How To Be a Successful Monopartite Begomovirus in a Bipartite-Dominated World: Emergence and Spread of Tomato Mottle Leaf Curl Virus in Brazil

Abstract

Worldwide, diseases of tomato caused by whitefly-transmitted geminiviruses (begomoviruses) cause substantial economic losses and a reliance on insecticides for management. Here, we describe the molecular and biological properties of tomato mottle leaf curl virus (ToMoLCV) from Brazil and establish that it is a NW monopartite begomovirus indigenous to northeastern Brazil.

Phylogeographic analysis ofBegomoviruscoat and replication-associated proteins

“…The CP phylogeny does not support a single origin for bipartitism from a monopartite ancestor, nor a single origin of monopartism from bipartitism in the Americas. There are five monopartite exemplars from the Americas in our data set with demonstrated ability to systematically infect wild host species (disregarding the highly susceptible experimental lab host Nicotiana benthamiana ) in the absence of a DNA-B segment - Corchorus yellow vein Cuba virus [32], tomato leaf curl purple vein virus [30], tomato leaf deformation virus [28, 60], tomato mottle leaf curl virus [27] and tomato twisted leaf virus [29] - and their placement on the tree indicates that their monopartite genome structure has evolved multiple times via independent loss of DNA-B.…”

“…Cell-to-cell movement is attributed mainly to V2 in monopartite viruses [34,115,124,126], with assistance of C5 for docking to the plasmodesmata [16]. Yet, the multiple examples of monopartite Americas begomoviruses lacking V2 [27][28][29][30][31][32]60] suggest that V2 is not essential for systemic movement for all begomoviruses. It is possible that other proteins may supply the movement functions of V2 in its absence, as begomovirus proteins are highly multifunctional [13,127].…”

“…Thus, movement is potentially a highly evolvable redundant function of multiple genes that may support inter-cellular movement for the no-V2 monopartite begomoviruses. Alternatively, it was proposed that phloem-limited begomoviruses may have a reduced need for protein- mediated inter-cellular movement [27, 128], although this needs experimental assessment. The phloem-limited monopartite Americas begomoviruses ToLDeV [60] and ToMoLCV [27] provide an excellent system to explore this hypothesis.…”

“…Alternatively, it was proposed that phloem-limited begomoviruses may have a reduced need for protein- mediated inter-cellular movement [27, 128], although this needs experimental assessment. The phloem-limited monopartite Americas begomoviruses ToLDeV [60] and ToMoLCV [27] provide an excellent system to explore this hypothesis. However, careful assessment of inter-cellular movement capabilities for these highly multifunctional proteins must be done on a case-by-case basis, given that (i) begomovirus positional homologs are not necessarily functional homologs [129] and (ii) many begomovirus proteins are also suppressors of RNA silencing and defective infection phenotypes may result from failure to suppress host defenses.…”

“…There is evidence that several features distinguish most begomoviruses isolated in the Americas from their AAEO region counterparts: a different number and arrangement of iterons in the CR [23,24], a conserved PWRsMaGT motif in the Nterminal domain of CP [14], an RFATDKS motif in the REn protein [25], shorter genome segments [26] and the aforementioned lack of V2/AV2. Additionally, Americas begomoviruses were thought to be exclusively bipartite until recent reports of monopartite begomoviruses in the Americas with Americas-type features [27][28][29][30][31][32]. It has been suggested that the preponderance of bipartite begomoviruses in the Americas may stem from the lack of V2/AV2 [8,14], because the V2 protein is thought to be the main mediator of inter-cellular movement during infection for monopartite viruses [16,33,34] -although this remains controversial [35].…”