The Plant Negative-Sense RNA Virosphere

REVIEW
published: 16 September 2020

doi: 10.3389/fmicb.2020.588427
The Plant Negative-Sense RNA

Virosphere: Virus Discovery Through
New Eyes
Nicolás Bejerman 1,2* , Humberto Debat 1,2 and Ralf G. Dietzgen 3
1
Instituto de Patología Vegetal – Centro de Investigaciones Agropecuarias – Instituto Nacional de Tecnología Agropecuaria,
Córdoba, Argentina, 2 Consejo Nacional de Investigaciones Científicas y Técnicas, Unidad de Fitopatología y Modelización
Agrícola, Buenos Aires, Argentina, 3 Queensland Alliance for Agriculture and Food Innovation, The University of Queensland,
St. Lucia, QLD, Australia
The use of high-throughput sequencing (HTS) for virus diagnostics, as well as the
importance of this technology as a valuable tool for discovery of novel viruses has been
Edited by: extensively investigated. In this review, we consider the application of HTS approaches
John Wesley Randles,
to uncover novel plant viruses with a focus on the negative-sense, single-stranded
University of Adelaide, Australia
RNA virosphere. Plant viruses with negative-sense and ambisense RNA (NSR) genomes
Reviewed by:
Elvira Fiallo-Olivé, belong to several taxonomic families, including Rhabdoviridae, Aspiviridae, Fimoviridae,
Institute of Subtropical Tospoviridae, and Phenuiviridae. They include both emergent pathogens that infect a
and Mediterranean Horticulture La
Mayora, Spain wide range of plant species, and potential endophytes which appear not to induce
Yi Xu, any visible symptoms. As a consequence of biased sampling based on a narrow
Nanjing Agricultural University, China
focus on crops with disease symptoms, the number of NSR plant viruses identified
Thierry Candresse,
Institut National de la Recherche so far represents only a fraction of this type of viruses present in the virosphere.
Agronomique (INRA), France Detection and molecular characterization of NSR viruses has often been challenging,
*Correspondence: but the widespread implementation of HTS has facilitated not only the identification
Nicolás Bejerman
nicobejerman@gmail.com but also the characterization of the genomic sequences of at least 70 NSR plant
viruses in the last 7 years. Moreover, continuing advances in HTS technologies and
Specialty section: bioinformatic pipelines, concomitant with a significant cost reduction has led to its
This article was submitted to
Virology, use as a routine method of choice, supporting the foundations of a diverse array of
a section of the journal novel applications such as quarantine analysis of traded plant materials and genetic
Frontiers in Microbiology
resources, virus detection in insect vectors, analysis of virus communities in individual
Received: 28 July 2020
Accepted: 27 August 2020
plants, and assessment of virus evolution through ecogenomics, among others. The
Published: 16 September 2020 insights from these advancements are shedding new light on the extensive diversity of
Citation: NSR plant viruses and their complex evolution, and provide an essential framework for
Bejerman N, Debat H and improved taxonomic classification of plant NSR viruses as part of the realm Riboviria.
Dietzgen RG (2020) The Plant
Negative-Sense RNA Virosphere: Thus, HTS-based methods for virus discovery, our ‘new eyes,’ are unraveling in real
Virus Discovery Through New Eyes. time the richness and magnitude of the plant RNA virosphere.
Front. Microbiol. 11:588427.
doi: 10.3389/fmicb.2020.588427 Keywords: HTS, virus discovery, plant NSR viruses, virosphere, bioinformactics
Frontiers in Microbiology | www.frontiersin.org 1 September 2020 | Volume 11 | Article 588427

Bejerman et al. Plant Negative-Sense RNA Virosphere
INTRODUCTION Most of the plant viruses described so far, whose nucleotide

sequences are available in public databases, were discovered in
Viruses are the most numerous biological entities on Earth, but exemplars of cultivated plant species that showed conspicuous
the number of reported and formally described virus species, disease symptoms, limiting our view of viral diversity (Wren
the known virosphere, is exiguous. This underestimated global et al., 2006). However, the steady increase in the last few years
virus landscape has led to a distorted view of virus diversity and of metagenomic studies to characterize the viromes of wild plant
function. Some aspects of virus biology including their small species, many of which did not show any visible symptoms,
size, rapid rate of evolution, or lack of universally conserved led to the identification of many new viruses. Moreover, several
viral genetic markers are likely the major cause for the lack recent reports provide evidence of viruses which appear to be
of knowledge of most of the viruses present on our planet essentially cryptic, identified from cultivated plants (Bernardo
(Koonin et al., 2015; Zhang et al., 2019). Thus, as we explore et al., 2018; Schoelz and Stewart, 2018; Susi et al., 2019; Ma et al.,
the virosphere, it becomes evident that only a tiny proportion 2020). Nevertheless, for most of the newly discovered viruses,
(about 1% according to some estimates) has been characterized, subsequent studies to characterize their biological properties,
with a major bias against the identification of the most divergent such as symptoms in different hosts, and potential vectors,
genomes (Zhang et al., 2018). among others, in both cultivated and wild plant species are
High-throughput sequencing (HTS) technology, also referred scarce, and likely will be neglected due to lack of economic
to as next generation sequencing, has revolutionized the significance or unavailability of preserved samples. The huge
nucleic acid characterization process since it allows the parallel gap between virus discovery and biological characterization of
sequencing of millions of nucleotides in a short period new viruses, is due to the latter requiring time-consuming
of time at a very high redundancy (depth of sequencing) research efforts. Therefore, we are advancing into a scenario
without any a priori knowledge. Thus, when combined with where the classification of most novel viruses will be based
specific bioinformatics tools, HTS provides a powerful, efficient only on their genomic sequences which constitutes a paradigm
and economical alternative that has enabled not only the shift in their taxonomical classification (Simmonds et al., 2017;
untargeted detection of both known and unknown viruses Kuhn et al., 2019), thus representing a major challenge for
that inhabit a particular organism or environment but also virologists and the International Committee on Taxonomy
a rapid characterization of their genomes (Massart et al., of Viruses (ICTV).
2017; Villamor et al., 2019). Thus, the steady increase in the Although many pipelines are available for plant virus
adoption of HTS in the past decade has accelerated virus discovery through HTS, all share a common backbone
discovery of both wild and cultivated plant species, which led (Villamor et al., 2019). Various HTS technologies are available
to the advancement of our knowledge about the diversity of commercially, but Illumina short read shotgun sequencing
viruses in nature. platforms are the most popular choice and most widely
High-throughput sequencing is also widely used to advance used for HTS of viruses because of their high throughput,
the molecular characterization not only of those viruses which low error rate and high cost effectiveness among currently
have a poorly characterized genome, but also of preserved available HTS platforms (Villamor et al., 2019). Four main
historic virus isolates which had been subjected to studies classes of nucleic acids have been targeted as templates for
of their biological properties some decades ago. For instance, HTS, (i) total plant RNA extracts, usually with a ribosomal
sterile stunt disease of maize, characterized by severe stunting depletion step (ii) virion-associated nucleic acids (VANA)
and top necrosis of susceptible maize genotypes, was first extracted from purified viral particles, (iii) double-stranded
reported in 1977 in Australia, but the genome of its etiological RNA (dsRNA), enriched through cellulose chromatography
agent, maize sterile stunt virus was only characterized by or monoclonal antibody pull-down, and (iv) small interfering
HTS and recently reported (Dietzgen and Higgins, 2019). RNAs (siRNAs) (Roossinck et al., 2015; Wu et al., 2015;
Similarly, sowthistle yellow vein virus (SYVV) was recently Blouin et al., 2016). These different strategies are characterized
rediscovered and its genome characterized after a hiatus of over by diverse caveats. For instance, VANA is inefficient in
30 years following pioneering virus and vector biology research detecting viruses that lack virions, or siRNA-based protocols
(Stenger et al., 2020). are not as reliable for complete genome assembly of novel
In spite of the many advantages of HTS, there are some viruses. Sequencing of siRNAs and total RNA are the two
limitations and constraints that should be considered approaches most generically applicable to viruses with different
when using this platform for virus discovery. Given genome types and replication strategies, and can be relatively
the high sensitivity of HTS, this technology may detect easily integrated into workflows of diagnostic laboratories
contaminant viral sequences or viruses that may not be (Pecman et al., 2017).
actually replicating in the sampled plant tissue where they Recent technological advances have led to the appreciation
were found (Blawid et al., 2017). In this context it is worth of exciting novel aspects of negative-sense and ambisense
emphasizing the importance of traditional wet bench virology RNA (NSR) viruses, as recently reviewed by German et al.
experiments to complement viral HTS data where possible, (2020). Plant NSR viruses are considered emerging viral
such as virus isolation and transmission experiments, pathogens (German et al., 2020). In light of the growing
in situ virus particle detection by electron microscopy or interest in these viruses, in this review we delve into the
immunoassays, to name a few. application of HTS approaches to uncover the abundance and

diversity of the negative-sense, single-stranded RNA virosphere possible. This may result in an increased number of identified
associated with plants. NSR viruses, which will allow us to deepen our understanding
about the evolution and diversity of NSR viruses. This is clearly
illustrated by the discovery of two NSR viruses associated with
apple rubbery wood disease. The initial attempt to determine by
HIGH-THROUGHPUT SEQUENCING TO NGS if any virus was associated with the disease was unsuccessful
UNCOVER THE NEGATIVE-SENSE, (Jakovljevic et al., 2016). However, the NGS data was later
SINGLE-STRANDED RNA VIROSPHERE reanalyzed in depth using a bioinformatics approach focused on
OF PLANTS viral conserved protein motifs that resulted in the identification
and genome assembly of two novel NSR viruses (Rott et al., 2018).
Hundreds of plant viruses have been characterized by HTS The use of HTS technologies has not only allowed the
in the last few years (Blawid et al., 2017; Villamor et al., identification and characterization of novel NSR viruses in several
2019), and most of them have positive-sense RNA genomes. plant hosts (Table 1), but has also enabled the completion of
On the other hand, RNA viruses with negative-sense and genome sequences of NSR viruses for which biological properties
ambisense genomes discovered through HTS represent only and only partial genome fragments were known (Table 2). The
a small fraction of the total number of viruses discovered, two nucleic acid classes mainly targeted when using HTS to
thus representing a tiny fraction of the plant virosphere. For sequence NSR viruses are total RNA and siRNAs (Tables 1, 2).
example, the characterization of the virome of different Solanum When Pecman et al. (2017) compared these approaches they
species resulted in the identification of viruses belonging to 20 found that both can be used to detect and identify a wide
different families, but only one was a NSR virus (Ma et al., array of known plant viruses in the tested samples including
2020). In addition, the characterization of a tomato virome orthotospoviruses. However, on this occasion a putative novel
resulted in the identification of 22 viruses belonging to 12 cytorhabdovirus genome could only be assembled de novo from
genera, but only three genomes corresponded to NSR viruses the sequencing data generated from total RNA and not from the
(Xu et al., 2017). Moreover, the characterization of a papaya small RNA dataset, due to the low number of short reads in
virome resulted in the identification of 52 viruses, but only the latter (Pecman et al., 2017), thus the choice of nucleic acid
one was a NSR virus (Alcalá-Briseño et al., 2020). It is worth types used in HTS may have an effect on the range of viruses
mentioning that typically, virome studies based on HTS generate that can be identified. However, a few novel plant rhabdoviruses
a significant amount of sequence contigs that lack detectable including cytorhabdoviruses have been identified using small
homology to both the sampled host and any microorganism. RNA as sequencing template (Table 1).
It has been suggested that a fraction of these sequences may Most plant NSR viruses are transmitted by arthropods in
correspond to viral ‘dark’ matter, which may imply that many a persistent-circulative and propagative manner, thus they are
deeply divergent viruses, or viruses lacking common ancestry or adapted to infect both arthropod and plant cells. In fact, it has
similarity with known virus families, remain to be discovered; been suggested that plant NSR viruses may have originated from
this may not happen until better frameworks are implemented arthropod viruses that evolved to also infect plants (Whitfield
to identify viral sequences regardless of their sequence similarity et al., 2018; Dolja et al., 2020). Therefore, another potential
to known viruses (Obbard et al., 2020). Current virome analyses source to discover novel plant-associated NSR viruses is the
usually rely on sequence similarity searches to identify virus- characterization of arthropod vector viromes. For instance,
like sequences through inferred homology. This approach limits Li et al. (2015) performed deep transcriptome sequencing
the identification of new viruses that can be discovered through of 70 arthropod species that resulted in the identification
traditional empirical search algorithms such as BLAST using of three novel cytorhabdoviruses (Wuhan insect viruses 4–
identity thresholds of target sequences to genomes, genes, 6) associated with the mealy plum aphid (Hyalopterus pruni).
proteins or protein motifs of known viruses (Obbard et al., Wuhan insect viruses 4–6 may be plant viruses based on
2020). As a consequence, in contrast to the more straightforward their clear phylogenetic relationship with plant rhabdoviruses
hypothesis that plant NSR viruses are relatively rare, it is plausible in the genus Cytorhabdovirus and that their genomes encode
that NSR virus sequences may have been overlooked due to a P3 protein that most resembles plant rhabdovirus cell-to-cell
extreme divergence from known viruses, thus providing an movement proteins.
alternative reason why so few NSR viruses have been identified Since most NSR viruses replicate in both the plant host
when the viromes of different plant hosts are characterized. and the arthropod vector, the true virus host origins cannot
Nevertheless, as novel bioinformatics tools are developed to be unambiguously discerned from the HTS data. Some of the
increase the sensitivity of similarity search algorithms and more newly discovered NSR viruses are highly divergent which makes
refined ab initio probabilistic methods are implemented, such it even more difficult to unequivocally determine if they are
as hidden Markov models that incorporate position-specific plant or plant-associated viruses, and it will require a significant
information into the alignment process of a group of highly amount of research to confirm their status, which is rarely carried
divergent, evolutionarily related sequences and use these profiles out. This is exemplified by the recently discovered coguviruses
to identify virus sequences (Skewes-Cox et al., 2014) or methods and rubodviruses, where the host assignment based on their
that rely on support vector machines (Liao and Noble, 2003), the phylogenetic relationships is only preliminary. Thus, further
identification of novel, more divergent viruses will likely become biological studies will be required to determine if they are plant,

Frontiers in Microbiology | www.frontiersin.org
Bejerman et al.
TABLE 1 | Novel NSR viruses discovered using HTS.
Virus family/genus Virus Type of target/sequencing technology References
Aspiviridae/Ophiovirus Blueberry mosaic associated ophiovirus Total nucleic acid/Illumina HiSeq Thekke-Veetil et al. (2014)
Phenuiviridae/Coguvirus Citrus concave gum-associated virus Small RNAs/Illumina HiSeq; total RNA/Illumina HiSeq Navarro et al. (2018a); Wright et al. (2018)
Phenuiviridae/Coguvirus Citrus virus A Small RNAs/Illumina Genome HiScan Navarro et al. (2018b)
Phenuiviridae/Coguvirus Watermelon crinkle leaf-associated virus 1 Small RNAs and total RNA/Illumina HiSeq Xin et al. (2017)
Phenuiviridae/Coguvirus Watermelon crinkle leaf-associated virus 2 Small RNAs and total RNA/Illumina HiSeq Xin et al. (2017)
Phenuiviridae/Coguvirus Grapevine associated cogu-like virus 1 Total RNA/Illumina HiSeq Chiapello et al. (2020)
Phenuiviridae/Coguvirus Grapevine associated cogu-like virus 4 Total RNA/Illumina NovaSeq Bertazzon et al. (2020)
Phenuiviridae/Rubodvirus Apple rubbery wood virus 1 Double-stranded RNA/Illumina HiSeq; total RNA/Illumina HiSeq Rott et al. (2018); Wright et al. (2018)
Phenuiviridae/Rubodvirus Apple rubbery wood virus 2 Double-stranded RNA/Illumina HiSeq; total RNA/Illumina HiSeq Rott et al. (2018); Wright et al. (2018)
Phenuiviridae/Rubodvirus Grapevine Muscat rose virus Total nucleic acid/Illumina HiSeq Diaz-Lara et al. (2019)
Phenuiviridae/Rubodvirus Grapevine Garan dmak virus Total nucleic acid/Illumina HiSeq Diaz-Lara et al. (2019)
Phenuiviridae/Tenuivirus Melon chlorotic spot virus Small RNAs/Illumina HiSeq; total RNA/Illumina MiSeq Lecoq et al. (2019); Gaafar et al. (2019a)
Phenuiviridae/Tenuivirus Ramu stunt virus Total RNA/Illumina HiSeq Mollov et al. (2016)
Phenuiviridae/Tenuivirus European wheat striate mosaic virus Small and total RNA/Illumina HiSeq and NextSeq Sõmera et al. (2020)
4
Tospoviridae/Orthotospovirus Alstroemeria yellow spot virus Total RNA/Illumina HiSeq Hassani-Mehraban et al. (2019)
Tospoviridae/Orthotospovirus Chili yellow ringspot virus Total RNA/Illumina MiSeq Zheng et al. (2020)
Fimoviridae/Emaravirus Blackberry leaf mottle associated virus Double-stranded RNA/Illumina and 454-Junior (Roche) Hassan et al. (2017)
Fimoviridae/Emaravirus Pigeonpea sterility mosaic virus 2 Double-stranded RNA/Illumina HiScan; small RNAs/Illumina GAIIx Elbeaino et al. (2015); Kumar et al. (2017)
Fimoviridae/Emaravirus Pistacia virus B Total RNA/Illumina NextSeq Buzkan et al. (2019)
Fimoviridae/Emaravirus Redbud yellow ringspot-associated virus Double-stranded RNA/Illumina Di Bello et al. (2016)
Fimoviridae/Emaravirus Ti ringspot-associated virus Double-stranded RNA/Illumina HiSeq and MiSeq Olmedo-Velarde et al. (2019)
Fimoviridae/Emaravirus Actinidia chlorotic ringspot-associated virus Small RNAs/Illumina Genome analyzer Zheng et al. (2017)
Fimoviridae/Emaravirus Jujube yellow mottle-associated virus Small RNAs/BGISEQ and total RNA/Illumina HiSeq Yang et al. (2019)
Fimoviridae/Emaravirus Blue palo verde broom virus Total RNA/Illumina HiSeq Ilyas et al. (2018)
September 2020 | Volume 11 | Article 588427
Fimoviridae/Emaravirus Camellia japonica associated emaravirus 1 Total RNA/Illumina HiSeq Peracchio et al. (2020)
Fimoviridae/Emaravirus Camellia japonica associated emaravirus 2 Total RNA/Illumina HiSeq Peracchio et al. (2020)
Plant Negative-Sense RNA Virosphere

Fimoviridae/Emaravirus Aspen mosaic-associated virus Total RNA/Illumina HiSeq von Bargen et al. (2020)
Fimoviridae/Emaravirus Perilla mosaic virus Total RNA/Illumina NovaSeq Kubota et al. (2020)
Fimoviridae/Emaravirus Lilac chlorotic ringspot-associated virus Total RNA/Illumina HiSeq Wang et al. (2020)
Rhabdoviridae/Cytorhabdovirus Strawberry associated virus 1 Small RNAs/Illumina MiSeq; total RNA/Illumina HiSeq and PCR Ding et al. (2019); Franova et al. (2019a)
products/Ion Proton
(Continued)
Bejerman et al.
TABLE 1 | Continued
Rhabdoviridae/Cytorhabdovirus Tomato yellow mottle-associated virus Small RNAs/Illumina HiSeq Xu et al. (2017)
Rhabdoviridae/Cytorhabdovirus Maize associated rhabdovirus Total RNA/Illumina HiSeq Willie and Stewart (2017)
Rhabdoviridae/Cytorhabdovirus Colocasia bobone disease-associated virus Total RNA/Illumina HiSeq Higgins et al. (2016)
Rhabdoviridae/Cytorhabdovirus Papaya virus E; bean-associated Total RNA/Illumina HiSeq; double stranded RNA/Illumina MiSeq; Medina-Salguero et al. (2019); Alves-Freitas
cytorhabdovirus; citrus-associated total RNA/Illumina HiSeq et al. (2019); Zhang et al. (2020)
rhabdovirus
Rhabdoviridae/Cytorhabdovirus Cabbage cytorhabdovirus 1 Total RNA/Illumina MiSeq Pecman et al. (2017)
Rhabdoviridae/Cytorhabdovirus Rice stripe mosaic virus Small RNAs/Illumina HiSeq Yang et al. (2017)
Rhabdoviridae/Cytorhabdovirus Wuhan insect virus 4 Total RNA/Illumina HiSeq Li et al. (2015)
Rhabdoviridae/Cytorhabdovirus Trifolium pratense virus A Total RNA/Illumina HiSeq Franova et al. (2019b)
Rhabdoviridae/Cytorhabdovirus Trifolium pratense virus B Total RNA/Illumina HiSeq Franova et al. (2019b)
Rhabdoviridae/Cytorhabdovirus Yerba mate chlorosis-associated virus Small RNAs/Illumina HiSeq Bejerman et al. (2017)
Rhabdoviridae/Cytorhabdovirus Yerba mate virus A Total RNA/Illumina HiSeq Bejerman et al. (2020)
Rhabdoviridae/Cytorhabdovirus Persimmon Virus A Total RNA/Illumina Genome Analyzer Ito et al. (2013)
5
Rhabdoviridae/Cytorhabdovirus Trichosantes associated rhabdovirus 1 Total RNA/Illumina HiSeq Goh et al. (2020)
Rhabdoviridae/Cytorhabdovirus Cucurbit cytorhabdovirus 1 Total RNA/Illumina NovaSeq Orfanidou et al. (2020)
Rhabdoviridae/Betanucleorhabdovirus Alfalfa-associated nucleorhabdovirus Total RNA/Illumina MiSeq Gaafar et al. (2019b)
Rhabdoviridae/Betanucleorhabdovirus Apple rootstock virus A Total RNA/Illumina HiSeq Baek et al. (2019)
Rhabdoviridae/Alphanucleorhabdovirus Physostegia chlorotic mottle virus Total RNA/Illumina MiSeq Menzel et al. (2016); Gaafar et al. (2018)
Rhabdoviridae/Alphanucleorhabdovirus Morogoro maize-associated virus Total RNA/Illumina HiSeq Read et al. (2019)
Rhabdoviridae/Betanucleorhabdovirus Black currant associated rhabdovirus Total RNA/Illumina NextSeq Wu et al. (2018)
Rhabdoviridae/Alphanucleorhabdovirus Wheat yellow striate virus Total RNA/Illumina HiSeq Liu et al. (2018)
Rhabdoviridae/Betanucleorhabdovirus Green Sichuan pepper nucleorhabdovirus Small RNAs and total RNA/Illumina HiSeq Cao et al. (2019)
Rhabdoviridae/Betanucleorhabdovirus Bird’s-foot trefoil-associated virus 1 Total RNA/Illumina HiSeq Debat and Bejerman (2019)
Rhabdoviridae/Alphanucleorhabdovirus Peach virus 1 Total RNA/Illumina HiSeq Zhou et al. (2020)

Rhabdoviridae/Betanucleorhabdovirus Cardamom vein clearing rhabdovirus 1 Small RNA/Illumina HiSeq Bhat et al. (2020)

Rhabdoviridae/Dichorhavirus Clerodendrum chlorotic spot virus Total RNA/Illumina HiSeq Ramos-González et al. (2018)
Rhabdoviridae/Dichorhavirus Citrus leprosis virus N Total RNA/Illumina HiSeq Ramos-González et al. (2017)
Rhabdoviridae/Dichorhavirus Citrus chlorotic spot virus Total RNA/Illumina HiSeq Chabi-Jesus et al. (2018)
Rhabdoviridae/Varicosavirus Red clover-associated varicosavirus Double stranded RNA/Illumina HiSeq Koloniuk et al. (2018a)
Rhabdoviridae/Varicosavirus Alopecurus myosuroides varicosavirus 1 Total RNA/454 (Roche) and Illumina HiSeq Sabbadin et al. (2017)
Bejerman et al.
TABLE 2 | NSR viruses with partial genome sequence already know, whose genomes were characterized using HTS.
Phenuiviridae/Tenuivirus Rice hoja blanca virus Small RNAs/Illumina HiSeq Jimenez et al. (2018)
Tospoviridae/Orthotospovirus Groundnut chlorotic fan-spot virus Total RNA/Illumina MiSeq Chou et al. (2017)
Tospoviridae/Orthotospovirus Chrysanthemum stem necrosis virus Viral RNA from ribonucleocapsid/454 (Roche) Dullemans et al. (2015)
Tospoviridae/Orthotospovirus Mulberry vein banding associated virus Small RNAs/Illumina Genome Analyzer Meng et al. (2015)
Tospoviridae/Orthotospovirus Alstroemeria necrotic streak virus Total RNA/Illumina HiSeq Gallo et al. (2018)
Tospoviridae/Orthotospovirus Melon severe mosaic virus Total RNA/Illumina NextSeq Ciuffo et al. (2017)
Tospoviridae/Orthotospovirus Zucchini lethal chlorosis virus Viral RNA from ribonucleocapsid/Illumina HiSeq Lima et al. (2016)
Tospoviridae/Orthotospovirus Tomato chlorotic spot virus Total RNA/Illumina HiSeq Martínez et al. (2018); Adegbola et al. (2019),
Fagundes Silva et al. (2019)
Tospoviridae/Orthotospovirus Polygonum ringspot virus Small RNAs Margaria et al. (2014)
Fimoviridae/Emaravirus Rose rosette virus Total nucleic acid/Illumina HiSeq and 454-Junior (Roche) Di Bello et al. (2015)
6
Fimoviridae/Emaravirus Pigeonpea sterility mosaic virus 1 Double-stranded RNA/Illumina HiScan; small RNAs/Illumina GAIIx Elbeaino et al. (2014); Kumar et al. (2017)
Fimoviridae/Emaravirus Raspberry leaf blotch virus Total RNA/Illumina MiSeq Lu et al. (2015)
Fimoviridae/Emaravirus European mountain ash ringspot-associated virus Total RNA/Illumina HiSeq von Bargen et al. (2019)
Fimoviridae/Emaravirus High plains wheat mosaic virus Partially purified virion RNA/Illumina MiSeq Tatineni et al. (2014)
Rhabdoviridae/Cytorhabdovirus Alfalfa dwarf virus Small RNAs/Illumina HiSeq Bejerman et al. (2015)
Rhabdoviridae/Cytorhabdovirus Raspberry vein chlorosis virus Total RNA/Illumina NextSeq Jones et al. (2019)
Rhabdoviridae/Cytorhabdovirus Barley yellow striate mosaic virus/maize sterile stunt virus Small RNAs/Illumina HiSeq; viral enriched RNA/454 (Roche) Yan et al. (2015); Dietzgen and Higgins (2019)
Rhabdoviridae/Cytorhabdovirus Strawberry crinkle virus Total RNA/Illumina HiSeq Koloniuk et al. (2018b)
Rhabdoviridae/Cytorhabdovirus Maize yellow striate virus Viral enriched RNA/Illumina HiSeq Maurino et al. (2018)
Rhabdoviridae/Betanucleorhabdovirus Datura yellow vein virus Total RNA/454 (Roche) Dietzgen et al. (2015)
Rhabdoviridae/Alphanucleorhabdovirus Maize mosaic virus Total RNA/Illumina HiSeq Martin and Whitfield (2019)
Rhabdoviridae/Alphanucleorhabdovirus Maize Iranian mosaic virus Total RNA/Illumina HiSeq Ghorbani et al. (2018)
Rhabdoviridae/Betanucleorhabdovirus Sowthistle yellow vein virus Total RNA/Oxford Nanopore Stenger et al. (2020)

Rhabdoviridae/Dichorhavirus Coffee ringspot virus Total RNA/ION Torrent Ramalho et al. (2014)
plant-associated, or insect viruses (Navarro et al., 2018b; Diaz- and plants. Six of these genera include 45 species of
Lara et al., 2019; Chiapello et al., 2020). phytoviruses: Cytorhabdovirus, Alphanucleorhabdovirus, Betanu-
cleorhabdovirus and Gammanucleorhabdovirus (unsegmented
genomes), and Dichorhavirus and Varicosavirus (bi-segmented
NEGATIVE-SENSE, SINGLE-STRANDED genomes) (Walker et al., 2018; Kuhn et al., 2020) (Figure 1).
RNA VIRUS DIVERSITY AND TAXONOMY The virions of these phytorhabdoviruses have bacilliform or
rod-shaped morphology, and those with unsegmented genomes
Negative-sense and ambisense RNA viruses belong to the phylum are enveloped. Plant-infecting rhabdovirus genomes are 10–
Negarnaviricota, which includes members characterized by (i) 16 kb in size and are composed of 6 to 10 genes (Walker et al.,
negative-sense or ambisense single-stranded unsegmented or 2018) (Figure 1).
segmented genomes, (ii) the presence or absence of a lipid The increased application of HTS has seen a significant rise
membrane enveloping the capsid, and (iii) a diverse host in the number of novel plant rhabdoviruses (Table 1), as well as
range (Diaz-Lara et al., 2019; Koonin et al., 2020; Kuhn the completion of genomic sequences of those viruses with poorly
et al., 2020). This phylum contains major groups of pathogenic characterized genomes (Table 2).
viruses and our current knowledge of these viruses is strongly High-throughput sequencing was used successfully to
biased toward agents with special importance for human and complete the genome sequences of previously reported plant
animal health, such as influenza virus (Orthomyxoviridae), Zaire rhabdoviruses where only partial sequence fragments were
ebolavirus (Filoviridae) or Crimean-Congo hemorrhagic fever available, such as Iranian citrus ringspot-associated virus
virus (Nairovirus). Most of the genera contain NSR viruses (Sadeghi et al., 2016), ivy vein banding virus (Petrzik, 2012),
that infect vertebrates and only about 10% contain phytoviruses and soybean blotchy mosaic virus (Lamprecht et al., 2010).
(Käfer et al., 2019) (Figure 1). Furthermore, HTS could be a key tool to characterize the
Most of the NSR viruses are divided into two large lineages genomes of some cyto- and nucleorhabdoviruses which have
based on whether their RNA genomes are unsegmented or only been characterized biologically, such as broccoli necrotic
segmented (Koonin et al., 2020) (Figure 1). The unsegmented yellows virus (Lin and Campbell, 1972) and festuca leaf streak
and some bi-segmented viruses with negative-sense RNA virus (Lundsgaard and Albrechtsen, 1976).
genomes, belong to the order Mononegavirales (Koonin et al., Moreover, partial genome fragments of three putative
2020; Kuhn et al., 2020). In contrast, most of the segmented cytorhabdoviruses and one unassigned rhabdovirus were
viruses with both negative-sense and ambisense RNA genomes reported, when the viromes of water lily, common bean,
belong to the order Bunyavirales (Koonin et al., 2020; Kuhn Lamprocephalus sp. and kalanchoe were analyzed by HTS
et al., 2020) (Figure 1). Other orders such as Serpentovirales (Kreuze, 2014; Verdin et al., 2017; Bernardo et al., 2018;
(which is the only one of these including NSR phytoviruses), Mwaipopo et al., 2018). However, the obtained sequences are
Muvirales, Articulavirales, among others, have been created to not available in any public database, so it is not possible to know
accommodate diverse viruses which have been placed in the if these viruses are novel or may correspond to already known
major phylogenetic gap between the two large groups of NSR viruses. Thus, it would be useful to apply HTS to complete
viruses (Wolf et al., 2018). the genome characterization of these viruses to increase our
Twelve genera (Alphanucleorhabdovirus, Betanucleor- understanding of plant rhabdovirus diversity. Furthermore,
habdovirus, Coguvirus, Cytorhabdovirus, Dichorhavirus, Emara- since a tentative nucleorhabdovirus associated with papaya was
virus, Gammanucleorhabdovirus, Ophiovirus, Orthotospovirus, recently discovered in a papaya virome (Alcalá-Briseño et al.,
Rubodvirus, Tenuivirus, and Varicosavirus) belonging to five 2020), it would be useful to employ HTS to characterize the
different families (Rhabdoviridae, Aspiviridae, Fimoviridae, molecular properties of papaya apical necrosis virus, a putative
Tospoviridae, and Phenuiviridae) include species of phytoviruses nucleorhabdovirus associated with papaya, which was only
(Figure 1). Two of the genera (Coguvirus and Rubodvirus) characterized biologically almost four decades ago (Lastra and
were recently created to accommodate novel species of Quintero, 1981), to determine if both viruses are related.
NSR viruses related to members of the Phenuiviridae family
(Navarro et al., 2018b; Diaz-Lara et al., 2019). Furthermore, Cytorhabdovirus
the ongoing discovery of many novel nucleorhabdoviruses The application of HTS has facilitated the discovery of at least
and dichorhaviruses by HTS in the last few years resulted in 17 novel cytorhabdoviruses during the last 7 years (Table 1).
a split of the genus Nucleorhabdovirus into three new genera Furthermore, the use of HTS has allowed characterization of the
(Freitas-Astúa et al., 2019). Therefore, as the pace of discovery genomes of five cytorhabdoviruses, for which only a fragment
of new NSR plant viruses using HTS is speedily increasing, the or only the biological properties were known (Table 2). The
creation of new genera and families to accommodate some of template mostly used as a source for HTS of these viruses was
these newly discovered viruses will be a common classification total RNA, sequenced usually on Illumina platforms (Tables 1, 2).
task in future years.
Alpha-, Beta-, Gammanucleorhabdovirus
Rhabdoviridae The application of HTS has facilitated the discovery of ten
The family Rhabdoviridae currently comprises 30 genera novel nucleorhabdoviruses during the last 4 years, four
for 191 species for viruses infectin vertebrates, invertebrates alphanucleorhabdoviruses and six betanucleorhabdoviruses

FIGURE 1 | Diagram showing an overview of plant NSR virus taxonomy and schematic genome graphs depicting organization and gene products of representative
members of each taxon. The predicted coding sequences are shown in orange arrowed boxes, virion-sense RNA (v) is depicted in black, while virion-complementary
sense RNA (vc) is depicted in red. The number of taxonomic categories included in each taxon are indicated. Species number indicate 2019 ICTV-accepted virus
species corresponding to each taxonomic rank.
(Table 1). Furthermore, the use of HTS has allowed re- Illumina and Roche 454 were the technologies employed in the
sequencing the genomes of two alphanucleorhabdoviruses HTS projects (Table 1).
which had previously been determined using Sanger dideoxy
sequencing (maize mosaic virus and maize Iranian mosaic Fimoviridae
virus). HTS also allowed sequencing of the genome of a This family is composed of only one genus, Emaravirus, for
betanucleorhabdovirus for which only a genome fragment viruses that are distantly related to orthotospoviruses, and
and the biological properties were known (datura yellow vein exclusively comprise members that have plants as their hosts.
virus), and one other for which only the biological properties Emaraviruses have enveloped, spherical virions, with a diameter
had been investigated 30 years earlier (sowthistle yellow vein of 80–100 nm and a segmented, linear, single-stranded genome
virus) (Table 2). The template mostly used as a source for with generally four to eight RNA segments (Elbeaino et al., 2018),
the HTS was total RNA, sequenced usually with Illumina but a recently described novel emaravirus, perilla mosaic virus,
instruments (Tables 1, 2). has 10 RNA segments (Kubota et al., 2020).
Most of the members of the genus Emaravirus have been
Dichorhavirus recently discovered (Table 1) or characterized in depth by HTS
The application of HTS has facilitated the discovery of three novel techniques (Table 2). The application of HTS resulted in the
dichorhaviruses during the last 3 years (Table 1). Furthermore, discovery of 13 emaraviruses during the last 5 years (Table 1).
the use of HTS has allowed characterization of the genome of Different templates, such as total RNA, small RNAs and dsRNA
a dichorhavirus for which only a fragment and the biological were used as sources for the HTS, and Illumina platforms have
properties were known (coffee ringspot virus) (Table 2). The been mostly used in the HTS projects (Table 1).
template used as a source for the HTS was total RNA, sequenced The use of HTS has revealed the genome sequence of
on Illumina platforms (Tables 1, 2). two emaraviruses for which only a genomic fragment and
some biological properties were known (high plains wheat
Varicosavirus mosaic virus and pigeonpea sterility mosaic virus 1) (Table 2).
The complete genome of only one varicosavirus, lettuce big- Furthermore, the application of HTS has resulted in the detailed
vein associated virus, was previously characterized using Sanger characterization of the complete genomes of three emaraviruses.
dideoxy sequencing (Sasaya et al., 2002, 2004); however, the A clearer picture of the genome organization of emaraviruses
application of HTS has facilitated the discovery of two novel was obtained by the identification of additional RNA segments.
varicosaviruses during the last 3 years (Table 1). The template HTS- based research resulted in the identification of three novel
used as a source for the HTS was total RNA and dsRNA, and genome segments of raspberry leaf blotch virus and rose rosette

virus (Di Bello et al., 2015; Lu et al., 2015), and two novel yellow spot virus (S RNA), lisianthus necrotic ringspot virus (S
segments for European mountain ash ringspot-associated virus RNA), pepper necrotic spot virus (S RNA) and tomato necrotic
genome (von Bargen et al., 2019). Different templates, including ringspot virus (S and M RNAs) (Satyanarayana et al., 1998;
total nucleic acids, total RNA, dsRNA and RNA from partially Seepiban et al., 2011; Torres et al., 2012; Shimomoto et al.,
purified virions were used as sources for the HTS. Illumina 2014); HTS could enable completion of the genome of these
platforms were mostly used in these HTS projects (Table 2). agronomically important viruses.
Finally, partial fragments of RNAs1, 2 and 4 of a putative novel
emaravirus infecting alfalfa in Australia, named alfalfa ringspot- Phenuiviridae
associated virus were recently identified using HTS (Samarfard Most phenuiviruses have enveloped particles with helical
et al., 2020). PCR amplification of the conserved termini of the morphology, except tenuiviruses that have non-enveloped
genome segments (Babu et al., 2016) and HTS could be used filamentous particles, and their genomes are comprised of
to characterize the complete genome sequence of this tentative two to four single-stranded, linear RNA segments. As of
novel emaravirus. 2019, the family Phenuiviridae includes 19 ICTV-recognized
genera (Figure 1). Only the established genus Tenuivirus
Aspiviridae and likely two recently accepted new genera Coguvirus and
This family, formerly named Ophioviridae, contains only one Rubodvirus (2019.026M.A.v1.Phenuiviridae_4gen79sp.xlsx)
genus, Ophiovirus, which is exclusively composed of members contain species of plant-infecting viruses (Navarro et al., 2018b;
that have plants as their hosts (Figure 1). Ophioviruses have non- Diaz-Lara et al., 2019). Phylogenetic relationships with other
enveloped, naked filamentous virions and a segmented, linear phenuiviruses support their classification within this family
open circle, serpentine, single-stranded RNA genome, consisting (Diaz-Lara et al., 2019).
of three to four segments (García et al., 2017).
One novel ophiovirus, blueberry mosaic associated Coguvirus
ophiovirus, has been discovered using HTS during the last 6 years This genus is composed of two previously unknown viruses
(Table 1). Partial genome fragments of three ophioviruses, freesia that have bi-segmented genomes, which have been discovered
sneak virus, ranunculus white mottle virus, and tulip mild mottle using HTS of citrus (Navarro et al., 2018a,b), while two
mosaic virus have been known for some years but their complete tentative coguviruses that have tri-segmented genomes, have
genomes remain elusive (García et al., 2017). HTS could be a been discovered using HTS in watermelon (Xin et al., 2017)
crucial tool to obtain the complete genomes of these viruses (Table 1). Total RNA and small RNAs were used as template
and to expand our understanding of the genomic cues and sources for HTS on Illumina platforms (Table 1). Recently, the
evolutionary diversity of ophioviruses. complete tri-segmented genomes of four cogu-like viruses were
determined when the virome of grapevine was characterized
Tospoviridae (Bertazzon et al., 2020; Chiapello et al., 2020) (Table 1).
This family contains the single genus Orthotospovirus, which Moreover, partial segments of a cogu-like virus were
is exclusively composed of species for viruses that have plants discovered when the virome of ornamental flowers was analyzed
as their hosts (Figure 1). Orthotospoviruses have enveloped, by HTS (Wylie et al., 2019). However, it will be necessary
spherical virions of 80–120 nm diameter and are transmitted to complete the genome characterization and perform further
by thrips insects in which they also replicate. The genome of analyses of these viruses to confirm if they are in fact plant-
orthotospoviruses is segmented with three linear single-stranded infecting viruses or arthropod-infecting viruses whose RNA
RNA segments named large (L), middle (M), and small (S). The L was co-purified along with the plant RNA. This additional
RNA contains one open reading frame in negative-sense polarity, information would enable further characterization of these
whereas the other two segments, M and S RNAs, are ambisense putative coguviruses, thus increasing our understanding of the
and have two open reading frames encoding proteins in opposite plant-infecting phenuivirus diversity and evolutionary history.
orientation (Oliver and Whitfield, 2016).
The application of HTS led to the discovery of two novel Rubodvirus
orthotospoviruses in 2019 and 2020 (Table 1). Total RNA This genus is composed of species for two previously unknown
was used as the template and Illumina platforms as the viruses that have tri-segmented genomes which have been
sequencing technology. discovered using HTS in apple (Rott et al., 2018; Wright et al.,
The use of HTS has also facilitated completion of the 2018), while two tentative rubodviruses were discovered using
sequence of eight orthotospoviruses for which only one genome HTS in grapevine (Diaz-Lara et al., 2019) (Table 1). DsRNA and
segment was available (mostly the S RNA) and their biological total RNA were the templates used as sources for HTS on Illumina
properties were known (Table 2). Different templates, including platforms (Table 1).
total RNA, small RNA and virus-enriched RNA from purified
ribonucleocapsids were used as RNA source, and Illumina Tenuivirus
platforms were mostly used as sequencing technology in the HTS Tenuiviruses have a segmented genome of four to eight single-
projects (Table 2). stranded RNA segments with negative-sense or ambisense
At the time of this review, only partial genome sequence of polarity (Gaafar et al., 2019a). The application of HTS led to
four other reported orthotospoviruses are available: groundnut the discovery of two new tenuiviruses, one infecting melon and

black medic (Gaafar et al., 2019a; Lecoq et al., 2019) and the other implementation of HTS, a cost-effective and efficient technology
from sugarcane associated with Ramu stunt disease (Mollov et al., platform, allowed the discovery and molecular characterization of
2016) (Table 1). In addition, a recent HTS study resulted in the the genome sequences of at least 70 NSR plant viruses in the last
molecular characterization of a wheat tenuivirus, the biological few years. Thus, we predict that the increasing use of HTS, not
properties of which had been previously characterized in the only for plant samples but also in arthropod vectors, will allow
1960s (Sõmera et al., 2020) (Table 1). Total RNA and small RNAs the identification of many novel NSR phytoviruses which will be
were used as sources for HTS on Illumina platforms (Table 1). crucial to unravel the evolutionary landscapes of many NSR virus
Moreover, the use of HTS facilitated sequencing of a tenuivirus clades that are poorly characterized today. Nevertheless, as many
from rice, for which only the sequence of RNA4 and its biological more novel NSR viruses are being discovered, careful analysis
properties were known previously (Table 2). At the time of will be essential to confirm their correct ecological context,
writing this review, only partial genomic sequence of four other to determine whether the new viral agents are plant-infecting
tenuiviruses are known: maize stripe virus (complete sequences viruses, fungi- or arthropod-infecting viruses whose RNA was
of RNAs 2, 3, 4 and 5), maize yellow stripe virus (partial sequences co-purified along with the plant RNA, or just contamination-
of RNAs 1, 2, 3, 4 and complete sequence of RNA 5), Iranian inadvertently sampled environmental viruses.
wheat stripe virus (complete sequences of RNAs 2, 3 and 4), As soon as the virome characterization of multiple samples of
wheat yellow head virus (complete sequence of the nucleoprotein cultivated and wild plants becomes more routine, more viruses
gene) (Huiet et al., 1991; Estabrook et al., 1996; Seifers et al., with unique features and novel phylogenetic relationships will
2005; Heydarnejad et al., 2006; Mahmoud et al., 2007). HTS likely be discovered. As we assess the viral ‘dark matter,’ we will
would be an essential tool to obtain the complete genomes of start to grasp the evolutionary history of plant viruses, eventually
these viruses and expand our knowledge of genomic architecture leading us to untangle the diversity of the NSR virosphere and
of tenuiviruses. gain increased knowledge about its complex evolutionary and
phylogenetic relationships. A rich picture of the plant virome
landscape will also provide an essential framework for improved
CONCLUSION AND PERSPECTIVES taxonomic classification of plant NSR viruses as part of the realm
Riboviria. In conclusion, HTS-based methods for virus discovery,
The number of NSR plant viruses identified so far represents our ‘new eyes,’ are unraveling in real time the richness and
a negligible fraction of the potential number of NSR viruses magnitude of the plant RNA virosphere.
present in the virosphere. The discovery and in-depth molecular
characterization of these viruses has been challenging given their
extensive divergence, their outstanding diversity in terms of AUTHOR CONTRIBUTIONS
genomic architecture, and mostly, the negligible share of plant
species studied for virus discovery. However, the widespread All authors wrote the manuscript and approved it for publication.
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published: 16 September 2020

The Plant Negative-Sense RNA

Frontiers in Microbiology | www.frontiersin.org 1 September 2020 | Volume 11 | Article 588427

INTRODUCTION Most of the plant viruses described so far, whose nucleotide

Frontiers in Microbiology | www.frontiersin.org 2 September 2020 | Volume 11 | Article 588427

Frontiers in Microbiology | www.frontiersin.org 3 September 2020 | Volume 11 | Article 588427

Virus family/genus Virus Type of target/sequencing technology References

Plant Negative-Sense RNA Virosphere

Virus family/genus Virus Type of target/sequencing technology References

Rhabdoviridae/Alphanucleorhabdovirus Peach virus 1 Total RNA/Illumina HiSeq Zhou et al. (2020)

Plant Negative-Sense RNA Virosphere

Virus family/genus Virus Type of target/sequencing technology References

Plant Negative-Sense RNA Virosphere

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