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Celebrating 50 Years of Viroid Discovery

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A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Plant, Algae and Fungi Cell Biology".

Deadline for manuscript submissions: closed (30 September 2022) | Viewed by 31811

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Special Issue Editors

Dr. Ahmed Hadidi

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Guest Editor

Lead Scientist Emeritus, U.S. Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USA
Interests: viroids; viroid diseases; mycoviroids; plant viruses; molecular virology; molecular biology; genomics; origin; evolution
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Henryk Hanokh Czosnek

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Professor Emeritus, Institute of Plant Sciences and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, Israel
Interests: plant–virus–insect interactions; plant stress responses; resistance to plant viruses
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Kriton Kalantidis

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Guest Editor

Professor, Institute of Molecular Biology and Biotechnology, University of Crete, 700 13 Heraklion, Greece
Interests: RNAi; RNA silencing; RNA biology; viroids
Special Issues, Collections and Topics in MDPI journals

Dr. Robert A. Owens

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Guest Editor

Molecular Plant Pathology Laboratory, U.S. Department of Agriculture, Beltsville, MD 200705, USA
Interests: viroids; plant viruses; mobile genetic elements (MGE); RNA trafficking; RNA virus evolution

Special Issue Information

Dear Colleagues,

Theodor O. Diener of the US Department of Agriculture, Beltsville, Maryland, U.S, discovered the first viroid in 1971, the causal agent of potato spindle tuber disease. He showed that the agent is a free RNA of 25,000–110,000 Daltons, much smaller than a viral genome, and that no viral coat proteins were synthesized in infected plants. He concluded that the RNA is too small to contain the genetic information necessary for self-replication and it must rely on host enzymes for its replication. Also, in the U.S., Joseph S. Semancik of the University of California, Riverside, showed in 1972 that the causal agent of citrus exocortis disease is also a viroid of 125, 000 Daltons. By 1977 it was found that viroids cause economically important diseases in vegetable crops, fruit trees, ornamentals and palm species. The host range of viroids has expanded over the years to include grapevine and other cultivated and wild plant species. Viroids, the smallest known infectious agents (246-401 nt) exist as circular and linear RNAs with a high degree of base pairing and replicate autonomously in infected cells. In contrast to viruses, viroids lack capsid proteins, do not code for proteins and are completely dependent on host cellular RNA polymerases and processing enzymes for their replication. Viroids belong to the new order of subviral agents, which currently includes two families, eight genera, and 32 species of viroids. Viroids have had an impact on the science of virology, plant pathology, botany, microbiology, genetics, genomics, molecular biology, and molecular evolution as they represent the frontiers of life.

The objective of this Special Issue is to present a collection of original research, review articles, brief reports, case reports, project reports, communications and hypotheses related to viroid research advances and developments. Viroid topics of particular interest include, but are not limited to, economic impact, characteristics, diseases and viroids associated with plant species, detection and identification methods, transmission, control measures, geographical distribution and epidemiology.

Dr. Ahmed Hadidi
Prof. Dr. Henryk Hanokh Czosnek
Prof. Dr. Kriton Kalanditis
Dr. Robert A. Owens
Guest Editors

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Keywords

Viroids
economic significance
biology
structure
replication
pathogenesis
movement
proteome and transcriptome
RNA silencing
origin and evolution
taxonomy
transmission
viroid diseases
detection and identification methods
control measures
CRISPR-Cas genome editing
recombinant DNA technology
Geographical distribution and epidemiology

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Published Papers (11 papers)

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Editorial

Jump to: Research, Review

4 pages, 462 KiB

Open AccessEditorial

Mycoviroids: Fungi as Hosts and Vectors of Viroids

by Liying Sun and Ahmed Hadidi

Cells 2022, 11(8), 1335; https://doi.org/10.3390/cells11081335 - 14 Apr 2022

Cited by 4 | Viewed by 2636

Abstract

Viroids were discovered by the American plant pathologist Theodor O [...] Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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5 pages, 19217 KiB

Open AccessEditorial

Viroids, and the Legacy of Ricardo Flores (1947–2020)

by Ahmed Hadidi and John W. Randles

Cells 2021, 10(10), 2570; https://doi.org/10.3390/cells10102570 - 28 Sep 2021

Cited by 1 | Viewed by 2481

Abstract

Viroids were discovered by Diener in 1971 [...] Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

Research

Jump to: Editorial, Review

8 pages, 859 KiB

Open AccessCommunication

Natural Infection of Pomegranate (Punica Granatum) by Apple Dimple Fruit Viroid

by Ana Belén Ruiz-García, Antonio Olmos, Armelle Marais, Chantal Faure and Thierry Candresse

Cells 2023, 12(1), 49; https://doi.org/10.3390/cells12010049 - 22 Dec 2022

Cited by 2 | Viewed by 2033

Abstract

The analysis by high throughput sequencing (HTS) and RT-PCR of Spanish pomegranate fruits showing yellow rings revealed the presence of viroid isolates closely related to fig isolates of apple dimple fruit viroid (ADFVd). The analysis of pomegranate public RNASeq data (Sequence Reads Archives, SRAs) from Israel provided evidence for the presence of similar ADFVd isolates in pomegranate trees in this country. In addition, reads or contigs of plum viroid I (PVd-I) isolates were also identified in two of the analyzed SRA datasets from Israel, suggesting the presence of this second viroid in pomegranate. Full length ADFVd genomic sequences have been recovered, increasing knowledge on the diversity of this viroid and on the pomegranate virome in which only four viruses and one viroid had previously been reported. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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14 pages, 4086 KiB

Open AccessArticle

Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi

by Mengyuan Tian, Shuang Wei, Ruiling Bian, Jingxian Luo, Haris Ahmed Khan, Huanhuan Tai, Hideki Kondo, Ahmed Hadidi, Ida Bagus Andika and Liying Sun

Cells 2022, 11(22), 3686; https://doi.org/10.3390/cells11223686 - 20 Nov 2022

Cited by 13 | Viewed by 2389

Abstract

Viroids are the smallest known infectious agents that are thought to only infect plants. Here, we reveal that several species of plant pathogenic fungi that were isolated from apple trees infected with apple scar skin viroid (ASSVd) carried ASSVd naturally. This finding indicates the spread of viroids to fungi under natural conditions and further suggests the possible existence of mycoviroids in nature. A total of 117 fungal isolates were isolated from ASSVd-infected apple trees, with the majority (85.5%) being an ascomycete Alternaria alternata and the remaining isolates being other plant-pathogenic or -endophytic fungi. Out of the examined samples, viroids were detected in 81 isolates (69.2%) including A. alternata as well as other fungal species. The phenotypic comparison of ASSVd-free specimens developed by single-spore isolation and ASSVd-infected fungal isogenic lines showed that ASSVd affected the growth and pathogenicity of certain fungal species. ASSVd confers hypovirulence on ascomycete Epicoccum nigrum. The mycobiome analysis of apple tree-associated fungi showed that ASSVd infection did not generally affect the diversity and structure of fungal communities but specifically increased the abundance of Alternaria species. Taken together, these data reveal the occurrence of the natural spread of viroids to plants; additionally, as an integral component of the ecosystem, viroids may affect the abundance of certain fungal species in plants. Moreover, this study provides further evidence that viroid infection could induce symptoms in certain filamentous fungi. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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16 pages, 1526 KiB

Open AccessArticle

Cytosine Methylation in Genomic DNA and Characterization of DNA Methylases and Demethylases and Their Expression Profiles in Viroid-Infected Hop Plants (Humulus lupulus Var. ‘Celeia’)

by Andrej Sečnik, Nataša Štajner, Sebastjan Radišek, Urban Kunej, Mitja Križman and Jernej Jakše

Cells 2022, 11(16), 2592; https://doi.org/10.3390/cells11162592 - 19 Aug 2022

Cited by 4 | Viewed by 2291

Abstract

Abiotic and biotic stresses can lead to changes in host DNA methylation, which in plants is also mediated by an RNA-directed DNA methylation mechanism. Infections with viroids have been shown to affect DNA methylation dynamics in different plant hosts. The aim of our research was to determine the content of 5-methylcytosine (5-mC) in genomic DNA at the whole genome level of hop plants (Humulus lupulus Var. ‘Celeia’) infected with different viroids and their combinations and to analyse the expression of the selected genes to improve our understanding of DNA methylation dynamics in plant-viroid systems. The adapted HPLC-UV method used proved to be suitable for this purpose, and thus we were able to estimate for the first time that the cytosine methylation level in viroid-free hop plants was 26.7%. Interestingly, the observed 5-mC level was the lowest in hop plants infected simultaneously with CBCVd, HLVd and HSVd (23.7%), whereas the highest level was observed in plants infected with HLVd (31.4%). In addition, we identified three DNA methylases and one DNA demethylase gene in the hop’s draft genome. The RT-qPCR revealed upregulation of all newly identified genes in hop plants infected with all three viroids, while no altered expression was observed in any of the other hop plants tested, except for CBCVd-infected hop plants, in which one DNA methylase was also upregulated. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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14 pages, 4896 KiB

Open AccessFeature PaperArticle

The Splicing Variant TFIIIA-7ZF of Viroid-Modulated Transcription Factor IIIA Causes Physiological Irregularities in Transgenic Tobacco and Transient Somatic Depression of “Degradome” Characteristic for Developing Pollen

by Jaroslav Matoušek and Gerhard Steger

Cells 2022, 11(5), 784; https://doi.org/10.3390/cells11050784 - 23 Feb 2022

Cited by 3 | Viewed by 2180

Abstract

Viroids are small, non-coding, pathogenic RNAs with a significant ability of adaptation to several basic cellular processes in plants. TFIIIA-7ZF, a splicing variant of transcription factor IIIA, is involved in replication of nuclear-replicating viroids by DNA-dependent polymerase II. We overexpressed NbTFIIIA-7ZF from Nicotiana benthamiana in tobacco (Nicotiana tabacum) where it caused morphological and physiological deviations like plant stunting, splitting of leaf petioles, pistils or apexes, irregular branching of shoots, formation of double-blade leaves, deformation of main stems, and modification of glandular trichomes. Plant aging and senescence was dramatically delayed in transgenic lines. Factors potentially involved in viroid degradation and elimination in pollen were transiently depressed in transgenic leaves. This depressed “degradome” in young plants involved NtTudor S-like nuclease, dicers, argonoute 5, and pollen extracellular nuclease I showing expression in tobacco anthers and leaves. Analysis of the “degradome” in tobacco leaves transformed with either of two hop viroids confirmed modifications of the “degradome” and TFIIIA expression. Thus, the regulatory network connected to TFIIIA-7ZF could be involved in plant pathogenesis as well as in viroid adaptation to avoid its degradation. These results support the hypothesis on a significant impact of limited TFIIIA-7ZF on viroid elimination in pollen. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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26 pages, 20938 KiB

Open AccessArticle

Revisiting the Non-Coding Nature of Pospiviroids

by Konstantina Katsarou, Charith Raj Adkar-Purushothama, Emilios Tassios, Martina Samiotaki, Christos Andronis, Purificación Lisón, Christoforos Nikolaou, Jean-Pierre Perreault and Kriton Kalantidis

Cells 2022, 11(2), 265; https://doi.org/10.3390/cells11020265 - 13 Jan 2022

Cited by 15 | Viewed by 3443

Abstract

Viroids are small, circular, highly structured pathogens that infect a broad range of plants, causing economic losses. Since their discovery in the 1970s, they have been considered as non-coding pathogens. In the last few years, the discovery of other RNA entities, similar in terms of size and structure, that were shown to be translated (e.g., cirRNAs, precursors of miRNA, RNA satellites) as well as studies showing that some viroids are located in ribosomes, have reignited the idea that viroids may be translated. In this study, we used advanced bioinformatic analysis, in vitro experiments and LC-MS/MS to search for small viroid peptides of the PSTVd. Our results suggest that in our experimental conditions, even though the circular form of PSTVd is found in ribosomes, no produced peptides were identified. This indicates that the presence of PSTVd in ribosomes is most probably not related to peptide production but rather to another unknown function that requires further study. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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16 pages, 678 KiB

Open AccessArticle

Conserved Motifs and Domains in Members of Pospiviroidae

by Kevin-Phil Wüsthoff and Gerhard Steger

Cells 2022, 11(2), 230; https://doi.org/10.3390/cells11020230 - 11 Jan 2022

Cited by 6 | Viewed by 2059

Abstract

In 1985, Keese and Symons proposed a hypothesis on the sequence and secondary structure of viroids from the family Pospiviroidae: their secondary structure can be subdivided into five structural and functional domains and “viroids have evolved by rearrangement of domains between different viroids infecting the same cell and subsequent mutations within each domain”; this article is one of the most cited in the field of viroids. Employing the pairwise alignment method used by Keese and Symons and in addition to more recent methods, we tried to reproduce the original results and extent them to further members of Pospiviroidae which were unknown in 1985. Indeed, individual members of Pospiviroidae consist of a patchwork of sequence fragments from the family but the lengths of fragments do not point to consistent points of rearrangement, which is in conflict with the original hypothesis of fixed domain borders. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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15 pages, 1372 KiB

Open AccessArticle

Precisely Monomeric Linear RNAs of Viroids Belonging to Pospiviroid and Hostuviroid Genera Are Infectious Regardless of Transcription Initiation Site and 5′-Terminal Structure

by Tatsuji Hataya and Takashi Naoi

Cells 2021, 10(11), 2971; https://doi.org/10.3390/cells10112971 - 1 Nov 2021

Cited by 5 | Viewed by 2331

Abstract

Infectious dimeric RNA transcripts are a powerful tool for reverse genetic analyses in viroid studies. However, the construction of dimeric cDNA clones is laborious and time consuming, especially in mutational analyses by in vitro mutagenesis. In this study, we developed a system to synthesize a precisely monomeric linear RNA that could be transcribed in vitro directly from the cDNA clones of four viroid species. The cDNA clones were constructed such that RNA transcription was initiated at the guanine nucleotide of a predicted processing and ligation site in the viroid replication process. Although the transcribed RNAs were considered to possess 5′-triphosphate and 3′-hydroxyl termini, the RNA transcripts were infectious even without in vitro modifications. Additionally, infectivity was detected in the monomeric RNA transcripts, in which transcription was initiated at guanine nucleotides distinct from the predicted processing/ligation site. Moreover, monomeric viroid RNAs bearing 5′-monophosphate, 5′-hydroxyl, or 5′-capped termini were found to be infectious. Northern blot analysis of the pooled total RNA of the plants inoculated with the 5′-terminal modified RNA of potato spindle tuber viroid (PSTVd) indicated that maximum PSTVd accumulation occurred in plants with 5′-monophosphate RNA inoculation, followed by the plants with 5′-triphosphate RNA inoculation. Our system for synthesizing an infectious monomeric linear viroid RNA from a cDNA clone will facilitate mutational analyses by in vitro mutagenesis in viroid research. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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Review

Jump to: Editorial, Research

20 pages, 5464 KiB

Open AccessReview

Mexico: A Landscape of Viroid Origin and Epidemiological Relevance of Endemic Species

by Katia Aviña-Padilla, Erika Janet Zamora-Macorra, Daniel Leobardo Ochoa-Martínez, Flor Citlally Alcántar-Aguirre, Maribel Hernández-Rosales, Loranda Calderón-Zamora and Rosemarie W. Hammond

Cells 2022, 11(21), 3487; https://doi.org/10.3390/cells11213487 - 3 Nov 2022

Cited by 4 | Viewed by 2848

Abstract

Viroids are single-stranded, circular RNA molecules (234-406 nt) that infect a wide range of crop species and cause economic losses in agriculture worldwide. They are characterized by the existence of a population of sequence variants, attributed to the low fidelity of RNA polymerases involved in their transcription, resulting in high mutation rates. Therefore, these biological entities exist as quasispecies. This feature allows them to replicate within a wide range of host plants, both monocots and dicots. Viroid hosts include economically important crops such as tomato, citrus, and fruit trees such as peach and avocado. Given the high risk of introducing viroids to viroid disease-free countries, these pathogens have been quarantined globally. As discussed herein, Mexico represents a geographical landscape of viroids linked to their origin and comprises considerable biodiversity. The biological features of viroid species endemic to Mexico are highlighted in this communication. In addition, we report the phylogenetic relationships among viroid and viroid strains, their economic impact, geographical distribution, and epidemiological features, including a broad host range and possible long-distance, seed, or insect-mediated transmission. In summary, this review could be helpful for a better understanding of the biology of viroid diseases and future programs on control of movement and spread to avoid economic losses in agricultural industries. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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14 pages, 2331 KiB

Open AccessReview

Viroids as a Tool to Study RNA-Directed DNA Methylation in Plants

by Michael Wassenegger and Athanasios Dalakouras

Cells 2021, 10(5), 1187; https://doi.org/10.3390/cells10051187 - 13 May 2021

Cited by 13 | Viewed by 4137

Abstract

Viroids are plant pathogenic, circular, non-coding, single-stranded RNAs (ssRNAs). Members of the Pospiviroidae family replicate in the nucleus of plant cells through double-stranded RNA (dsRNA) intermediates, thus triggering the host’s RNA interference (RNAi) machinery. In plants, the two RNAi pillars are Post-Transcriptional Gene Silencing (PTGS) and RNA-directed DNA Methylation (RdDM), and the latter has the potential to trigger Transcriptional Gene Silencing (TGS). Over the last three decades, the employment of viroid-based systems has immensely contributed to our understanding of both of these RNAi facets. In this review, we highlight the role of Pospiviroidae in the discovery of RdDM, expound the gradual elucidation through the years of the diverse array of RdDM’s mechanistic details and propose a revised RdDM model based on the cumulative amount of evidence from viroid and non-viroid systems. Full article

(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)

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