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Viroids

Viroids are circular, single-stranded, non-coding RNAs that are able to infect certain plants. Because viroids do not code for any peptide or protein, they have to utilize proteins of the host for most biological functions like replication, processing or transport. Therefore, viroids can be regarded as minimal parasites of the host machinery. To do so, viroids have to present to the host machinery the appropriate signals that have to be based either on the sequence or the structure of viroid RNA.

Potato spindle tuber viroid (PSTVd) is the type member of the viroid family Pospiviroidae. The replication cycle of PSTVd is an asymmetric "rolling circle" mechanism (see figure to the left). Under native conditions the mature circular, (+)-stranded viroid has a rod-like secondary structure consisting of short helices and loops (top in the figure). This structure makes it partially resistant against nucleases. The circular, single-stranded (+)-RNA is transcribed by the DNA-dependent RNA polymerase II (polII) of the host plant into an oligomeric (-)-strand (right in the figure). During transcription the (-)-RNA folds into a thermodynamically metastable conformation containing hairpin II (HPII), which is critical for the transcription of (-)-stranded oligomers by polII into oligomeric (+)-strands (bottom in the figure). The (+)-oligomers---5' and 3' ends are marked in blue in the figure---are processed by host enzymes at a unique structural element, which contains thermodynamically extra-stable tetraloops (tl) and a G:U base pair (red arrow), to monomers and ligated to circles.

The mature PSTVd is thought to be responsible for intracellular and systemic transport. PSTVd strains differing in the left part of the rod-like secondary structure (pathogenicity-modulating region; PM) by only a few mutations produce symptoms in the host ranging from mild to "lethal". The figure shows tomato plants of identical age and duration of PSTVd infection: the first is non-inoculated (mock), the others are inoculated with a mild (QFA), an intermediate, and a strong (AS1) symptoms producing PSTVd strain. Besides the standard stunted habitus of PSTVd-infected tomato plants, PSTVd-AS1 shows symptoms up to necrosis of stem and leaves.

The molecular mechanism of viroid-induced pathogenesis is not clarified until now. A recent pathogenicity model favors the hypothesis that viroids are the source for production of "silencing" or microRNAs (siRNAs or miRNAs with a length of 21--24 nt). These are able to interact in gene regulation of the host for example by post-transcriptional gene silencing (PTGS).

The analysis of PSTVd-induced siRNAs and their connection to pathogenicity is at present supported by a common grant from the undefinedAlexander von Humboldt Foundation to G. Steger and J. Matoušek (undefinedBiology Centre, Academy of Sciences of the Czech Republic) and from the Graduate School undefinedE-Norm in the project undefined"Viroid evolution and viroid-induced pathogenesis networks in host plants". G. Steger and J. Matoušek organized the undefined"International Conference on Viroids and Viroid-like RNA" (2015).

Publications

  • Matoušek J, Steinbachová L, Záveská Drábková L, Kocábek T, Potěšil D, Mishra KA, Honys D, Steger G 
    Elimination of Viroids from Tobacco Pollen Involves a Decrease in Propagation Rate and an Increase of the Degradation Processes 
    International Journal of Molecular Sciences 21, 3029 (2020) 
    https://doi.org/10.3390/ijms21083029  
    Special Issue "Molecular Mechanisms of Viroids and Viroid Diseases" 
  • Shrestha A, Mishra AK, Matoušek J, Steinbachová L, Potěšil D, Nath VS, Awasthi P, Kocábek T, Jakse J, Drábková LZ, Zdráhal Z, Honys D, Steger G 
    Integrated Proteo-Transcriptomic Analyses Reveal Insights into Regulation of Pollen Development Stages and Dynamics of Cellular Response to Apple Fruit Crinkle Viroid (AFCVd)-Infection in Nicotiana tabacum 
    International Journal of Molecular Sciences 21, 8700 (2020) 
    https://doi.org/10.3390/ijms21228700  
    Special Issue "Molecular Mechanisms of Viroids and Viroid Diseases" 
  • Steger, G, Riesner, D 
    Viroid research and its significance for RNA technology and basic biochemistry. 
    Nucleic Acids Res. 46, 10563-10576 (2018) 
    http://dx.doi.org/10.1093/nar/gky903  
  • Brass JRJ, Owens RA, Matoušek J, Steger G 
    Viroid quasispecies revealed by deep sequencing 
    RNA Biology 14, 317-325 (2017) 
    http://dx.doi.org/10.1080/15476286.2016.1272745  
  • Matoušek J, Siglová K, Jakše J, Radišek S, Brass JR, Tsushima T, Guček T, Duraisamy GS, Sano T, Steger G 
    Propagation and some physiological effects of Citrus bark cracking viroid and Apple fruit crinkle viroid in multiple infected hop (Humulus lupulus L.) 
    J. Plant Physiol. 213, 166-177 (2017) 
    http://dx.doi.org/10.1016/j.jplph.2017.02.014  
  • Steger G 
    Modelling the three-dimensional structure of the right-terminal domain of pospiviroids. 
    Sci. Rep. 7, 711 (2017) 
    http://dx.doi.org/10.1038/s41598-017-00764-x  
  • Steger G, Riesner D, Maurel M-C, Perreault J-P 
    Viroid structure 
    In Viroids and Satellites; Hadidi A, Flores, R, Randles JW, Palukaitis P (eds), Oxford: Academic Press , 63-70 (2017) 
    https://www.elsevier.com/books/viroids-and-satellites/hadidi/978-0-12-801498-1  
  • Steger G, Perreault JP 
    Structure and associated biological functions of viroids 
    Adv. Virus Res. 94, 141-172 (2016) 
    http://dx.doi.org/10.1016/bs.aivir.2015.11.002  
  • Týcová A, Piernikarczyk RJJ, Kugler M, Lipovová P, Podzimek T, Steger G, Matoušek J 
    A 5'P degradation hot spot influences molecular farming of anticancerogenic nuclease TBN1 in tobacco cells. 
    Plant Cell Tiss Organ Cult 127, 347-358 (2016) 
    http://dx.doi.org/10.1007/s11240-016-1054-x  
  • Matousek J, Piernikarczyk RJJ, Týcová A, Duraisamy GS, Kocábek T, Steger G 
    Expression of SANT/HTH Myb mRNA, a plant morphogenesis-regulating transcription factor, changes due to viroid infection 
    Journal of Plant Physiology 183, 85-94 (2015) 
    http://dx.doi.org/10.1016/j.jplph.2015.06.001  
  • Matousek J, Piernikarczyk RJJ, Dědič P, Mertelík J, Uhlířová K, Duraisamy GS, Orctová L, Kloudová K, Ptáček J, Steger G 
    Characterization of Potato spindle tuber viroid (PSTVd) incidence and new variants from ornamentals 
    Europ J Plant Path 138, 93-101 (2014) 
    http://dx.doi.org/10.1007/s10658-013-0304-6  
  • Hammann C, Steger G 
    Viroid-specific small RNA in plant disease 
    RNA Biology 9, 809-819 (2012) 
    http://dx.doi.org/10.4161/rna.19810  
  • Matousek J, Riesner D, Steger G 
    Viroids: the smallest known infectious agents cause accumulation of viroid-specific small RNAs 
    In "From Nucleic Acids Sequences to Molecular Medicine" (Erdmann VA, Barciszewski J) Springer-Verlag, Heidelberg IX, 629-644 (2012) 
    http://www.springer.com/biomed/molecular/book/978-3-642-27425-1  
  • Matousek J, Stehlík J, Procházková J, Orctová L, Wullenweber J, Füssy Z, Kovácik J, Duraisamy GS, Ziegler A, Schubert J, Steger G 
    Biological and molecular analysis of the pathogenic variant C3 of potato spindle tuber viroid (PSTVd) evolved during adaptation to chamomile (Matricaria chamomilla) 
    Biol Chem 393, 605-615 (2012) 
    http://dx.doi.org/10.1515/hsz-2011-0286  
  • Ziegler A, Matousek J, Steger G, Schubert J 
    Complete sequence of a cryptic virus from hemp (Cannabis sativa) 
    Arch. Virol. 157, 383-385 (2012) 
    http://dx.doi.org/10.1007/s00705-011-1168-8  
  • Bajaj P, Steger G, Hammann C 
    Sequence elements outside the catalytic core of natural hairpin ribozymes modulate the reactions differentially 
    Biol. Chem. 392, 593-600 (2011) 
    http://dx.doi.org/10.1515/BC.2011.071  
  • Seehafer C, Kalweit A, Steger G, Gräf S, Hammann C 
    From alpaca to zebrafish: hammerhead ribozymes wherever you look 
    RNA 17, 21-26 (2011) 
    http://dx.doi.org/10.1261/rna.2429911  
  • Diermann N, Matousek 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 391, 1379-1390 (2010) 
    http://dx.doi.org/10.1515/BC.2010.148  
  • Teune, J-H, Steger G 
    novoMIR: de novo prediction of microRNA-coding regions in a single plant genome. 
    J. Nucleic Acids 2010, (2010) 
    http://dx.doi.org/10.4061/2010/495904  
  • Matoušsek J, Orctová L, ŠSkopek J, Pesšina K, Steger G 
    Elimination of hop latent viroid upon developmental activation of pollen nucleases. 
    Biol. Chem. 389, 905-918 (2008) 
    http://dx.doi.org/10.1515/BC.2008.096  
  • Matoušek 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. 388, 1-13 (2007) 
    http://dx.doi.org/10.1515/BC.2007.0  
  • Matoušek J, Orctová L, Ptácek J, Patzak J, Dedic P, Steger G, Riesner D 
    Experimental transmission of Pospiviroid populations to weed species characteristic for potato and hop fields. 
    J. Virol. 81, 11891-11899 (2007) 
    http://dx.doi.org/10.1128/JVI.01165-07  
  • Schmitz M, Steger G 
    Potato spindle tuber viroid (PSTVd). 
    Plant viruses. 1, 106-115 (2007) 
  • Kolonko N, Bannach O, Aschermann K, Hu KH, 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 347, 392-404 (2006) 
    http://dx.doi.org/10.1016/j.virol.2005.11.039  
  • Matoušek J, Orctová L, Steger G, Riesner D 
    Biolistic inoculation of plants with viroid nucleic acids. 
    J. Virol. Methods 122, 153-164 (2004) 
    http://dx.doi.org/j.jviromet.2004.08.011  
  • Matoušek J, Orctová L, Steger G, Škopek J, Moors M, Dědič P, Riesner D 
    Analysis of thermal stress-mediated PSTVd variation and biolistic inoculation of progeny of viroid "thermomutants" to tomato and Brassica species. 
    Virology 323, 9-23 (2004) 
    http://dx.doi.org/10.1016/j.virol.2004.02.010  
  • Riesner D, Steger G 
    Viroids and viroid-like agents. 
    Polish J. Pathology 4, 67-78 (2004) 
    http://www.poljpathol.cm-uj.krakow.pl/suplement/04_4_s.pdf  
  • Riesner D, Steger G 
    Temperature-gradient gel-electrophoresis. 
    In Bindereif, A., Hartmann, R., Schön, A. & Westhof, E. (Hrsg.), Handbook of RNA Biochemistry, Wiley-VCH , 398-414 (2004) 
  • Steger, G & Riesner, D 
    Properties of Viroids: Molecular characteristics. 
    In Hadidi, A., Flores, R., Randles, J.W. & Semancik, J.S. (Hrsg.), Viroids, CSIRO Publishing, Australia , 15-29 (2004) 
  • Dingley AJ, Steger G, Esters B, Riesner D, Grzesiek S 
    Structural characterization of the 69 nucleotide potato spindle tuber viroid left-terminal domain by NMR and thermodynamic analysis. 
    J. Mol. Biol. 334, 751-767 (2003) 
    http://dx.doi.org/10.1016/j.jmb.2003.10.015  
  • Owens RA, Sano T, Feldstein PA, Hu Y, Steger G 
    Identification of a novel structural interaction in Columnea latent viroid. 
    Virology 313, 604-614 (2003) 
    http://dx.doi.org/10.1016/S0042-6822(03)00352-0  
  • Steger G, Riesner D 
    Properties of Viroids: Molecular characteristics. 
    In "Viroids" (Hadidi A, Flores R, Randles JW, Semancik JS, eds.) CSIRO Publishing , 15-29 (2003) 
  • Yukawa Y, Matousek J, Grimm M, Vrba L, Steger G, Sugiura M, Beier H 
    Plant 7SL RNA and tRNA(Tyr) genes with inserted antisense sequences are efficiently expressed in an in vitro system from Nicotiana tabacum cells. 
    Plant Mol. Biol. 50, 713-723 (2002) 
    http://dx.doi.org/10.1023/A:1019905730397  
  • Matoušek J, Patzak J, Orctová L, Schubert J, Vrba L, Steger G, Riesner D 
    The variability of hop latent viroid as induced upon heat treatment. 
    Virology 287, 349-358 (2001) 
    http://dx.doi.org/10.1006/viro.2001.1044  
  • Matoušek J, Junker V, Vrba L, Schubert J, Patza, J, Steger G  
    Molecular characterization and genome organization of 7SL RNA genes from hop (Humulus lupulus L)  
    Gene 239, 173-183 (1999) 
    http://dx.doi.org/10.1016/S0378-1119(99)00352-2  
  • Repsilber D, Wiese U, Rachen M, Schröder AR, Riesner D, Steger G 
    Formation of metastable RNA structures by sequential folding during transcription: Time-resolved structural analysis of potato spindle tuber viroid (-)-stranded RNA by temperature-gradient gel electrophoresis. 
    RNA 5, 574-584 (1999) 
    Publisher  
  • Owens RA, Steger G, Hu Y, Fels A, Hammond RW, Riesner D 
    RNA structural features responsible for potato spindle tuber viroid pathogenicity. 
    Virology 222, 144-158 (1996) 
    http://dx.doi.org/10.1006/viro.1996.0405  
  • Schmitz M, Steger G 
    Description of RNA folding by ``simulated annealing''. 
    J Mol Biol 255, 254-266 (1996) 
  • Chen X, Baumstark T, Steger G, Riesner D  
    High resolution SSCP by optimization of the temperature by transverse TGGE 
    Nucleic Acids Res 23(21), 4524-5 (1995) 
  • Gruner R, Fels A, Qu F, Zimmat R, Steger G, Riesner D  
    Interdependence of pathogenicity and replicability with potato spindle tuber viroid 
    Virology 209(1), 60-9 (1995) 
  • Matousek J, Trena L, Dedic P, Rakousky S, Steger G, Riesner D 
    Inhibition of viroid infection by antisense RNA expression in transgenic plants. 
    Biol Chem Hoppe-Seyler 375, 765-777 (1994) 
  • Qu F, Heinrich C, Loss P, Steger G, Tien P, Riesner D  
    Multiple pathways of reversion in viroids for conservation of structural elements 
    EMBO J. 12(5), 2129-39 (1993) 
  • Riesner D, Baumstark T, Qu F, Klahn T, Loss P, Rosenbaum V, Schmitz M, Steger G 
    Physical basis and biological examples of metastable RNA structures. 
    In "Structural tools for the analysis of protein-nucleic acids complexes. Advances in Life Sciences" (Lilley D, Heumann H, Suck D, eds.) Birkhäuser , 401-435 (1992) 
  • Schmitz M, Steger G 
    Base-pair probability profiles of RNA secondary structures. 
    CABIOS 8, 389-399 (1992) 
  • Steger G, Baumstark T, Mörchen M, Tabler M, Tsagris M, Sänger HL, Riesner D 
    Structural requirements for viroid processing by RNase T1. 
    J Mol Biol 227, 719-737 (1992) 
  • Loss P, Schmitz M, Steger G, Riesner D  
    Formation of a thermodynamically metastable structure containing hairpin II is critical for infectivity of potato spindle tuber viroid RNA  
    EMBO J 10(3), 719-27 (1991) 
  • Owens RA, Thompson SM, Steger G 
    Effects of random mutagenesis upon potato spindle tuber viroid replication and symptom expression. 
    Virology 185, 18-31 (1991) 
  • Riesner D, Harders J, Hecker R, Klaff P, Lukacs N, Steger G  
    Viroid structures involved in protein binding and replication. 
    In "Plant Molecular Biology 2" (Herrmann RG, Larkins BA, eds.) NATOA ASI Series A, Life Sciences, Plenum Press 212, 75-90 (1991) 
  • Riesner D, Henco K, Steger G 
    Temperature-gradient gel electrophoresis: A method for the analysis of conformational transitions and mutations in nucleic acids and proteins. 
    In "Advances in electrophoresis" (Chrambach A, Dunn MJ, Radola BJ, eds.) VCH Weinheim Vol. 4, 169-250 (1991) 
  • Riesner D, Steger G 
    Viroids and viroid-like RNA. 
    In "Nucleic Acids, Subvol. d, Physical Data II, Theoretical Investigations, Landolt-Börnstein. Group VII Biophysics, 1, 194-243 (1990) 
  • Riesner D, Steger G, Zimmat R, Owens RA, Wagenhofer M, Hillen W, Vollbach S, Henco K  
    Temperature-gradient gel electrophoresis of nucleic acids: analysis of conformational transitions, sequence variations, and protein-nucleic acid interactions  
    Electrophoresis 10(5-6), 377-89 (1989) 
  • Riesner D, Steger G, Zimmat R, Owens RA, Wagenhöfer M, Hillen W, Vollbach S, Henco K  
    Temperature-gradient gel electrophoresis: Analysis of conformational transitions, sequence variations, and protein-nucleic acid interactions. 
    Electrophoresis 10, 377-389 (1989) 
  • Zimmat R, Gruner R, Hecker R, Steger G, Riesner D 
    Analysis of mutations in viroid RNA by non-denaturing and temperature-gradient gel electrophoresis. 
    In "Proceedings of the Sixth Conversation in Biomolecular Stereodynamics" (Sarma RH, Sarma MH, eds.) AdeninePress, Schenectady, New York , 339-357 (1989) 
  • Hecker R, Wang ZM, Steger G, Riesner D  
    Analysis of RNA structures by temperature-gradient gel electrophoresis: viroid replication and processing  
    Gene 72(1-2), 59-74 (1988) 
  • Riesner D, Hecker R, Steger G 
    Structure of viroid replication intermediates as studied by thermodynamics and temperature-gradient gel electrophoresis. 
    In "Structure and expression. From Proteins to ribosomes" (Sarma RH, Sarma MH, eds.) Adenine Press 1, 261-285 (1988) 
  • Riesner D, Klaff P, Steger G, Hecker R 
    Viroids: Subcellular location and structure of replicative intermediates. 
    In "Endocytobiology III" (Lee JJ, Fredrick JF, eds.) The New York Academy of Sciences, New York , 212-237 (1987) 
  • Steger G, Rosenbaum V, Riesner D 
    Viroids: Structure formation and function. 
    In "Structure and dynamics of RNA" NATO ASI Series A, Life Sciences, Plenum Press 110, 315-329 (1986) 
  • Steger G, Tabler M, Brüggemann W, Colpan M, Klotz G, Sänger HL, Riesner D 
    Structure of viroid replicative intermediates: Physico-chemical studies on SP6 transcripts of cloned oligomeric potato spindle tuber viroid. 
    Nucleic Acids Res 14, 9613-9630 (1986) 
  • Steger G, Hofmann H, Förtsch J, Gross HJ, Randles JW, Sänger HL, Riesner D 
    Conformational transitions in viroids and virusoids: Comparison of results from energy minimization algorithm and from experimental data. 
    J Biomol Struct Dyn 2, 543-571 (1984) 
  • Gross HJ, Sänger HL, Schumacher J, Steger G, Riesner D  
    Viroids: their structure and possible origin. 
    In "Endocytobiology III" (Lee JJ, Fredrick JF, eds.) The New York Academy of Sciences, New York , 48-55 (1983) 
  • Riesner D, Colpan M, Goodman TC, Nagel L, Schumacher J, Steger G, Hofmann H 
    Dynamics and interactions of viroids. 
    J Biomol Struct Dyn 1, 669-688 (1983) 
  • Randles JW, Steger G, Riesner D 
    Structural transitions in viroid-like RNAs associated with cadang-cadang disease, velvet tobacco mottle virus, and Solanum nodiflorum mottle virus. 
    Nucleic Acids Res 10, 5569-5586 (1982) 
  • Gross HJ, Krupp G, Domdey H and, Steger G, Riesner D, Sänger HL 
    The structure of the plant viroids. 
    Nucleic Acids Res Symp Ser 10, 91-98 (1981) 
  • Henco K, Steger G, Riesner D 
    Melting curves on less than 1 ug of nucleic acid. 
    Analyt Biochem 101, 225-229 (1980) 
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