Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen

Arvind Varsani, Dionne N. Shepherd, Adérito L. Monjane, Betty E. Owor, Julia B. Erdmann, Edward P. Rybicki, Michel Peterschmitt, Rob W. Briddon, Peter G. Markham, Sunday Oluwafemi, Oliver P. Windram, Pierre Lefeuvre, Jean Michel Lett, Darren P. Martin

Research output: Contribution to journalArticle

81 Citations (Scopus)

Abstract

Maize streak virus (MSV; family Geminiviridae, genus Mastrevirus), the causal agent of maize streak disease, ranks amongst the most serious biological threats to food security in subSaharan Africa. Although five distinct MSV strains have been currently described, only one of these - MSV-A - causes severe disease in maize. Due primarily to their not being an obvious threat to agriculture, very little is known about the 'grass-adapted' MSV strains, MSV-B, -C, -D and -E. Since comparing the genetic diversities, geographical distributions and natural host ranges of MSV-A with the other MSV strains could provide valuable information on the epidemiology, evolution and emergence of MSV-A, we carried out a phylogeographical analysis of MSVs found in uncultivated indigenous African grasses. Amongst the 83 new MSV genomes presented here, we report the discovery of six new MSV strains (MSV-F to -K). The non-random recombination breakpoint distributions detectable with these and other available mastrevirus sequences partially mirror those seen in begomoviruses, implying that the forces shaping these breakpoint patterns have been largely conserved since the earliest geminivirus ancestors. We present evidence that the ancestor of all MSV-A variants was the recombinant progeny of ancestral MSV-B and MSV-G/-F variants. While it remains unknown whether recombination influenced the emergence of MSV-A in maize, our discovery that MSV-A variants may both move between and become established in different regions of Africa with greater ease, and infect more grass species than other MSV strains, goes some way towards explaining why MSV-A is such a successful maize pathogen.

Original languageEnglish (US)
Pages (from-to)2063-2074
Number of pages12
JournalJournal of General Virology
Volume89
Issue number9
DOIs
StatePublished - 2008
Externally publishedYes

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Maize streak virus
Geminiviridae
Host Specificity
Genetic Recombination
Zea mays
Poaceae
Begomovirus
Food Supply
Africa South of the Sahara
Agriculture
Epidemiology
Genome

ASJC Scopus subject areas

  • Virology

Cite this

Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen. / Varsani, Arvind; Shepherd, Dionne N.; Monjane, Adérito L.; Owor, Betty E.; Erdmann, Julia B.; Rybicki, Edward P.; Peterschmitt, Michel; Briddon, Rob W.; Markham, Peter G.; Oluwafemi, Sunday; Windram, Oliver P.; Lefeuvre, Pierre; Lett, Jean Michel; Martin, Darren P.

In: Journal of General Virology, Vol. 89, No. 9, 2008, p. 2063-2074.

Research output: Contribution to journalArticle

Varsani, A, Shepherd, DN, Monjane, AL, Owor, BE, Erdmann, JB, Rybicki, EP, Peterschmitt, M, Briddon, RW, Markham, PG, Oluwafemi, S, Windram, OP, Lefeuvre, P, Lett, JM & Martin, DP 2008, 'Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen', Journal of General Virology, vol. 89, no. 9, pp. 2063-2074. https://doi.org/10.1099/vir.0.2008/003590-0
Varsani, Arvind ; Shepherd, Dionne N. ; Monjane, Adérito L. ; Owor, Betty E. ; Erdmann, Julia B. ; Rybicki, Edward P. ; Peterschmitt, Michel ; Briddon, Rob W. ; Markham, Peter G. ; Oluwafemi, Sunday ; Windram, Oliver P. ; Lefeuvre, Pierre ; Lett, Jean Michel ; Martin, Darren P. / Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen. In: Journal of General Virology. 2008 ; Vol. 89, No. 9. pp. 2063-2074.
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abstract = "Maize streak virus (MSV; family Geminiviridae, genus Mastrevirus), the causal agent of maize streak disease, ranks amongst the most serious biological threats to food security in subSaharan Africa. Although five distinct MSV strains have been currently described, only one of these - MSV-A - causes severe disease in maize. Due primarily to their not being an obvious threat to agriculture, very little is known about the 'grass-adapted' MSV strains, MSV-B, -C, -D and -E. Since comparing the genetic diversities, geographical distributions and natural host ranges of MSV-A with the other MSV strains could provide valuable information on the epidemiology, evolution and emergence of MSV-A, we carried out a phylogeographical analysis of MSVs found in uncultivated indigenous African grasses. Amongst the 83 new MSV genomes presented here, we report the discovery of six new MSV strains (MSV-F to -K). The non-random recombination breakpoint distributions detectable with these and other available mastrevirus sequences partially mirror those seen in begomoviruses, implying that the forces shaping these breakpoint patterns have been largely conserved since the earliest geminivirus ancestors. We present evidence that the ancestor of all MSV-A variants was the recombinant progeny of ancestral MSV-B and MSV-G/-F variants. While it remains unknown whether recombination influenced the emergence of MSV-A in maize, our discovery that MSV-A variants may both move between and become established in different regions of Africa with greater ease, and infect more grass species than other MSV strains, goes some way towards explaining why MSV-A is such a successful maize pathogen.",
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AU - Varsani, Arvind

AU - Shepherd, Dionne N.

AU - Monjane, Adérito L.

AU - Owor, Betty E.

AU - Erdmann, Julia B.

AU - Rybicki, Edward P.

AU - Peterschmitt, Michel

AU - Briddon, Rob W.

AU - Markham, Peter G.

AU - Oluwafemi, Sunday

AU - Windram, Oliver P.

AU - Lefeuvre, Pierre

AU - Lett, Jean Michel

AU - Martin, Darren P.

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N2 - Maize streak virus (MSV; family Geminiviridae, genus Mastrevirus), the causal agent of maize streak disease, ranks amongst the most serious biological threats to food security in subSaharan Africa. Although five distinct MSV strains have been currently described, only one of these - MSV-A - causes severe disease in maize. Due primarily to their not being an obvious threat to agriculture, very little is known about the 'grass-adapted' MSV strains, MSV-B, -C, -D and -E. Since comparing the genetic diversities, geographical distributions and natural host ranges of MSV-A with the other MSV strains could provide valuable information on the epidemiology, evolution and emergence of MSV-A, we carried out a phylogeographical analysis of MSVs found in uncultivated indigenous African grasses. Amongst the 83 new MSV genomes presented here, we report the discovery of six new MSV strains (MSV-F to -K). The non-random recombination breakpoint distributions detectable with these and other available mastrevirus sequences partially mirror those seen in begomoviruses, implying that the forces shaping these breakpoint patterns have been largely conserved since the earliest geminivirus ancestors. We present evidence that the ancestor of all MSV-A variants was the recombinant progeny of ancestral MSV-B and MSV-G/-F variants. While it remains unknown whether recombination influenced the emergence of MSV-A in maize, our discovery that MSV-A variants may both move between and become established in different regions of Africa with greater ease, and infect more grass species than other MSV strains, goes some way towards explaining why MSV-A is such a successful maize pathogen.

AB - Maize streak virus (MSV; family Geminiviridae, genus Mastrevirus), the causal agent of maize streak disease, ranks amongst the most serious biological threats to food security in subSaharan Africa. Although five distinct MSV strains have been currently described, only one of these - MSV-A - causes severe disease in maize. Due primarily to their not being an obvious threat to agriculture, very little is known about the 'grass-adapted' MSV strains, MSV-B, -C, -D and -E. Since comparing the genetic diversities, geographical distributions and natural host ranges of MSV-A with the other MSV strains could provide valuable information on the epidemiology, evolution and emergence of MSV-A, we carried out a phylogeographical analysis of MSVs found in uncultivated indigenous African grasses. Amongst the 83 new MSV genomes presented here, we report the discovery of six new MSV strains (MSV-F to -K). The non-random recombination breakpoint distributions detectable with these and other available mastrevirus sequences partially mirror those seen in begomoviruses, implying that the forces shaping these breakpoint patterns have been largely conserved since the earliest geminivirus ancestors. We present evidence that the ancestor of all MSV-A variants was the recombinant progeny of ancestral MSV-B and MSV-G/-F variants. While it remains unknown whether recombination influenced the emergence of MSV-A in maize, our discovery that MSV-A variants may both move between and become established in different regions of Africa with greater ease, and infect more grass species than other MSV strains, goes some way towards explaining why MSV-A is such a successful maize pathogen.

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