Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1 -- 3644 2022-11-03 15:51:33 |
2 format Meta information modification 3644 2022-11-04 02:30:56 |

Video Upload Options

Do you have a full video?


Are you sure to Delete?
If you have any further questions, please contact Encyclopedia Editorial Office.
Venkataraman, S.;  Badar, U.;  Shoeb, E.;  Hashim, G.;  Abouhaidar, M.;  Hefferon, K. Molecular Mechanisms of Viroids. Encyclopedia. Available online: (accessed on 20 April 2024).
Venkataraman S,  Badar U,  Shoeb E,  Hashim G,  Abouhaidar M,  Hefferon K. Molecular Mechanisms of Viroids. Encyclopedia. Available at: Accessed April 20, 2024.
Venkataraman, Srividhya, Uzma Badar, Erum Shoeb, Ghyda Hashim, Mounir Abouhaidar, Kathleen Hefferon. "Molecular Mechanisms of Viroids" Encyclopedia, (accessed April 20, 2024).
Venkataraman, S.,  Badar, U.,  Shoeb, E.,  Hashim, G.,  Abouhaidar, M., & Hefferon, K. (2022, November 03). Molecular Mechanisms of Viroids. In Encyclopedia.
Venkataraman, Srividhya, et al. "Molecular Mechanisms of Viroids." Encyclopedia. Web. 03 November, 2022.
Molecular Mechanisms of Viroids

Viroids are one of the most inscrutable single-stranded, structured, circular RNA pathogens of plants as well as the smallest infectious agents ever known. Despite being incapable of coding for any proteins, viroids affect susceptible plant hosts with visually discernible symptoms resembling those induced by several plant viruses. Diener, 1967, 1971 discovered and exemplified the Potato Spindle Tuber Viroid (PSTVd), the first viroid ever known. He coined the term “viroid” to represent this diminutive, naked, protein-free, circular RNA plant pathogen. This conceptualization of the viroid was further substantiated by Sänger, 1972 as well as Semancik and Weathers, 1972, who identified the citrus exocortis viroid (CEVd) that is responsible for causing the citrus exocortis disease. Another viroid, the chrysanthemum stunt viroid (CSVd) is also one of the viroids initially identified. 

viroids replication rolling circle pathogenicity

1. Biology of Viroids

Discovered in 1971, viroids are the smallest and simplest plant pathogens, ranging from 250 to 400 nucleotides of RNA, and are known as “living fossils of the hypothetical RNA World” [1]. These autonomous infectious agents are devoid of any protein coding capability and can survive without any protected membrane around their single-stranded, circular RNA genomes. Viroids can not only fight the host cellular mechanisms of RNA degradation but can also successfully replicate themselves using factors from the host plant, resulting in their spread throughout the plants and disease symptoms [2]. Angiosperms are reported as the only natural hosts of viroids [3].
The processes involved in viroid infection after entry into cells includes [4][5][6][7].
entry into a subcellular organelle (chloroplast or nucleus according to the type of viroid),
rolling circle replication within chloroplast or nucleus,
release out of the cell following replication,
transport into nearby cells,
entry into and within the phloem,
invasion of nonvascular cells from the phloem and,
repeat of the infection cycle.
The viroid genome does not encode for any protein, but instead spreads throughout the plant by recruiting host proteins using their own RNA folded structure. Functional motifs within the RNA structure are required for cellular trafficking in host plants [8]. The nucleotide sequence of the viroid is also important for interacting with the genome of the host. RNA-directed DNA methylation (RdDM) has been reported in viroid-infected plants [9][10] and examples of silencing of functional genes by individual viroid derived small RNA (vd-sRNA) have been reported [11][12][13].
Viroids replicate in host plants using host RNA polymerases that interact with the viroid RNA template, resulting in a higher than usual rate of errors in comparison to DNA replication. Hence, a given replicating viroid produces several mutants along with its original sequence, the mix being termed quasispecies [14][15]. These closely related quasispecies exhibit vast variation in their host invading capability, demonstrating that the property of infecting the host depends mainly on nucleotide sequence of the viroids. Furthermore, the cause of variability in symptoms of viroid infections also depends on viroid-host-environment interactions.
The cytopathology of family Pospiviroidae include cavity formation within the cell membrane and cell wall thickening [16]. Peach latent mosaic viroid (PLMVd) infections were demonstrated to lead to chloroplast malformations [17]. Tracking viroid cytopathic effects represents a promising approach to understand the links between disturbances at the cellular level and macroscopic symptoms [18][19].
Viroids are distinguished on the basis of their transmission within host plants following either vertical or horizontal patterns [20]. Pollen and ovules of a plant are responsible for transmission of viroid infections from parental plants through seeds and then seedlings to the next generation in the vertical mode of transmission; an example is the PSTVd. During horizontal transmission (an example is Tomato planta macho viroid), infection is transmitted to the next generation through the ovaries of a plant getting infected from physical contact of another plant without fertilization [21]. The degree of vertical and/or horizontal transmission of viroids depends on the molecular interaction of the viroid with the host plant, resulting in recognition and elimination of viroid RNA in the male gametophyte [22].
Mediator (MED) is a conserved protein complex in plants. According to recent reports, MED subunits exhibited differential expression patterns against different viroids, suggesting that the connection of the MED subunit transcriptional reprogramming with viroid infections resulted in differences in symptom development for different viroids [23].

2. Taxonomy and Classification of Viroids

According to the International Committee on Virus Taxonomy (ICTV), “rules concerned with the classification of viruses shall also apply to the classification of viroids” [24].
Viroid classification is based on secondary structure. Currently 32 species of viroids are recognized by ICTV. The observation of quasispecies poses an important taxonomic question for considering related viroid variants as of the same or different species. Less than 90% genome sequence identity was the first criterion taken into consideration and to be accompanied later by the possession of another distinguishing biological feature, in order to classify any two viroid species as distinct, as per the ICTV classification requirements [25].
Viroids are divided into two families: Avsunviroidae and Pospiviroidae [3][4][5][7][26][27][28]. Family Avsunviroidae contain three genera with members resembling ASBVd with branched secondary structures chloroplast-based symmetric rolling-circle replication mechanism and most importantly having ribozyme activities. On the other hand, family Pospiviroidae with five genera has PSTVd-like members, consisting of five major domains as secondary structures, asymmetric rolling-circle replication that occurs in the nucleus and are commonly devoid of any ribozyme activities. Avsunviroidae infect only dicotyledonous plants, both herbaceous and woody [29] while viroids of the family Pospiviroidae can infect both monocot and dicot plants [30].
The three genera of family Avsunviroidae are: Avsunviroid, Pelamoviroid, and Elaviroid. Species in the genus Avsunviroid, have a low content of G + C with rod-like secondary structure. Species of genus pelamoviroids have high G + C content with branched secondary structures. The single species of genus elaviroid have intermediate structural properties that are between those of the other two genera of the family [19].
Five genera of family Pospiviroidae are: Apscaviroid, Cocadviroid, Coleviroid, Hostuviroid and Pospiviroid. Each genus has a characteristic central conserved region (CCR) with least modifications, while the species of genera apscaviroids and pospiviroids have terminal conserved regions (TCR) and those of cocadviroids and hostuviroids have terminal conserved hairpins (TCH). The Coleviroid species are devoid of TCR and TCH [31]

3. Viroid Structure and Replication

PSTVd was the first viroid structure ever determined [32]; electron microscopy revealed that PSTV forms a secondary structure, and this was confirmed in 1978 [33][34].
Most of the known viroid species belong to the Pospiviroidae family, named after the type member, the PSTVd [4]. The Pospiviroidae adopt circular, internally base-paired, rod-like structures and their genomes consist of five distinct domains: The terminal left (TL), terminal right (TR), central (C), pathogenic (P) and variable (V) domains. The pathogenicity domain possesses relatively low thermodynamic stability (or pre-melting) due to the presence of an oligopyrimidine stretch in most of the Pospiviroidae, the V domain is the most variable region, and the C domain is most highly conserved.
To date, only four viroids have been identified as belonging to the Avsunviroidae family, named after ASBVd. These types of viroids lack a conserved central region but retain rod-like and branched regions like Pospiviroidae viroids. However, unlike Pospiviroidae viroids, Avsunviriodae members can form hammerhead ribozyme motifs in both polarities which mediate cleavage of their replication intermediates, while RNA cleavage within Pospiviroidae family members takes place using host enzymes [4].
The replicative mechanism of viroids operates through two alternative pathways depending in whether it is mediated by one or two rolling circles [35]. The first pathway is called asymmetric, typical of Pospiviroidae and is mediated by a single rolling circle wherein the incoming circular positive sense viroid RNA genome is repeatedly transcribed to form multimeric, linear (−) strands. Thereupon, in the next step, these (−) sense concatemers serve as templates for the synthesis of multimeric, linear (+) strand concatemers which subsequently are cleaved into monomeric (+) circles. In the alternate second pathway called symmetric, typical of Avsunviroidae [36], replication operates through two rolling circles wherein the multimeric linear (−) strands generated from the (+) sense RNA genome of the viroid undergo cleavage and ligation to generate circular (−) strand RNA monomers. These (−) strand circles then act as templates for the subsequent generation of linear, multimeric (+) strands which then cleave into (+) sense monomer genomes.
For PSTVd, the type member of Pospiviroidae, the absence of circular monomeric (−) sense RNA in plants after natural infection supports the asymmetric model of replication [37][38]. On the other hand, for the ASBVd (the type member of Avsunviroidae) it has been shown by in vitro studies that both (+) and (−) dimeric RNAs are able to self-cleave, thus supporting the model of symmetric replication [39][40]. Additionally, it has been observed in ASBVd-infected avocado that both monomeric circular (+) and (−) strands occur in multistranded complexes substantiating that ASBVd replication occurs through two rolling circles [41][42].
Members of the Pospiviriodae replicate in the nucleus [43]. Replication is initiated from a precise site, thus implying the possibility of existing viroid promoters. The processes of cleavage and ligation in the Pospiviroidae family are thought to be catalyzed by a host enzyme similar to RNase III and an RNA ligase that supports the circularization process. The two enzymes can circularize the viroid by covalent fusion of both 5′ and 3′ termini. Researchers have not identified whether chloroplastic RNA ligase is necessary for the circulation process or whether autocatalysis takes place.
Avsunviroidae replication takes place within chloroplasts. The mode of entry and exit into the chloroplasts is still debatable as it is not well identified [43].
The accumulation of Avsunviriodae (+) and (−) strands in the chloroplast indicates the involvement of enzymatic machinery of the chloroplast in the replication cycle; in contrast, accumulation of the Pospiviroidea RNA strands in the nucleus suggests the involvement of nuclear RNA polymerase and other cellular enzymes in their replication cycle [35].

4. Movement and Systemic Trafficking of Viroid RNAs

Viroids are subviral pathogens that cause infection in several crop plants, leading to considerable yield losses [44]. Within the plants, viroid RNA moves to adjacent cells through plasmodesmata and, via the phloem, to distant sink organs [45]. Viroids have recently emerged as ideal model systems to study RNA transport within and between cells [45]. Conventional viroid infection of a host plant comprises a series of coordinated steps that involve both intracellular movement and intercellular movement.
Mutational experiments of viroids have identified RNA motifs within the viroid genome that are important for cell-to-cell trafficking. For PSTVd, this consists of 27 RNA loop motifs separated by short helices [41][46][47]. An RNA motif of PSTVd was found to be essential for trafficking from bundle-sheath cells into mesophyll cells when the viroid was exiting in the phloem of young tobacco leaves [48]. Whereas in Nicotiana benthamiana, a different RNA motif was required for movement of PSTVd from the bundle sheath cells into the phloem [49]. Furthermore, 11 out of 27 loops of PSTVd RNA motifs are important for cell-to-cell movement and intercellular spread and these RNA motifs could also be involved in the trafficking of viral and cellular RNAs [50]. Loop 19 was identified for viroid movement from palisade to spongy mesophyll cell of N. benthamiana [51], while loop 6 had previously been shown to be essential for palisade-to-spongy mesophyll trafficking [52]. These studies enlighten the potential functions of plasmodesmata (PD), as different RNA motifs are required to transit PD at different cell-to-cell interfaces. It was also identified that different RNA motifs can be used to transit across the same cellular interface.
Various experiments have been performed to identify viroid RNA movement. Microinjection experiments using infectious RNA transcripts and labeled with the fluorescent dye TOTO-1 iodide have shown that PSTVd can move rapidly from cell to cell via the plasmodesmata in tobacco mesophyll cells [53]. It was also observed that PSTVd RNA accumulates in the nuclei of both the injected cell and neighboring cells. Using dot-blot hybridization to monitor PSTVd distribution in infected tomato seedlings, it was found that the movement pattern of PSTVd was indistinguishable from that of most plant viruses at the whole plant level [53].

5. Seed, Pollen and Insect Transmission of Viroids

Most of the viroids are disseminated through human activities during planting and through trade in materials of the plants, such as seeds and tissue culture stocks, but some viroids have evolved specific mechanisms exploiting the plants′ processes of reproduction and are transmitted via seed and/or pollen [54][55][56]. Pollen is an important breeding biological tool of germplasm naturally found to be associated with number of viroids, known as being pollen-transmitted [57]. Transmission of viroids by pollen can be horizontal, contaminating a fertilized flower, or can be vertical which is more common when infected pollen fertilize and infect the resulting seed [58]. Pollen transmitted PSTVd and PCFVd have been detected in tomato (Solanum lycopersicum) crops [59].
The rate at which infected seeds produce infected plants is called the seed transmission rate. The lower rate of seed-transmission in PSTVd could be due to the restricted movement of viroids in floral organs. In Nicotiana benthamiana and Solanum lycopersicum, the accumulation of PSTVd was not observed in the petals, ovary and stamens, but detected only in the sepals [60]. In petunia, PSTVd is seed-transmitted either through viroid-carrying pollen grains or embryo sacs.
Tomato chlorotic dwarf viroid (TCDVd) of the genus Pospiviroid infects Solanum lycopersicum and is distributed in the ovary and ovules but not in the shoot apical meristem [61][62]. Matsushita et al. [62] reported that TCDVd was found on the surface of the seed coat.
In Capsicum annuum L. PCFVd, another Pospiviroid, was reported to be seed-transmitted [63]. The presence of the Pospiviroids GYSVd 1 and HSVd were found in Vitis vinifera seedlings [64].
ASBVd is an example of Avsunviroid transmitted from infected trees to the seeds of the next generation [65][66][67]. Another species of family Avsunviroidae genus Pelamoviroid, PLMVd, is not reported to be pollen transmitted and is not seed-transmitted [68][69][70]. The only known species of genus Elaviroid in the family Avsunviroidae Eggplant latent viroid (ELVd), which is reported to be seed-transmitted via eggplants [71][72].
Additionally, insect-transmitted mechanical inoculation of viroids was demonstrated to be a source of infection through plants via pollen [73]. Insect pests are known for their tendency to transmit PSTVd to Solanum tuberosum (potato) [74]. Myzus persicae, commonly known as green peach, aphid-transmitted PSTVd from other plants coinfected with viruses [75][76][77]. Apple scar skin viroid (ASSVd) was found to be transmitted by Trialeurodes vaporariorum (whitefly) from viroid-infected plants to cucumber, bean, tomato and pea plants [78].

6. Pathogenicity of Viroids

The first complete sequence of the PSTVd was reported by Gross et al. [33]. However, it was assumed that viroid pathogenicity was due to direct interaction with one or more of the host cellular constituents and or by indirect interaction via RNA silencing. Viroid pathogenesis has been shown to be increased due to the interaction with nuclear and cytoplasmic RNAs which results in the activation of protein kinases. It has been reported by Hiddinga et al. [79] that a 68-kDa protein extracted from viroid infected tissues is differentially phosphorylated, and that dsRNA dependent protein kinases similar to their equivalents in mammalian cells are involved in the regulation of viroid synthesis. In this case, the binding of protein kinases enhanced viroid pathogenicity. The PSTVd strains produced different symptoms with only 3–4 nucleotides changed [80] and this change could alter the protein binding site resulting in abnormal function [81]. Infectious cDNA clones were first constructed for PSTVd [82] and then for other viroids to determine their pathogenic determinants [83][84][85]. It is also noticeable that in some cases, viroid accumulation to high titers is observed although the plants are asymptomatic or while on the contrary, other viroids at low titers cause severe symptoms, which represents the contribution of alternative mechanisms [86].
At the microscopic level, the cytopathogenic effects of viroids on host cellular structures have been reported. For example, for some viroid infections, there is an abnormal development of cytoplasmic membranes to form “plasmalemmasomes”, irregular thickening of cell walls [87], chloroplast abnormalities and electron-dense deposits in the cytoplasm and chloroplasts [18].
In recent studies, various molecular mechanisms are involved in the induction of viroid diseases and in this context, RNA silencing has a crucial role in viroid pathogenesis. RNA silencing was first identified in plants and then in other eukaryotes, where it provides other novel regulatory roles in addition to translation. There is very strong evidence that the combined action of the structure-specific dicer-like proteins and the sequence-specific RNA induced silencing complex curb plant RNA and DNA virus infections as well as viroid infections [88][89][90][91][92][93].

7. Viroid-Host Interactions

Being naked, noncoding RNA molecules, viroids induce disease through direct interaction of their genome with some of the host factors. Despite their simplicity in both genome and structure, viroids elicit complex responses in their host plants wherein even with minor changes in their nucleotide sequence, they can induce entirely different symptoms in their host plants based on the cultivar [94]. In general, all viroids elicit “pathogenesis-related” [PR] proteins during their infection cycle [95].
Earlier, the PSTVd was shown to associate with several nuclear and histone proteins of tomato [96]. Initial investigations of the leaf proteins of tomato plants infected with PSTVd revealed a significant increase in the levels of the PR protein, P14 [97]. Introspection into the expression of genes involved in stress response, defense response, chloroplast function and cell wall structure revealed altered expression depending on severity of PSTVd infection [98][99]. In another study, the wheat germ RNA polymerase II was shown to interact with terminal loops of the PSTVd [100]. Martínez de Alba et al. [101], demonstrated that the tomato Virp1 bromodomain-containing protein bound to the PSTVd 71-nucleotide bulged TR hairpin structure and that this association played a significant role in systemic spread of the PSTVd [102]. The tomato protein, p68 involved with the ds-RNA-induced protein kinase activity was shown to be differentially phosphorylated by the PSTVd [103][104]. Moreover, the PSTVd was demonstrated to differentially activate the p68 protein based on the severity of the viroid strain, thus implicating the p68 protein in viroid pathogenesis. Interestingly, this differential p68 activation was detected with strains of PSTVd that varied only by a single two-nucleotide inversion within the lower pathogenicity domain of the PSTVd which caused minor variations in their secondary structures. Hammond and Zhao, [105] reported increased transcription of a novel protein kinase (PKV protein) in tomatoes infected by PSTVd depending on the severity of infection. Additionally, they also showed down-regulation of genes responsible for chloroplast biogenesis as well as impacts on the mRNA levels involved in gibberellin biosynthesis and those of some of the signaling hormones. The PSTVd replicates in the nucleus for which the replication start site is present within the hairpin loop of the TL region of its secondary structure and transcription is mediated by the host DNA-dependent RNA polymerase II [106]. In Arabidopsis thaliana, the transcription factor IIIA [TFIIIA] and the ribosomal protein L5 [RPL5] have been shown to play a role in PSTVd replication by binding to the (+) strand of the viroid [107]. Additionally, in Nicotiana benthamiana, the canonical 9-zinc finger [ZF] Transcription Factor IIIA [TFIIIA-9ZF] as well as its variant TFIIIA-7ZF were demonstrated to interact with the PSTVd (+) strand while only the latter recognized the PSTVd (−) strand. Plus, the expression levels of TFIIIA-7ZF directly correlated with viroid replication [108]. PSTVd reportedly recruits the RPL5 splicing regulator to interact with the CCR that plays a critical role in its replication [109][110].
The Cucumis sativus Phloem Protein 2 RNA binding protein [CsPP2] was shown to be associated with long distance movement of HSVd RNA by forming a ribonucleoprotein complex [111][112]. The CsPP2 was also demonstrated to enhance the efficiency of transfer of the ASSVd through the Trialeurodes vaporariorum [Tv] Whitefly [78]. To-date, the Virp1 and CsPP2 proteins are the best elucidated factors shown to be involved in translocation of the Pospiviroidae. Among Avsunviroidae, the ASBVd infection in avocado revealed the involvement of PARBP33 and PARBP35 chloroplast RNA-binding proteins with the self-cleavage of ASBVd multimer transcripts mediated through hammerhead ribozyme [113].
Tomato plants infected with CEVd showed changes in levels of proteins involved in translation [114]. Additionally, CEVd reportedly induced as well as reduced in vitro phosphorylation of a wide range of proteins when infecting its host plants particularly, at the beginning of symptom appearance [115]. These changes in phosphorylation were enhanced in the presence of Mn2+, demonstrating the significance of Mn2+-dependent protein kinase action on the varied phosphorylation patterns. In this context, Hidding et al., 1988 [79] reported enhancement in the phosphorylation of a 68 kDa host protein homologous to the human ds-RNA-dependent protein kinase in tomato plants infected with PSTVd. Cottilli et al., 2019 [116] demonstrated changes in the translational machinery of tomato plants infected with the CEVd. They detected the presence of the CEVd within the ribosomal fractions and the CEVd impacted the polysome profiles, specifically causing the accumulation of the 40S ribosomal subunit. The CEVd was also shown to alter ribosome biogenesis and 18S rRNA maturation. Further, the levels of the ribosomal stress mediator NAC082 was increased in infected leaves. These changes correlated with the extent of disease symptoms caused by CEVd. Therefore, these findings showed that in tomato plants CEVd causes defective ribosome biogenesis and impacts the machinery of translation resulting in ribosomal stress.
Viroids, even without having any ability to code for proteins, impact the translational machinery. The CEVd has been demonstrated to cause changes in the accretion of ribosomal proteins such as S3, S5 and L10 in tomato plants [114]. It also impacts the levels of the eEF1A, eEF2 and eIF5A eukaryotic translation factors in these plants. Certain viroids have been reported to associate with the eIF1A or with the L5 ribosomal protein [107][114][117]. The HSVd elicits alterations in the DNA methylation patterns of the rRNA genes in host plants and results in increased accumulation of some of the rRNA-derived sRNAs [118]. HSVd caused demethylation of some of the rRNA genes leading to transcriptional reactivation of these genes, suggesting a novel molecular mechanism putatively involved in viroid pathogenicity. Moreover, it has been shown that the PSTVd induces degradation of ribosomal protein S3a-like mRNAs in infected tomato plants [119].
Further, an augmented number of differentially regulated genes was observed in peach plants doubly infected with both PLMVd and Prunus necrotic ringspot virus (PNRSV) when compared to those of single infections with either of the two viroids. The double infection also caused a synergistic impact on the peach fruit transcriptome [120]. The PLMVd (that replicates in chloroplasts) upon infection of Prunus persica (peach) induced the expression of six potential RNA-binding polypeptides, one of which is the elongation factor 1-alpha [eEF1A].


  1. Steger, G.; Riesner, D. Viroid research and its significance for RNA technology and basic biochemistry. Nucleic Acids Res. 2018, 46, 10563–10576. [Google Scholar] [CrossRef][Green Version]
  2. Tsagris, E.M.; Martínez de Alba, A.E.; Gozmanova, M.; Kalantidis, K. Viroids. Cell. Microbiol. 2008, 10, 2168–2179. [Google Scholar]
  3. Diener, T.O. Viroids: “Living fossils” of primordial RNAs? Biol. Direct 2016, 11, 15. [Google Scholar] [CrossRef][Green Version]
  4. Singh, R.P.; Ready, K.F.M.; Nie, X. Biology; CSIRO Publishing: Collingwood, VIC, Australia, 2003. [Google Scholar]
  5. Góra-Sochacka, A. Viroids: Unusual small pathogenic RNAs. Acta Biochim. Pol. 2004, 51, 587–607. [Google Scholar] [CrossRef][Green Version]
  6. Takeda, R.; Ding, B. Viroid intercellular trafficking: RNA motifs, cellular factors and broad impacts. Viruses 2009, 1, 210–221. [Google Scholar] [CrossRef][Green Version]
  7. Dalakouras, A.; Dadami, E.; Wassenegger, M. Viroid-induced DNA methylation in plants. Biomol. Concepts 2013, 4, 557–565. [Google Scholar] [CrossRef]
  8. Dalakouras, A.; Dadami, E.; Wassenegger, M.; Krczal, G.; Wassenegger, M. RNA-directed DNA methylation efficiency depends on trigger and target sequence identity. Plant J. 2016, 87, 202–214. [Google Scholar] [CrossRef][Green Version]
  9. Matousek, J.; Kozlová, P.; Orctová, L.; Schmitz, A.; Pesina, K.; Bannach, O.; Diermann, N.; Steger, G.; Riesner, D. Accumulation of viroid-specific small RNAs and increase in nucleolytic activities linked to viroid-caused pathogenesis. Biol. Chem. 2007, 388, 1–13. [Google Scholar]
  10. Diermann, N.; Matoušek, J.; Junge, M.; Riesner, D.; Steger, G. Characterization of plant miRNAs and small RNAs derived from potato spindle tuber viroid (PSTVd) in infected tomato. Biol. Chem. 2010, 391, 1379–1390. [Google Scholar] [CrossRef]
  11. Adkar-Purushothama, C.R.; Brosseau, C.; Giguère, T.; Sano, T.; Moffett, P.; Perreault, J.-P. Small RNA derived from the virulence modulating region of the potato spindle tuber viroid silences callose synthase genes of tomato plants. Plant Cell 2015, 27, 2178–2194. [Google Scholar] [CrossRef][Green Version]
  12. Flores, R.; De La Peña, M.; Navarro, J.-A.; Ambrós, S.; Navarro, B. Molecular biology of viroids. In Molecular Biology of Plant Viruses; Mandahar, C.L., Ed.; Springer: Boston, MA, USA, 1999; pp. 225–239. [Google Scholar]
  13. Bull, J.J.; Meyers, L.A.; Lachmann, M. Quasispecies Made Simple. PLoS Comput. Biol. 2005, 1, e61. [Google Scholar] [CrossRef][Green Version]
  14. Serra, P.; Hashemian, S.M.B.; Fagoaga, C.; Romero, J.; Ruiz-Ruiz, S.; Gorris, M.T.; Bertolini, E.; Duran-Vila, N. Virus-viroid interactions: Citrus tristeza virus enhances the accumulation of citrus dwarfing viroid in mexican lime via virus-encoded silencing suppressors. J. Virol. 2013, 88, 1394–1397. [Google Scholar] [CrossRef][Green Version]
  15. Rodio, M.-E.; Delgado, S.; De Stradis, A.; Gómez, M.-D.; Flores, R.; Di Serio, F. A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell 2007, 19, 3610–3626. [Google Scholar]
  16. Di Serio, F.; De Stradis, A.; Delgado, S.; Flores, R.; Navarro, B. Cytopathic effects incited by viroid RNAs and putative underlying mechanisms. Front. Plant Sci. 2013, 3, 288. [Google Scholar] [CrossRef][Green Version]
  17. Di Serio, F.; Li, S.-F.; Matoušek, J.; Owens, R.A.; Pallás, V.; Randles, J.W.; Sano, T.; Verhoeven, J.T.J.; Vidalakis, G.; Flores, R.; et al. ICTV virus taxonomy profile: Avsunviroidae. J. Gen. Virol. 2018, 99, 611–612. [Google Scholar] [CrossRef]
  18. Faggioli, F.; Luigi, M.; Sveikauskas, V.; Olivier, T.; Marn, M.V.; Plesko, I.M.; De Jonghe, K.; Van Bogaert, N.; Grausgruber-Gröger, S. An assessment of the transmission rate of four pospiviroid species through tomato seeds. Eur. J. Plant Pathol. 2015, 143, 613–617. [Google Scholar] [CrossRef]
  19. Matsushita, Y.; Yanagisawa, H.; Sano, T. Vertical and horizontal transmission of pospiviroids. Viruses 2018, 10, 706. [Google Scholar] [CrossRef][Green Version]
  20. Matoušek, J.; Steinbachová, L.; Drábková, L.Z.; Kocábek, T.; Potěšil, D.; Mishra, A.K.; Honys, D.; Steger, G. Elimination of viroids from tobacco pollen involves a decrease in propagation rate and an increase of the degradation processes. Int. J. Mol. Sci. 2020, 21, 3029. [Google Scholar] [CrossRef]
  21. Nath, V.S.; Shrestha, A.; Awasthi, P.; Mishra, A.K.; Kocábek, T.; Matoušek, J.; Sečnik, A.; Jakše, J.; Radišek, S.; Hallan, V. Mapping the gene expression spectrum of mediator subunits in response to viroid infection in plants. Int. J. Mol. Sci. 2020, 21, 2498. [Google Scholar] [CrossRef][Green Version]
  22. King, A.M.Q.; Lefkowitz, E.; Adams, M.J.; Carstens, E.B. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses; Elsevier: Amsterdam, The Netherlands, 2011; Volume 9. [Google Scholar]
  23. Rocheleau, L.; Pelchat, M. The subviral RNA database: A toolbox for viroids, the hepatitis delta virus and satellite RNAs research. BMC Microbiol. 2006, 6, 24. [Google Scholar]
  24. Ding, B.; Zhong, X. Viroids/Virusoids. In Microbiology, 3rd ed.; Elsevier: Amsterdam, The Netherlands, 2009; pp. 535–545. [Google Scholar]
  25. Matsushita, Y.; Tsuda, S. Host ranges of Potato spindle tuber viroid, Tomato chlorotic dwarf viroid, Tomato apical stunt viroid, and Columnea latent viroid in horticultural plants. Eur. J. Plant Pathol. 2014, 141, 193–197. [Google Scholar] [CrossRef]
  26. Flores, R.; Di Serio, F.; Hernández, C. Viroids: The noncoding genomes. Semin. Virol. 1997, 8, 65–73. [Google Scholar] [CrossRef]
  27. Adkar-Purushotama, C.R.; Perreault, J.P. Impact of nucleic acid sequencing on viroid biology. Int. J. Mol. Sci. 2020, 21, 5532. [Google Scholar]
  28. Gross, H.J.; Domdey, H.; Lossow, C.; Jank, P.; Raba, M.; Alberty, H.; Singer, H.L. Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 1978, 273, 203–208. [Google Scholar]
  29. Daròs, J.; Elena, S.F.; Flores, R. Viroids: An Ariadne’s thread into the RNA labyrinth. EMBO Rep. 2006, 7, 593–598. [Google Scholar] [CrossRef][Green Version]
  30. Clark, D.P.; Pazdernik, N.J.; McGehee, M.R. Chapter 24-viruses, viroids, and prions. In Molecular Biology, 3rd ed.; Clark, D.P., Pazdernik, N.J., McGehee, M.R., Eds.; Academic Cell; Elsevier: Amsterdam, The Netherlands, 2019; pp. 749–792. [Google Scholar]
  31. Branch, A.D.; Benenfeld, B.J.; Robertson, H.D. Evidence for a single rolling circle in the replication of potato spindle tuber viroid. Proc. Natl. Acad. Sci. USA 1988, 85, 9128–9132. [Google Scholar]
  32. Feldstein, P.A.; Hu, Y.; Owens, R.A. Precisely full length, circularizable, complementary RNA: An infectious form of potato spindle tuber viroid. Proc. Natl. Acad. Sci. USA 1998, 95, 6560–6565. [Google Scholar] [CrossRef][Green Version]
  33. Flores, R.; Daròs, J.A.; Hernandez, C. The Avsunviroidae family: Viroids with hammerhead ribozymes. Adv. Virus Res. 2000, 55, 271–323. [Google Scholar]
  34. Hutchins, C.J.; Rathjen, P.D.; Forster, A.C.; Symons, R.H. Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res. 1986, 14, 3627–3640. [Google Scholar] [CrossRef]
  35. Navarro, J.A.; Daròs, J.A.; Flores, R. Complexes containing both polarity strands of avocado sunblotch viroid: Identification in chloroplasts and characterization. Virology 1999, 253, 77–85. [Google Scholar]
  36. Daròs, J.A.; Marcos, J.F.; Hernandez, C.; Flores, R. Replication of avocado sunblotch viroid: Evidence for a symmetric pathway with two rolling circles and hammerhead ribozyme processing. Proc. Natl. Acad. Sci. USA 1994, 91, 12813–12817. [Google Scholar]
  37. Flores, R.; Minoia, S.; López-Carrasco, A.; Delgado, S.; De Alba, A.E.M.; Kalantidis, K. Viroid replication. In Viroids and Satellites; Academic Press: Oxford, UK, 2017; pp. 71–81. [Google Scholar]
  38. Diener, T.O. Viroids and the Nature of Viroid Diseases; Springer: Vienna, Austria, 1999; Volume 15. [Google Scholar]
  39. Zhong, X.; Archual, A.J.; Amin, A.A.; Ding, B. A Genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 2008, 20, 35–47. [Google Scholar] [CrossRef][Green Version]
  40. Steger, G.; Perreault, J.-P. Structure and associated biological functions of viroids. Adv. Virus Res. 2016, 94, 141–172. [Google Scholar] [CrossRef]
  41. Zhong, X.; Tao, X.; Stombaugh, J.; Leontis, N.B.; Ding, B. Tertiary structure and function of an RNA motif required for plant vascular entry to initiate systemic trafficking. EMBO J. 2007, 26, 3836–3846. [Google Scholar] [CrossRef]
  42. Jiang, D.; Wang, M.; Li, S. Functional analysis of a viroid RNA motif mediating cell-to-cell movement in Nicotiana benthamiana. J. Gen. Virol. 2017, 98, 121–125. [Google Scholar] [CrossRef]
  43. Takeda, R.; Petrov, A.I.; Leontis, N.B.; Ding, B. A Three-Dimensional RNA Motif in Potato spindle tuber viroid Mediates Trafficking from Palisade Mesophyll to Spongy Mesophyll in Nicotiana benthamiana. Plant Cell 2011, 23, 258–272. [Google Scholar] [CrossRef][Green Version]
  44. Ding, B.; Kwon, M.-O.; Hammond, R.; Owens, R. Cell-to-cell movement of potato spindle tuber viroid. Plant J. 1997, 12, 931–936. [Google Scholar] [CrossRef]
  45. Palukaitis, P. Potato spindle tuber viroid: Investigation of the long-distance, intra-plant transport route. Virology 1987, 158, 239–241. [Google Scholar] [CrossRef]
  46. Mink, G.I. Pollen and seed-transmitted viruses and viroids. Annu. Rev. Phytopathol. 1993, 31, 375–402. [Google Scholar]
  47. Johansen, E.; Edwards, M.C.; Hampton, R.O. Seed transmission of viruses: Current perspectives. Annu. Rev. Phytopathol. 1994, 32, 363–386. [Google Scholar]
  48. Hull, R. Transmission 2: Mechanical, Seed, Pollen and Epidemiology; Elsevier Academic Press: Amsterdam, The Netherlands, 2004. [Google Scholar]
  49. Card, S.D.; Pearson, M.N.; Clover, G.R.G. Plant pathogens transmitted by pollen. Australas. Plant Pathol. 2007, 36, 455–461. [Google Scholar] [CrossRef]
  50. Constable, F.E.; Chambers, G.; Penrose, L.; Daly, A.; Mackie, J.; Davis, K.; Rodoni, B.; Gibbs, M. Viroid-infected tomato and capsicum seed shipments to Australia. Viruses 2019, 11, 98. [Google Scholar] [CrossRef][Green Version]
  51. Zhu, Y.; Qi, Y.; Xun, Y.; Owens, R.; Ding, B. Movement of potato spindle tuber viroid reveals regulatory points of phloem-mediated RNA Traffic. Plant Physiol. 2002, 130, 138–146. [Google Scholar] [CrossRef][Green Version]
  52. Matsushita, Y.; Tsuda, S. Distribution of potato spindle tuber viroid in reproductive organs of petunia during its developmental stages. Phytopathology 2014, 104, 964–969. [Google Scholar] [CrossRef][Green Version]
  53. Singh, R.P.; Dilworth, A.D. Tomato chlorotic dwarf viroid in the ornamental plant Vinca minor and its transmission through tomato seed. Eur. J. Plant Pathol. 2008, 123, 111–116. [Google Scholar] [CrossRef]
  54. Matsushita, Y.; Usugi, T.; Tsuda, S. Distribution of tomato chlorotic dwarf viroid in floral organs of tomato. Eur. J. Plant Pathol. 2011, 130, 441–447. [Google Scholar] [CrossRef]
  55. Verhoeven, J.T.J.; Jansen, C.C.C.; Roenhorst, J.W.; Flores, R.; de la Penã, M. Pepper chat fruit viroid: Biological and molecular properties of a proposed new species of the genus Pospiviroid. Virus Res. 2009, 144, 209–214. [Google Scholar]
  56. Wan Chow Wah, Y.F.; Symons, R.H. Transmission of viroids via grape seeds. J. Phytopathol. 1999, 147, 285–291. [Google Scholar]
  57. Wallace, J.M.; Drake, R.J. A high rate of seed transmission of avacado sun bloth virus from symptomless trees and the origin of such trees. Phytopathology 1962, 52, 237–241. [Google Scholar]
  58. Desjardins, P.R.; Drake, R.J.; Atkins, E.L.; Bergh, O. Pollen transmission of Avacado Sunblotch Virus experimentally demonstrated. Calif. Agric. 1979, 33, 14–15. [Google Scholar]
  59. Desjardins, P.R.; Drake, R.J.; Sasaki, P.J.; Atkins, E.L.; Bergh, O. Pollen transmission of avocado sunblotch viroid and the fate of the pollen recipient tree. Phytopathology 1984, 74, 845. [Google Scholar]
  60. Howell, W.; Skrzeczkowski, L.; Mink, G.; Nunez, A.; Wessels, T. Non-transmission of apple scar skin viroid and peach latent mosaic viroid through seed. Acta Hortic. 1998, 472, 635–640. [Google Scholar] [CrossRef]
  61. Flores, R.; Hernández, C.; Avinent, L.; Hermoso, A.; Llácer, G.; Juárez, J.; Arregui, L.; Navarro Desvignes, J.C. Studies of the detection, transmission and distribution of Peach latent mosaic viroid (PLMVd) in peach trees. Acta Hortic. 1992, 309, 325–330. [Google Scholar]
  62. Barba, M.; Ragozzino, E.; Faggioli, F. Pollen transmission of peach latent mosaic viroid. J. Plant Pathol. 2007, 89, 287–289. [Google Scholar]
  63. Fadda, Z.; Daros, J.A.; Fagoaga, C.; Flores, R.; Duran-Vila, N. Eggplant latent viroid, the candidate type species for a new genus within the family Avsunviroidae (hammerhead viroids). J. Virol. 2003, 77, 6528–6532. [Google Scholar]
  64. Fagoaga, C.; Duran-Vila, N. Eggplant Latent; CSIRO Publishing: Collingwood, VIC, Australia, 2003. [Google Scholar]
  65. Hammond, R.W. Seed, pollen, and insect transmission of viroids. In Viroids and Satellites; Academic Press: Cambridge, MA, USA, 2017; pp. 521–530. [Google Scholar]
  66. Schumann, G.L.; Tingey, W.M.; Thurston, H.D. Evaluation of six insect pests for transmission of potato spindle tuber viroid. Am. J. Potato Res. 1980, 57, 205–211. [Google Scholar] [CrossRef]
  67. Querci, M.; Lazarte, V.; Bartolini, I.; Salazar, L.F.; Owens, R.A. Evidence for heterologous encapsidation of potato spindle tuber viroid in particles of potato leafroll virus. J. Gen. Virol. 1997, 78, 1207–1211. [Google Scholar] [CrossRef]
  68. Salazar, L.F.; Querci, M.; Bartolini, I.; Lazarte, V. Aphid transmission of potato spindle tuber viroid assisted by potato leafroll virus. Fitopatologia 1995, 30, 56–58. [Google Scholar]
  69. Syller, J.; Marczewski, W.; Pawłowicz, J. Transmission by aphids of potato spindle tuber viroid encapsidated by potato leafroll luteovirus particles. Eur. J. Plant Pathol. 1997, 103, 285–289. [Google Scholar] [CrossRef]
  70. Walia, Y.; Dhir, S.; Zaidi, A.A.; Hallan, V. Apple scar skin viroid naked RNA is actively transmitted by the whitefly Trialeurodes vaporariorum. RNA Biol. 2015, 12, 1131–1138. [Google Scholar] [CrossRef][Green Version]
  71. Hidding, H.J.; Grum, C.J.; Hu, J.; Roth, D.A. Viroid-induced phosphorylation of a host protein related to a dsRNA-dependent protein kinase. Science 1988, 241, 451–453. [Google Scholar]
  72. Gross, H.J.; Liebl, U.; Alberty, H.; Krupp, G.; Domdey, H.; Ramm, K.; Sänger, H.L. A severe and a mild potato spindle tuber viroid isolate differ in three nucleotide exchanges only. Biosci. Rep. 1981, 1, 235–241. [Google Scholar]
  73. Owens, R.A.; Steger, G.; Hu, Y.; Fels, A.; Hammond, R.W.; Riesner, D. RNA structural features responsible for potato spindle tuber viroid pathogenicity. Virology 1996, 222, 144–158. [Google Scholar] [CrossRef]
  74. Cress, D.E.; Kiefer, M.C.; Owens, R.A. Construction of infectious potato spindle tuber viroid cDNA clones. Nucleic Acids Res. 1983, 11, 6821–6835. [Google Scholar] [CrossRef][Green Version]
  75. Qi, Y.; Ding, B. Inhibition of cell growth and shoot development by a specific nucleotide sequence in a noncoding viroid RNA. Plant Cell 2003, 15, 1360–1374. [Google Scholar] [CrossRef][Green Version]
  76. De la Peña, M.; Navarro, B.; Flores, R. Mapping the molecular determinant of pathogenicity in a hammerhead viroid: A tetraloop within the in vivo branched RNA conformation. Proc. Natl. Acad. Sci. USA 1999, 96, 9960–9965. [Google Scholar]
  77. Malfitano, M.; Di Serio, F.; Covelli, L.; Ragozzino, A.; Hernández, C.; Flores, R. Peach latent mosaic viroid variants inducing peach calico (Extreme chlorosis) contain a characteristic insertion that is responsible for this symptomatology. Virology 2003, 313, 492–501. [Google Scholar]
  78. Flores, R.; Owens, R.A.; Taylor, J. Pathogenesis by subviral agents: Viroids and hepatitis delta virus. Curr. Opin. Virol. 2016, 17, 87–94. [Google Scholar] [CrossRef]
  79. Momma, T.; Takahashi, T. Cytopathology of shoot apical meristem of hop plants infected with hop stunt viroid. J. Phytopathol. 1983, 106, 272–280. [Google Scholar] [CrossRef]
  80. Molnár, A.; Csorba, T.; Lakatos, L.; Várallyay, E.; Lacomme, C.; Burgyán, J. Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J. Virol. 2005, 79, 7812–7818. [Google Scholar] [CrossRef][Green Version]
  81. Omarov, R.T.; Cioperlik, J.J.; Sholthof, H.B. RNAi-associated ssRNA-specific ribonucleases in Tombusvirus P19 mutant-infected plants and evidence for a discrete siRNA-containing effector complex. Proc. Natl. Acad. Sci. USA 2007, 104, 1714–1719. [Google Scholar]
  82. Pantaleo, V.; Szittya, G.; Burgyán, J. Molecular bases of viral RNA targeting by viral small interfering RNA-programmed RISC. J. Virol. 2007, 81, 3797–3806. [Google Scholar]
  83. Aregger, M.; Borah, B.K.; Seguin, J.; Rajeswaran, R.; Gubaeva, E.G.; Zvereva, A.S.; Windels, D.; Vazquez, F.; Blevins, T.; Farinelli, L.; et al. Primary and secondary siRNAs in geminivirus-induced gene silencing. PLoS Pathog. 2012, 8, e1002941. [Google Scholar]
  84. Itaya, A.; Matsuda, Y.; Gonzales, R.A.; Nelson, R.S.; Ding, B. Potato spindle tuber viroid strains of different pathogenicity induces and suppresses expression of common and unique genes in infected tomato. Mol. Plant Microbe Interact. 2002, 15, 990–999. [Google Scholar] [CrossRef][Green Version]
  85. Owens, R.A.; Hammond, R.W. Viroid pathogenicity: One process, many faces. Viruses 2009, 1, 298–316. [Google Scholar] [CrossRef][Green Version]
  86. Wolff, P.; Gilz, R.; Schumacher, J.; Riesner, D. Complexes of viroids with histones and other proteins. Nucleic Acids Res. 1985, 13, 355–367. [Google Scholar] [CrossRef][Green Version]
  87. Henriquez, A.C.; Sänger, H.L. Purification and partial characterization of the major “pathogenesis-related” tomato leaf protein P14 from potato spindle tuber viroid (PSTV)-infected tomato leaves. Arch. Virol. 1984, 81, 263–284. [Google Scholar]
  88. Goodman, T.C.; Nagel-Steger, L.; Rappold, W.; Klotz, G.; Riesner, D. Viroid replication: Equilibrium association constant and comparative activity measurements for the viroid-polymerase interaction. Nucleic Acids Res. 1984, 12, 6231–6246. [Google Scholar] [CrossRef][Green Version]
  89. De Alba, A.E.M.; Sägesser, R.; Tabler, M.; Tsagris, M. A Bromodomain-containing protein from tomato specifically binds potato spindle tuber viroid rna in vitro and in vivo. J. Virol. 2003, 77, 9685–9694. [Google Scholar] [CrossRef][Green Version]
  90. Maniataki, E.; Tabler, M.; Tsagris, M. Viroid RNA systemic spread may depend on the interaction of a 71-nucleotide bulged hairpin with the host protein VirP1. RNA 2003, 9, 346–354. [Google Scholar] [CrossRef][Green Version]
  91. Diener, T.; Hammond, R.; Black, T.; Katze, M. Mechanism of viroid pathogenesis: Differential activation of the interferon-induced, double-stranded RNA-activated, Mr 68 000 protein kinase by viroid strains of varying pathogenicity. Biochimie 1993, 75, 533–538. [Google Scholar] [CrossRef]
  92. Langland, J.O.; Jin, S.; Jacobs, B.L.; Roth, D.A. Identification of a plant-encoded analog of PKR, the mammalian double-stranded RNA-dependent protein kinase. Plant Physiol. 1995, 108, 1259–1267. [Google Scholar] [CrossRef][Green Version]
  93. Hammond, R.W.; Zhao, Y. Characterization of a tomato protein kinase gene induced by infection by potato spindle tuber viroid. Mol. Plant Microbe Interact. 2000, 13, 903–910. [Google Scholar] [CrossRef][Green Version]
  94. Kolonko, N.; Bannach, O.; Aschermann, K.; Hu, K.-H.; Moors, M.; Schmitz, M.; Steger, G.; Riesner, D. Transcription of potato spindle tuber viroid by RNA polymerase II starts in the left terminal loop. Virology 2006, 347, 392–404. [Google Scholar] [CrossRef]
  95. Eiras, M.; Nohales, M.A.; Kitajima, E.W.; Flores, R.; Daròs, J.A. Ribosomal protein L5 and transcription factor IIIA from Arabidopsis thaliana bind in vitro specifically Potato spindle tuber viroid RNA. Arch. Virol. 2010, 156, 529–533. [Google Scholar] [CrossRef]
  96. Wang, Y.; Qu, J.; Ji, S.; Wallace, A.J.; Wu, J.; Li, Y.; Gopalan, V.; Ding, B. A land plant-specific transcription factor directly enhances transcription of a pathogenic noncoding RNA template by DNA-dependent RNA Polymerase II. Plant Cell 2016, 28, 1094–1107. [Google Scholar] [CrossRef][Green Version]
  97. Mudiyanselage, S.D.D.; Qu, J.; Tian, N.; Jiang, J.; Wang, Y. Potato spindle tuber viroid RNA-templated transcription: Factors and regulation. Viruses 2018, 10, 503. [Google Scholar] [CrossRef][Green Version]
  98. Jiang, J.; Smith, H.N.; Ren, D.; Mudiyanselage, S.D.D.; Dawe, A.L.; Wang, L.; Wang, Y. Potato spindle tuber viroid modulates its replication through a direct interaction with a splicing regulator. J. Virol. 2018, 92, e01004-18. [Google Scholar] [CrossRef][Green Version]
  99. Gómez, G.; Pallás, V. Identification of an in vitro ribonucleoprotein complex between a viroid RNA and a phloem protein from cucumber plants. Mol. Plant Microbe Interact. 2001, 14, 910–913. [Google Scholar] [CrossRef][Green Version]
  100. Gómez, G.; Pallás, V. A Long-distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with hop stunt viroid RNA. J. Virol. 2004, 78, 10104–10110. [Google Scholar] [CrossRef][Green Version]
  101. Daròs, J.A.; Flores, R. A chloroplast protein binds a viroid RNA In Vivo and facilitates its hammerhead-mediated self-cleavage. EMBO J. 2002, 21, 749–759. [Google Scholar] [CrossRef][Green Version]
  102. Lisón, P.; Tárraga, S.; López-Gresa, P.; Saurí, A.; Torres, C.; Campos, L.; Bellés, J.M.; Conejero, V.; Rodrigo, I. A noncoding plant pathogen provokes both transcriptional and posttranscriptional alterations in tomato. Proteomics 2013, 13, 833–844. [Google Scholar] [CrossRef]
  103. Vera, P.; Conejero, V. Citrus exocortis viroid infection alters the in vitro pattern of protein phosphorylation of tomato leaf proteins. Mol. Plant Microbe Interact. 1990, 3, 28–32. [Google Scholar]
  104. Cottilli, P.; Belda-Palazón, B.; Adkar-Purushothama, C.R.; Perreault, J.-P.; Schleiff, E.; Rodrigo, I.; Ferrando, A.; Rubio, C. Citrus exocortis viroid causes ribosomal stress in tomato plants. Nucleic Acids Res. 2019, 47, 8649–8661. [Google Scholar] [CrossRef]
  105. Dubé, A.; Bisaillon, M.; Perreault, J.-P. Identification of proteins from Prunus persica that interact with peach latent mosaic viroid. J. Virol. 2009, 83, 12057–12067. [Google Scholar] [CrossRef][Green Version]
  106. Martinez, G.; Castellano, M.; Tortosa, M.; Pallas, V.; Gomez, G. A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants. Nucleic Acids Res. 2014, 42, 1553–1562. [Google Scholar] [CrossRef]
  107. Adkar-Purushothama, C.R.; Iyer, P.S.; Perreault, J.-P. Potato spindle tuber viroid infection triggers degradation of chloride channel protein CLC-b-like and Ribosomal protein S3a-like mRNAs in tomato plants. Sci. Rep. 2017, 7, 1–12. [Google Scholar] [CrossRef][Green Version]
  108. Herranz, M.C.; Niehl, A.; Rosales, M.; Fiore, N.; Zamorano, A.; Granell, A.; Pallás, V. A remarkable synergistic effect at the transcriptomic level in peach fruits doubly infected by prunus necrotic ringspot virus and peach latent mosaic viroid. Virol. J. 2013, 10, 164. [Google Scholar] [CrossRef][Green Version]
  109. Itaya, A.; Zhong, X.; Bundschuh, R.; Qi, Y.; Wang, Y.; Takeda, R.; Harris, A.R.; Molina, C.; Nelson, R.S.; Ding, B. A Structured viroid RNA serves as a substrate for dicer-like cleavage to produce biologically active small RNAs but is resistant to RNA-induced silencing complex-mediated degradation. J. Virol. 2007, 81, 2980–2994. [Google Scholar] [CrossRef][Green Version]
  110. Itaya, A.; Folimonov, A.; Matsuda, Y.; Nelson, R.S.; Ding, B. Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol. Plant Microbe Interact. 2001, 14, 1332–1334. [Google Scholar] [CrossRef][Green Version]
  111. De Alba, A.E.M.; Flores, R.; Hernández, C. Two chloroplastic viroids induce the accumulation of small rnas associated with posttranscriptional gene silencing. J. Virol. 2002, 76, 13094–13096. [Google Scholar] [CrossRef][Green Version]
  112. Papaefthimiou, I.; Hamilton, A.; Denti, M.; Baulcombe, D.; Tsagris, M.; Tabler, M. Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res. 2001, 29, 2395–2400. [Google Scholar]
  113. Bolduc, F.; Hoareau, C.; St-Pierre, P.; Perreault, J.-P. In-depth sequencing of the siRNAs associated with peach latent mosaic viroid infection. BMC Mol. Biol. 2010, 11, 16. [Google Scholar] [CrossRef][Green Version]
  114. Ivanova, D.; Milev, I.; Vachev, T.; Baev, V.; Yahubyan, G.; Minkov, G.; Gozmanova, M. Small RNA analysis of Potato Spindle Tuber Viroid infected Phelipanche ramosa. Plant Physiol. Biochem. 2014, 74, 276–282. [Google Scholar] [CrossRef]
  115. Navarro, B.; Pantaleo, V.; Gisel, A.; Moxon, S.; Dalmay, T.; Bisztray, G.; Di Serio, F.; Burgyan, J. Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plant-viroid interaction. PLoS ONE 2009, 4, e7686. [Google Scholar] [CrossRef][Green Version]
  116. Sano, T.; Matsuura, Y. Accumulation of short interfering RNAs characteristic of RNA silencing precedes recovery of tomato plants from severe symptoms of potato spindle tuber viroid infection. J. Gen. Plant Pathol. 2004, 70, 50–53. [Google Scholar] [CrossRef]
  117. Tsushima, T.; Murakami, S.; Ito, H.; He, Y.-H.; Raj, A.P.C.; Sano, T. Molecular characterization of Potato spindle tuber viroid in dahlia. J. Gen. Plant Pathol. 2011, 77, 253–256. [Google Scholar] [CrossRef]
  118. Wang, Y.; Shibuya, M.; Taneda, A.; Kurauchi, T.; Senda, M.; Owens, R.A.; Sano, T. Accumulation of Potato spindle tuber viroid-specific small RNAs is accompanied by specific changes in gene expression in two tomato cultivars. Virology 2011, 413, 72–83. [Google Scholar] [CrossRef][Green Version]
  119. Adkar-Purushothama, C.R.; Perreault, J.-P. Alterations of the viroid regions that interact with the host defense genes attenuate viroid infection in host plant. RNA Biol. 2018, 15, 955–966. [Google Scholar] [CrossRef]
  120. Navarro, B.; Gisel, A.; Rodio, M.E.; Delgado, S.; Flores, R.; Di Serio, F. Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host mRNA as predicted by RNA silencing. Plant J. 2012, 70, 991–1003. [Google Scholar] [CrossRef]
Subjects: Virology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to : , , , , ,
View Times: 691
Revisions: 2 times (View History)
Update Date: 04 Nov 2022