Maintenance of an Old World Betasatellite by a New World Helper Begomovirus and Possible Rapid Adaptation of the Betasatellite

Abstract

Begomoviruses (family Geminiviridae) cause major losses to crops throughout the tropical regions of the world. Begomoviruses originating from the New World (NW) and the Old World (OW) are genetically distinct. Whereas the majority of OW begomoviruses have monopartite genomes and whereas most of these associate with a class of symptom-modulating satellites (known as betasatellites), the genomes of NW begomoviruses are exclusively bipartite and do not associate with satellites. Here, we show for the first time that a betasatellite (cotton leaf curl Multan betasatellite [CLCuMuB]) associated with a serious disease of cotton across southern Asia is capable of interacting with a NW begomovirus. In the presence of CLCuMuB, the symptoms of the NW cabbage leaf curl virus (CbLCuV) are enhanced in Nicotiana benthamiana. However, CbLCuV was unable to interact with a second betasatellite, chili leaf curl betasatellite. Although CbLCuV can transreplicate CLCuMuB, satellite accumulation levels in plants were low. However, progeny CLCuMuB isolated after just one round of infection with CbLCuV contained numerous mutations. Reinoculation of one such progeny CLCuMuB with CbLCuV to N. benthamiana yielded infections with significantly higher satellite DNA levels. This suggests that betasatellites can rapidly adapt for efficient transreplication by a new helper begomovirus, including begomoviruses originating from the NW. Although the precise mechanism of transreplication of betasatellites by begomoviruses remains unknown, an analysis of betasatellite mutants suggests that the sequence(s) required for maintenance of CLCuMuB by one of its cognate begomoviruses (cotton leaf curl Rajasthan virus) differs from the sequences required for maintenance by CbLCuV. The significance of these findings and, particularly, the threat that betasatellites pose to agriculture in the NW, are discussed.

Molecular Characterization of Tomato leaf curl Palampur virus and Pepper leaf curl betasatellite Naturally Infecting Pumpkin (Cucurbita moschata) in India

“…PeLCB would have come through whiteflies from the nearby chilli crop that showed severe leaf curl symptoms. Betasatellites are associated with majority of monopartite begomoviruses [15] ToLCPMV is not known to have an associated betasatellite [9,7]. Due to the limited number of clones sequenced or using a restricted primer rather than the universal primer for the detection of DNA-A of begomoviruses, we were unable to detect the presence of any monopartite begomovirus from the same sample.…”

Genetic diversity and phylogeography of begomoviruses infecting legumes in Pakistan

“…So far only bipartite begomoviruses have been shown to be native to the New World, although a monopartite Old World (OW) begomovirus has been inadvertently introduced there recently (Polston et al, 1999). In the OW monopartite begomoviruses outnumber bipartite viruses and the vast majority of these monopartite viruses associate with DNA satellites that are symptom determining (Briddon & Stanley, 2006;Nawaz-ul-Rehman et al, 2009). …”

Mutational Analysis of Effectors Encoded by Monopartite Begomoviruses and Their Satellites

“…Similarly, deletion of betasatellite sequences from 1130 to 116 that is conserved (between all betasatellites) stopped the betasatellite's ability to be trans-replicated and maintained by helper viruses both from OW (CLCuRaV) and New world and Cabbage leaf curl virus (CbLCuV). Trans-replication of CLCuMuB remained unaffected by deletion of the sequence between coordinates 995 and 1095 by CLCuRaV [59].…”

“…Betasatellites are approximately half the size of their helper begomoviruses (approx.1.4 kb) and are required by the helper virus to induce typical disease symptoms in their original hosts. The success of begomovirus-betasatellite disease complexes appears to be due to the promiscuous nature of betasatellites that allows them to be trans-replicated by several distinct begomoviruses [53,59]. These begomovirusbetasatellite disease complexes are widespread throughout OW and outnumber bipartite begomoviruses whereas in the NW only bipartite begomoviruses are native.…”

“…Generally, sequences between the βC1 gene and the A-rich region are not essential for transreplication by begomoviruses. Nevertheless, deletion of these sequences abolish the ability of the betasatellite to upregulate virus levels in plants and the symptoms expression [59]. For geminiviruses hairpin structure that contains the nonanucleotide sequence is an essential part of the virion sense origin of replication that is recognized and nicked (within the nonanucleotide sequence) by Rep to initiate rolling-circle replication of the virion strand.…”