SUMMARY

Higher plants are commonly subjected to multiple virus infections. In some cases, infection with one virus protects the plant from subsequent infection with a closely related virus, a phenomenon known as cross protection. It is possible to confer this kind of protection by engineering the plant to express an individual viral gene and this fact has been exploited to produce transgenic plants resistant to a variety of agronomically important diseases. However, the mechanism(s) by which expression of virally encoded genes mediate protection are not well understood and, in the absence of a comprehensive understanding of the phenomenon, the question of the safety of engineered cross protection has been raised. One potential risk in the use of such plants involves another class of viral interactions which also occurs very commonly in plants, viral synergism. In synergistic viral interactions, coinfection with two independent unrelated viruses results in a much more serious disease than either virus induces in a single infection. As with the cross protection type of interaction, it has been shown that at least one such synergistic disease is mediated by expression of a subset of the genome of one of the interacting viruses in transgenic plants. Thus, it is possible that viral genes expressed in transgenic plants for the purpose of protecting the plant could actually confer sensitivity to a synergistic disease. Due to the deficiency of basic background information about viral synergism, the actual risk of accidentally inducing one disease in engineered plants while protecting them from another is unknown.

Plant viral synergisms may be divided into two major classes: the potyvirus-associated synergisms, in which one of the synergistic pair of viruses is a member of the potyvirus group of plant viruses, and the much less well characterized non-potyvirus synergisms, in which neither virus is a member of this group. In potyvirus associated synergisms, the non-potyvirus virus of the pair may be any of a broad range of unrelated viruses, including pararetroviruses such as cauliflower mosaic virus (Khan and Demski, 1982) and RNA viruses of both the alphavirus supergroup [for example potato virus X (PVX), Rochow and Ross, 1955] and the picornavirus supergroup (for example cowpea mosaic virus, Anjos et al., 1992). Several such potyvirus-associated synergistic diseases have been examined in some detail, and in each, a dramatic increase in host symptoms is observed in doubly infected plants compared to singly infected plants. The increase in symptoms is correlated with an increase in the accumulation of the non-potyvirus of the synergistic pair, but there is no corresponding increase or decrease in the level of the potyvirus (Calvert and Ghabrial, 1983; Goldberg and Brakke, 1987; Rochow and Ross, 1955; Vance, 1991).

The best studied of the potyvirus -associated synergisms is the interaction of PVX with a number of viruses in the potyvirus group, including potato virus Y (PVY), tobacco vein mottling virus (TVMV) and tobacco etch virus (TEV). The PVX/potyviral interaction in tobacco results not only in the increase in host symptoms and PVX virus mentioned above, but also in a disproportionately large increase in the level of PVX (-) strand RNA (Vance, 1991). PVX/potyviral synergism does not require a co-infecting potyvirus, and synergistic disease is mimicked in transgenic plants expressing the 5' proximal region of the potyviral genome and infected singly with PVX (Vance et al., 1995). The region of the potyviral genome that mediates synergism encodes a polyprotein comprising the first two mature potyviral gene products, P1 and helper component-proteinase (HC-Pro), and a small portion of the third (P3). Both HC-Pro and P1 are multifunctional proteins. P1 has proteinase activity that cleaves the potyviral polyprotein, creating the carboxy-terminus of P1 and the amino-terminus of HC-Pro (Verchot et al., 1991). P1 also functions in trans as an accessory factor for genome replication (Verchot and Carrington, 1995) and has RNA binding activity (Brantley and Hunt, 1993). HC-Pro has at least three functional domains: an amino-terminal domain required for aphid transmission, a central domain involved in pathogenicity, RNA replication and leaf to leaf movement of the virus through the phloem, and a carboxy-terminal domain required for autoproteolytic processing of the HC-Pro carboxy-terminus (see Maia et al., 1996, for a recent review). The fact that this region of the potyviral genome mediates the PVX/potyvirus synergistic disease raises the possibility that many or all potyvirus-associated synergisms might be mediated by this same sequence.

A number of viral synergisms which do not involve a member of the potyvirus group have been reported (Blood, 1928; Garces-Orejuela and Pound, 1957; Khan and Demski, 1982; Rochow and Ross, 1954); however, in contrast to the potyvirus-associated synergisms, none of these non-potyviral synergisms has been well characterized at the molecular level. Probably the best studied of the non-potyviral synergisms is the interaction of tobacco mosaic virus (TMV) and PVX, which causes a synergistic disease in tomatoes called double virus streak (Blood, 1928). This synergistic interaction has been reported to result in an increase in the level of PVX in the doubly infected plants (Rochow and Ross, 1955). One possibility is that the non-potyvirus synergisms are mediated by expression of a subset of one viral genome, in a manner similar to that shown for the PVX/potyviral synergism.

The extent to which synergistic viral interactions occur in higher plants and the role they play in mediating plant disease is not really clear at this point. Although many such interactions are known and more are reported each year, most are completely unstudied. Thus basic research into the mechanism of plant viral synergism and the extent to which such interactions impact plants in nature and in the field is warranted, and should include model viral systems for both potyvirus-associated and non-potyvirus synergisms.

REFERENCES

Anjos, J. R., Jarlfors, U. And Ghabral, S. A. (1992) Soybean mosaic potyvirus enhances the titer of two comoviruses in dually infected soybean plants. Phytopathology 82, 17-23.

Blood, H.L. (1928). A "streak" of tomatoes produced by a disturbing principle from apparently healthy potatoes in combination with tomato mosaic virus. Phytopathology 18, 311.

Brantley, J. D. and Hunt, A. G. (1993). The N-terminal protein of the polyprotein encoded by the potyvirus tobacco vein mottling virus is an RNA-binding protein. J. Gen. Virol. 74, 1157-1162.

Calvert, L.A. and Ghabrial (1983) Enhancement by soybean mosaic virus of bean pod mottle virus titer in doubly infected soybean. Phytopathology 73, 992-997.

Garces-Orejuela, C. and Pound, G.S. (1957). The multiplication of tobacco mosaic virus in the presence of cucumber mosaic virus or tobacco ringspot virus in tobacco. Phytopathology 47, 232-239.

Goldberg, K-B. And Brakke, M.K. (1987) Concentration of maize chlorotic mottle virus increased in mixed infections with maize dwarf mosaic virus, strain B. Phytopathology 77, 162-167.

Khan, M.A. and Demski, J.W. (1982). Identification of turnip mosaic and cauliflower mosaic viruses naturally infecting collards. Plant Disease 66, 253-256.

Maia, I.G., Haenni, A-L. and Bernardi, F. (1996). Potyviral HC-Pro: a multifunctional protein. J. Gen. Virol. 77, 1335-1341.

Rochow, W.F. and Ross, A.F. (1954) Phytopath. 44, 504.

Rochow, W.F. and Ross, F. (1955). Virus multiplication in plants doubly infected by potato viruses X and Y. Virology 1, 10-27.

Vance, V.B. (1991). Replication of potato virus X RNA is altered in coinfections with potato virus Y. Virology 182, 486-494.

Vance, V.B., Berger, P.H., Carrington, J.C., Hunt, A. G. and Shi, X.M. (1995). 5' proximal potyviral sequences mediate potato virus X/potyviral synergistic disease in transgenic tobacco. Virology 206, 583-590.

Verchot, J., and Carrington, J.C. (1995). Evidence that the potyvirus P1 proteinase functions in trans as an accessory factor for genome amplification. J. Virol. 69, 3668-3674.

Verchot, J., Koonin, E.V. and Carrington, J.C. (1991). The 35-kDa protein from the N-terminus of the potyviral polyprotein functions as a third virus-encoded proteinase. Virology 185, 527-535.