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Journal of Virology, September 2009, p. 9347-9355, Vol. 83, No. 18
0022-538X/09/$08.00+0     doi:10.1128/JVI.00795-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

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

Muhammad Shah Nawaz-ul-Rehman,1 Shahid Mansoor,2 Rob W. Briddon,2 and Claude M. Fauquet1*

International Laboratory for Tropical Agricultural Biotechnology, Danforth Plant Science Center, 975 North Warson Road, St. Louis, Missouri 63132,1 National Institute for Biotechnology and Genetic Engineering, Jhang Road, Faisalabad, Pakistan2

Received 20 April 2009/ Accepted 22 June 2009

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.

* Corresponding author. Mailing address: ILTAB/Donald Danforth Plant Science Center, 975 North Warson Road, St. Louis, MO 63132. Phone: (314) 587-1241. Fax: (314) 587-1956. E-mail: iltab{at}danforthcenter.org

{triangledown} Published ahead of print on 1 July 2009.

Journal of Virology, September 2009, p. 9347-9355, Vol. 83, No. 18
0022-538X/09/$08.00+0     doi:10.1128/JVI.00795-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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