Evolutionary trajectory of turnip mosaic virus populations adapting to a new host

Abstract

Little is known about how some plant viruses establish successful cross-species transmission whilst others do not; the genetic basis for adaptation is largely unknown. This study investigated the genetic changes that occurred using the progeny of an infectious clone, p35Tunos, derived from the turnip mosaic virus (TuMV) UK 1 isolate, which has a Brassica host type, but rarely infects Raphanus systemically and then only asymptomatically. The genetic trajectory leading to viral adaptation was studied in a TuMV isolate passaged in Nicotiana benthamiana (parental), Brassica rapa, the old (susceptible) host and Raphanus sativus, the new (almost insusceptible) host. Almost-complete consensus genomic sequences were obtained by RT-PCR of viral populations passaged up to 35 times together with 59 full sequences of 578 200 nt. There were significant differences in the nucleotide and encoded amino acid changes in the consensus genomes from the old and new hosts. Furthermore, a 3264 nt region corresponding to nt 3222-6485 of the UK 1 genome was cloned, and 269 clones from 23 populations were sequenced; this region covered 33 % of the genome and represented a total of 878 016 nt. The results showed that the nucleotide diversity and the non-synonymous/synonymous ratio of the populations from the new host were higher than those from the old host. An analysis of molecular variance showed significant differences among the populations from the old and new hosts. As far as is known, this is the first report comparing the evolutionary trajectory dynamics of plant virus populations in old and new hosts.

The ‘emergence’ of turnip mosaic virus was probably a ‘gene-for-quasi-gene’ event

“…In vivo and in silico studies all indicate that the P3 and CI genes of TuMV, together with the small 6K2 and VPg genes, are involved in host determination, but there is little evidence that one or a small number of unique SNP sites within those genes specify the reaction to particular hosts; none of the TuMV sites found to be pathogenicity determinants for particular B. napus cultivars [20], nor those that may have changed when TuMV emerged, were among the sites that changed non-synonymously when cloned TuMV was grown in a nearly insusceptible host [21].…”

“…Plants were inoculated, virus genomes were sequenced, and two host genes were found to interact individually, but epistatically, with the P3 and cylindrical inclusion protein (CI) genes of TuMV, each with a controlling SNP. Ohshima et al [21], recognizing the 'quasi-species' nature of TuMV, made more detailed studies of the SNPs that appeared when TuMV switched from a fully susceptible host, Brassica rapa, to a nearly insusceptible host, Raphanus sativus by obtaining both consensus and cloned sequences. They maintained several populations of TuMV in parallel, all derived from a single infectious DNA clone.…”

Nucleotide bias of DCL and AGO in plant anti-virus gene silencing

“…For example, Poaceae-infecting sobemovirus genomes display GC% > 50 because the viruses adapt to host codon usages (Zhou et al, 2005). For the Potyviridae, molecular evolution may also be affected by other factors, e.g., transmission bottlenecks , and positive selection during host adaptation (Tan et al, 2005;Ohshima et al, 2010). Therefore, similar to the strategy of PTGS suppressor Figure 5.…”

High Variability and Rapid Evolution of a Nanovirus

“…However, nothing is known about the nature of host polymerases replicating ssDNA plant viruses and the associated DNA damage repair processes. Another clear host effect is the enhancement of the overall mutation frequency that was observed, for instance, when using pepper (Capsicum annuum) as opposed to tomato (Solanum lycopersicum) or muntju (N. benthamiana) for propagation of the two alpha-like plant viruses tobacco mosaic virus and cucumber mosaic virus (64) or in turnip mosaic virus populations adapted from the susceptible host turnip (Brassica rapa) to radish (Raphanus sativus) as a new and almost insusceptible host (56).…”