RESISTANCE TO VIRUS MOVEMENT WITHIN AND BETWEEN PLANT CELLS

Once viral multiplication has been established in the cytoplasm and/or nucleus of a single plant cell from a susceptible host, plant viruses must move from the initially infected cells to adjoining cells, eventually resulting in systemic infection. An important class of host response to viral infection is apparent when the virus appears to establish infection in one or a few cells, but cannot move beyond the initial focus of infection. Resistance at this level can result from either failure of interactions between plant and viral factors necessary for cell-to-cell movement, or from active host defense responses that rapidly limit virus spread. As described above for viral replication and translation, intra- and intercellular viral movement also requires both virus-encoded components and specific host factors. For some viral families, mainly viruses with DNA genomes, crossing the nuclear membrane represents a potential barrier for virus movement. For these viruses, it is necessary to import the viral genome to the nucleus for replication and export progeny genomes back to the cytoplasm for translation and virion assembly.

The viral proteins required for these functions are known, at least for some viruses. For example, the nuclear import and export of bipartite geminivirus DNA is mediated by the BV1 (BR1) protein, but interference with these processes by host factors resulting in resistance has not yet been reported. With respect to intercellular movement, it is well established that movement proteins (MP), identified for most families of both DNA and RNA plant viruses, perform dedicated functions required for cell-to-cell movement by modifying pre-existing pathways in the plant for macromolecular movement such that viral material can translocate between plant cells  In the case of potyviruses, which do not encode a dedicated MP, the movement functions have been allocated to several proteins, including CP, HC-Pro, the cylindrical inclusion (CI) protein, and the genome-linked protein (VPg). In mutant viruses defective in these proteins, movement from the initially infected cell to adjacent noninfected cells did not occur.

A number of mutations in host genes are known that prevent cell-to-cell movement of plant viruses. The Arabidopsis cum1 and cum2 mutations inhibit CMV movement. In protoplasts prepared from plants homozygous for these alleles, CMV RNA and CP accumulate to wild-type levels, but the accumulation of the CMV 3a protein, necessary for cell-to-cell movement of the virus, is strongly reduced. Positional cloning demonstrated that CUM1 and CUM2 encode eukaryotic translation initiation factors 4E and 4G, respectively. Similar results for members of a different viral family have been obtained from tobacco, pepper, and pea.

In tobacco, the movement of Tobacco vein mottling virus and PVY is controlled by the recessive gene va. In pepper and pea, pvr11 (formerly pvr21) and sbm1 were identified as mutations at a locus encoding eIF4E. A functional analysis of the product of the dominant allele suggested a function for eIF4E in cell-to-cell movement, in addition to its proposed role in viral RNA replication or translation. The HR also serves to disrupt cell-to-cell movement of plant viruses. Recognition of the viral elicitor results in the induction of a cascade of host defense responses that include oxidative H2O2 bursts and up-regulation of hydrolytic enzymes, PR proteins, and callose and lignin biosynthesis. As a consequence, viral movement may be limited to a small number of cells, illustrated by such classic examples as the tobacco N gene and the tomato Tm-2 and Tm-22 alleles. Protoplasts isolated from the plants carrying these R genes allowed replication of TMV; no cell death was observed. Despite the strong correlation of HR and disease resistance, necrotic cell death is now thought to be an ancillary consequence of the resistant response, not necessary for pathogen suppression. For example, in Phaseolus vulgaris carrying the I allele to BCMV, a continuum of viral infection phenotype responses that range from no necrosis to a lethal systemic response can be manipulated by allele dosage and temperature. The defense no death (dnd1) mutant in Arabidopsis is another example of independent resistance and HR, consistent with results from several viral-host systems including Sw-5-mediated resistance against Tomato spotted wilt virus, Rsv-1-mediated virus resistance to SMV in soybean, and resistance against Cauliflower mosaic virus in tobacco. Furthermore, when HRT was introgressed into Col-1, most of the HRT-transformed plants developed HR upon TCV infection, yet the virus spread systemically without systemic necrosis.