Association of Satellites with a Mastrevirus in Natural Infection: Complexity of Wheat Dwarf India Virus Disease

Abstract

In contrast to begomoviruses, mastreviruses have not previously been shown to interact with satellites. This study reports the first identification of the association of satellites with a mastrevirus in field-grown plants. Two alphasatellite species were detected in different field samples of wheat infected with Wheat dwarf India virus (WDIV), a Cotton leaf curl Multan alphasatellite (CLCuMA) and a Guar leaf curl alphasatellite (GLCuA). In addition to the alphasatellites, a betasatellite, Ageratum yellow leaf curl betasatellite (AYLCB), was also identified in the wheat samples. No begomovirus was detected in the wheat samples, thus establishing association of the above-named satellites with WDIV. Agrobacterium-mediated inoculation of WDIV in wheat, in the presence of either of the alphasatellites or the betasatellite, resulted in infections inducing more severe symptoms. WDIV efficiently maintained each of the alphasatellites and the betasatellite in wheat. The satellites enhanced the level of WDIV DNA in wheat. Inoculation of the satellites isolated from wheat with various begomoviruses into Nicotiana tabacum demonstrated that these remain capable of interacting with the viruses with which they were first identified. Virus-specific small RNAs accumulated in wheat upon infection with WDIV but were lower in abundance in plants coinfected with the satellites, suggesting that both the alphasatellites and the betasatellite suppress RNA silencing. These results suggest that the selective advantage for the maintenance of the alphasatellites and the betasatellite by WDIV in the field is in overcoming RNA silencing-mediated host defense. IMPORTANCE Wheat is the most widely cultivated cereal crop in the world. A number of viruses are important pathogens of wheat, including the viruses of the genus

Wheat dwarf India Virus and associated betasatellite infecting wheat in Pakistan

“…Leaf samples from 59 symptomatic wheat plants were collected during 2017-18 from commercial crops and research fields. The symptomatic plants showed dwarfing and/ or yellowing, similar to those previously reported in India by Kumar et al (2012Kumar et al ( , 2014a. Young leaf samples were collected and stored in a tube with ethanol at room temperature for a week.…”

“…The virus genomes amplified from all of the plant samples were 2783 bp long and showed sequence identities of 99% with WDIV reported previously (Kumar et al 2012(Kumar et al , 2014a2015). Based on the mastrevirus species and strain demarcation thresholds of >78% and > 94% identity, respectively (Muhire et al 2013) the viral genomes detected under study are isolates of WDIV.…”

Geminiviridae

“…Although alphasatellites have mainly been identified with begomoviruses associated with betasatellites, not all begomovirus/betasatellite complexes maintain alphasatellites, and alphasatellites have been identified in association with bipartite begomoviruses and in the NW. Recently, the helper virus range of these satellites has been shown to extend beyond begomoviruses with identification of both alpha-and betasatellites in association with a mastrevirus, wheat dwarf India virus, and this was also the first identification of these satellites in a monocotyledonous host (Kumar et al, 2014). See also: Plant Virus Satellites…”

Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites

“…Furthermore, it was isolated from a monocotyledonous host. Two geminialphasatellites have been isolated from monocotyledonous plants and both of these have features typical of the Geminialphasatellitinae [24]; and twelve have been isolated from bananas and cardamom, all of which have similarities to other nanoalphasatellites [2,11,18,25,53]. We therefore propose this molecule to represent an unassigned species in the family Alphasatellitidae.…”

“…Alphasatellites associated with nanoviruses have a similar size to that of typical nanovirus components (~ 1100 nucleotides), lack the CR-SL and CRM of their helper viruses and are also unable to trans-replicate the bona fide genome components of these helper viruses [18,[43][44][45]. Alphasatellites have also been identified in association with begomoviruses and, in one reported case, a mastrevirus [4,24]. Typically comprising ~ 1400 nucleotides, the geminivirus associated alphasatellites are significantly larger than both nanovirus components and nanovirus alphasatellites [4].…”