An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation

Abstract

The Oman strain of Tomato yellow leaf curl virus (TYLCV-OM) and its associated betasatellite, an isolate of Tomato leaf curl betasatellite (ToLCB), were previously reported from Oman. Here we report the isolation of a second, previously undescribed, begomovirus [Tomato leaf curl Oman virus (ToLCOMV)] and an alphasatellite from that same plant sample. This alphasatellite is closely related (90 % shared nucleotide identity) to an unusual DNA-2-type Ageratum yellow vein Singapore alphasatellite (AYVSGA), thus far identified only in Singapore. ToLCOMV was found to have a recombinant genome comprising sequences derived from two extant parents, TYLCV-OM, which is indigenous to Oman, and Papaya leaf curl virus from the Indian subcontinent. All possible combinations of ToLCOMV, TYLCV-OM, ToLCB and AYVSGA were used to agro-inoculate tomato and Nicotiana benthamiana. Infection with ToLCOMV yielded mild leaf-curl symptoms in both hosts; however, plants inoculated with TYLCV-OM developed more severe symptoms. Plants infected with ToLCB in the presence of either helper begomovirus resulted in more severe symptoms. Surprisingly, symptoms in N. benthamiana infected with the alphasatellite together with either of the helper viruses and the betasatellite were attenuated and betasatellite DNA accumulation was substantially reduced. However, in the latter plants no concomitant reduction in the accumulation of helper virus DNA was observed. This is the first example of an attenuation of begomovirus-betasatellite symptoms by this unusual class of alphasatellites. This observation suggests that some DNA-2 alphasatellites encode a pathogenicity determinant that may modulate begomovirus-betasatellite infection by reducing betasatellite DNA accumulation.

Complexity of begomovirus and betasatellite populations associated with chilli leaf curl disease in India

“…The bC1 ORF has been characterized as a pathogenicity determinant that suppresses host antiviral silencing and is involved in virus movement (Cui et al, 2005;Li et al, 2014;Saunders et al, 2004;Yang et al, 2011). A class of autonomously replicating satellite-like molecules identified as alphasatellites require helper begomoviruses for their intra-and intercellular movement and are reported to ameliorate symptoms in a few cases (Idris et al, 2011;Nawaz-ulRehman et al, 2010).…”

Tomato Leaf Curl Sudan Virus (TLCSDV) causing leaf curl disease on a new host Amaranthus cruentus L.

“…On the other side, Yemen is separated from Oman and Saudi Arabia by a vast harsh desert condition which plays potential barriers to virus and whitefly movement. However, the extant occurrence in both locations of two closely related viruses indicates that what may serve as deterrents to human movement, do not present impervious barriers to virus-vector dispersal, having fostered instead the apparently, unrestricted natural dispersal of TYLCV and ToLCSDV isolates in the kingdom (Idris et al, 2011).…”

“…The sequence identity and phylogenetic analysis results strongly support the causative agent is a variant of Tomato leaf curl Sudan virus (ToLCSDV), a virus that has been reported earlier to cause tomato leaf curl disease in Sudan, Oman and Yemen. The association of begomovirus with leaf curl disease on various crops in Arabian Peninsula has been published in many reports (Ajlan et al, 2007;Khan et al, 2008;Idris et al, 2012;Akhtar et al, 2014;Idris et al, 2011;Khan et al, 2013a;(Ajlan et al, 2007;Khan et al, 2008;Idris et al, 2012;Akhtar et al, 2014;Idris et al, 2011;Khan et al, 2013bAl-Saleh et al, 2014Hosseinzadeh et al, 2014;Idris et al, 2014).…”

Mutational Analysis of Effectors Encoded by Monopartite Begomoviruses and Their Satellites

“…However [35] hypothesize that symptom attenuation and a relative reduction in betasatellite accumulation might result from DNA-2-mediated modulation of betasatellite activity. Possibly alphasatellite modulates begomovirus-betasatellite pathogenicity by interfering with C1, a key virulence factor [8].…”