ANNOTATED SEQUENCE RECORD

Bromus catharticus striate mosaic virus: a new mastrevirusinfecting Bromus catharticus from Australia

James Hadfield • Darren P. Martin • Daisy Stainton • Simona Kraberger •

Betty E. Owor • Dionne N. Shepherd • Francisco Lakay • Peter G. Markham •

Ray S. Greber • Rob W. Briddon • Arvind Varsani

Received: 12 August 2010 / Accepted: 20 November 2010 / Published online: 12 December 2010

� Springer-Verlag 2010

Abstract Although monocotyledonous-plant-infecting

mastreviruses (in the family Geminiviridae) are known to

cause economically significant crop losses in certain areas

of the world, in Australia, they pose no obvious threat to

agriculture. Consequently, only a few Australian monocot-

infecting mastreviruses have been described, and only two

have had their genomes fully sequenced. Here, we present

the third full-genome sequence of an Australian monocot-

infecting mastrevirus from Bromus catharticus belonging

to a distinct species, which we have tentatively named

Bromus catharticus striate mosaic virus (BCSMV).

Although the genome of this new virus shares only 57.7%

sequence similarity with that of its nearest known relative,

Digitaria didactyla striate mosaic virus (DDSMV; also

from Australia), it has features typical of all other known

mastrevirus genomes. Phylogenetic analysis showed that

both the full genome and each of its probable expressed

proteins group with the two other characterised Australian

monocot-infecting mastreviruses. Besides the BCSMV

genome sequence revealing that Australian monocot-

infecting mastrevirus diversity rivals that seen in Africa, it

has enabled us, for the first, to time detect evidence of

recombination amongst the Australian viruses. Specifically,

it appears that DDSMV possesses a short intergenic region

sequence that has been recombinationally derived from

either BCSMV or a close relative that has not yet been

identified.

The members of the virus family Geminiviridae uniquely

possess circular, single-stranded DNA (ssDNA) genomes

that are encapsidated within twinned quasi-isometric

(‘geminate’) virions [21]. There are currently four estab-

lished geminivirus genera: Mastrevirus, Begomovirus,Electronic supplementary material The online version of thisarticle (doi:10.1007/s00705-010-0872-0) contains supplementarymaterial, which is available to authorized users.

J. Hadfield � D. Stainton � S. Kraberger � A. Varsani (&)

School of Biological Sciences, University of Canterbury,

Private Bag 4800, Christchurch, New Zealand

e-mail: arvind.varsani@canterbury.ac.nz

D. P. Martin

Institute of Infectious Diseases and Molecular Medicine,

University of Cape Town, Observatory,

Cape Town 7925, South Africa

B. E. Owor

Department of Plant Sciences,

University of Cambridge, Cambridge CB2 3EA, UK

D. N. Shepherd � F. Lakay

Department of Molecular and Cell Biology,

University of Cape Town, Rondebosch,

Cape Town 7701, South Africa

P. G. Markham

Department of Disease and Stress Biology,

John Innes Centre, Norwich NR4 7UH, UK

R. S. Greber

Queensland Department of Primary Industries,

Maroochy Horticulture Research Station, Nambour,

QLD, Australia

R. W. Briddon

National Institute for Biotechnology and Genetic Engineering,

Jhang Road, P.O. Box 577, Faisalabad, Pakistan

A. Varsani

Electron Microscope Unit, University of Cape Town,

Rondebosch, Cape Town 7701, South Africa

123

Arch Virol (2011) 156:335–341

DOI 10.1007/s00705-010-0872-0

Curtovirus, and Topocuvirus. Additionally, three highly

divergent geminiviruses have recently been characterised:

beet curly top Iran virus (BCTIV [30]), Eragrostis curvula

streak virus (ECSV [27]) and turnip curly top virus (TCTV

[3]). The four established genera have been classified based

on variations in virus host ranges, vector specificity and

genome organisation [21]. Whereas the mastreviruses are

capable of infecting both monocotyledonous (monocot)

and dicotyledonous (dicot) hosts, all known members of

the other geminivirus genera infect only dicot hosts.

Mastreviruses and curtoviruses are transmitted by leaf-

hoppers, the single identified topocuvirus is transmitted by

treehoppers, and begomoviruses are transmitted by white-

flies. Finally, although the genomes of most known gem-

iniviruses occur as a single component *2.6-3.0 kb in

size, all begomoviruses native to the New World, and a few

from the Old World, have genomes consisting of two

components, each *2.8 kb in size. The single-component

genome of mastreviruses is known to encode only four

proteins: a movement protein [MP], a coat protein [CP], a

replication-associated protein [Rep] and a replication-

associated protein A [RepA]).

Most known monocot-infecting mastreviruses have been

identified in Africa. However, quite a few monocot-infecting

mastreviruses have also been identified outside of Africa

including Miscanthus streak virus (MiSV [5]) from Japan,

Digitaria streak virus (DSV [6, 7]) from Vanuatu, Chloris

striate mosaic virus (CSMV [2]) and Digitaria didactyla

striate mosaic virus (DDSMV) [4] from Australia, and wheat

dwarf virus, oat dwarf virus and barley dwarf virus [12, 18,

28, 29] from Europe, Asia and the Middle East. Being one of

the first geminiviruses sequenced, CSMV is well studied,

especially with reference to the unusual twinned particle

structure of geminiviruses. DDSMV, on the other hand, was

not sequenced until 2010 [4]. Additionally, two mastrevi-

ruses, paspalum striate mosaic virus (PSMV) infecting

Paspalum sp. and a Bromus catharticus-infecting gemini-

virus sampled in the late 1980 s, have previously been bio-

logically and serologically characterised by Greber [9] and

Pinner et al. [17]. Pinner et al. [17] concluded that Greber’s

[9] B. catharticus-infecting geminivirus was a ‘‘strain’’ of

paspalum striate mosaic virus (PSMV-BC) but found that

PSMV and PSMV-BC had slightly different serological

properties. Nonetheless, neither PSMV nor the B. catharti-

cus-infecting geminivirus sampled by Greber [9] have been

characterised at the molecular level. Here, we present

an analysis of the complete nucleotide sequence of the

B. catharticus-infecting geminivirus described by Greber [9].

B. catharticus-infecting geminiviruses have been repor-

ted to produce fine striation symptoms, whereas PSMV

produces blotchy mottle symptoms in natural and experi-

mental hosts (see Greber [9] for details). The B. catharticus-

infecting geminivirus has been readily transmitted by the

leafhopper Nesoclutha pallida to Aegilops variabilis, Avena

sativa, Choris gayana, Dactyloctenium austral, Hordeum

vulgare, Leptochloa filiformis, and Triticum aestivum, and

less readily to Lolium multiflorum, Panicum miliaceum,

Phalaris canariensis, Urochloa panicoides and Zea mays

[9]. On the other hand, PSMV naturally infects at least

seven grass species: Paspalum (P. conjugatum, P. dilata-

tum, P. longiflorum, P. plicatulum, P. urvilli), Chloris

gayana and Zea mays [9]. Greber [9] was additionally able to

transmit PSMV to Avena sativa, Dactyloctenium aegyptium,

Hordeum vulgare, Leptochloa filiformis and Triticum

aestivum (common wheat) and noticed that Paspalum

grasses were readily infected only by PSMV. Interestingly,

the PSMV vector N. pallida was unable to breed on other

hosts—even hosts infected by PSMV [9]. Similarly, vectors

habouring CSMV would not survive on Paspalum hosts [9].

Despite host-range differences (most notably its inability to

infect Paspalum species), based upon serological compari-

sons, Pinner et al. [17] concluded that the B. catharticus-

infecting geminivirus was simply a strain of PSMV.

The B. catharticus-infecting geminivirus was maintained

in B. catharticus by insect transmission using N. pallida at

the John Innes Centre (Norwich, UK) until 1999 [17]. DNA

was isolated from frozen B. catharticus leaf tissue, and the

virus was amplified by rolling-circle amplification using

Phi29 DNA polymerase (TempliPhiTM, GE Healthcare,

USA) as described previously [16, 19]. Amplified conca-

tamers were digested with BglII to yield a unit-length gen-

ome of *2.8 kb (various restriction enzymes were tested,

but BglII was the only one that yielded unit-length genomes).

These linearised genome fragments were ligated into a

BamHI-cut pUC19 cloning vector (BamHI/BglII have

compatible cloning sites). The resulting cloned product was

sequenced by primer walking at Macrogen Inc. (South

Korea). Assembly of the genome was carried out with

Geneious Pro (version 4.8.5; Reel Two) and aligned (Clustal

W [24]; gap open penalty = 10; gap extension penalty = 5)

with a representative sequence from each known mastrevirus

species (Fig. 1) using MEGA version 4 [23].

The assembled genome was 2797 bp long and was ori-

ented according to the canonical virion-strand origin of

replication (v-ori) TAATATTAC sequence. We identified

two virion-strand open reading frames (ORFs), which

probably encode a movement protein (MP) and a coat

protein (CP), the predicted amino acid sequences of which

are provided in Supplementary Figures 2 and 3, respec-

tively. Probable replication-associated protein (Rep and

RepA)-encoding genes were identified on the comple-

mentary strand (Supplementary Figure 1). The predicted

intron and replication-associated protein (Rep) amino acid

sequence, which is probably expressed from a spliced

complementary-sense mRNA molecule, were tentatively

identified (Supplementary Figures 1 and 4). Conserved

336 J. Hadfield et al.

123

catalytic and ATP-binding domains were identified along

with rolling-circle replication (RCR) motifs (FLTYSKC)

and (SYHLHCLVQ) and the dNTP-binding domain

(CGX4GKTSX30DD) [11]. Putative retinoblastoma-rela-

ted protein-binding (LQQFQ) and oligomerisation domains

(SAESLFPSVPTPY) were also present.

A maximum-likelihood (ML) phylogenetic tree (Fig. 1),

constructed using aligned full-length genomes of members

of candidate mastrevirus species (PhyML [10] with

GTR ? G4 ? I chosen as the best-fit model by RDP3 [15])

and rooted on ECSV, clearly indicates that the B. cathart-

icus-infecting geminivirus should be considered a member

of a new species of mastrevirus and is most closely related

to the other Australian monocot-infecting mastreviruses,

DDSMV and CSMV. Pairwise Hamming- or p-distance

comparisons (Mega 4 [23] with pairwise exclusion of

alignment gaps) indicated that the B. catharticus-infecting

geminivirus genome shares 57.7% nucleotide sequence

identity with DDSMV, 55.3% with CSMV and 43.7% with

MiSV.

The B. catharticus-infecting geminivirus therefore

shares no more than 40.8-57.7% sequence similarity with

any other mastrevirus and thus clearly meets the ICTV

75% identity species demarcation criterion for mastrevi-

ruses. Hence, we propose the name Bromus catharticus

striate mosaic virus (BCSMV) for this new species, with

the descriptor [Australia: Queensland:1999] (BCSMV–

[AU:QL:99]; accession HQ113104).

The four proteins encoded by BCSMV are also most

similar to those of the other two characterised Australian

monocot-infecting mastreviruses (Fig. 2). The BCSMV

Rep shares 48.9-54.2% amino acid identity with the

homologous proteins of CSMV and DDSMV, and 45.3-

49.2% identity with the Reps of other mastrevirus species.

Similarly, the CP is 56.3-58% similar to those of CSMV

and DDSMV and 25.1-42.9% similar to the CPs of all other

Monocot infecting mastreviruses

Dicot infecting mastreviruses

45

50

55

60

65

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75

80

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90

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100

PanSV-C EU224264

PanSV-D EU224265

CpCDPKV AM850136

CpCDSDV AM933134

MSV-A Y00514

MSV-B EU628597

MSV-F EU628629

MSV-G EU628631

MSV-H EU628638

MSV-J EU628641

MSV-C AF007881

MSV-D AF329889

MSV-K EU628643

MSV-E EU628626

MSV-I EU628639

DSV M23022

SSRV-A AF072672

SSRV-B EU244916

ESV EU244915

SSV-A M82918

SSV-B EU244914

SSEV AF239159

USV EU445697

SacSV GQ273988

PanSV-A L396381

PanSV-B X60168

CSMV M20021

DDSMV HM122238

MiSV D01030

BDV-A AM921991

BDV-B FJ620684

WDV AM040732

ODV AM296025

BeYDV AM849096

TbYDV M81103

BCSMV HQ113104

75

94

100

97

100

100

93

90

98

100

100

100

100

61

100

91

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97

100

100

68

99

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100

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60100

100

100

100

100

100

100

0.2

Pan

SV

-C E

U22

4264

Pan

SV

-D E

U22

4265

CpC

DP

KV

AM

8501

36

CpC

DS

DV

AM

9331

34

MS

V-A

Y00

514

MS

V-B

EU

6285

97

MS

V-F

EU

6286

29

MS

V-G

EU

6286

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MS

V-H

EU

6286

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MS

V-J

EU

6286

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MS

V-C

AF

0078

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MS

V-D

AF

3298

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MS

V-K

EU

6286

43

MS

V-E

EU

6286

26

MS

V-I

EU

6286

39

DS

V M

2302

2

SS

RV

-A A

F07

2672

SS

RV

-B E

U24

4916

ES

V E

U24

4915

SS

V-A

M82

918

SS

V-B

EU

2449

14

SS

EV

AF

2391

59

US

V E

U44

5697

Sac

SV

GQ

2739

88

Pan

SV

-A L

3963

81

Pan

SV

-B X

6016

8

CS

MV

M20

021

DD

SM

V H

M12

2238

MiS

VD

0103

0

BD

V-A

AM

9219

91

BD

V-B

FJ6

2068

4

WD

V A

M04

0732

OD

V A

M29

6025

BeY

DV

AM

8490

96

TbY

DV

M81

103

BC

SM

V H

Q11

3104

Per

cent

age

pairw

sie

iden

tity

BA

Origin:AfricaAustraliaEurope & Middle EastJapanVanuatu

Fig. 1 A Maximum-likelihood (ML) tree (based on an alignment of

complete-genome nucleotide sequences) depicting the evolutionary

relationships between BCSMV and representative mastreviruses. The

ML tree was constructed using PhyML [10], with GTR ? G4 ? I

chosen as the best-fit model by RDP3 [15]. The tree was rooted with

ECSV (not shown), an African monocot-infecting virus that should

potentially be assigned to a new geminivirus genus. The numbers

associated with tree branches are indicative of the percentage of 100

full maximum-likelihood bootstrap replicates supporting the existence

of the branches. B Two-dimensional graphical representation of

pairwise genome-wide nucleotide sequence similarities (calculated

with pairwise deletion of gaps; scale represents percentage identity)

between BCSMV and representative mastreviruses

Bromus catharticus striate mosaic virus 337

123

Monocot infecting mastreviruses

Dicot infecting mastreviruses

Rep

BA

cp

rep

C

Percentage pairw

ise identity

PanSV-C EU224264

PanSV-D EU224265

CpCDPKV AM850136

CpCDSDV AM933134

MSV-A Y00514

MSV-B EU628597

MSV-F EU628629

MSV-G EU628631

MSV-H EU628638

MSV-J EU628641

MSV-C AF007881

MSV-D AF329889

MSV-K EU628643

MSV-E EU628626

MSV-I EU628639

DSV M23022

SSRV-A AF072672

SSRV-B EU244916

ESV EU244915

SSV A M82918

SSV-B EU244914

SSEV AF239159

USV EU445697

SacSV GQ273988

PanSV-A L396381

PanSV-B X60168

CSMV M20021

DDSMVHM122238

MiSV D01030

BDV-A AM921991

BDV-B FJ620684

WDV AM040732

ODV AM296025

BeYDV AM849096

TbYDV M81103

BCSMV HQ113104

ECSV FJ665630

Pan

SV

-C E

U22

4264

Pan

SV

-D E

U22

4265

CpC

DP

KV

AM

8501

36

CpC

DS

DV

AM

9331

34

MS

V-A

Y00

514

MS

V-B

EU

6285

97

MS

V-F

EU

6286

29

MS

V-G

EU

6286

31

MS

V-H

EU

6286

38

MS

V-J

EU

6286

41

MS

V-C

AF

0078

81

MS

V-D

AF

3298

89

MS

V-K

EU

6286

43

MS

V-E

EU

6286

26

MS

V-I

EU

6286

39

DS

V M

2302

2

SS

RV

-A A

F07

2672

SS

RV

-B E

U24

4916

ES

V E

U24

4915

SS

V-A

M82

918

SS

V-B

EU

2449

14

SS

EV

AF

2391

59

US

V E

U44

5697

Sac

SV

GQ

2739

88

Pan

SV

-A L

3963

81

Pan

SV

-B X

6016

8

CS

MV

M20

021

DD

SM

VH

M12

2238

MiS

VD

0103

0

BD

V-A

AM

9219

91

BD

V-B

FJ6

2068

4

WD

V A

M04

0732

OD

V A

M29

6025

BeY

DV

AM

8490

96

TbY

DV

M81

103

BC

SM

V H

Q11

3104

EC

SV

FJ6

6563

0

0.5

ECSV FJ66

MSV-A

MSV-H

MSV-F

MSV-G

MSV-B

MSV-I

MSV-E

MSV-J

MSV-C

MSV-D

MSV-K

DSV

USV

SacSV

SSV-A

SSV-B

ESV

SSRV-A

SSRV-B

SSEV

PanSV-A

PanSV-C

PanSV-B

PanSV D

BCSMV

CMSV

DDSMV

MiSV

ODV

BDV-A

WDV

BDV-B

CpCDPKV

CpCDSDV

BeYDV

TbYDV

84

97

87

89

87

71

6365

100

85

81

100

77

100

72

93

70

60

98

100

100

100

100

100

84

100

55

100

100

97

86

0.5

Origin:AfricaAustraliaEurope & Middle EastJapanVanuatu

Monocot infecting mastreviruses

Dicot infecting mastreviruses

CP

MSV-A

MSV-B

MSV-H

MSV-F

MSV-G

MSV-C

MSV-D

MSV-K

MSV-E

MSV-J

MSV-I

USV

SacSV

DSV

SSV-A

SSV-B

SSRV-A

SSRV-B

ESV

SSEV

PanSV-A

PanSV-B

PanSV-C

PanSV-D

BCSMV

CSMV

DDSMV

MiSV

BDV-A

BDV-B

WDV

ODV

ECSV

CpCDSDV

CpCDPKV

BeYDV

TbYDV

64

68

8194

94

86

74

100

93

97

97

79

92

61

95

100

87

100

60

99

100

99

90

99

100

100

72

87

100

70

68

Cicadulina sp.

Nesoclutha pallida

Psammotettix alienus

Orosius argentatus

Orosius orientalis

?

?

Nesoclutha declivata

Cicadulina sp.

0

10

20

30

40

50

60

70

80

90

100

Fig. 2 Maximum-likelihood (ML) phylogenetic relationships based

on alignments of the predicted amino acid sequences of replication-

associated (Rep) (A) and coat (CP) (B) proteins. The ML trees were

constructed with PhyML [10] using the LG model as determined by

ProtTest [1] and rooted by BCTIV (not shown). Numbers associated

with tree branches are indicative of the percentage of 100 full

maximum-likelihood bootstrap replicates supporting the existence of

the branches. (C) Two-dimensional graphical representation of

pairwise amino acid sequence similarities (calculated with pairwise

deletion of gaps; scale represents percentage identity) between the

predicted Rep and CP of BCSMV and those of other representative

mastreviruses

338 J. Hadfield et al.

123

mastreviruses (Fig. 2). It is interesting to note that the CP

and Rep of MiSV are more closely related to those of Asian

and European mastreviruses, as noted previously [3, 27].

The CP of ECSV, a novel geminivirus infecting Eragrostis

curvula from South Africa, is most similar to those of oat

dwarf virus (ODV), barley dwarf virus (BDV) and wheat

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

1 243 472 654 945 1255 1499 1744 2109 2386 2645 2855

CSMV - BCSMV

CSMV - DDSMV

BCSMV - DDSMV

MSV-A

MSV-B

MSV-H

MSV-F

MSV-G

MSV-C

MSV-D

MSV-K

MSV-J

MSV-E

MSV-I

DSV

SSEV

SSV-A

SSV-B

ESV

SSRV-A

SSRV-B

PanSV-A

PanSV-C

PanSV-B

PanSV-D

USV

SacSV

MiSV

BCSMV

DDSMV

CSMV

BDV-A

BDV-B

WDV

ODV

BeYDV

CpCDPKV

CpCDSDV

TbYDV

ECSV

100100

100

100

100

100

100

100

85100

100

100

100

65

71

77

100

100

97

58

100

99

100

97100

100

88

72100

100

9250

100

0.1

MSV-A

MSV-G

MSV-K

MSV-C

MSV-D

MSV-I

MSV-H

MSV-E

MSV-J

MiSV

MSV-F

MSV-B

DSV

USV

CSMV

ECSV

BDV-A

BDV-B

WDV

ODV

TbYDV

CpCDPKV

BeYDV

CpCDSDV

82

83

85

72

SSV-B

BCSMV

DDSMV

SSEV

9371

50

64

PanSV-D

PanSV-A

PanSV-B

PanSV-C

99

77

SacSV

SSV-A

SSRV-B

ESV ZM

SSRV A59

80

55

64

72

52

72

56

0.2

Pai

rwis

e id

entit

y

Position in alignment

1503-1458(non-recombinant region)

1459-1502Recombinant region

A

B

Potential major parent

Potential minor parent

Potential recombinant

mp cprepA

rep

Fig. 3 A Phylogenetic support

(bootstrapped neighbour-joining

trees of the non-recombinant

and recombinant region) for

detection of recombination

amongst the Australian

monocotyledonous-plant-

infecting mastreviruses

BCSMV, DDSMV and CSMV.

B Pairwise identity plots of

BCSMV, DDSMV and CSMV

showing the recombinant region

and recombination breakpoints

Bromus catharticus striate mosaic virus 339

123

dwarf virus (WDV), also as noted previously [27]. The MP

of BCSMV is the most divergent of the encoded proteins,

sharing only 37.8-40.9% identity with the Australian

monocot-infecting mastreviruses and only 11.2-16.9%

similarity with all other mastreviruses (Supplementary

Figure 5).

Recombination has featured heavily in the evolution of

mastreviruses [25, 26], and recombination hot-spots have

been identified in the long- and short-intergenic (non-

coding) regions of mastrevirus genomes [13, 14, 16, 25]. It

was not entirely surprising, therefore, when recombination

analysis of BCSMV along with members of other repre-

sentative mastrevirus species (using RDP3 [15] as descri-

bed previously by Varsani et al. [25, 26]) revealed what

appears to be a small tract of recombination-derived

BCSMV-like sequence (position 1321–1362; Supplemen-

tary Figure 1) within the short intergenic region (SIR) of

DDSMV (p-value: RDP 5.2 9 10-9; GENECOV 1.7 9

10-11; BootScan 1.9 9 10-14; MaxChi 3.6 9 10-7; Chi-

maera 9.7 9 10-6 and 3Seq 9.2 9 10-7). Phylogenetic

support and pairwise identity plots for BCSMV, DDSMV

and CSMV are provided in Fig. 3.

Our determination of the full-genome sequence of

BCSMV has revealed that the depth of genetic diversity

between the Australian striate mosaic mastreviruses most

likely mirrors that found amongst the African streak

mastreviruses. Among the African streak virus species,

Maize streak virus is the only one whose members threaten

agriculture [20], whereas members of the species Wheat

dwarf virus are economically important in Europe and

China. It is therefore perhaps not surprising that no Aus-

tralian monocot-infecting mastreviruses have caused sig-

nificant losses to commercial crops. Nevertheless, the

possibility remains that these viruses could emerge as

significant agricultural pathogens. For example, although

no monocot-infecting mastreviruses have been found

infecting wheat in Australia, BCSMV, CSMV, PSMV and

DDSMV are all transmissible to and produce symptoms in

wheat and related crop species under controlled conditions

[9]. Also, emergent geminiviruses are not unknown in

Australia, with the begomovirus tomato leaf curl virus

causing severe losses to Australian tomato production [22].

Finally, it has been widely speculated that recombination is

a major process contributing to the emergence of novel

mastrevirus pathogens [8, 13, 20, 29], and it is therefore

significant that we have now shown for the first time that

recombination also occurs amongst the Australian mono-

cot-infecting mastreviruses.

GenBank accession - BCSMV –[AU:QL:99]; accession

HQ113104

Acknowledgements This study was partly supported by the Mars-

den fund of New Zealand. R.W.B. is supported by the Higher

Education Commission (HEC), Government of Pakistan, under the

‘‘Foreign Faculty Hiring Program’’.

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