The Bunyavirales: The Plant-Infecting Counterparts

Negative-strand (-) RNA viruses (NSVs) comprise a large and diverse group of viruses that are generally divided in those with non-segmented and those with segmented genomes. Whereas most NSVs infect animals and humans, the smaller group of the plant-infecting counterparts is expanding, with many causing devastating diseases worldwide, affecting a large number of major bulk and high-value food crops. In 2018, the taxonomy of segmented NSVs faced a major reorganization with the establishment of the order Bunyavirales. This article overviews the major plant viruses that are part of the order, i.e., orthospoviruses (Tospoviridae), tenuiviruses (Phenuiviridae), and emaraviruses (Fimoviridae), and provides updates on the more recent ongoing research. Features shared with the animal-infecting counterparts are mentioned, however, special attention is given to their adaptation to plant hosts and vector transmission, including intra/intercellular trafficking and viral counter defense to antiviral RNAi.

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New Technologies for Studying Negative-Strand RNA Viruses in Plant and Arthropod Hosts

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-10-19-0281-fi ◽

2020 ◽

Vol 33 (3) ◽

pp. 382-393 ◽

Cited By ~ 6

Author(s):

Thomas L. German ◽

Marcé D. Lorenzen ◽

Nathaniel Grubbs ◽

Anna E. Whitfield

Keyword(s):

Functional Analysis ◽

New Technologies ◽

Rna Viruses ◽

Control Strategies ◽

Plant Viruses ◽

Negative Strand ◽

Transmission Cycle ◽

Technological Advances ◽

Biological Vector ◽

Host Virus Interactions

The plant viruses in the phylum Negarnaviricota, orders Bunyavirales and Mononegavirales, have common features of single-stranded, negative-sense RNA genomes and replication in the biological vector. Due to the similarities in biology, comparative functional analysis in plant and vector hosts is helpful for understanding host–virus interactions for negative-strand RNA viruses. In this review, we will highlight recent technological advances that are breaking new ground in the study of these recalcitrant virus systems. The development of infectious clones for plant rhabdoviruses and bunyaviruses is enabling unprecedented examination of gene function in plants and these advances are also being transferred to study virus biology in the vector. In addition, genome and transcriptome projects for critical nonmodel arthropods has enabled characterization of insect response to viruses and identification of interacting proteins. Functional analysis of genes using genome editing will provide future pathways for further study of the transmission cycle and new control strategies for these viruses and their vectors.

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Faculty Opinions recommendation of Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1032149.373802 ◽

2006 ◽

Author(s):

Lynn Enquist

Keyword(s):

Rna Viruses ◽

Dna Viruses ◽

Double Stranded Rna ◽

Positive Strand ◽

Negative Strand ◽

Positive Strand Rna

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Faculty Opinions recommendation of Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1032149.372810 ◽

2006 ◽

Author(s):

Grant McFadden

Keyword(s):

Rna Viruses ◽

Dna Viruses ◽

Double Stranded Rna ◽

Positive Strand ◽

Negative Strand ◽

Positive Strand Rna

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Faculty Opinions recommendation of Construction of a Sonchus Yellow Net Virus minireplicon: a step toward reverse genetic analysis of plant negative-strand RNA viruses.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718046996.793484160 ◽

2013 ◽

Author(s):

Vitaly Citovsky

Keyword(s):

Genetic Analysis ◽

Rna Viruses ◽

Reverse Genetic ◽

Negative Strand

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Viral Hemorrhagic Fevers of Animals Caused by Negative-Strand RNA Viruses

Global Virology I - Identifying and Investigating Viral Diseases ◽

10.1007/978-1-4939-2410-3_11 ◽

2015 ◽

pp. 247-317

Author(s):

Knut Falk ◽

Maria Aamelfot ◽

Ole Bendik Dale ◽

Theodore R. Meyers ◽

Sally Ann Iverson ◽

...

Keyword(s):

Rna Viruses ◽

Negative Strand ◽

Hemorrhagic Fevers ◽

Viral Hemorrhagic Fevers

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Replication of Nonsegmented Negative Strand RNA Viruses

RNA Genetics ◽

10.1201/9781351076425-7 ◽

2018 ◽

pp. 137-158

Author(s):

Paul S. Masters ◽

Amiya K. Banerjee

Keyword(s):

Rna Viruses ◽

Negative Strand

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A synergistic effect between 3′ terminal noncoding and adjacent coding regions of influenza A virus HA segment on template preference

Journal of Virology ◽

10.1128/jvi.00878-21 ◽

2021 ◽

Author(s):

Yue Xiao ◽

Wenyu Zhang ◽

Minglei Pan ◽

David L. V. Bauer ◽

Yuhai Bi ◽

...

Keyword(s):

Synergistic Effect ◽

Influenza A Virus ◽

Influenza A ◽

Rna Viruses ◽

Nucleotide Position ◽

Virus Growth ◽

Noncoding Regions ◽

Negative Strand ◽

Coding Regions ◽

Growth Phenotype

The influenza A virus genome is comprised of eight single-stranded negative-sense viral RNA (vRNA) segments. Each of the eight vRNA segments contains segment-specific nonconserved noncoding regions (NCRs) of similar sequence and length in different influenza A virus strains. However, in the subtype-determinant segments, encoding haemagglutinin (HA) and neuraminidase (NA), the segment-specific noncoding regions are subtype-specific, varying significantly in sequence and length at both the 3´ and 5´ termini among different subtypes. The significance of these subtype-specific noncoding regions (ssNCR) in the influenza virus replication cycle is not fully understood. In this study, we show that truncations of the 3´-end H1-subtype-specific noncoding region (H1-ssNCR) resulted in recombinant viruses with decreased HA vRNA replication and attenuated growth phenotype, although the vRNA replication was not affected in single-template RNP reconstitution assays. The attenuated viruses were unstable and point mutations at nucleotide position 76 or 56 in the adjacent coding region of HA vRNA were found after serial passage. The mutations restored the HA vRNA replication and reversed the attenuated virus growth phenotype. We propose that the terminal noncoding and adjacent coding regions act synergistically to ensure optimal levels of HA vRNA replication in a multi-segment environment. These results, provide novel insights into the role of the 3´-end nonconserved noncoding regions and adjacent coding regions on template preference in multiple-segmented negative-strand RNA viruses. IMPORTANCE While most influenza A virus vRNA segments contain segment-specific nonconserved noncoding regions of similar length and sequence, these regions vary considerably both in length and sequence in the segments encoding HA and NA, the two major antigenic determinants of influenza A viruses. In this study, we investigated the function of the 3´-end H1-ssNCR and observed a synergistic effect between the 3´-end H1-ssNCR nucleotides and adjacent coding nucleotide(s) of HA segment on template preference in a multi-segment environment. The results unravel an additional level of complexity in the regulation of RNA replication in multiple-segmented negative-strand RNA viruses.

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