Abstract
Two distinct full-length begomovirus DNA-A components and a DNA-B component were PCR amplified, cloned and sequenced from Jamaican Malvastrum americanum plants exhibiting yellow mosaic symptoms. Whereas one of the DNA-A components is from a potentially new species that we have tentatively named Malvastrum yellow mosaic Helshire virus (MaYMHV), the other DNA-A and the DNA-B form a cognate pair and represent a new virus species tentatively named Malvastrum yellow mosaic Jamaica virus (MaYMJV). The MaYMJV genome components together infected M. americanum and produced yellow mosaic symptoms similar to those seen in naturally infected plants. Both the MaYMJV and MaYMHV DNA-A components are typical of those of bipartite begomoviruses from the Western Hemisphere. The DNA-As of MaYMJV and MaYMHV are most closely related to each other (sharing 84% sequence identity) and cluster phylogenetically with begomoviruses found infecting malvaceous weeds in Cuba and Florida. The DNA-B component of MaYMJV is most similar to that of Sida golden mosaic virus-[USA:Florida] (SiGMV-[US:Flo]) and Sida golden mosaic Costa Rica virus-[Costa Rica] (SiGMCRV-[CR]). As with many other geminivirus species, the genomes of MaYMJV and MaYMHV bear traces of inter-species recombination.
Similar content being viewed by others
References
A.J. Howarth, R.M. Goodman, Divergence and evolution of geminivirus genomes. J. Mol. Evol. 23, 313–319 (1986)
E.J. Duffus, in Current Topics in Vector Research, vol. 4, ed. by K. Harris (Springer-Verlag, New York, 1987), pp. 73–91
S.G. Lazarowitz, Geminiviruses: genome structure and gene function. Crit. Rev. Plant Sci. 11, 327–349 (1992)
A.O. Noueiry, W.J. Lucas, R.L. Gilbertson, Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76, 925–932 (1994)
J. Stanley, A. von Arnim, Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology 186, 286–293 (1992)
D.J. Ingham, E. Pascal, S.G. Lazarowitz, Both bipartite geminiviruses movement proteins determine viral host range, but only BL1 determines viral pathogenicity. Virology 207, 191–204 (1995)
G.R. Argüello-Astorga, R.G. Guevara-González, L.R. Herrera-Estrella, R.F. Rivera-Bustamante, Geminivirus replication origins have a group-specific organization of iterative elements: a model for replication. Virology 203, 90–100 (1994)
E.P.B. Fontes, H.J. Gladfelter, R.L. Schaffer, I.T.D. Petty, L. Hanely-Bowdion, Geminivirus replication origins have a modal organization. Plant Cell 6, 405–416 (1994)
A. Varma, V.G. Malathi, Emerging geminivirus problems: a serious threat to crop production. Ann. Appl. Biol. 142, 145–164 (2003)
F.J. Morales, P.K. Anderson, The emergence and dissemination of whitefly-transmitted geminiviruses in Latin America. Arch. Virol. 146, 415–441 (2001)
M.E. Roye, W.A. McLaughlin, J.D. Spence, D.P. Maxwell, The common weed Macroptilium lathyroides is not a source of crop-infecting geminiviruses from Jamaica. J. Trop. Agric. (Trinidad) 76, 1–7 (1999)
M.E. Roye, S. Brown, J.D. Spence, K. Smith, W.A. McLaughlin, Ten years of molecular biology research on whitefly transmitted geminivirus from Jamaica: a review. Jam. J. Sci. Technol. 14, 98–118 (2003)
M. Roye, A. Collins, M. Brown, C. Stewart, S. Turner, M. Chin, L. Fisher, P. Tennant, W. McLaughlin, Plant virus and phytopathology research in Jamaica: a review. Am. J. Plant Sci. Biotechnol. 1, 36–46 (2007)
J. Méndez-Lozano, L.L. Perea-Araujo, R.D. Ruelas-Ayala, N.E. Leyva-López, A Begomovirus isolated from chlorotic and stunted soybean plants in Mexico is a new strain of Rhynchosia golden mosaic virus. Plant Dis. 90, 972 (2006)
J.T. Ascencio-Ibáñez, G.R. Argüello-Astorga, J. Méndez-Lozano, F. Rivera-Bustamante, First report of Rhynchosia golden mosaic virus (RhGMV) infecting tobbaco in Chiapas, Mexico. Plant Dis. 88, 692 (2002)
A.M. Idris, E. Hiebert, J. Bird, J.K. Brown, Two newly described begomoviruses of Macroptilium lathyroides and common bean. Phytopathology 93, 774–783 (2003)
I.D. Bedford, A. Kelly, G.K. Banks, R.W. Briddon, J.L. Cenis, P.G. Markham, Solanium nigrum: an indigenous weed reservoir for a tomato yellow leaf curl geminivirus in southern Spain. Eur. J. Plant Pathol. 104, 221–222 (1998)
S. Sánchez-Campos, J. Navas-Castillo, F. Monci, J.A. Díaz, E. Moriones, Mercurialis ambigua and Solanum luteum: two newly discovered natural hosts of tomato yellow leaf curl geminiviruses. Eur. J. Plant Pathol. 106, 391–394 (2000)
P. Umaharan, M. Padidam, R.H. Phelps, R.N. Beachy, C.M. Fauquet, Distribution and diversity of geminiviruses in Trinidad and Tobago. Phytopathology 88, 1262–1268 (1998)
A.P. Graham, C.S. Stewart, M.E. Roye, First report of a begomovirus infecting two common weeds: Malvastrum americanum and Sida spinosa in Jamaica. Plant Pathol. 56, 340 (2007)
M.R. Rojas, R.L. Gilbertson, D.R. Russell, D.P. Maxwell, Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Dis. 77, 340–347 (1993)
D.G. Higgins, A.J. Bleasby, R. Fuchs, CLUSTAL V: improved software for multiple sequence alignment. Comput. Appl. Biosci. 8, 189–191 (1992)
J. Felsenstein, Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791 (1985)
N. Saitou, M. Nei, The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987)
J.C. Faria, R.L. Gilbertson, S.F. Hanson, F.J. Morales, P. Ahlquist, A.O. Loniello, D.P. Maxwell, Bean golden mosaic geminivirus type II isolates from the Dominican Republic and Guatemala: nucleotide sequence, infectious pseudorecombinants, and phylogenetic relationships. Phytopathology 84, 321–329 (1994)
L. Heath, E. van der Walt, A. Varsani, D.P. Martin, Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J. Virol. 80, 11827–11832 (2006)
D.P. Martin, C. Williamson, D. Posada, RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262 (2005)
J.L. Marsh, M. Erfl, E.J. Wykes, The PIC plasmid and phage vectors with versatile cloning sites for recombinant selection by insertional inactivation. Gene 32, 481–485 (1984)
R.L. Gilbertson, S.H. Hidayat, E.J. Paplomatas, M.R. Rojas, Y.-M. Hou, D.P. Maxwell, Pseudorecombination between the infectious cloned DNA components of tomato mottle and bean dwarf mosaic geminiviruses. J. Gen. Virol. 74, 23–31 (1993)
J. Stanley, Analysis of African cassava mosaic virus recombinants suggests strand nicking occurs within the conserved nonanucleotide motif during the initiation of rolling DNA circle replication. Virology 206, 707–712 (1995)
P.A. Eagle, L. Hanley-Bowdoin, cis elements that contribute to geminivirus transcriptional regulation and the efficiency of DNA replication. J. Virol. 71, 6947–6955 (1997)
J.K. Brown, K.M. Ostrow, A.M. Idris, D.C. Stenger, Biotic, molecular, and phylogenetic characterization of Bean calico mosaic virus, a distinct Begomovirus species with affiliation in the squash leaf curl virus cluster. Phytopathology 89, 273–280 (1999)
I. Jupin, F. Hericourt, B. Benz, B. Gronenborn, DNA replication specificity of TYLCV geminivirus is mediated by amino-terminal 116 amino acids of the Rep protein. FEBS Lett. 362, 116–120 (1995)
G.R. Argüello-Astorga, R. Ruiz-Medrano, An iteron related domain is associated to Motif 1 in the replication proteins of geminiviruses: identification of potential interacting amino acid-base pairs by a comparative approach. Arch. Virol. 146, 1465–1485 (2001)
G.C. Hall, A.P. Graham, M.E. Roye, Tobacco leaf curl Cuba virus infects the weed Malachra alceifolia in Jamaica. Plant Pathol. 57, 398 (2008)
C.M. Fauquet, R.W. Briddon, J.K. Brown, E. Moriones, J. Stanley, M. Zerbini, X. Zhou, Geminivirus strain demarcation and nomenclature. Arch. Virol. 153, 783–821 (2008)
M. Padidam, S. Sawyer, C.M. Fauquet, Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218–225 (1999)
P. Lefeuvre, J.M. Lett, B. Reynaud, D.P. Martin, Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3(11), e181 (2007). doi:10.1371/journal.ppat.0030181
C.M. Fauquet, D.M. Bisaro, R.W. Briddon, J. Brown, B.D. Harrison, E.P. Rybicki, D.C. Stenger, J. Stanley, Revision of taxonomic criteria for species demarcation in the family Geminiviridae, and an updated list of begomovirus species. Arch. Virol. 148, 405–421 (2003)
V.N. Fondong, J.S. Pita, M.E.C. Rey, A. de Kochko, R.N. Beachy, C.M. Fauquet, Evidence of synergism between African cassava mosaic virus and a new double-recombinant geminivirus infecting cassava in Cameroon. J. Gen. Virol. 81, 287–297 (2000)
J.P. Legg, C.M. Fauquet, Cassava mosaic geminiviruses in Africa. Plant Mol. Biol. 56, 585–599 (2004)
J. Méndez-Lozano, I. Torres-Pacheco, C.M. Fauquet, R.F. Rivera-Bustamante, Interactions between geminiviruses in a naturally occurring mixture: Pepper huasteco virus and Pepper golden mosaic virus. Phytopathology 93, 270–277 (2003)
A. Chatterji, U. Chatterji, R.N. Beachy, C.M. Fauquet, Sequence parameters that determine specificity of binding of the replication-associated protein to its cognate in two strains of Tomato leaf curl virus-New Delhi. Virology 273, 341–350 (2000)
E.C. Andrade, G.G. Manhani, P.F. Alfenas, R.F. Calegario, E.P.B. Fontes, F.M. Zerbini, Tomato yellow spot virus, a tomato-infecting begomovirus from Brazil with a closer relationship to viruses from Sida sp., forms pseudorecombinants with begomoviruses from tomato but not from Sida. J. Gen. Virol. 87, 3687–3696 (2006)
S. Chakraborty, R. Vanitharani, B. Chattopadhyay, C.M. Fauquet, Supervirulent pseudorecombination and asymmetric synergism between genomic components of two distinct species of begomovirus associated with severe tomato leaf curl disease in India. J. Gen. Virol. 89, 818–828 (2008)
R.M. Galvão, A.C. Mariano, D.F. Luz, P.F. Alfenas, E.C. Andrade, F.M. Zerbini, M.R. Almeida, E.P.B. Fontes, A naturally occurring recombinant DNA-A of a typical bipartite begomovirus does not require the cognate DNA-B to infect Nicotiana benthamiana systemically. J. Gen. Virol. 84, 715–726 (2003)
P.L. Ramos, R.G. Guevara-González, R. Peral, J.T. Ascencio-Ibáñez, J.E. Polston, G.R. Argüello-Astorga, J.C. Vega-Arreguín, R.F. Rivera-Bustamante, Tomato mottle Taino virus pseudorecombines with PYMV but not with ToMoV: Implications for the delimitation of cis- and trans-acting replication specificity determinants. Arch. Virol. 148, 1697–1712 (2003)
P. Lefeuvre, D.P. Martin, M. Hoareau, F. Naze, H. Delatte, M. Thierry, A. Varsani, N. Becker, B. Reynaud, J.M. Lett, Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. J. Gen. Virol. 88, 3458–3468 (2007)
L.P. Ambrozevicius, R.F. Calegario, E.P.B. Fontes, M.G. Carvalho, F.M. Zerbini, Genetic diversity of begomovirus infecting tomato and associated weeds in Southeastern Brazil. Fitopatol. Bras. 27, 372–377 (2002)
H. Delatte, D.P. Martin, F. Naze, R. Goldbach, B. Reynaud, M. Peterschmitt, J.M. Lett, South West Indian Ocean islands tomato begomovirus populations represent a new major monopartite begomovirus group. J. Gen. Virol. 86, 1533–1542 (2005)
J.S. Pita, V.N. Fondong, A. Sangaré, G.W. Otim-Nape, S. Ogwal, C.M. Fauquet, Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. J. Gen. Virol. 82, 655–665 (2001)
N. Kirthi, C.G.P. Priyadarshini, P. Sharma, S.P. Maiya, V. Hemalatha, P. Sivaraman, P. Dhawan, N. Rishi, H.S. Savithri, Genetic variability of begomoviruses associated with cotton leaf curl disease originating from India. Arch. Virol. 149, 2047–2057 (2004)
Acknowledgements
Funding for this work was provided by The Principal’s New Initiative Fund and The School of Graduate Studies and Research at the University of the West Indies (Mona campus). The authors are also grateful for the photographic assistance of Mr. Darshan Young and for his help along with Miss Cheryl Stewart in gathering DNA sequence data for the recombination analysis.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
These files are unfortunately not in the Publisher's archive anymore:
-
DNA-B.rdp RDP project files that can be opened in the program RDP3 (which may be downloaded from http://darwin.uvigo.es/rdp/rdp.html) and used to interactively explore the patterns of recombination evident among Western Hemisphere begomovirus DNA-B sequences (RDP 965 kb)
-
DNA-A.rdp RDP project files that can be opened in the program RDP3 and used to interactively explore the patterns of recombination events among Western Hemisphere begomovirus DNA-A sequences (RDP 432 kb)
Rights and permissions
About this article
Cite this article
Graham, A.P., Martin, D.P. & Roye, M.E. Molecular characterization and phylogeny of two begomoviruses infecting Malvastrum americanum in Jamaica: evidence of the contribution of inter-species recombination to the evolution of malvaceous weed-associated begomoviruses from the Northern Caribbean. Virus Genes 40, 256–266 (2010). https://doi.org/10.1007/s11262-009-0430-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-009-0430-6