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Review
. 2011 Dec;12(9):938-54.
doi: 10.1111/j.1364-3703.2011.00752.x. Epub 2011 Oct 21.

Top 10 plant viruses in molecular plant pathology

Karen-Beth G Scholthof  1 , Scott Adkins, Henryk Czosnek, Peter Palukaitis, Emmanuel Jacquot, Thomas Hohn, Barbara Hohn, Keith Saunders, Thierry Candresse, Paul Ahlquist, Cynthia Hemenway, Gary D Foster
Affiliations
Review

Top 10 plant viruses in molecular plant pathology

Karen-Beth G Scholthof et al. Mol Plant Pathol. 2011 Dec.

Abstract

Many scientists, if not all, feel that their particular plant virus should appear in any list of the most important plant viruses. However, to our knowledge, no such list exists. The aim of this review was to survey all plant virologists with an association with Molecular Plant Pathology and ask them to nominate which plant viruses they would place in a 'Top 10' based on scientific/economic importance. The survey generated more than 250 votes from the international community, and allowed the generation of a Top 10 plant virus list for Molecular Plant Pathology. The Top 10 list includes, in rank order, (1) Tobacco mosaic virus, (2) Tomato spotted wilt virus, (3) Tomato yellow leaf curl virus, (4) Cucumber mosaic virus, (5) Potato virus Y, (6) Cauliflower mosaic virus, (7) African cassava mosaic virus, (8) Plum pox virus, (9) Brome mosaic virus and (10) Potato virus X, with honourable mentions for viruses just missing out on the Top 10, including Citrus tristeza virus, Barley yellow dwarf virus, Potato leafroll virus and Tomato bushy stunt virus. This review article presents a short review on each virus of the Top 10 list and its importance, with the intent of initiating discussion and debate amongst the plant virology community, as well as laying down a benchmark, as it will be interesting to see in future years how perceptions change and which viruses enter and leave the Top 10.

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Figures

Figure 1
Figure 1
Tobacco mosaic virus (TMV). (A) Systemic infection of Nicotiana tabacum cv. Turk plants showing TMV‐associated mosaic. (B) Necrotic local lesions on N. tabacum cv. Glurk leaf, demonstrating Holmes' N‐gene resistance following inoculation with TMV.
Figure 2
Figure 2
Tobacco mosaic virus (TMV) particles and encapsidation. Foreground: schematic diagram showing TMV protein aggregate binding to the RNA origin‐of‐assembly loop; additional aggregates then bind to the initial complex, pulling the 5′ end of the RNA up through the hole in the middle of the growing virus particle. Background: negative‐stain electron micrograph of TMV virions. (Photomontage courtesy of Amy Kendall and Gerald Stubbs, Vanderbilt University, Nashville, TN, USA.)
Figure 3
Figure 3
Tomato spotted wilt virus (TSWV) symptoms. (A) Stunted tomato plant (foreground) as a result of TSWV infection at an early stage of growth. Noninfected tomato plant (background) is shown for comparison. (B) Ring/line patterns on desert rose (Adenium obesum) leaf from plant infected with TSWV.
Figure 4
Figure 4
Transmission electron micrograph of isolated Tomato spotted wilt virus (TSWV) virions. Nonfixed virion preparation stained with 1% (w/v) methylamine tungstate.
Figure 5
Figure 5
(A) Geminate Tomato yellow leaf curl virus (TYLCV) particles. (B) Genome organization of TYLCV. The single‐stranded virion DNA comprises 2787 nucleotides. Open reading frames (ORFs) of virion‐sense and complementary‐sense strand polarity are designated (V) and (C), respectively. ORFs are represented by arrows; numbers indicate first and last nucleotides of each ORF. The conserved inverted repeat flanking the conserved sequence TAATATT/AC is symbolized by a stem‐loop; an arrowhead indicates the cleaving position of replication‐associated protein (Rep) in the TAATATT/AC loop; A at the cutting site (/) is nucleotide number one, by definition.
Figure 6
Figure 6
(A) Numerous whiteflies on a tomato leaf. (B) Top panel, noninfected tomato plant; bottom panel, typical Tomato yellow leaf curl virus (TYLCV) disease on a tomato plant. (C) Infected susceptible (left) and resistant (right) tomato lines bred for resistance to begomoviruses.
Figure 7
Figure 7
Cucumber mosaic virus (CMV). (A) Negatively stained isometric particles of 29 nm in diameter. (B) Genome organization.
Figure 8
Figure 8
Electron micrograph of negatively stained, purified, Potato virus Y (PVY) particles (A), organization of the PVY genome (B) and symptoms on Solanum tuberosum (C, D) and Nicotiana tabacum (E, F). The viral RNA in (B) is illustrated by a thin line with the viral genome‐linked protein (VPg) (grey circle) and poly‐A tail ((A)n) attached at the 5′ and 3′ ends, respectively. The grey box corresponds to the large open reading frame (ORF); the names of the different proteins are listed. The scales [nucleotide (Nt) and amino acid (aa)] are according to isolate PVYN‐605 (Jakab et al., 1997; GenBank accession no. X97895). Local lesions (C) and tuber necrosis (D) on S. tuberosum. Vein necrosis (E) and mosaic (F) on N. tabacum. Copyrights ©: (A) NIB‐INRA, M. Tušek (NIB); (C)–(F) INRA, L. Glais.
Figure 9
Figure 9
Cauliflower mosaic virus (CaMV). Top row, left to right: virion double‐stranded DNA (dsDNA) with single‐strand overlaps (background virus particles: diameter, 50 nm); knotted DNA; minichromosome (from Ménissier et al., 1983); electron micrograph: section through infected cells showing inclusion body harbouring virus particles and a tubular structure bridging two cells transporting a virus particle. Bottom left: the three types of RNA: 8S, 19S and 35S. The process of shunting and transactivation/viroplasmin protein (TAV)‐guided polycistronic translation of the open reading frames (ORFs) is shown. Centre: particle showing the icosahedral arrangement of the GAG (name borrowed from retrovirus ‘group‐specific antigen’) (yellow) and virion‐associated (VAP) (blue) proteins (from Hoh et al., 2010). Bottom right: map of CaMV showing the ORFs and RNAs. ITF, insect transmission factor.
Figure 10
Figure 10
Varied symptoms of disease caused by African cassava mosaic virus (ACMV) in cassava: (A) mild; (B) severe; (C) noninfected.
Figure 11
Figure 11
Genomic components of African cassava mosaic virus (ACMV). DNA‐A encodes six open reading frames: AV1, coat protein; AV2, precoat protein; AC1, replication‐associated protein; AC2, transcriptional activator protein; AC3, replication enhancer protein; AC4, silencing suppressor protein. DNA‐B encodes two genes required for plant virus movement: BC1, movement protein (cell to cell); BV1, nuclear shuttle protein. C, complementary‐sense open reading frames (ORFs); V, virus‐sense ORFs. Black box, location of the nucleotide sequence common to both genomic components. Light grey boxes designate ORFs.
Figure 12
Figure 12
Severe symptoms of Plum pox virus (PPV) infection on plums of the Pozegaca type.
Figure 13
Figure 13
Symptoms of Plum pox virus (PPV) infection in Arabidopsis thaliana (ecotype Ler). The plant on the left is a noninfected control.
Figure 14
Figure 14
Cryo‐electron microscope three‐dimensional image reconstructions of Brome mosaic virus (BMV) virions from BMV‐infected barley plants (BMVP, left panel) and from Saccharomyces cerevisiae yeast cells expressing BMV coat protein and BMV genomic RNA2 as an encapsidation substrate (BMVSc, right panel). From Krol et al. (1999).
Figure 15
Figure 15
Schematic diagram of the Brome mosaic virus (BMV) genome, showing genomic RNA1 (3.2 kb), RNA2 (2.9 kb) and RNA3 (2.1 kb), plus subgenomic RNA4. The shaded boxes indicate the open reading frames for RNA replication proteins 1a and 2aPol, the movement protein (MP) and coat protein (CP). Brackets indicate the conserved RNA capping methyltransferase and NTPase/helicase domains in 1a and the RNA polymerase domain in 2aPol. The red cloverleaf structures represent the aminoacylatable tRNA‐like regions at the 3′ ends of RNAs 1–4.
Figure 16
Figure 16
Electron micrograph of the Potato virus X (PVX) particle.
Figure 17
Figure 17
Potato virus X (PVX) genome. Interacting cis‐acting elements near the termini of viral RNA and complementary internal conserved elements are marked with red and black asterisks, respectively.
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