Role of a novel type of double infection in the geminivirus‐induced epidemic of severe cassava mosaic in Uganda

Abstract

To study the cause of the current epidemic of severe mosaic in Ugandan cassava, PCR analysis was used to detect and identify African cassava mosaic virus (ACMV), East African cassava mosaic virus (EACMV) and the recently reported recombinant geminivirus (UgV), which is derived from ACMV and EACMV, in leaf extracts from cassava plants grown from cuttings in the glasshouse at Dundee. The cuttings were collected from plants showing symptoms of different severities and growing at different sites in Uganda inside, at the periphery of, and outside, the area affected by the epidemic. ACMV occurred throughout the nine districts sampled but UgV was detected only in the area affected by the epidemic. EACMV was not found in Uganda. Most plants containing ACMV alone expressed mild or moderate mosaic, whereas very severe mosaic developed in most plants containing UgV plus ACMV and a few of those containing UgV only. Very severe mosaic in cassava from southern Sudan was likewise associated with co-infection by UgV and ACMV. The very severe disease was reproduced by graft-inoculating geminivirus-free cassava with UgV plus ACMV; plants inoculated with either UgV or ACMV developed severe or moderate symptoms, respectively. Unlike ACMV, Malawian EACMV did not enhance the severity of symptoms induced by UgV. However, a very severely affected plant from Ukerewe Island, Tanzania, contained ACMV and EACMV but not UgV. UgV attained a much greater concentration in cassava than did ACMV but the opposite occurred in Nicotiana benthamiuna. In neither host was total virus antigen concentration affected by co-infection.Factors affecting the genesis, selection and spread of UgV are discussed. The evidence indicates that UgV is probably of relatively recent origin, that such variants do not appear often, and that the current epidemic has resulted from the rapid spread of UgV to infect plants and to invade regions in which ACMV already occurred. The novel type of virus complex so produced, consisting of an interspecific recombinant virus (UgV) and one of its parents (ACMV), typically has even more severe effects than UgV alone. 0 1997 Association of Applied Biologists 438 B D HARRISON ET AL.

Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda

“…However, Southern blot analysis of naturally CMD-infected cassava plants showed a greater accumulation of EACMV-UG2 DNA-A and EACMV-UG3 DNA-B in mixed-infected plants compared with singly infected plants. Such a synergistic interaction between ACMV and EACMV has been suggested by Harrison et al (1997) and demonstrated by Fondong et al (2000) with infectious clones of ACMV-CM and EACMV-CM isolated from Cameroon.…”

Synonymous site variation due to recombination explains higher genetic variability in begomovirus populations infecting non-cultivated hosts

“…It appears to heavily contribute to begomovirus genetic diversity, increasing the evolutionary potential and local adaptation of strains (Berrie et al, 2001;Graham et al, 2010;Harrison & Robinson, 1999;Monci et al, 2002;Padidam et al, 1999). There is ample opportunity for recombination because multiple begomovirus species are often found co-infecting the same plant (Davino et al, 2009;García-Andrés et al, 2006;Harrison et al, 1997;Pita et al, 2001;Ribeiro et al, 2003;Sanz et al, 2000;Torres-Pacheco et al, 1996), and more than one virus can simultaneously replicate in the same nucleus (Morilla et al, 2004). Additionally, the high recombination frequency observed for begomoviruses may be explained by a theoretical recombination-dependent replication mechanism (RDR) (Jeske et al, 2001), in addition to the welldocumented rolling circle replication (RCR) (Saunders et al, 2001).…”

Supervirulent pseudorecombination and asymmetric synergism between genomic components of two distinct species of begomovirus associated with severe tomato leaf curl disease in India

“…Synergism between members of two distinct geminivirus species has been demonstrated previously (Harrison et al, 1997;Fondong et al, 2000;Pita et al, 2001). However, no information about pseudorecombination between the components of different isolates of two begomovirus species causing leaf curl disease of tomato is currently available and synergism between such isolates has not been demonstrated.…”

“…Harrison et al (1997) suggested the possibility of synergism between isolates of the two cassava begomovirus species, African cassava mosaic virus and East African cassava mosaic virus. Molecular evidence for synergism between the cassava-infecting begomoviruses African cassava mosaic virus from Cameroon (ACMV- [CM:98]) and East African cassava mosaic virus from Cameroon (EACMV- [CM:98]) has been demonstrated (Fondong et al, 2000;Pita et al, 2001;Vanitharani et al, 2004).…”