Reassortments in single-stranded DNA multipartite viruses: Confronting expectations based on molecular constraints with field observations

Abstract

Single-stranded DNA multipartite viruses, which mostly consist of members of the genus Begomovirus, family Geminiviridae, and all members of the family Nanoviridae, partly resolve the cost of genomic integrity maintenance through two remarkable capacities. They are able to systemically infect a host even when their genomic segments are not together in the same host cell, and these segments can be separately transmitted by insect vectors from host to host. These capacities potentially allow such viruses to reassort at a much larger spatial scale, since reassortants could arise from parental genotypes that do not co-infect the same cell or even the same host. To assess the limitations affecting reassortment and their implications in genome integrity maintenance, the objective of this review is to identify putative molecular constraints influencing reassorted segments throughout the infection cycle and to confront expectations based on these constraints with empirical observations. Trans-replication of the reassorted segments emerges as the major constraint, while encapsidation, viral movement, and transmission compatibilities appear more permissive. Confronting the available molecular data and the resulting predictions on reassortments to field population surveys reveals notable discrepancies, particularly a surprising rarity of interspecific natural reassortments within the Nanoviridae family. These apparent discrepancies unveil important knowledge gaps in the biology of ssDNA multipartite viruses and call for further investigation on the role of reassortment in their biology.

Keywords: Begomovirus; Geminiviridae; Nanoviridae; multipartite viruses; reassortment; ssDNA viruses.

Figure 1.

Comparison of the reassortant production processes in multipartite and segmented viruses. (1) Two viral genotypes co-infect the same cell. A reassortment results from the co-packaging of two segments, each originating from a distinct parental genotype in the case of segmented viruses and from the production of a population of particles containing complementary segments from two parental genotypes for multipartite viruses. (2) Two viral genotypes co-infect the same host. Some ssDNA multipartite viruses follow a multicellular infection cycle where functional complementation occurs at a supra-cellular level. When a host is co-infected by two parental genotypes, their distinct segments can infect separate cells and interact through complementation, which can result in the formation of a reassorted genotype. (3) Two viral genotypes infect different hosts. Reconstitution of a reassorted genome can result from the separate transmission of two particles containing complementary genomic segments originating from distinct host and parental genotypes. Triangles represent individual cells; rectangles represent host individuals. Parental and reassorted genotypes are indicated for both segmented and multipartite viruses. Distinct segments of a given genotype are colored and oriented differently.

Figure 2.

Overview of the infection cycle key steps where molecular constraints may impact segment compatibility upon reassortment of multipartite viruses. (1) This scenario illustrates a host plant co-infected by two bipartite virus genotypes (green and red) first released into the sieve element. (2) All types of viral particles can invade companion cells through plasmodesmata. (3) Decapsidation enables viral DNA to replicate within the nucleus and leads to the transcription and translation of associated proteins. (4) A reassortant is produced when, e.g. the replication protein of the green genotype can replicate the complementary segment of the red genotype, which can then be successfully encapsidated and transmitted, or vice versa. (5) Reassorted viral DNA is packaged by the CP. There, reassortment might be facilitated by the capacity of the CP to package heterologous ssDNA. (6/7/8) Viral particles leave the nucleus thanks to the intra- and intercellular MPs allowing any ssDNA segment to invade neighboring cells. (9) Virions travel long distance in the vasculature. The movement and CPs can be involved for this long-distance progression, and thus, compatibility between them may be required. (10) Insect vectors acquire viral particles while feeding on the host plant. Reassortant transmission depends on the compatibility between the vector species, the CP, and a potential transmission helper protein. Distinct segments of a given genotype are colored and oriented differently.

Figure 3.

(A) Genome organization of a bipartite begomovirus. Both genomic components DNA-A and DNA-B are represented by a DNA molecule (black circle). The colored arrows represent the identified ORFs. The corresponding proteins are indicated with the same color as the arrows. Intergenic NCRs are represented overlapping the black circles. At the top of each DNA circle, a highly conserved stem-loop structure is represented. Rep: replication-associated protein; RepA: replication-associated protein A; CR-IR: common region of DNA-A and DNA-B corresponding to the highly conserved 200-nucleotide stretch within the large intergenic region of bipartite begomoviruses. (B and C) Genome organization of the Nanoviridae family. The five genomic segments (DNA-C, DNA-M, DNA-N, DNA-R, and DNA-S) shared between nanoviruses and babuviruses are shown in (B). The four genomic components specific to nanoviruses (DNA-U1, DNA-U2, and DNA-U4) and babuviruses (DNA-U3) are shown in (C). The name of each component is indicated within the corresponding circle. Colored arrows indicate the approximate size and position of ORFs with the corresponding name of the encoded protein accordingly indicated in the same color. At the top of each circle, two CRs (CR-M and CR-SL) including a stem-loop are represented inside the NCR. Rep: replication-associated protein; Clink: cell cycle link protein; U1, U2, U3, and U4: proteins of unknown functions.