Tobacco mosaic virus

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Tobacco mosaic virus
TobaccoMosaicVirus.jpg
Transmission electron micrograph of TMV particles negative stained to enhance visibility at 160,000× magnification
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Kitrinoviricota
Class: Alsuviricetes
Order: Martellivirales
Family: Virgaviridae
Genus: Tobamovirus
Species:
Tobacco mosaic virus

Tobacco mosaic virus (TMV) is a positive-sense single-stranded RNA virus species in the genus Tobamovirus that infects a wide range of plants, especially tobacco and other members of the family Solanaceae. The infection causes characteristic patterns, such as "mosaic"-like mottling and discoloration on the leaves (hence the name). TMV was the first virus to be discovered. Although it was known from the late 19th century that a non-bacterial infectious disease was damaging tobacco crops, it was not until 1930 that the infectious agent was determined to be a virus. It is the first pathogen identified as a virus. The virus was crystallised by Wendell Meredith Stanley. It has a similar size to the largest synthetic molecule, known as PG5. [1]

Contents

History

In 1886, Adolf Mayer first described the tobacco mosaic disease that could be transferred between plants, similar to bacterial infections. [2] [3] In 1892, Dmitri Ivanovsky gave the first concrete evidence for the existence of a non-bacterial infectious agent, showing that infected sap remained infectious even after filtering through the finest Chamberland filters. [3] [4] Later, in 1903, Ivanovsky published a paper describing abnormal crystal intracellular inclusions in the host cells of the affected tobacco plants and argued the connection between these inclusions and the infectious agent. [5] However, Ivanovsky remained rather convinced, despite repeated failures to produce evidence, that the causal agent was an unculturable bacterium, too small to be retained on the employed Chamberland filters and to be detected in the light microscope. In 1898, Martinus Beijerinck independently replicated Ivanovsky's filtration experiments and then showed that the infectious agent was able to reproduce and multiply in the host cells of the tobacco plant. [3] [6] Beijerinck adopted the term of "virus" to indicate that the causal agent of tobacco mosaic disease was of non-bacterial nature. Tobacco mosaic virus was the first virus to be crystallized. It was achieved by Wendell Meredith Stanley in 1935 who also showed that TMV remains active even after crystallization. [3] For his work, he was awarded 1/4 of the Nobel Prize in Chemistry in 1946, [7] [8] even though it was later shown some of his conclusions (in particular, that the crystals were pure protein, and assembled by autocatalysis) were incorrect. [9] The first electron microscopical images of TMV were made in 1939 by Gustav Kausche, Edgar Pfankuch and Helmut Ruska – the brother of Nobel Prize winner Ernst Ruska. [10] In 1955, Heinz Fraenkel-Conrat and Robley Williams showed that purified TMV RNA and its capsid (coat) protein assemble by themselves to functional viruses, indicating that this is the most stable structure (the one with the lowest free energy). The crystallographer Rosalind Franklin worked for Stanley for about a month at Berkeley, and later designed and built a model of TMV for the 1958 World's Fair at Brussels. In 1958, she speculated that the virus was hollow, not solid, and hypothesized that the RNA of TMV is single-stranded. [11] This conjecture was proven to be correct after her death and is now known to be the + strand. [12] The investigations of tobacco mosaic disease and subsequent discovery of its viral nature were instrumental in the establishment of the general concepts of virology. [3]

Structure

Schematic model of TMV: 1. nucleic acid (RNA), 2. capsomer protein (protomer), 3. capsid TMV structure full.png
Schematic model of TMV: 1. nucleic acid (RNA), 2. capsomer protein (protomer), 3. capsid

Tobacco mosaic virus has a rod-like appearance. Its capsid is made from 2130 molecules of coat protein and one molecule of genomic single strand RNA, 6400 bases long. The coat protein self-assembles into the rod-like helical structure (16.3 proteins per helix turn) around the RNA, which forms a hairpin loop structure (see the electron micrograph above). The structural organization of the virus gives stability. [13] The protein monomer consists of 158 amino acids which are assembled into four main alpha-helices, which are joined by a prominent loop proximal to the axis of the virion. Virions are ~300 nm in length and ~18 nm in diameter. [14] Negatively stained electron microphotographs show a distinct inner channel of radius ~2 nm. The RNA is located at a radius of ~4 nm and is protected from the action of cellular enzymes by the coat protein. [15] X-ray fiber diffraction structure of the intact virus was studied based on an electron density map at 3.6 Å resolution. [16] Inside the capsid helix, near the core, is the coiled RNA molecule, which is made up of 6,395 ±10 nucleotides. [17] [18] The structure of the virus plays an important role in the recognition of the viral DNA. This happens due to the formation of an obligatory intermediate produced from a protein allows the virus to recognize a specific RNA hairpin structure. [19] The intermediate induces the nucleation of TMV self-assembly by binding with the hairpin structure. [20]

Genome

Genome of tobacco mosaic virus OPSR.Virga.Fig17.v4.png
Genome of tobacco mosaic virus

The TMV genome consists of a 6.3–6.5 kbp single-stranded (ss) RNA. The 3’-terminus has a tRNA-like structure, and the 5’-terminus has a methylated nucleotide cap. (m7G5’pppG). [21] The genome encodes 4 open reading frames (ORFs), two of which produce a single protein due to ribosomal readthrough of a leaky UAG stop codon. The 4 genes encode a replicase (with methyltransferase [MT] and RNA helicase [Hel] domains), an RNA-dependent RNA polymerase, a so-called movement protein (MP) and a capsid protein (CP). [22] The coding sequence starts with the first reading frame, which is 69 nucleotides away from the 5' end of the RNA. [23] The noncoding region at the 5' end can be varied in different individual virions, but there hasn't been any variation found between virions in the noncoding region at the 3' end. [23]

Physicochemical properties

TMV is a thermostable virus. On a dried leaf, it can withstand up to 50 °C (120 degree Fahrenheit) for 30 minutes. [24]

TMV has an index of refraction of about 1.57. [25]

Disease cycle

TMV does not have a distinct overwintering structure. Rather, it will over-winter in infected tobacco stalks and leaves in the soil, on the surface of contaminated seed (TMV can even survive in contaminated tobacco products for many years, so smokers can accidentally transmit it by touch, although not in the smoke itself). [26] [27] With the direct contact with host plants through its vectors (normally insects such as aphids and leafhoppers), TMV will go through the infection process and then the replication process.

Infection and transmission

After its multiplication, it enters the neighboring cells through plasmodesmata. The infection does not spread through contact with insects, [28] but instead spreads by direct contact to the neighboring cells. For its smooth entry, TMV produces a 30 kDa movement protein called P30 which enlarges the plasmodesmata. TMV most likely moves from cell-to-cell as a complex of the RNA, P30, and replicate proteins.

It can also spread through phloem for longer distance movement within the plant. Moreover, TMV can be transmitted from one plant to another by direct contact. Although TMV does not have defined transmission vectors, the virus can be easily transmitted from the infected hosts to the healthy plants by human handling.

Replication

Following entry into its host via mechanical inoculation, TMV uncoats itself to release its viral [+]RNA strand. As uncoating occurs, the MetHel:Pol gene is translated to make the capping enzyme MetHel and the RNA Polymerase. Then the viral genome will further replicate to produce multiple mRNAs via a [-]RNA intermediate primed by the tRNAHIS at the [+]RNA 3' end. The resulting mRNAs encode several proteins, including the coat protein and an RNA-dependent RNA polymerase (RdRp), as well as the movement protein. Thus TMV can replicate its own genome.

After the coat protein and RNA genome of TMV have been synthesized, they spontaneously assemble into complete TMV virions in a highly organized process. The protomers come together to form disks or 'lockwashers' composed of two layers of protomers arranged in a helix. The helical capsid grows by the addition of protomers to the end of the rod. As the rod lengthens, the RNA passes through a channel in its center and forms a loop at the growing end. In this way the RNA can easily fit as a spiral into the interior of the helical capsid. [29]

Host and symptoms

Tobacco mosaic virus symptoms on tobacco Tobacco mosaic virus symptoms tobacco.jpg
Tobacco mosaic virus symptoms on tobacco
Tobacco mosaic virus symptoms on orchid Tobacco mosaic virus symptoms orchid.jpg
Tobacco mosaic virus symptoms on orchid

Like other plant pathogenic viruses, TMV has a very wide host range and has different effects depending on the host being infected. Tobacco mosaic virus has been known to cause a production loss for flue cured tobacco of up to two percent in North Carolina. [30] It is known to infect members of nine plant families, and at least 125 individual species, including tobacco, tomato, pepper (all members of the Solanaceae), cucumbers, a number of ornamental flowers, [31] and beans including Phaseolus vulgaris and Vigna unguiculata . [32] There are many different strains. The first symptom of this virus disease is a light green coloration between the veins of young leaves. This is followed quickly by the development of a "mosaic" or mottled pattern of light and dark green areas in the leaves. Rugosity may also be seen where the infected plant leaves display small localized random wrinkles. These symptoms develop quickly and are more pronounced on younger leaves. Its infection does not result in plant death, but if infection occurs early in the season, plants are stunted. Lower leaves are subjected to "mosaic burn" especially during periods of hot and dry weather. In these cases, large dead areas develop in the leaves. This constitutes one of the most destructive phases of Tobacco mosaic virus infection. Infected leaves may be crinkled, puckered, or elongated. However, if TMV infects crops like grape and apple, it is almost symptomless. TMV is able to infect and complete its replication cycle in a plant pathogenic fungus,TMV is able to enter and replicate in cells of C. acutatum, C. clavatum, and C. theobromicola, which may not be an exception, although it has neither been found nor probably searched for in nature. [33]

Environment

TMV is one of the most stable viruses and has a wide survival range. As long as the surrounding temperature remains below approximately 40 degrees Celsius, TMV can sustain its stable form. All it needs is a host to infect. If necessary, greenhouses and botanical gardens would provide the most favorable condition for TMV to spread out, due to the high population density of possible hosts and the constant temperature throughout the year. It also could be useful to culture TMV in vitro in sap because it can survive up to 3000 days. [34]

Treatment and management

One of the common control methods for TMV is sanitation, which includes removing infected plants and washing hands in between each planting. Crop rotation should also be employed to avoid infected soil/seed beds for at least two years. As for any plant disease, looking for resistant strains against TMV may also be advised. Furthermore, the cross protection method can be administered, where the stronger strain of TMV infection is inhibited by infecting the host plant with a mild strain of TMV, similar to the effect of a vaccine.

In the past ten years, the application of genetic engineering on a host plant genome has been developed to allow the host plant to produce the TMV coat protein within their cells. It was hypothesized that the TMV genome will be re-coated rapidly upon entering the host cell, thus it prevents the initiation of TMV replication. Later it was found that the mechanism that protects the host from viral genome insertion is through gene silencing. [35]

TMV is inhibited by a product of the myxomycete slime mold Physarum polycephalum . Both tobacco and the beans P. vulgaris and V. sinensis suffered almost no lesioning in vitro from TMV when treated with a P. polycephalum extract. [32]

Research has shown that Bacillus spp. can be used to reduce the severity of symptoms from TMV in tobacco plants. In the study, treated tobacco plants had more growth and less build-up of TMV virions than tobacco plants that hadn't been treated. [36]

A research has been conducted by H.Fraenkel-Conrat to show the influence of acetic acid on the Tobacco Mosaic Virus. According to the research, 67% acetic acid resulted as degradation of the virus. [37]

Another possible source of prevention for TMV is the use of salicylic acid. A study completed by a research team at the University of Cambridge found that treating plants with salicylic acid reduced the amount of TMV viral RNAs and viral coat protein present in the tobacco plants. Their research showed that salicylic acid most likely was disrupting replication and transcription and more specifically, the RdRp complex. [38]

A research was conducted and revealed that humans have antibodies against Tobacco Mosaic Virus. [39]

Scientific and environmental impact

TMV virus: super resolution light microscopy TMV virus super resolution microscopy Christoph Cremer Christina Wege.jpg
TMV virus: super resolution light microscopy

The large amount of literature about TMV and its choice for many pioneering investigations in structural biology (including X-ray diffraction), virus assembly and disassembly, and so on, are fundamentally due to the large quantities that can be obtained, plus the fact that it does not infect animals. After growing several hundred infected tobacco plants in a greenhouse, followed by a few simple laboratory procedures, a scientist can produce several grams of the virus. [40] In fact, tobacco mosaic virus is so proliferate that the inclusion bodies can be seen with only a light microscope. [28]

James D. Watson, in his memoir The Double Helix , cites his x-ray investigation of TMV's helical structure as an important step in deducing the nature of the DNA molecule. [41]

Applications

Plant viruses can be used to engineer viral vectors, tools commonly used by molecular biologists to deliver genetic material into plant cells; they are also sources of biomaterials and nanotechnology devices. [42] [43] Viral vectors based on TMV include those of the magnICON and TRBO plant expression technologies. [43] [44] Due to its cylindrical shape, high aspect ratio, self-assembling nature, and ability to incorporate metal coatings (nickel and cobalt) into its shell, TMV is an ideal candidate to be incorporated into battery electrodes. [45] Addition of TMV to a battery electrode increases the reactive surface area by an order of magnitude, resulting in an increase in the battery's capacity by up to six times compared to a planar electrode geometry. [45] [46] The TMV-based vector also enabled C. acutatum to transiently express exogenous GFP up to six subcultures and for at least 2 mo after infection, without the need to develop transformation technology, RNAi can be expressed in the phytopathogenic fungus Colletotrichum acutatum by VIGS using a recombinant vector based on TMV in which the ORF of the gene encoding the green fluorescent protein (GFP) was transcribed in fungal cells from a duplicate of the TMV coat protein (CP) subgenomic mRNA promoter and demonstrated that the approach could be used to obtain foreign protein expression in fungi. [33]

Related Research Articles

Cauliflower mosaic virus (CaMV) is a member of the genus Caulimovirus, one of the six genera in the family Caulimoviridae, which are pararetroviruses that infect plants. Pararetroviruses replicate through reverse transcription just like retroviruses, but the viral particles contain DNA instead of RNA.

<span class="mw-page-title-main">Plant virus</span> Virus that affects plants

Plant viruses are viruses that affect plants. Like all other viruses, plant viruses are obligate intracellular parasites that do not have the molecular machinery to replicate without a host. Plant viruses can be pathogenic to vascular plants.

<i>Geminiviridae</i> Family of viruses

Geminiviridae is a family of plant viruses that encode their genetic information on a circular genome of single-stranded (ss) DNA. There are 520 species in this family, assigned to 14 genera. Diseases associated with this family include: bright yellow mosaic, yellow mosaic, yellow mottle, leaf curling, stunting, streaks, reduced yields. They have single-stranded circular DNA genomes encoding genes that diverge in both directions from a virion strand origin of replication. According to the Baltimore classification they are considered class II viruses. It is the largest known family of single stranded DNA viruses.

<i>Tombusviridae</i> Family of viruses

Tombusviridae is a family of single-stranded positive sense RNA plant viruses. There are three subfamilies, 17 genera, and 95 species in this family. The name is derived from Tomato bushy stunt virus (TBSV).

<i>Brome mosaic virus</i> Species of virus

Brome mosaic virus (BMV) is a small, positive-stranded, icosahedral RNA plant virus belonging to the genus Bromovirus, family Bromoviridae, in the Alphavirus-like superfamily.

<i>Tobamovirus</i> Genus of viruses

Tobamovirus is a genus of positive-strand RNA viruses in the family Virgaviridae. Many plants, including tobacco, potato, tomato, and squash, serve as natural hosts. Diseases associated with this genus include: necrotic lesions on leaves. The name Tobamovirus comes from the host and symptoms of the first virus discovered.

<i>Tomato bushy stunt virus</i> Species of virus

Tomato bushy stunt virus (TBSV) is a virus of the tombusvirus family. It was first reported in tomatoes in 1935 and primarily affects vegetable crops, though it is not generally considered an economically significant plant pathogen. Depending upon the host, TBSV causes stunting of growth, leaf mottling, and deformed or absent fruit. The virus is likely to be soil-borne in the natural setting, but can also be transmitted mechanically, for example through contaminated cutting tools. TBSV has been used as a model system in virology research on the life cycle of plant viruses, particularly in experimental infections of the model host plant Nicotiana benthamiana.

<span class="mw-page-title-main">Movement protein</span>

In order for a virus to infect a plant, it must be able to move between cells so it can spread throughout the plant. Plant cell walls make this moving/spreading quite difficult and therefore, for this to occur, movement proteins must be present. A movement protein (MP) is a specific virus-encoded protein that is considered to be a general feature of plant genomes. They allow for local and systemic viral spread throughout a plant. MPs were first studied in the Tobacco Mosaic Virus (TMV) where it was found that viruses were unable to spread without the presence of a specific protein. In general, the plant viruses first, move within the cell from replication sites to the plasmodesmata (PD). Then, the virus is able to go through the PD and spread to other cells. This process is controlled through MPs. Different MPs use different mechanisms and pathways to regulate this spread of some viruses. Nearly all plants express at least one MP, while some can encode many different MPs which help with cell to cell viral transmission. They serve to increase the size exclusion limits (SEL) of plasmodesmata to allow for greater spread of the virus.

<i>Potyvirus</i> Genus of positive-strand RNA viruses in the family Potyviridae

Potyvirus is a genus of positive-strand RNA viruses in the family Potyviridae. Plants serve as natural hosts. Like begomoviruses, members of this genus may cause significant losses in agricultural, pastoral, horticultural, and ornamental crops. More than 200 species of aphids spread potyviruses, and most are from the subfamily Aphidinae. The genus contains 190 species and potyviruses account for about thirty percent of all currently known plant viruses.

<i>Tobacco virtovirus 1</i> Species of satellite virus

Tobacco virtovirus 1, informally called Tobacco mosaic satellite virus, Satellite tobacco mosaic virus (STMV), or tobacco mosaic satellite virus, is a satellite virus first reported in Nicotiana glauca from southern California, U.S.. Its genome consists of linear positive-sense single-stranded RNA.

<span class="mw-page-title-main">Viroplasm</span>

A viroplasm, sometimes called "virus factory" or "virus inclusion", is an inclusion body in a cell where viral replication and assembly occurs. They may be thought of as viral factories in the cell. There are many viroplasms in one infected cell, where they appear dense to electron microscopy. Very little is understood about the mechanism of viroplasm formation.

<span class="mw-page-title-main">Viral vector</span> Biotechnology to deliver genetic material into a cell

Viral vectors are tools commonly used by molecular biologists to deliver genetic material into cells. This process can be performed inside a living organism or in cell culture. Viruses have evolved specialized molecular mechanisms to efficiently transport their genomes inside the cells they infect. Delivery of genes or other genetic material by a vector is termed transduction and the infected cells are described as transduced. Molecular biologists first harnessed this machinery in the 1970s. Paul Berg used a modified SV40 virus containing DNA from the bacteriophage λ to infect monkey kidney cells maintained in culture.

<i>Cowpea chlorotic mottle virus</i> Species of virus

Cowpea chlorotic mottle virus, known by the abbreviation CCMV, is a virus that specifically infects the cowpea plant, or black-eyed pea. The leaves of infected plants develop yellow spots, hence the name "chlorotic". Similar to its "brother" virus, Cowpea mosaic virus (CPMV), CCMV is produced in high yield in plants. In the natural host, viral particles can be produced at 1–2 mg per gram of infected leaf tissue. Belonging to the bromovirus genus, cowpea chlorotic mottle virus (CCMV) is a small spherical plant virus. Other members of this genus include the brome mosaic virus (BMV) and the broad bean mottle virus (BBMV).

<i>Alfalfa mosaic virus</i> Species of virus

Alfalfa mosaic virus (AMV), also known as Lucerne mosaic virus or Potato calico virus, is a worldwide distributed phytopathogen that can lead to necrosis and yellow mosaics on a large variety of plant species, including commercially important crops. It is the only Alfamovirus of the family Bromoviridae. In 1931 Weimer J.L. was the first to report AMV in alfalfa. Transmission of the virus occurs mainly by some aphids, by seeds or by pollen to the seed.

<i>Cucumber mosaic virus</i> Species of virus

Cucumber mosaic virus (CMV) is a plant pathogenic virus in the family Bromoviridae. This virus has a worldwide distribution and a very wide host range, having the reputation of the widest host range of any known plant virus. It can be transmitted from plant to plant both mechanically by sap and by aphids in a stylet-borne fashion. It can also be transmitted in seeds and by the parasitic weeds, Cuscuta sp. (dodder).

<span class="mw-page-title-main">Introduction to viruses</span> Non-technical introduction to viruses

A virus is a tiny infectious agent that reproduces inside the cells of living hosts. When infected, the host cell is forced to rapidly produce thousands of identical copies of the original virus. Unlike most living things, viruses do not have cells that divide; new viruses assemble in the infected host cell. But unlike simpler infectious agents like prions, they contain genes, which allow them to mutate and evolve. Over 4,800 species of viruses have been described in detail out of the millions in the environment. Their origin is unclear: some may have evolved from plasmids—pieces of DNA that can move between cells—while others may have evolved from bacteria.

<span class="mw-page-title-main">Virus</span> Infectious agent that replicates in cells

A virus is a submicroscopic infectious agent that replicates only inside the living cells of an organism. Viruses infect all life forms, from animals and plants to microorganisms, including bacteria and archaea. Viruses are found in almost every ecosystem on Earth and are the most numerous type of biological entity. Since Dmitri Ivanovsky's 1892 article describing a non-bacterial pathogen infecting tobacco plants and the discovery of the tobacco mosaic virus by Martinus Beijerinck in 1898, more than 11,000 of the millions of virus species have been described in detail. The study of viruses is known as virology, a subspeciality of microbiology.

Vesivirus is a genus of viruses, in the family Caliciviridae. Swine, sea mammals, and felines serve as natural hosts. There are two species in this genus. Diseases associated with this genus include: respiratory disease, Feline calicivirus (FCV); conjunctivitis, and respiratory disease.

<i>Sepik virus</i> Mosquito transmitted virus endemic to Papua New Guinea

Sepik virus (SEPV) is an arthropod-borne virus (arbovirus) of the genus Flavivirus and family Flaviviridae. Flaviviridae is one of the most well characterized viral families, as it contains many well-known viruses that cause diseases that have become very prevalent in the world, like Dengue virus. The genus Flavivirus is one of the largest viral genera and encompasses over 50 viral species, including tick and mosquito borne viruses like Yellow fever virus and West Nile virus. Sepik virus is much less well known and has not been as well-classified as other viruses because it has not been known of for very long. Sepik virus was first isolated in 1966 from the mosquito Mansoniaseptempunctata, and it derives its name from the Sepik River area in Papua New Guinea, where it was first found. The geographic range of Sepik virus is limited to Papua New Guinea, due to its isolation.

<i>Orthornavirae</i> Kingdom of viruses

Orthornavirae is a kingdom of viruses that have genomes made of ribonucleic acid (RNA), including genes which encode an RNA-dependent RNA polymerase (RdRp). The RdRp is used to transcribe the viral RNA genome into messenger RNA (mRNA) and to replicate the genome. Viruses in this kingdom share a number of characteristics which promote rapid evolution, including high rates of genetic mutation, recombination, and reassortment.

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