Cucumber mosaic virus Is Unable to Self-Assemble in Tobacco Plants When Transmitted by Seed

Cucumber mosaic virus (CMV), which has great impact on agronomic production worldwide, is both aphid and seed transmitted. Although the mechanisms of aphid transmission have been widely studied, those underlying the ability of CMV to survive and remain infectious during the passage from one generation to the next through the seeds are still to be clarified. Moreover, the viral determinants of seed transmission rate are poorly understood. Three viral genotypes produced from same RNA 1 and 2 components of CMV-Fny but differing in RNA 3 (the wild type CMV-Fny, a pseudorecombinant CMV-Fny/CMV-S and a chimeric CMV previously obtained by our group, named F, FS and CS, respectively) were propagated in Nicotiana tabacum cv Xanthi plants in order to assess differences in tobacco seed transmission rate and persistence through plant generations in the absence of aphid transmission. Seed-growth tests revealed CMV infection in the embryos, but not in the integuments. Seedlings from seed-growth tests showed the presence of all considered viruses but at different rates: from 4% (F, FS) to 16% (CS). Electron microscopy revealed absence (CS) of viral particles or virions without the typical central hole (F and FS). In agreement, structural characteristics of purified CMV particles, assessed by circular dichroism spectroscopy, showed anomalous spectra of nucleic acids rather than the expected nucleoproteins. These alterations resulted in no seed transmission beyond the first plant generation. Altogether, the results show for the first time that correct virion assembly is needed for seed infection from the mother plant but not to seedling invasion from the seed. We propose that incorrect virion formation, self-assembly and architecture stability might be explained if during the first stages of germination and seedling development some tobacco seed factors target viral regions responsible for protein-RNA interactions.