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potato interveinal mosaic

Potato virus X

Distribution

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Host plants / species affected

Main hosts

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Capsicum annuum (bell pepper)
Capsicum frutescens (chilli)
Nicotiana tabacum (tobacco)
Solanum lycopersicum (tomato)
Solanum tuberosum (potato)

List of symptoms / signs

Leaves - abnormal patterns

Symptoms

Many strains of PVX induce only inconspicuous interveinal chlorosis in some leaves of most potato cultivars and almost symptomless infection in those of others. Other strains cause severe mosaic and leaf crinkling, or acute tip necrosis usually followed by plant death as in cultivars King Edward, Arran Crest and Epicure. Symptom development, however, is dependent upon the interaction of cultivar, virus strain and environmental conditions. Thus, although symptoms develop at 16-22°C they are often masked at higher ambient temperatures. In tomato, PVX causes mosaic leaf mottling with occasional necrotic rings and necrosis. In tobacco the virus induces faint leaf mottling to severe chlorotic ringspots.

Diseases in potato and tomato are especially severe when PVX is present together with other viruses. Thus, in potato with potato A potyvirus or potato Y potyvirus it causes crinkle or rugose mosaic, respectively (Smith, 1931; Murphy and McKay, 1932); the presence of PVX is associated with a significant increase in the replication of potato Y potyvirus (Stouffer and Ross,1961). In tomato, PVX and tomato mosaic tobamovirus cause tomato double virus streak (Vanterpool, 1926; Uschdraweit, 1952; Smith, 1957; Linnasalmi, 1964; Parent et al., 1985).

Prevention and control

Resistant Cultivars

The most effective method of protecting potato crops is the use of potato cultivars containing major genes for resistance; such cultivars have been grown for many years and resistance has been durable. The cultivar Prestile is reported to be immune to PVX (Reeves et al., 1994).

Some strain-specific genes, including those designated Nx and Nb, result in hypersensitivity when plants are exposed to infection (Cockerham, 1955). Two other genes, Rxadg and Rxacl, confer extreme resistance to all four groups of strains (Cockerham, 1970). The Nb and Rx2 genes are now known to be located on chromosome 5 (Jong et al., 1997). One strain (designated PVX/HB) is able to overcome all known genes for resistance, but is mostly restricted to South America (Moreira et al., 1980). Resistance to PVX-HB has been found in Solanum sucrense (Querci et al., 1995).

Within the last decade, virus resistant plants have been produced by genetic engineering techniques and an understanding of resistant mechanisms obtained (Angell and Baulcombe, 1997; English et al., 1997); although not yet used commercially, the resistance of such plants has proved durable and so has great future potential (Jongedijk et al., 1992). After infection, transgenic potato (cultivars Bintje and Escort) and tobacco plants expressing the virus coat protein gene develop symptoms much more slowly and significantly suppress virus replication (Hemenway et al., 1988; Hoekema et al., 1989). Such plants are resistant to both virus particles and viral RNA. Similarly, transgenic plants containing the viral replicase gene are also resistant to PVX (Braun and Hemenway, 1992; Davenport and Baulcombe, 1997).

PVX-resistant potato and tomato cultivars have also been produced by conventional breeding techniques (Rashid et al., 1989), and sources of genetic resistance for peppers identified (Edwardson and Christie, 1997).

Cultural Practices

The most appropriate and effective method of control in potato crops is to use virus-free planting stock of virus-resistant and/or tolerant cultivars and, during cropping, to inspect crops and remove any plants shown to be or suspected of being infected. Well established methods (meristem tip culture combined with thermotherapy and/or chemotherapy) are available for the production of virus-free plants of cultivars that have become totally infected. Schemes for the use of such elite stocks, described fully by van der Zaag (1987) and Salazar (1996), are now in operation in many countries.

Impact

Introduction

PVX has a wide natural host range, occurring in at least 62 plant species of 27 families (Edwardson and Christie, 1997). The virus is especially important worldwide in potato (Bode, 1968; Beemster and de Bokx, 1987) and in many countries in a few major solanaceous crops including peppers (Paulus et al., 1960; Steepy et al., 1967; Fribourg and Fernandez-Northcote, 1972; Makkouk and Gumpf, 1974), tobacco (Hansen, 1946; Bode, 1953; Bode and Klinkowski, 1968), and tomato (Vanterpool, 1926; Ainsworth, 1934). Although many of its natural hosts are weeds, PVX also occurs naturally in other crop species including winter cherry (Nicandra physalodes) and turnip (Brassica rapa) in India (Sangar et al., 1980; Samad et al., 1991), artichoke (Cynara scolymus) and grapevine (Vitis vinifera) in Italy (Chabbouh et al., 1990; Giunchedi, 1973), and red clover (Trifolium pratense) in Belarus (Ambrosov and Bltoskaya, 1978)

Potato

Earlier reports of the effects of PVX on the growth and yield of infected potatoes are inconsistent, probably due to infection by virus strains of different virulence, the use of cultivars differing in tolerance and/or resistance, the occurrence of unsuspected virus mixtures, different environmental conditions (especially soil fertility and fertilizer treatments), date of harvest and the earlier lack of comparable virus-free plants necessary for critical comparative tests.

As most strains of PVX induce only inconspicuous or symptomless infections in many potato cultivars, mild strains were earlier thought to be of little economic importance (Bald, 1944; Clinch and McKay, 1947). For example, no statistically significant yield reductions were recorded in cvs Up-to-Date, Arran Banner, Majestic or President in Eire (Clinch and McKay, 1947: McKay and Loughnane, 1953), cvs Kennebec and Katahdin in Maine, USA (Murphy et al., 1966), and in cv. Sebago in Ontario (Rowberry and Johnston, 1975) and cv Netted Gem (syn. Russet Burbank) in British Columbia, Canada (Wright, 1970). By contrast, commonly-occurring isolates of the virus have been reported to reduce tuber yields of many potato cultivars by 2-23% (Emilsson and Gustafsson, 1956; Sung, 1967; Bode, 1968; Mellor and Stace-Smith, 1977; Beemster and de Bokx, 1987). Thus, tuber yield losses of 2-7% have been recorded in cvs Alpha and Up-to-Date, of 7-9% in cv Bintje in Denmark (Hansen, 1963), and of 5-20% in several cultivars in Australia (Norris, 1953). Yield reductions of 12% have been recorded in cv Up-to-Date in Australia (Bald, 1943) and cv Russet Burbank (from 40.6 to 35.7 t/ha) in British Columbia, Canada (Wright, 1977) and, in the USA, of 7.3% in cv Mohawk, 11.2% in cv Kennebec, 13.7% in cv Chippewa, 14.9% in cv Katahdin, 16% in cv Sebago, and 18.3% in cv Teton in Maine (Bonde and Merriman, 1951), 17.5% in cv Sebago (Lim et al., 1966), 21.9% in cv Red Pontiac (Hoyman, 1964), and 9-32 % depending on year (Davies and Allen, 1984) or 23% (from 353 to 272 cwt/acre) in cv Russet Burbank in Idaho (Ohms et al., 1977). It has been estimated that from 1931-1951 PVX caused an annual yield loss in the USA of 13% (110,000 bushels), a reduction two times greater than the combined effects of late blight and Rhizoctonia (Chester, 1955).

More virulent strains can reduce yields of intolerant cultivars by up to 50% (Broadbent et al., 1962; Romanova and Reifman, 1978; Beemster and de Bokx, 1987). In England, PVX caused an average annual yield loss of three cultivars over three years of 30% (from 2.25 to 0.72 lb/plant). Similarly, a virulent strain in the USSR caused a yield reduction of 43% in the fourth year of production (Romanova and Reifman, 1978). Such yield losses usually result from the production of smaller tubers (Broadbent et al., 1962; Sung, 1967; Manzer 1978, 1979; Davies and Allen, 1984).

In addition to reducing yield, PVX also reduces the dry matter content of tubers which is especially important in the potato processing industry (Emilsson and Gustafsson, 1956; Hansen, 1974); in Denmark, PVX-infected cv Dianella yielded 12.3 t dry matter/ha, 3% less than virus-free stock (Hansen, 1974). PVX also reduces the number and weight of microtubers produced in vitro by infected plants derived from meristem tip culture (El-Fiki et al., 1992).

PVX can also have differential effects on plants infected during the current growing season (primary infection) and those grown from infected seed potatoes (secondary infection). Thus, although a mild strain had no effect on marketable yield (i.e. of tubers >3.5 cm in diameter) of primarily infected cv Kerr's Pink in Eire (Dowley, 1973), secondary infection resulted in a yield reduction of 5.7% (from 47,910 to 45,170 kg/ha).

Environmental conditions can also greatly affect the growth of infected potato plants. Thus, in a comparison of virus free plants and those infected with a mild strain of PVX, a significant yield loss was recorded at only one of three experimental sites (Richmond) in New York State, USA (Teri et al., 1977): mean annual yields of cvs Hudson, Katahdin and Bake King over three years were reduced by 8.5%, i.e. from 44.39 to 40.64 lb/plot (20 ft single row). In Armenia, PVX-induced crop losses were 8.2 and 11.3% from crops grown in unfavourable or favourable production areas, respectively (Sgoyan, 1974). Similar results have been reported from the former USSR (Bobryshev et al., 1972).

Fertiliser applications also affected the comparative yields of healthy and infected cv Russet Burbank plants in Idaho (Ohms et al., 1977); thus, virus-free plants outyielded infected plants by 70, 78, 81 and 95 cwt/ha after applications of 0, 80, 160 and 240 lb/acre of nitrogen, respectively.

Yield loss of potato tubers is also correlated with the incidence of infection in a crop; thus, infection levels of 10, 50 and 100% of cv Bintje by a mild PVX strain in the Netherlands resulted in reduced yields of ca 1, 4 and 10%, respectively (Beukema and van der Zaag, 1979). In Idaho, infection levels of 36 and 88% in cv Russet Burbank resulted in yield losses of 21 and 36%, repectively (Davis and Allen, 1984).

There are conflicting reports on the effects of virus infection on the susceptibility of potatoes to fungal pathogens. PVX-infected potatoes were reported to be less susceptible to Phytophthora infestans (Muller and Munro, 1951) and Fusarium roseum in the USA (Jones and Mullin, 1974; Mullen and Bateman, 1975; Manzer et al., 1978), but to be more susceptible to Rhizoctonia solani in eastern Europe (Komkov, 1975). It has also been reported that PVX-infection may increase the susceptibility of some cultivars to blight (Pietkiewicz, 1974; Dowley, 1973); however, the increased susceptibility reported by Dowley (1973) occurred in tubers harvested from primary-infected, but not secondary-infected, plants.

PVX is of much greater importance when it occurs together with other viruses, especially potato virus Y (PVY), potato virus A (PVA) or potato virus S (PVS). It has long been known that PVX and PVA in combination, but neither alone, cause the so-called crinkle disease of potato in North America and Europe. Plants containing both viruses are severely stunted and bushy with puckered, brittle and diffusely chlorotic leaves; some affected plants may die (Murphy, 1921; Murphy and McKay, 1932; Clinch and Loughnane, 1933; Bode, 1968). In Italy, the presence of both viruses caused a yield reduction in cv San Michele of 40%, from 1.042 to 0.633 kg/plant (Gregorini and Lorenzi, 1974).

PVX and PVYo together cause the unusually severe rugose mosaic disease of potato which, although originally described in the USA, also occurs in S. America, Europe and elsewhere (Smith, 1931; Bode, 1968; Guerrero-Guerrero and Martinez-Lopez, 1980). Mature leaves of infected plants have black necrotic veins and younger leaves are mottled; such plants are often dwarfed, produce smaller tubers and, if severely affected (for example, cv Green Mountain) often die prematurely (Brentzel, 1935). In such mixed infections, PVYo induces a tenfold increase in the concentration of PVX in potato and tobacco plants (Rochow and Ross, 1955; Ross, 1957). Yield losses resulting from infection by PVY alone and with PVX were 57 and 71%, respectively (Corsini et al., 1983).

Yield losses induced by PVS are increased when PVX also occurs in infected plants. Thus the tuber yield of cv Russet Burbank plants infected by PVS alone in Maine, USA was reduced by 3.8%, but by 6.2% and 6.8% when co-infected with a mild and a moderately severe strain of PVX, respectively (Manzer et al., 1978); yield losses in cv Kennebec were 4% (PVS alone), and 3.9% (PVS plus mild PVX) and 8.1% (PVS plus moderate PVX) and in cv Katahdin were 1% (PVS alone), 4.2% (PVS plus mild PVX) and 9% (PVS plus moderate PVX).

Average tuber yields (kg/plot*) over 3 years of 3 potato cultivars infected with PVS and PVX

Russet Kennebec Katahdin
Burbank

Virus-free 23.18 27.86 24.00
PVS 22.28 (3.8%)** 26.74 (4.0%) 23.75 (1.0%)
PVS + mild PVX 21.73 (6.2%) 26.78 (3.9%) 22.98 (4.2%)
PVS + 21.59 (6.8%) 25.59 (8.1%) 21.84 (9.0%)
moderate PVX

* Each plot was a single row of 6.1 m
** Yield loss (%) compared with virus-free plants.

In Bulgaria, PVS alone reduced the yield of cv Saskia by 4.3% whereas infection by both PVS and PVX caused a loss of 22.3% (Asenov, 1986). In the USA, PVS alone reduced the yield of cv Sebago by 6% whereas together with PVX the loss was 15% (Lim et al., 1966).

The length of the growing season can also influence the effect that infection has on yield (Manzer et al., 1979). Thus, late harvested, but not early harvested, virus-free plants of cv Kennebec in Maine, USA outyielded those infected with PVS and a mild strain of PVX by 5.9% (from 26.25 to 24.70 kg/plot of 6.1 m single row; mean yields over three years). Although the yield of the virus-free plants was higher, those infected with both viruses produced more but smaller tubers (i.e. a yearly average over three years of 144 and 136 tubers from infected and healthy plants, respectively.

Peppers (Capsicum annuum and C. pendulum)

In C. annuum in the USA, PVX causes mottling and severe necrosis of leaves and stems and, eventually, defoliation of some cultivars including cvs Yolo Wonder and Trueheart Perfection (Paulus et al., 1960; Steepy et al., 1967; Makkouk and Gumpf 1974). PVX and Potato virus Y together are the cause of severe systemic leaf chlorosis and deformation of C. pendulum plants in Peru (Fribourg and and Fernandez-Northcote, 1972). Although the effects of virus infection on the growth and yield of peppers has not been determined, its severe effects on infected plants indicate that it would cause significant yield reductions.

Tobacco

PVX causes severe leaf mottling and/or necrotic spotting in naturally infected tobacco plants, but the effect of infection on yield and quality has not been reported (Hansen, 1946; Bode, 1953; Bode and Klinkowski, 1968).

Tomato

PVX alone causes leaf mosaic and slight stunting in naturally infected glasshouse-grown tomato plants in the UK, Germany, Crete and elsewhere (Ainsworth, 1934; Klinkowski and Uschdraweit, 1968; Avgelis, 1986). A severe necrotic disease, designated tomato double virus streak, has long been known to be induced in tomato plants infected with both PVX and tomato mosaic virus (Berkeley, 1926; Vanterpool, 1926; Clinch, 1941; Uschdraweit, 1952; Valleau and Johnson, 1957; Brcak, 1961, 1979; Linnasalmi, 1964). Fruits are deformed and have irregularly shaped lesions which, although initially raised, are later sunken (Clinch, 1941); such affected fruits are unmarketable. Tomato double virus streak disease is still occasionally a problem where adjacent field crops of potatoes and tomatoes are grown (Parent et al., 1985).

In Poland, tomato plants infected with both viruses after the formation of fruits suffered a yield loss of 50% (Blaszczak and Weber, 1973). PVY and PVX together cause more severe symptoms than either alone in tomato plants; PVY alone induces leaf chlorosis, the severity of which is dependent on the virulence of the virus strain, but symptom severity is greater in plants co-infected with PVX (Klinkowski and Uschdraweit, 1968; Brcak, 1979).