figure 2. sRNAs-mediated viral pathogenic and resistant mechanisms. Left column of the figure is resistant mechanisms (A–D), right column of the figure is susceptible mechanisms (E–G). (A) Cotton leaf curl Burewala virus (CLCuBV) induces the expression of miR168. The miRNA can directly target virus genome, enhancing viral resistance. (B) Rice stripe virus (RSV) induces the accumulation of miR444. MADS23/27a/57 are targets of miR444, and they can bind to the promoter of RDR1 (RNA-dependent RNA polymerase), inhibiting the expression of RDR1. So, miR444 indirectly triggered RDR1-mediated viral resistance. (C) Plant hormone JA mediated viral resistance. Responsive to rice ragged stunt virus (RRSV) infection, miR319 is induced and negatively regulates TCP21, and further suppresses JA-mediated viral resistance. (D) In rice, AGO18 functions as a miRNA locker, competitively binding to miR168 or miR528 to increase AGO1- or ROS-mediated viral resistance. (E) CMV Y-Sat prompts the production of siRNAs by inducing the expression of AGO1. These siRNAs direct the cleavage of Chll (chlorophyll biosynthetic gene) mRNA. Tobacco Chll is responsible for the chlorophyll biogenesis, so, the plant displayed viral disease symptoms. (F) RSV infection suppresses the accumulation level of miR171b, which targets OsSCL6-IIabc to accelerate the accumulation of virus. (G) In tobacco, 21-nt nta-miR6020, which is derived from 22-nt miR3019, targets R protein, suppressing domain resistance.
Figure 2. sRNAs-mediated viral pathogenic and resistant mechanisms. Left column of the figure is resistant mechanisms (A–D), right column of the figure is susceptible mechanisms (E–G). (A) Cotton leaf curl Burewala virus (CLCuBV) induces the expression of miR168. The miRNA can directly target virus genome, enhancing viral resistance. (B) Rice stripe virus (RSV) induces the accumulation of miR444. MADS23/27a/57 are targets of miR444, and they can bind to the promoter of RDR1 (RNA-dependent RNA polymerase), inhibiting the expression of RDR1. So, miR444 indirectly triggered RDR1-mediated viral resistance. (C) Plant hormone JA mediated viral resistance. Responsive to rice ragged stunt virus (RRSV) infection, miR319 is induced and negatively regulates TCP21, and further suppresses JA-mediated viral resistance. (D) In rice, AGO18 functions as a miRNA locker, competitively binding to miR168 or miR528 to increase AGO1- or ROS-mediated viral resistance. (E) CMV Y-Sat prompts the production of siRNAs by inducing the expression of AGO1. These siRNAs direct the cleavage of Chll (chlorophyll biosynthetic gene) mRNA. Tobacco Chll is responsible for the chlorophyll biogenesis, so, the plant displayed viral disease symptoms. (F) RSV infection suppresses the accumulation level of miR171b, which targets OsSCL6-IIabc to accelerate the accumulation of virus. (G) In tobacco, 21-nt nta-miR6020, which is derived from 22-nt miR3019, targets R protein, suppressing domain resistance.
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Table
Table 1. The list of sRNAs involved in virus-plant interactions.
Table 1. The list of sRNAs involved in virus-plant interactions.
sRNA NamePutative Target(s)Virus(es)Putative Pathway(s)Reference
Osa-miR164OsNACRice ragged stunt virus (RRSV)leaf morphogenesis[40]
Osa-miR168OsAGO1aRice stripe virus (RSV)RNA silencing[41]
Osa-miR171bOsSCL6-IIa/b/cRSVchlorophyll biosynthesis[35]
Osa-miR319Teosinte branched/cycloidea/pcfRRSVJA biosynthesis and signaling pathway[40]
Osa-miR444OsMADS23/27a/57RSVviral immunity[32]
Osa-miR528OsAORSVL-ascorbic acid oxygen[33]
Tae-miR164TaNMORice black streaked dwarf virus (RBSDV)unknown[40]
Tae-miR319TaPCF8RBSDVJA biosynthesis and signaling pathway[40]
Ath-miR159AtMYB33/55Cucumber mosaic virus (CMV)unknown [42]
Ath-miR162AtDCL1Turnip yellow mosaic virus TuMVmiRNAs’ biogenesis[43]
Ath-miR165/166unknownCMV-LSunknown[42]
Nta-miR168AGO1CymRSV, crTMV, PVX, TEVantiviral mechanism[37]
Y-Satchlorophyll biosynthetic genesCMV Y-Satchlorophyll biogenesis[44]
Gh-miR162GhDCL2cotton leafroll dwarf polerovirus (CLRDV)pathogenic mechanism[31]
Gh-miR168cotton leaf curl Burewala virus (CLCuBV) genomeCLCuBVantiviral mechanism[45]
Gh-miR395adCLCuBV genomeCLCuBVantiviral mechanism[45]
vsi3114Contig28334CLCuDpathogenic mechanism[46]

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Zhang, B.; Li, W.; Zhang, J.; Wang, L.; Wu, J. Roles of Small RNAs in Virus-Plant Interactions. Viruses 2019, 11, 827. https://doi.org/10.3390/v11090827

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Zhang B, Li W, Zhang J, Wang L, Wu J. Roles of Small RNAs in Virus-Plant Interactions. Viruses. 2019; 11(9):827. https://doi.org/10.3390/v11090827

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Zhang, Baogang, Wenji Li, Jialin Zhang, Lu Wang, and Jianguo Wu. 2019. "Roles of Small RNAs in Virus-Plant Interactions" Viruses 11, no. 9: 827. https://doi.org/10.3390/v11090827

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