Non-replicative Integral Membrane Proteins Encoded by Plant Alpha-Like Viruses: Emergence of Diverse Orphan ORFs and Movement Protein Genes

Abstract

Fast accumulation of sequencing data on plant virus genomes and plant transcriptomes demands periodic re-evaluation of current views on the genome evolution of viruses. Here, we substantiate and further detail our previously mostly speculative model on the origin and evolution of triple gene block (TGB) encoding plant virus movement proteins TGB1, TGB2, and TGB3. Recent experimental data on functional competence of transport gene modules consisting of two proteins related to TGB1 and TGB2, as well as sequence analysis data on similarity of TGB2 and TGB3 encoded by a viral genome and virus-like RNAs identified in a plant transcriptomes, suggest that TGB evolution involved events of gene duplication and gene transfer between viruses. In addition, our analysis identified that plant RNA-seq data assembled into RNA virus-like contigs encode a significant variety of hydrophobic proteins. Functions of these orphan proteins are still obscure; however, some of them are obviously related to hydrophobic virion proteins of recently sequenced invertebrate (mostly insect) viruses, therefore supporting the current view on a common origin for many groups of plant and insect RNA-containing viruses. Moreover, these findings may suggest that the function of at least some orphan hydrophobic proteins is to provide plant viruses with the ability to infect insect hosts. In general, our observations emphasize that comparison of RNA virus sequences in a large variety of land plants and algae isolated geographically and ecologically may lead to experimental confirmation of previously purely speculative schemes of evolution of single genes, gene modules, and whole genomes.

Small hydrophobic viral proteins involved in intercellular movement of diverse plant virus genomes

“…CsVX is rather inefficiently transmitted to Nicotiana benthamiana , whereas CsNAV causes no infection of this plant host [130] . These data support our earlier hypothesis [129] , [131] , [132] that a TGB3-related gene could be an accessory, rather than essential, TGB component, which can be necessary in certain hosts species or plant tissues at least in potexviruses [133] , [134] .…”

“…TGB3 proteins form two distinct groups, potex-like and hordei-like TGBs, depending on the presence of a single (genera Potexvirus , Carlavirus , Foveavirus and Allexivirus ) or two (genera Hordeivirus , Pomovirus , Goravirus and Pecluvirus ) TMDs ( Tables S2 and S3 ). Recently, we have revealed two additional TGB classes, one of which combines TGBs of several related viruses belonging to the genus Benyvirus (see below), whereas another one is represented by the TGB of virus-like RNA assembly in the transcriptome of Colobanthus quitensis (Cq-VLRA) resembling a plant virus genome fragment encoding proteins distantly related to the respective proteins of the genus Benyvirus [131] , [132] ( Table S4 ). Like the hordei-like TGB3 proteins, the benyvirus TGB3 has two transmembrane domains; however, the benyvirus TGB3 protein differs from hordei-like proteins by the location of N-terminal transmembrane domain very close to the protein terminus and a conserved sequence signature found only in the genus Benyvirus [52] , [131] , [132] , [135] ( Table S4 ).…”

Virome Analysis of Aphid Populations That Infest the Barley Field: The Discovery of Two Novel Groups of Nege/Kita-Like Viruses and Other Novel RNA Viruses

“…The ML phylogenetic tree, based on RdRp sequences encoded by the RNA1 segments, showed that WhIV-21 is clustered with a bee pathogen, Chronic bee paralysis virus (CBPV, proposed genus "Chroparavirus"), and several invertebrate tombus-like viruses (Shi et al, 2016a;Bigot et al, 2017; Supplementary Figure S7D). Similar to CBPV, which may form a ellipsoidal virion, the WhIV-21 RNA2 segment seems to encode two proteins; a putative virion glycoprotein and SP24 homolog that probably have features of the major structural components, similar to what was previously proposed for CBPV and some negeviruses (Kuchibhatla et al, 2014;Solovyev and Morozov, 2017).…”

“…In the case of contigs BaA1_c637 (1,390 reads) and BaA1_c28720 (210 reads), an attempt to connect their sequences using RT-PCR failed, possibly because of a very low level of virus titer in the samples (data not shown). These two newly assembled contigs derived from four above-mentioned virus-like sequences have large replicase-like ORFs (ORF1) followed by two putative structural protein genes for predicted glycoprotein and membrane protein SP24 (ORFs 2 and 3) (Kuchibhatla et al, 2014;Solovyev and Morozov, 2017), except for the BaA1_c12 contig, which has an additional small ORF in its 3 -proximal region, or the BaA1_c14/63 contig, which lacks the 3 -terminal region sequence (Shi et al, 2016a; Figure 2 and Supplementary Figures S3, S4). The nucleotide sequence and encoded proteins of BaA1_c12 are almost identical (>99% nucleotide and 99-100% amino .…”

Passion Fruit Green Spot Virus Genome Harbors a New Orphan ORF and Highlights the Flexibility of the 5′-End of the RNA2 Segment Across Cileviruses

“…The shaping of current cilevirus genomes might have undergone the action of evolutionary forces biased not only by their plant hosts but also by their vectors. Horizontal gene transfer among viruses, or even between viruses and plants, has been suggested as a suitable mechanism for the acquisitions of new genes by plant virus genomes, as properly explained in the case of the binary movement block genes of the kitavirus hibiscus green spot virus 2 (Solovyev and Morozov, 2017). Moreover, blunerviruses and cileviruses encode a 30K MP displaying their best identities with those from virgavirids (Supplementary Figure S4) from which it could likely have been integrated by recombination (Quito-Avila et al, 2013).…”