Limitations on Geminivirus Genome Size Imposed by Plasmodesmata and Virus-Encoded Movement Protein: Insights into DNA Trafficking

Abstract

Animals and plants evolved systems to permit non-cell-autonomous trafficking of RNA, whereas DNA plays a cell-autonomous role. In plants, plasmodesmata serve as the conduit for this phenomenon, and viruses have evolved to use this pathway for the spread of infectious nucleic acids. In this study, a plant DNA virus was used to explore the constraints imposed on the movement of DNA through this endogenous RNA trafficking pathway. The combined properties of the geminivirusencoded movement protein and plasmodesmata were shown to impose a strict limitation on the size of the viral genome at the level of cell-to-cell movement. Size-increased viral genome components underwent homologous and nonhomologous recombination to overcome this strict limitation. Our results provide insights into the genetic mechanisms that underlie viral evolution and provide a likely explanation for why relatively few types of plant DNA viruses have evolved: they would have had to overcome the constraints imposed by an endogenous system operating to ensure that DNA acts in a cell-autonomous manner.

Replication promiscuity of DNA-β satellites associated with monopartite begomoviruses; deletion mutagenesis of the Ageratum yellow vein virus DNA-β satellite localizes sequences involved in replication

“…In contrast, deletion of this region in AYVV DNA-b (mutant D3) did not affect the phenotype, at least in N. benthamiana, although the phenotype of this deletion mutant remains to be investigated in the natural host of the disease complex, A. conyzoides. Large deletions within non-essential regions of the begomovirus genome are not tolerated and the deletion mutants revert to wildtype size by both intra-and intermolecular recombination during systemic movement (Etessami et al, 1989;Gilbertson et al, 2003). In contrast, removal of 361 nt of DNA-b in mutant D2, representing 27 % of the satellite, was tolerated, although it remains to be seen if multiple passages of the mutant progeny result in reversion to wildtype size.…”

Caulimoviridae Tubule-Guided Transport Is Dictated by Movement Protein Properties

“…It is tempting to speculate that, in CaMV, this structure could have evolved to prevent NPC formation and thus mediate only encapsidated virus transport, thus avoiding direct access of the CaMV DNA genome to the plant cell-to-cell trafficking pathway specialized for RNA molecule traffic. With the same aim, geminivirus, moving as an NPC, evolved to have DNA genome molecules small enough to be restrictively selected by MP and elude detection by the RNA recognition system of the PD pathway (3,4,9). A very restrictive evolution of geminivirus MP could explain the inability of MYMV MP to mediate AMV movement with and without the addition of RBDs (data not shown).…”

Agroinfection of tobacco by croton yellow vein mosaic virus and designing of a replicon vector for expression of foreign gene in plant

“…Efforts to develop geminiviral replicons for gene expression vector began long back, but the genome size constraints have hindered the use of full viruses for heterologous protein expression. Virus genome size constraints are imposed by cell-to-cell movement through plasmodesmata and not by replication [6]. Therefore, virus genes involved in encapsidation and cell-to-cell movement can be deleted to increase the cargo capacity for large heterologous sequences.…”