DNA Satellites Impact Begomovirus Diseases in a Virus-Specific Manner

Abstract

Begomoviruses infect many crops and weeds globally, especially in the tropical and subtropical regions, where there are waves of epidemics. These begomovirus epidemics are frequently associated with three DNA satellites: betasatellites, alphasatellites, and deltasatellites. Except for the origin of replication, these satellites show no sequence identity with the helper begomovirus. Alphasatellites and betasatellites encode the α-Rep and βC1 proteins, respectively, while deltasatellites encode no proteins. α-Rep, which functions like the Rep of the helper begomoviruses, ensures alphasatellite replication autonomy, while betasatellites and deltasatellites depend wholly on the helper virus for replication. The betasatellite βC1 protein is a pathogenicity determinant and suppressor of RNA silencing. The associations between satellites and helper viruses vary, depending on the virus and the host, and the roles of these satellites in disease development are an active area of investigation. This review highlights current information on the role of DNA satellites in begomovirus diseases and examines commonalities and differences between and within these satellites under prevailing conditions. Furthermore, two episomes, SEGS-1 and SEGS-2, associated with cassava mosaic geminiviruses, and their possible status as DNA satellites are discussed. DNA satellites are a major factor in begomovirus infections, which are a major constraint to crop production, especially in tropical and subtropical regions. Thus, areas for future research efforts, as well as implications in the biotechnological management of these viruses, are discussed in this review.

Keywords: alphasatellites; begomoviruses; betasatellites; deltasatellites.

Figure 1

Genome organization of bipartite and monopartite begomovirus genomes. (A) Bipartite begomovirus sida golden yellow vein virus (SiGYVV) DNA-A and DNA-B genome components and (B) monopartite begomovirus sweet potato leaf curl virus (SPLCV). Canonical viral proteins are represented by curved arrows and include coat protein (CP), replication-associated proteins (Reps), transcriptional activator protein (TrAP), replication enhancer protein (REn), C4, movement protein (MP), and nuclear shuttle protein (NSP).

Figure 2

Representative genomes of begomovirus DNA satellites discussed in this review. (A) Cotton leaf curl Multan betasatellite (CLCuMuB), (B) cotton leaf curl Multan alphasatellite (CLCuMuA), (C) New World deltasatellite (NW Deltasatellite), (D) sweet potato leaf curl deltasatellite (SPLCV-SPLCD1), and (E) tomato leaf curl deltasatellite (ToLCD). Betasatellite encodes βC1, which is a pathogenicity determinant, while alphasatellites encode the α-Rep protein for autonomous DNA replication. The hairpin structures shown harbor the DNA replication origin (a), and CLCuMuA, ToLCD, and NW deltasatellites show other predicted hairpins identified as (b), (c), and (d). The confidence levels of these structures were predicted using the SnapGene software 8.1 (GLS Biotech, San Diego, CA, USA).

Figure 3

Proteins encoded by betasatellites and alphasatellites show variation. (A) βC1 sequence variation throughout the protein sequence, except for the PFDFN motif (red box); (B) there is considerable sequence variation between New World and Old World α-Reps, especially at the N- and C-termini. Conserved amino acid residues are highlighted yellow.

Figure 4

Asystasia yellow mosaic alphasatellite (AYMA) causes intense yellowing symptoms in Asystasia gangetica in the presence of West African asystasia virus (WAAV).

Figure 5

Phylogenetic tree generated using maximum-likelihood method from alignment of α-Reps. α-Reps of GDarSLA and GMusSLA that suppress PTGS group together in a phylogenetic tree.

Figure 6

Representation of cassava mosaic geminivirus episomes. (A) SEGS-1 sequence has identity with the cassava protein prefoldin subunit 6 (PFDN6). (B) SEGS-2 shows sequence identity with the cassava pentatricopeptide repeat (PPR) family, as well as a potential protein of 68 amino acids that maps to the N-terminal first 68-amino acid segment of the pre-mRNA-splicing factor ATP-dependent RNA helicase DEAH1 isoform X2 (DHX16 isoform X2). Like SEGS-1, SEGS-2 has a CpG island, as well as two predicted stem–loop structures. Episome stem-loops are represented by a and b. The confidence levels of these structures were predicted using the SnapGene software 8.1 (GLS Biotech, San Diego, CA, USA).

Figure 7

Sequence alignment of SEGS-2, PPR; DHX16 isoform X2 shows specific DNA fragment that became part of SEGS-2 molecule. Conserved nucleotides are highlighted yellow.

Figure 8

SEGS episomes cause severe symptoms when mixed-infected with cassava mosaic geminiviruses. CMG-resistant cassava showing (A) ACMV-free plant, (B) plant infected by ACMV alone, and (C) plant mixed-infected by episomes and ACMV displays leaves that are reduced to the midrib with a total absence of the leaf blade.