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Plantwise Technical Factsheet

tobacco mosaic (Tobacco mosaic virus)

Host plants / species affected
Abutilon theophrasti (velvet leaf)
Allium chinense (spring onion)
Allium sativum (garlic)
Amaranthus retroflexus (redroot pigweed)
Apium graveolens (celery)
Beta vulgaris (beetroot)
Brassicaceae (cruciferous crops)
Calendula officinalis (Pot marigold)
Canavalia ensiformis (gotani bean)
Capsicum annuum (bell pepper)
Citrullus lanatus (watermelon)
Cucumis sativus (cucumber)
Cymbidium
Dahlia
Euphorbia pulcherrima (poinsettia)
Glycine max (soyabean)
Helianthus annuus (sunflower)
Malus domestica (apple)
Mentha gracilis
Nicotiana glauca (tree tobacco)
Nicotiana tabacum (tobacco)
Petunia
Petunia hybrida
Phaseolus vulgaris (common bean)
Physalis (Groundcherry)
Pimpinella brachycarpa
Plantago (Plantain)
Prunus persica (peach)
Pyrus communis (European pear)
Robinia pseudoacacia (black locust)
Rosa (roses)
Sesamum indicum (sesame)
Solanum (nightshade)
Solanum lycopersicum (tomato)
Solanum melongena (aubergine)
Solanum tuberosum (potato)
Vicia faba (faba bean)
Vigna unguiculata (cowpea)
List of symptoms/signs
Fruit  -  abnormal shape
Fruit  -  lesions: black or brown
Fruit  -  reduced size
Growing point  -  distortion
Inflorescence  -  distortion (non-graminaceous plants)
Leaves  -  abnormal colours
Leaves  -  abnormal forms
Leaves  -  abnormal patterns
Stems  -  discoloration of bark
Stems  -  distortion
Whole plant  -  distortion; rosetting
Whole plant  -  dwarfing
Symptoms
Burnt streak symptoms often occur of old leaves on mosaic-susceptible tobacco (Lucas, 1975). Necrotic systemic symptoms may occur on tobacco genotypes bearing the N-gene (hypersensitive reaction) when TMV is inoculated on plants at the second to third leaf stage (Culver et al., 1991), or after keeping infected plants at temperatures above 30°C for several hours during the day (Piccirillo and Piro, 1996).

Tobacco

In tobacco, three genes (N', n and N) control the response to tobamoviruses. N' and n are wild genes of N. tabacum, while the N-gene was introduced from the wild species Nicotiana glutinosa (Holmes, 1938). The N-gene elicits a local necrotic response against all TMV strains known, N' causes necrotic reaction to TMV and mosaic reaction to ToMV, and n gives mosaic with both TMV and ToMV (Piccirillo and Piro, 1996).

Hypersensitive hosts

Local necrotic lesions (1-2 mm) elicited at the infection points localize both TMV and ToMV, preventing virus spread within the plant. While lesions are clearly visible on inoculated plants in the greenhouse, they are difficult to discern in the field.

N-genotype plantlets (50-60 days) inoculated with TMV show systemic necrosis after the local reaction when kept at 30°C for several hours during the day (Piccirillo, unpublished data, 1992). At temperatures constantly above 28-30°C, mosaic symptoms develop on N genotypes (White and Sugars, 1996).

Necrotic spots on the stem of N-genotype plants may appear in the field if the temperature rises above 30°C for a few hours during the day and can be reproduced in greenhouse by keeping inoculated plants at the same temperature conditions (Piccirillo, 1992; Piccirillo, unpublished data, 1995).

Sensitive hosts

Native tobacco genotypes react to TMV with progressive symptoms: veinal discoloration on young leaves 5-6 days after inoculation, followed by a mottling or mosaic pattern of light and dark-green areas which gives the disease its name, and later by blistering and fern-shaped leaves. Abnormal growth and stunting, with distorted and dwarfed leaves, also occur.

Plants infected at the late stages only develop symptoms on the apical leaves. Flowers rarely show symptoms of blotch mosaic and distortion. Roots of infected plants do not show symptoms. An asymptomatic reaction occurs in Ambalema, a native tobacco from Colombia (Nolla, 1938), with the virus spreading throughout the whole plant without evident symptoms.

Tomato

On tomato, tomato mosaic virus (ToMV) or the tomato strain of TMV is mainly present.

Hypersensitive hosts

The hypersensitivity reaction with local necrotic lesions is triggered by three near-dominant genes: Tm1 (from Lycopersicon hirsutum) inhibiting viral multiplication of some ToMV pathotypes; Tm2 and Tm2-2 alleles (from Lycopersicon peruvianum) enabling the plants to stop the virus at the infection point (Marchoux and Gebre-Selassie, 1989). A gene-for-gene relationship holds for the system tomato/ToMV: more genes in the hosts in parallel with related genes of the virus. At high temperatures the hypersensitivity reaction is followed by systemic necrosis.

Sensitive hosts

Sensitive hosts show light mosaic (type aucuba), leaf distortion, blistering, shoestring and fruit deformation. Fruits appear malformed with either slightly raised or depressed spots (pitting) and sometimes black or brown necrotic lesions inside.

Graywall or internal browning symptoms have been ascribed also to other agents (Boyle et al., 1992).

Pepper

Capsicum is sensitive to both TMV and ToMV, but the strains found on Capsicum crops in every part of the world belong mainly to ToMV.

Hypersensitive hosts

A local necrotic reaction against ToMV pathotypes is regulated by an L gene of the genus Capsicum, with a wild allele (L1) of C. annuum and alleles introgressed from C. frutescens (L2), C. chinensis (L3) and C. chacoense (Marchoux and Gebre-Selassie, 1989; Rusko et al., 1995). Different nomenclatures for both ToMV strains and hypersensitivity genes of TMV have been used in the literature.

Sensitive hosts

Yellow mosaic, mottling and leaf distortion are caused both by TMV and ToMV in sensitive hosts.

Tobamoviruses not related to TMV (Xiang et al., 1994) causing severe yield losses on pepper are pepper mild mottle virus (PMMV) (Garcia-Luque et al., 1992) and tobacco mild green mosaic virus (TMGMV) (Green and Wu, 1991).
Prevention and control

Host-Plant Resistance

Tobacco

N-gene hypersensitivity was first recommended as a crop resistance strategy against TMV spread by Holmes (1938), who also bred the Samsun NN cultivar by transferring the N gene from N. glutinosa via the synthetic amphidiploid N. digluta (N. glutinosa (n=24) x N. tabacum (n=12)). The reaction localizes TMV and most tobamoviruses at the infection point. This type of resistance has proved durable (Piccirillo and Piro, 1996; Nielsen, 1997). A reported tobamovirus (OB strain) causing mosaic on NN tobacco has recently been classified as a different virus (Padgett and Beachy, 1993).

N-gene resistance has proved practically valuable only in Burley type varieties; in other types resistance is correlated with lower quality of the cured leaf (Lucas 1975; Nielsen and Kennedy, 1994; Aycock and McKee, 1995). The introduction via biotechnology of the single N-gene could help overcome the correlated negative traits in the latter types (Whitham et al., 1994; Baker et al., 1996). Genetic engineering is being used extensively to introduce resistance to tobamoviruses in tobacco.

Sensitive tobacco plants transformed with a gene expressing the coat protein of TMV acquired considerable resistance to virus replication (Reimann-Philipp and Beachy, 1993). Likewise a mutant gene of TMV coat protein interfered with disassembly in viral replication (Bin-Lu et al., 1998).

Insertion of a TMV-RNA antisense construct in sensitive tobacco inhibits the gene encoding of both 126-183 kDa replicase proteins (Nelson et al., 1993). Transgenic tobacco plants expressing the gene for TMV replicase with an additional insertion in the middle of 183-kDa has been shown to be highly resistant to systemic infection by TMV and other tobamoviruses (Donson et al., 1993).

Plants transformed with a gene encoding a defective mutant of the TMV movement protein had delayed symptom appearance and reduced systemic spread of infection to upper leaves (Cooper et al., 1995).

A gene for ribosome inactivating protein gives resistance to infection by different viruses (Smirnov et al., 1997).

Tomato

The Tm1, Tm2 and Tm2-2 resistance genes against ToMV have been overcome by the occurrence of the 1, 2, 1-2 and 2-2 virulent pathotypes (Marchoux and Gebre-Selassie, 1989; Betti et al., 1997). Pathotype frequency varies region by region and depends also on the presence of matching resistance genes (Feng et al., 1996).

Transgenic tomato with the N-gene from tobacco shows the hypersensitive type of resistance (Baker et al., 1996).

Pepper

The L1, L2, L3 and L4 genes for resistance to tobamoviruses are matched by pathotypes P0, P1, P1-2, P1-2-3 (Garcia-Luque et al., 1992; Rusko et al., 1995). L1 is wild in Capsicum annuum, L2 in C. frutescens, L3 in C. chinensis and L4 in C. chacoense. The P0 pathotype is considered to belong to tobacco mild green mosaic virus (Green and Wu, 1991), while pathotypes P1-2 and P1-2-3 are considered strains of pepper mild mottle tobamovirus (Garcia et al., 1992).

Biological Control

In some cases systemic acquired resistance (SAR), induced by a previous infection with a pathogen or by application of salicylic acid, has been effective against TMV (Ward et al., 1991). Salicylic acid, levels of which increase during the hypersensitivity reaction in tobacco in both inoculated and virus-free leaves, is considered a precursor of SAR (Enyedi et al., 1992; Shulaev et al., 1995). A disease resistant state develops in plants after the hypersensitive reaction.

Proteins inactivating the virus in vitro and in vivo have been isolated from numerous vegetable species (Sadasivam et al., 1991) including Phytolacca sp. (Watanabe et al., 1997), Chenopodium murale (Neeta Srivastava and Verma, 1995) and Amaranthus viridis (Kwon et al., 1997). Ribosome inactivating proteins isolated from Phytolacca americana, inhibit ribosome activity by depurinating rRNA at a specific site. Ribosome inactivating proteins expressing transgenic tobaccos are resistant to a broad spectrum of plant viruses (Smirnov et al., 1997).

Cross-protection by inoculation with avirulent or attenuated strains of TMV can prevent the sensitive mosaic reaction causing further infection with virulent strains of TMV (Todoroki and Chiba, 1995). For tobacco, pepper and tomato, pre-inoculation with attenuated virus hinders viral replication, reduces symptom expression and improves product quality (Hayama and Nagai, 1993; Todoroki and Chiba, 1995).

Sat-TMV, a TMV satellite found in association with TMV in naturally infected plants of N. glauca in California, USA, has been correlated with a reduction of the amount of virus replication (Valverde et al., 1991). In pepper the presence of Sat-TMV attenuated the severe blistering caused by TMV (Rodriguez-Alvarado et al., 1994).

A new approach to the control of virus infection is based on plant immunological response: a reduction in TMV symptoms was obtained in tobacco plants producing antibodies against TMV after transformation with a gene from mice immunized with TMV (Voss et al., 1995).

Cultural Control and Sanitary Methods

Prophylactic measures are the only means to prevent virus infection and spread on tobacco crops, though minimizing nitrogen fertilization may reduce viral replication. Hand and tool washing with soap or milk at intervals during planting, topping and other cultural operations reduces the spread of TMV on crops. Locating seedbeds and nurseries far away from tobacco storage warehouses and eradicating weeds around these areas may also help to reduce inoculum sources and save sensitive varieties from infection.

Seed sanitation can be effective in preserving seedbeds of tomato and pepper from primary infection.

Chemical Control

Due to the variable regulations around (de-)registration of pesticides, we are for the moment not including any specific chemical control recommendations. For further information, we recommend you visit the following resources:


Impact
TMV causes heavy yield losses for tobacco, tomato and pepper worldwide (Piccirillo and Diana, 1991; Gao et al., 1994; Palloix et al., 1994; Xu et al., 1994; Sikora et al., 1998). Lower levels of loss are reported for aubergine.

Yield reductions of up to 90% have been estimated on pepper for TMV in association with other viruses (Escudero, 1996). Up to 34% losses have been produced experimentally in tomato (Giri and Mishra, 1991).

Early infection by TMV may damage young tobacco plants in both nurseries and in the field. A high percentage of plants infected at, or soon after, transplanting can reduce yield by up to 50% (Lucas, 1975). Late field attacks are not infrequent and can injure the middle and apical leaves.

'Flue cured', 'sun cured', Havana and Kentucky tobacco types are most affected, beacuse they lack the N-gene for hypersensitivity reaction. On 'flue cured', yearly losses above US$ 1 million are caused by TMV in the USA (Lucas, 1975) and heavy losses have been reported in China (Gao et al., 1994).

Burley tobacco cultivars mostly have the N-gene, with the hypersensitive reaction functioning as resistance. On sensitive burley cultivars, losses above 50% have been recorded in southern Italy (Piccirillo and Diana, 1991).

TMV infection reduces tobacco quality by modifying ratios of major chemical constituents such as nitrogen, sugar and nicotine (Patel and Patel, 1995). The sugar content of infected leaves is reduced while protein content is increased (Gao et al., 1994).
Related treatment support
Plantwise Factsheets for Farmers
Ding, S.; CABI, 2014, Chinese language
Soa Paing Oo; Zaw Lin Myo Htun; Swe Swe Min; Htay Htay Hlaing; CABI, 2016, Spanish language
Soa Paing Oo; Zaw Lin Myo Htun; Swe Swe Min; Htay Htay Hlaing; CABI, 2016, Portuguese language
Soa Paing Oo; Zaw Lin Myo Htun; Swe Swe Min; Htay Htay Hlaing; CABI, 2016, English language
 
Pest Management Decision Guides
Moses, E.; Brentu, F. C.; Nyarko, F. A.; CABI, 2016, English language
 
External factsheets
University of Illinois Extension Factsheets, University of Illinois, 1990, English language
AVRDC International Cooperators' Fact Sheets, Asian Vegetable Research and Development Center (AVRDC), 2004, English language
RHS Gardening Advice Factsheets, Royal Horticultural Society, 2011, English language
APSnet Plant Disease Lessons, APSnet, 2005, English language
Ontario CropIPM factsheets, Ontario Ministry of Agriculture, Food and Rural Affairs, Canada, 2015, English language
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