capulavirus and grablovirus: two new genera in the family ... · capulavirus and grablovirus: two...

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Capulavirus and Grablovirus: two new genera in the familyGeminiviridae

Arvind Varsani1,2• Philippe Roumagnac3

• Marc Fuchs4• Jesus Navas-Castillo5

•

Enrique Moriones5• Ali Idris6

• Rob W. Briddon7• Rafael Rivera-Bustamante8

•

F. Murilo Zerbini9 • Darren P Martin10

Received: 20 January 2017 / Accepted: 27 January 2017 / Published online: 17 February 2017

� Springer-Verlag Wien 2017

Abstract Geminiviruses are plant-infecting single-stran-

ded DNA viruses that occur in most parts of the world.

Currently, there are seven genera within the family Gem-

iniviridae (Becurtovirus, Begomovirus, Curtovirus, Era-

grovirus, Mastrevirus, Topocuvirus and Turncurtovirus).

The rate of discovery of new geminiviruses has increased

significantly over the last decade as a result of new

molecular tools and approaches (rolling-circle amplifica-

tion and deep sequencing) that allow for high-throughput

workflows. Here, we report the establishment of two new

genera: Capulavirus, with four new species (Alfalfa leaf

curl virus, Euphorbia caput-medusae latent virus, French

bean severe leaf curl virus and Plantago lanceolata latent

virus), and Grablovirus, with one new species (Grapevine

red blotch virus). The aphid species Aphis craccivora has

been shown to be a vector for Alfalfa leaf curl virus, and

the treehopper species Spissistilus festinus is the likely

vector of Grapevine red blotch virus. In addition, two

highly divergent groups of viruses found infecting citrus

and mulberry plants have been assigned to the new species

Citrus chlorotic dwarf associated virus and Mulberry

mosaic dwarf associated virus, respectively. These species

have been left unassigned to a genus by the ICTV because

their particle morphology and insect vectors are unknown.

Introduction

The family Geminiviridae includes plant-infecting viruses

with circular ssDNA genomes that are encapsidated in

virions comprised of 22 pentameric capsomeres arranged

in a *18- to 30-nm twinned icosahedral (or geminate)

& Arvind Varsani

[email protected]

& Darren P Martin

[email protected]

1 The Biodesign Center for Fundamental and Applied

Microbiomics, Center for Evolution and Medicine and

School of Life Sciences, Arizona State University,

Tempe 85287-5001, AZ, USA

2 Structural Biology Research Unit, Department of Clinical

Laboratory Sciences, University of Cape Town,

Cape Town 7701, South Africa

3 CIRAD-INRA-SupAgro, UMR BGPI, Campus International

de Montferrier-Baillarguet, 34398 Montpellier Cedex-5,

France

4 Section of Plant Pathology and Plant-Microbe Biology,

School of Integrative Plant Science, Cornell University, New

York State Agricultural Experiment Station, Geneva,

NY 14456, USA

5 Instituto de Hortofruticultura Subtropical y Mediterranea ‘‘La

Mayora’’, Universidad de Malaga-Consejo Superior de

Investigaciones Cientıficas (IHSM-UMA-CSIC),

29750 Algarrobo-Costa, Malaga, Spain

6 School of Plant Sciences, University of Arizona, Tucson,

AZ 85721-0107, USA

7 National Institute for Biotechnology and Genetic Engineering

(NIBGE), Faisalabad, Pakistan

8 Departamento de Ingenierıa Genetica, Centro de

Investigacion y de Estudios Avanzados del IPN (Cinvestav),

Unidad Irapuato, 36821 Irapuato, GTO, Mexico

9 Dep. de Fitopatologia/Bioagro, Universidade Federal de

Vicosa, Vicosa, Minas Gerais 36570-900, Brazil

10 Computational Biology Group, Institute of Infectious

Diseases and Molecular Medicine, University of Cape Town,

Cape Town 7925, South Africa

123

Arch Virol (2017) 162:1819–1831

DOI 10.1007/s00705-017-3268-6

http://orcid.org/0000-0003-4111-2415

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configuration [7, 41]. Geminiviruses have a near-global

distribution and infect both monocotyledonous and

dicotyledonous plants. Geminiviruses are often responsible

for serious yield losses in economically important crops,

including tomato, maize, cotton, chickpea and cassava

[25]. Symptoms of geminivirus infections can include

foliar crinkling, curling, yellowing, stunting, mosaic and/or

striations.

The Geminiviridae Study Group of the International

Committee on Taxonomy of Viruses (ICTV) has provided

a series of guidelines for the classification of viruses within

the seven currently recognised genera of the family: Be-

curtovirus, Begomovirus, Curtovirus, Eragrovirus, Mas-

trevirus, Topocuvirus and Turncurtovirus. The criteria

include host range, insect vector, genome organisation and

genome-wide pairwise sequence identities

[1, 11, 12, 26, 38, 39].

Over the last decade, the development of new molecular

tools such as rolling-circle amplification (RCA) and high-

throughput sequencing have greatly facilitated the discov-

ery of novel geminiviruses in a range of cultivated and non-

cultivated host species [29]. Accordingly, these techniques

have accelerated the discovery of highly divergent gemi-

nivirus-like viruses. For some of these viruses, a large

number of closely related full genome sequences have been

determined. Analyses of these sequences (pairwise identi-

ties and phylogenetics), coupled with the identification of

insect vectors and particle morphology, have allowed us to

determine with great confidence that some of these diver-

gent viruses should be classified as members of two new

genera in the family Geminiviridae, which was approved

by the Executive Committee of the ICTV:

1) Capulavirus, which will for now include four

species, Alfalfa leaf curl virus, Euphorbia caput-

medusae latent virus, French bean severe leaf curl

virus and Plantago lanceolata latent virus

[5, 6, 30, 36]

2) Grablovirus, which will for now include one species,

Grapevine red blotch virus [18, 28, 35]

In addition, two other species of highly divergent viruses

that are closely related to geminiviruses have been accep-

ted by the Executive Committee of the ICTV for inclusion

in the family Geminiviridae and will remain unassigned to

a genus, awaiting identification of the vector species and

confirmation of particle morphology. These new species

are:

1) Citrus chlorotic dwarf associated virus [17, 21]

2) Mulberry mosaic dwarf associated virus [23, 24]

Furthermore, recently, a single virus isolated from an

apple tree in China (tentatively referred to as apple gemi-

nivirus; AGmV) [20] and 13 virus isolates from grapevine

in Hungary, Israel, Japan and South Korea (tentatively

referred to as grapevine geminivirus A; GGVA) sharing

[97% pairwise identity have been discovered [2]. These

have distinctly geminivirus-like genome organisations and

are more closely related to members of some established

geminivirus species than they are to citrus chlorotic dwarf

associated virus (CCDaV) and mulberry mosaic dwarf

associated virus (MMCaV). The taxonomic assignment of

AGmV and GGVA still needs to be discussed by the ICTV.

Whereas the arrangements of genes and intergenic

regions in the genomes of curtoviruses, topocuviruses,

turncurtoviruses, AGmV, GGVA and genomes/DNA A

components of begomoviruses are all very similar, the

becurtoviruses, capulaviruses, eragroviruses, grabloviruses

and mastreviruses all have distinctly unique genome

organisations (Fig. 1). Furthermore, the genome organisa-

tion of CCDaV is also apparently unique [21]. Particularly

noteworthy in the CCDaV genome (3640 nt) is the *921-

nt-long virion-sense ORF, V3, which results in the CCDaV

genome being 600-800 nt larger than those of the other

known monopartite geminiviruses (Fig. 1).

Although the genomes of the known geminiviruses can

have up to eight genes, only two of them, the replication-

associated protein gene (rep) and the coat protein gene (cp)

are obviously conserved across viruses in all of the genera,

whereas the replication enhancer gene (ren), symptom

determinant gene (sd) and silencing suppressor gene (ss)

homologues are found in begomoviruses, curtoviruses,

topocuviruses and turncurtoviruses (Fig. 1), and transcrip-

tion activator gene (trap) homologues are additionally

found in eragroviruses (Fig. 1). The genomes of viruses in

all of the established genera also have either proven or

putative movement protein genes (mp), which, in the

monopartite members of the family, are immediately

upstream of cp. It is currently unknown, however, if these

genes in viruses from different genera have a common

evolutionary origin, because the amino acid sequences that

they encode have such low degrees of similarity that it is

not possible to conclude that they are homologous.

The genomes of becurtoviruses, capulaviruses, gra-

bloviruses, eragroviruses, mastreviruses, and CCDaVs all

have two intergenic regions (Fig. 1). In general, the longer

of these is referred to as the long intergenic region (LIR)

and contains a conserved nonanucleotide within a hairpin

structure that forms the origin of virion-strand replication

[3, 22]. Similarly, the shorter intergenic region is referred

cFig. 1 Genome organisation of viruses in the genera of the family

Geminiviridae. Citrus chlorotic dwarf associated virus and Mulberry

mosaic dwarf associated virus have been accepted by the Executive

Committee of the International Committee on Taxonomy of Viruses

(ICTV) as a species within the family Geminiviridae but have not

been assigned to a genus. AGmV and GGVA have not yet been

considered as representatives of a species by ICTV

1820 A. Varsani et al.

123

LIRSIR

cpmp

possible reg

possible mpreg

unknown

reprepArentrap/sspossible trap/sssdpossible sd

V2

V1

C1

C1:C2

Mastreviruses(MSV)V1

C1

V2

C2

Eragroviruses(ECSV)

V1C1

Topocuviruses(TPCTV)

V2C4

C2

C3

Turncurtoviruses(TCTV)

V2

C1

C2

C3

C4

V1

Becurtoviruses(BCTIV)

C1

C1:C2V1

V3

V2

Begomoviruses

Unassigned

Unclassified

V1

C1

C2

C4V2

C3

Monopartite(TYLCV)

AC1

AC2

AC4

AC3

DNA-A(BGMV)

DNA-B(BGMV)

Bipartite

nsp

AV1 BV1

BC1

CRBCRA

CR

V1

C1

C4

C2

V2V3

Curtoviruses(BCTV)

C3

V3

V1

V2

C1:C2

C2

C1

C3

Grabloviruses

C1:C2C1

C3

V4

V3

V4:V2

V1

Capulaviruses

V2 V2V2

V2

V1

V1V1

V1

V3

V4V3

C1

C1:C2

C1:C2

C1

C3

C2

C2

C4

C4

C1

C1

CCDaV MMCaV AGmV

GGVA

The genera Capulavirus and Grablovirus 1821

123

to as the short intergenic region (SIR) and contains tran-

scription termination signals and, for mastreviruses at least,

the origin of complementary-strand replication.

Introns are present in several geminivirus genes. Rep

and RepA proteins in becurtoviruses, capulaviruses, gra-

bloviruses, mastreviruses, MMCaV and CCDaV are either

proven to be, or inferred to be, expressed from alternatively

spliced complementary-sense transcripts [8, 13, 40]

(Fig. 1). Further, an intron occurs in the mp of mastre-

viruses [40], and an intron has been inferred to occur in the

mp of the capulavirus EcmLV (Fig. 1) [5].

Recombination has played a significant role in the

evolution of geminiviruses, and it can therefore be difficult

to accurately infer the evolutionary relationships of viruses

in different genera. Whereas non-homologous recombina-

tion has potentially contributed to the loss or gain of large

genome regions in particular genera, homologous recom-

bination has also likely contributed to the exchange of

genome regions between viruses in different genera

[6, 9, 31, 33].

Nonetheless, we inferred the approximate genome-wide

evolutionary relationships between representative members

of the various established geminivirus genera, CCDaV,

MMCaV, AGmV and GGVA (Fig. 1). The full genome

sequences of these representative viruses were aligned

using MUSCLE [15] and used to infer a neighbor-joining

phylogenetic tree with the Jukes-Cantor nucleotide substi-

tution model and 1000 bootstrap replicates. Branches with

\60% support were collapsed using TreeGraph2 [34], and

the tree was rooted at the midpoint (Fig. 2). From this

phylogenetic tree, it is apparent that the capulaviruses and

grabloviruses are closely related to one another and that

CCDaV and MMCaV are closely related to one another.

We also analysed the evolutionary relationships of the

inferred CP and Rep amino acid sequences of the same set

of representative geminiviruses. The CP and Rep sequence

datasets were aligned using MUSCLE [15] and used to

infer maximum-likelihood phylogenetic trees using

PHYML3.0 [16], applying the WAG?I?G and LG?I?G

substitution model, respectively (selected as the best-fit

models by ProtTest [14]; Fig. 2). Branch support in these

trees was determined using approximate likelihood ratio

tests (aLRT). The Rep phylogenetic tree was rooted with

sequences from the family Genomoviridae [19], whereas

the CP tree was rooted at the midpoint. Branches with

\80% aLRT support were collapsed using TreeGraph2

[34]. Pairwise CP and Rep amino acid sequence identities

were determined using SDT v1.2 [27] (Fig. 3).

Discordance in the phylogenetic placement of cur-

toviruses, becurtoviruses, topocuviruses, eragroviruses,

turncurtoviruses and CCDaV in the CP and Rep phyloge-

netic trees likely reflects the fact that the most recent

common ancestors of the known viruses in these genera are

possibly the products of inter-genus recombination events

[10, 37]. For example, the becurtovirus CPs are most clo-

sely related to those of curtoviruses, whereas the becur-

tovirus Reps are most closely related to those of CCDaV

and MMCaV (Fig. 2 and Fig. 3).

Capulavirus

A group of closely related viruses isolated from Euphorbia

caput-medusae (South Africa), Medicago sativa (France

and Spain), Phaseolus vulgaris (India) and Plantago

lanceolata (Finland) have been assigned to the new genus

Capulavirus. The genus name Capulavirus was derived

from the type member of the genus: euphorbia caput-me-

dusae latent virus. As with viruses in the genera Mastre-

virus and Becurtovirus, capulaviruses have two intergenic

regions and express Rep from a spliced complementary-

strand transcript. In common with begomoviruses and

curtoviruses, they have a large complementary-sense ORF

(C3) that is completely embedded within rep. A unique

feature of capulavirus genomes is a complex arrangement

of possible MP-encoding ORFs located in the 5’direction

from cp (Fig. 1). Two or more of these ORFs may con-

stitute an intron-containing mp (Fig. 1). Geminate particles

have been observed in purified preparations of EcmLV by

transmission electron microscopy [30]. Aphids of the spe-

cies Aphis craccivora have been shown to transmit ALCV

[30]. All known capulaviruses have the nonanucleotide

motif ‘‘TAATATTAC’’ at their presumed origins of virion-

strand replication.

An analysis of the distribution of pairwise identities (one

minus Hamming distances of pairwise aligned sequences

with pairwise deletion of gaps) of known capulavirus

genomes using SDT v1.2 [27] (n = 47; Table 1) indicates

that a pairwise-identity-based species demarcation criterion

that would minimize conflicts (i.e., possible assignments of

cFig. 2 A. Unrooted neighbour-joining tree inferred from aligned full-

genome sequences of representative isolates from various genera in

the family Geminiviridae. Numbers associated with branches indicate

percentage bootstrap support for these branches (determined with

1000 bootstrap replicates). B. Maximum-likelihood phylogenetic tree

(applying the WAG?I?G amino acid substitution model) inferred

from aligned CP sequences of representative isolates from various

genera in the family Geminiviridae. Numbers associate with branches

indicate percentage aLRT support for these branches. The CP

phylogenetic tree is rooted at the midpoint. Branches with less than

80% aLRT support have been collapsed. C. Maximum-likelihood

phylogenetic tree (applying the LG?I?G amino acid substitution

model) inferred from aligned Rep sequences of representative isolates

from various genera in the family Geminiviridae. Numbers associated

with branches indicate percentage aLRT support for these branches.

The Rep phylogenetic tree is rooted with the Rep sequences of

members of the family Genomoviridae (not included here). Branches

with less than 80% aLRT support have been collapsed


123

0.5 amino acid substitutions per site

Becurtovirus

Begomovirus

Capulavirus

unclassified

Curtovirus

Eragrovirus

Grablovirus

Mastrevirus

Topocuvirus

Turncurtovirus

Genera

Turncurtovirus

Curtovirus

Becurtovirus

Eragrovirus

Grablovirus

unclassified

unclassified

unclassified

Mastrevirus

Begomovirus

Capulavirus

Topocuvirus

Turncurtovirus

Curtovirus

Becurtovirus

Eragrovirus

Grablovirus

unclassified

unclassified

Mastrevirus

Begomovirus

CurtovirusBegomovirus

Capulavirus

Topocuvirus

0.1 nucleotide substitutions per site

0.2 amino acid substitutions per site

GU456685 Turnip curly top virus KC108902 Turnip curly top virus

KT388086 Turnip leaf roll virus KT388088 Turnip leaf roll virus

AF379637 Beet curly top virus EU921828 Pepper yellow dwarf virus

KX618694 Grapevine geminivirus A KM386645 Apple geminivirus

FM877473 African cassava mosaic virus JF502373 Cotton leaf curl Burewala virus

X84735 Tomato pseudo-curly top virus FJ665283 Bean golden mosaic virus KC706535 Sida micrantha mosaic virus

GU734126 Spinach severe curly top virus U49907 Horseradish curly top virus

FJ665630 Eragrostis curvula streak virus FJ665634 Eragrostis curvula streak virus

JX559642 Grapevine red blotch virus KF147918 Grapevine red blotch virus

KT214389 Plantago lanceolata latent virus KT214386 Euphorbia caput-medusae latent virus

KT214373 Alfalfa leaf curl virus JX094280 French bean severe leaf curl virus

EF536860 Wheat dwarf virus AF003952 Maize streak virus

KJ437671 Axonopus compressus streak virus DQ458791 Chickpea chlorotic dwarf virus

JQ920490 Citrus chlorotic dwarf associated virus KR131749 Mulberry crinkle-associated virus

HQ443515 Spinach curly top Arizona virus KP410285 Beet curly top Iran virus

10096100

99

9491

100

10091

96

100

96

100

100

100

91100

84

8290100

97

10099

82

AF379637 Beet curly top virus EU921828 Pepper yellow dwarf virus U49907 Horseradish curly top virus

GU734126 Spinach severe curly top virus KP410285 Beet curly top Iran virus

HQ443515 Spinach curly top Arizona virus GU456685 Turnip curly top virus KC108902 Turnip curly top virus


AF003952 Maize streak virus KJ437671 Axonopus compressus streak virus

DQ458791 Chickpea chlorotic dwarf virus EF536860 Wheat dwarf virus


X84735 Tomato pseudo-curly top virus JX094280 French bean severe leaf curl virus

KT214373 Alfalfa leaf curl virus KT214386 Euphorbia caput-medusae latent virus

KT214389 Plantago lanceolata latent virus KM386645 Apple geminivirus

KX618694 Grapevine geminivirus A JX559642 Grapevine red blotch virus

KF147918 Grapevine red blotch virus JQ920490 Citrus chlorotic dwarf associated virus

KR131749 Mulberry crinkle-associated virus FJ665283 Bean golden mosaic virus KC706535 Sida micrantha mosaic virus

FM877473 African cassava mosaic virus JF502373 Cotton leaf curl Burewala virus

100

100

85

9199

99

99

9589100

91

92100

88

97

97

99

10096

93

98

88

92

KP410285 Beet curly top Iran virus HQ443515 Spinach curly top Arizona virus

U49907 Horseradish curly top virus GU734126 Spinach severe curly top virus

AF379637 Beet curly top virus EU921828 Pepper yellow dwarf virus

KC108902 Turnip curly top virus GU456685 Turnip curly top virus


KM386645 Apple geminivirus KX618694 Grapevine geminivirus A

X84735 Tomato pseudo-curly top virus FM877473 African cassava mosaic virus

JF502373 Cotton leaf curl Burewala virus FJ665283 Bean golden mosaic virus KC706535 Sida micrantha mosaic virus


EF536860 Wheat dwarf virus DQ458791 Chickpea chlorotic dwarf virus

KJ437671 Axonopus compressus streak virus AF003952 Maize streak virus

KF147918 Grapevine red blotch virus JX559642 Grapevine red blotch virus

JQ920490 Citrus chlorotic dwarf associated virus KR131749 Mulberry crinkle-associated virus

KT214389 Plantago lanceolata latent virus JX094280 French bean severe leaf curl virus KT214373 Alfalfa leaf curl virus

KT214386 Euphorbia caput-medusae latent virus

100

100

100

100

100

100

100100

94

100

100100

100

100

100

6893

100

100

100100

6789

CP

Rep

Genome


123

individual isolates to two or more species) could be placed

either in the 72 to 84% identity interval, or in the 87-94%

interval (Fig. 4). Whereas a species demarcation threshold

within the 87-94% range would yield five species, placing

it within the 72-84% range would yield four species. In the

case of a threshold within the 87-94% range, the alfalfa leaf

curl virus (ALCV) sequences, which have all been isolated

from alfalfa plants, would be split into two species. Given

that there seems to be no good biological reason to split the

ALCVs into two species, we have opted to tentatively

place the species demarcation threshold in the 72-84%

range. To bring the capulavirus species demarcation

threshold in line with that of the genus Mastrevirus (the

recognized genus of geminiviruses that the capulaviruses

are most closely related to; Fig. 4) we have opted to ten-

tatively select 78% as the pairwise identity value above

which two sequences should be considered isolates of the

same species. The four proposed capulavirus species to

which the 47 known capulavirus full genome

sequences (Table 1) have been assigned are Alfalfa leaf

curl virus (n = 26), Euphorbia caput-medusae latent virus

(n = 17), French bean severe leaf curl virus (n = 2) and

Plantago lanceolata latent virus (n = 2). Based on pair-

wise identity comparisons, all isolates (ALCV; EcmLV;

french bean severe leaf curl virus, FbSLCV; plantago

lanceolata latent virus, PlLV) within each of these species

share between 63% and 73% genome-wide sequence

identity with all isolates that have been assigned to other

proposed capulavirus species (Fig. 2).

Regardless of whether the full-genome nucleotide

sequence, the inferred Rep amino acid sequence, or the

inferred CP amino acid sequence is considered, all of the

viruses belonging to the proposed capulavirus species

group with 100% aLRT support with other proposed

capulaviruses (Fig. 2). The viruses assigned to the genus

Capulavirus share\22% CP amino acid sequence identity

and\45% Rep amino acid sequence identity with viruses

in other established genera of the family Geminiviridae

(Fig. 3).

Grablovirus

A group of closely related viruses discovered infecting

grapevines in Canada, South Korea and the USA have been

assigned to the genus Grablovirus. The genus name is

based on the name of the type member: grapevine red

blotch virus (GRBV), the first and currently the only

member of this genus [18]. These viruses have the virion-

strand origin of replication nonanucleotide motif TAA-

TATTAC and a unique genome arrangement (Fig. 1;

Table 2). The natural vector is likely the three-cornered

alfalfa treehopper (Spissistilus festinus Say) [4].

Analysis of the 27 known grablovirus full-genome

sequences indicate that they all share[91% genome-wide

nucleotide sequence identity (Fig. 5) and are therefore all

assigned to the species Grapevine red blotch virus. All of

the GRBV isolates share\45% Rep amino acid sequence

identity with all viruses in other geminivirus genera

(Fig. 3). Regardless of whether the full-genome nucleotide

sequence, Rep amino acid sequence or CP amino acid is

considered, the GRBV isolates cluster together with 100%

aLRT support (Fig. 2).

In the absence of additional related sequences in the

genus, we suggest that, based on the species demarcation

criteria used for most other geminivirus genera, grablovirus

isolates sharing\80% genome-wide pairwise identity with

members of accepted grablovirus species should be clas-

sified as members of distinct grablovirus species. This is a

tentative species demarcation criterion that will need to be

refined as more full-genome sequences of grabloviruses are

determined.

New geminivirus species that remain unassignedto a genus

Citrus chlorotic dwarf associated virus and Mulberry

mosaic dwarf associated virus

Two complete CCDaV genomes, isolated from citrus trees

in Turkey (JQ920490) [21] and China (KF561253), and

eight complete MMCaV genomes, isolated from mulberry

bushes in China (KP303687, KP699128-KP699132,

KP728254, KR131749) [23, 24], are clearly closely related

to those of geminiviruses, based on both their geminivirus-

like genome organization and the fact that their inferred

Rep and CP amino acid sequences cluster phylogenetically

with those of the known geminiviruses (Fig. 1 and Fig. 2).

All known CCDaV and MMDaV isolates also have the

nonanucleotide TAATATTAC, which is characteristic of

the virion-strand origin of replication of the majority of

geminiviruses.

The two CCDaV sequences share 99.5% genome-wide

pairwise identity, whereas the eight MMDaV sequences

share[97% identity. The predicted Rep proteins of these

CCDaV and MMDaV isolates share *58% amino acid

sequence similarity with one another, but only 33-42%

similarity with those of other geminiviruses (Fig. 3).

Regardless of whether full genome nucleotide sequences,

inferred Rep amino acid sequences, or inferred CP

amino acid sequences are considered, the two proposed

species group separately from all other geminiviruses,

with 100% aLRT branch support (Fig. 2).


123

Rep

CP

Becurtovirus

Begomovirus

Capulav

irus

Curtovirus

Eragrovirus

Grablov

irus

Mastrevirus

Topocuvirus

Turncurtovirus

Uncla

ssifie

d

Becurtovirus

Begomovirus

Capulavirus

Curtovirus

Eragrovirus

Grablovirus

Mastrevirus

Topocuvirus

Turncurtovirus

Unclassified

French bean severe leaf curl virus [JX094280] Alfalfa leaf curl virus [KT214373]

Euphorbia caputmedusae latent virus [KT214386]Plantago lanceolata latent virus [KT214389 ]

Maize streak virus [AF003952] Axonopus compressus streak virus [KJ437671]

Wheat dwarf virus [EF536860] Chickpea chlorotic dwarf virus [DQ458791] Eragrostis curvula streak virus [FJ665630] Eragrostis curvula streak virus [FJ665634]

Beet curly top virus [AF379637] Beet curly top virus [EU921828]

Horseradish curly top virus [U49907] Spinach severe curly top virus [GU734126]

Spinach curly top Arizona virus [HQ443515] Beet curly top Iran virus [KP410285]

Turnip curly top virus [GU456685] Turnip curly top virus [KC108902]

Turnip leaf roll virus [KT388086] Turnip leaf roll virus [KT388088]

Tomato pseudocurly top virus [X84735] Bean golden mosaic virus [FJ665283]

Sida micrantha mosaic virus [KC706535] Cotton leaf curl Burewala virus [JF502373] African cassava mosaic virus [FM877473]

Citrus chlorotic dwarf associated virus [JQ920490] Mulberry mosaic dwarf associated virus [KP303687]

Apple geminivirus [KM386645] Grapevine geminivirus A [KX618694]

Grapevine red blotch virus [JX559642] Grapevine red blotch virus [KF147918]

Fre

nch b

ean s

ever

e lea

f cur

l viru

s [JX

0942

80]

Alfa

lfa le

af cu

rl viru

s [KT

2143

73]

Eup

horb

ia ca

putm

edus

ae la

tent v

irus [

KT21

4386

] P

lantag

o lan

ceola

ta lat

ent v

irus [

KT21

4389

] M

aize s

treak

viru

s [AF

0039

52]

Axo

nopu

s com

pres

sus s

treak

viru

s [KJ

4376

71]

Whe

at dw

arf v

irus [

EF53

6860

] C

hickp

ea ch

loroti

c dwa

rf vir

us [D

Q458

791]

Era

gros

tis cu

rvula

strea

k viru

s [FJ

6656

30]

Era

gros

tis cu

rvula

strea

k viru

s [FJ

6656

34]

Bee

t cur

ly top

viru

s [AF

3796

37]

Bee

t cur

ly top

viru

s [EU

9218

28]

Hor

sera

dish c

urly

top vi

rus [

U499

07]

Spin

ach s

ever

e cur

ly top

viru

s [GU

7341

26]

Spin

ach c

urly

top A

rizon

a viru

s [HQ

4435

15]

Bee

t cur

ly top

Iran

viru

s [KP

4102

85]

Turn

ip cu

rly to

p viru

s [GU

4566

85]

Turn

ip cu

rly to

p viru

s [KC

1089

02]

Turn

ip lea

f roll

viru

s [KT

3880

86]

Turn

ip lea

f roll

viru

s [KT

3880

88]

Toma

to ps

eudo

curly

top v

irus [

X847

35]

Bea

n gold

en m

osaic

viru

s [FJ

6652

83]

Sida

micr

antha

mos

aic vi

rus [

KC70

6535

] C

otton

leaf

curl B

urew

ala vi

rus [

JF50

2373

] A

frican

cass

ava m

osaic

viru

s [FM

8774

73]

Citru

s chlo

rotic

dwar

f ass

ociat

ed vi

rus [

JQ92

0490

] M

ulber

ry mo

saic

dwar

f ass

ociat

ed vi

rus [

KP30

3687

] A

pple

gemi

niviru

s [KM

3866

45]

Gra

pevin

e gem

inivir

us A

[KX6

1869

4] G

rape

vine r

ed bl

otch v

irus [

JX55

9642

] G

rape

vine r

ed bl

otch v

irus [

KF14

7918

]

Pairwise identity (%)

100

91

83

74

66

57

48

40

31

23

14

78 72 48 24 26 25 23 26 26 25 26 24 23 24 24 24 23 23 24 21 26 24 20 24 24 24 22 23 19 2275 75 47 22 23 24 23 26 25 25 24 22 20 22 24 25 25 26 23 23 23 24 20 24 25 26 23 23 21 2480 77 53 23 24 24 25 24 24 24 24 24 24 22 24 22 22 24 25 22 24 23 20 23 26 23 24 23 20 2069 68 73 24 24 24 24 26 26 25 25 24 24 24 23 27 28 22 21 23 21 21 23 22 25 22 24 24 24 2439 44 40 38 39 35 36 34 34 28 28 26 25 28 25 28 28 28 28 27 21 21 19 20 22 23 21 21 22 2541 43 44 43 46 35 34 35 35 24 24 22 23 22 22 28 28 26 27 23 20 19 23 20 21 24 22 25 25 2439 40 40 39 47 47 36 45 44 24 28 29 29 29 26 24 24 26 29 26 22 21 19 20 16 23 20 19 25 2444 45 45 44 49 51 48 35 35 29 29 29 28 31 30 25 26 27 26 24 20 22 23 24 19 24 23 27 22 2339 43 39 42 31 36 32 35 98 27 27 29 25 26 26 27 27 27 27 28 21 22 20 21 17 21 19 21 26 2639 42 40 42 31 37 32 35 91 27 27 29 23 26 26 29 29 27 28 28 21 23 21 21 17 21 19 21 26 2638 38 40 36 32 36 37 36 42 43 93 81 82 85 79 41 41 42 41 23 25 29 24 28 24 30 14 24 23 2336 38 37 37 34 37 34 37 43 42 66 84 82 84 78 40 40 41 41 24 25 29 23 28 22 29 19 24 24 2342 42 41 40 33 34 35 37 45 46 56 56 77 82 76 44 44 40 43 24 25 28 23 28 23 27 18 23 25 2342 45 44 40 35 39 36 38 46 47 56 55 79 86 82 45 45 42 43 24 26 26 26 26 24 28 20 22 24 2334 37 34 35 32 36 31 38 31 31 31 31 29 34 84 45 45 43 42 24 25 29 27 27 23 28 15 21 24 2433 37 34 37 33 36 33 38 32 31 31 32 29 33 86 41 41 40 40 23 27 27 26 27 22 29 19 26 24 2137 40 40 39 33 36 35 34 42 41 62 65 49 49 32 32 99 79 77 28 21 20 24 25 24 24 26 27 27 2637 40 40 39 33 36 35 35 41 40 63 66 49 49 32 32 93 81 77 28 21 19 24 21 23 24 24 27 27 2636 38 38 38 33 37 37 37 41 41 64 66 53 53 33 31 76 75 96 24 23 22 21 20 23 23 18 24 24 2639 41 42 38 36 37 34 36 42 42 64 59 53 55 33 30 68 66 75 24 20 20 22 20 20 23 21 24 24 2439 39 40 36 35 38 36 38 45 45 71 65 60 59 33 32 62 61 65 62 21 24 23 24 21 23 19 22 23 2038 39 40 38 30 36 34 35 44 44 64 63 59 59 30 28 58 57 63 59 75 93 75 70 31 29 17 19 23 2237 37 37 36 30 37 31 36 42 42 67 62 60 57 31 29 60 59 64 60 76 80 75 71 31 29 19 19 23 2438 39 41 38 34 36 37 35 41 42 66 58 52 52 30 29 56 56 58 60 70 67 67 74 29 29 18 22 23 2438 41 39 37 35 36 36 35 44 44 60 57 52 52 34 32 59 57 60 57 65 63 65 79 32 30 17 21 25 2437 39 40 39 35 40 37 39 38 37 36 34 33 35 40 38 39 40 40 38 39 37 36 36 37 38 21 23 21 1939 42 42 40 35 41 37 37 39 39 37 36 33 38 42 42 35 36 34 39 36 34 34 35 33 53 21 27 26 2740 40 40 39 34 37 34 35 46 45 57 55 52 50 30 29 55 54 56 54 63 59 59 68 64 37 34 48 25 2436 36 35 34 33 35 32 34 45 45 58 57 49 53 30 30 57 55 55 57 60 59 60 62 62 33 35 60 24 2544 45 44 44 39 38 36 39 38 39 38 40 33 40 31 29 36 37 38 39 39 37 37 38 39 39 40 35 38 9644 45 44 45 39 39 36 40 38 38 39 41 34 40 31 32 37 38 39 39 40 37 38 38 39 39 40 35 39 91

Fig. 3 Pairwise identities of the Rep and CP sequences of representative isolates from various genera in the family Geminiviridae as determined

using SDT v1.2 (Muhire et al., 2014)


123

Table 1 Details of virus isolates that have been assigned to the four proposed species within the genus Capulavirus

Capulavirus Accession no. Virus acronym Isolate Country Host

Alfalfa leaf curl virus KP732474 ALCV 44-1E France Medicago sativa

KT214350 ALCV TDV14_44-16 France Medicago sativa

KT214351 ALCV PB14_LUZ166 France Medicago sativa

KT214352 ALCV ASS14_Assas2 France Medicago sativa

KT214353 ALCV BON14_LUZ075 France Medicago sativa

KT214354 ALCV SSL14_Toul1 France Medicago sativa

KT214355 ALCV ALB14_LUZ147 France Medicago sativa


KT214357 ALCV SSL14_Toul7 France Medicago sativa

KT214358 ALCV TDV12_48-2A France Medicago sativa


KT214360 ALCV ASS14_Assas1 France Medicago sativa

KT214361 ALCV VAU14_LUZ136 France Medicago sativa

KT214362 ALCV GAG14_LUZ193 France Medicago sativa



KT214365 ALCV PB14_LUZ-GS4 France Medicago sativa




KT214369 ALCV PB14_LUZ-GS6 France Medicago sativa

KT214370 ALCV BON14_LUZ076 France Medicago sativa



KT214373 ALCV VAU14_LUZ142 France Medicago sativa

KT214374 ALCV PB14_GS8 France Medicago sativa


Euphorbia caput-medusae latent virus HF921459 EcmLV Dar10 South Africa Euphorbia caput-medusae

HF921460 EcmLV Dar11 South Africa Euphorbia caput-medusae

HF921477 EcmLV Lap11 South Africa Euphorbia caput-medusae

KT214376 EcmLV DAR12_CM243 South Africa Euphorbia caput-medusae








KT214384 EcmLV PAT12_CM96 South Africa Euphorbia caput-medusae





French bean severe leaf curl virus JX094280 FbSLCV FbSLCV-1 India Phaseolus vulgaris

JX094281 FbSLCV FbSLCV-2 India Phaseolus vulgaris

Plantago lanceolata latent virus KT214389 PlLV ALA13_Pl11 Finland Plantago lanceolata

KT214390 PlLV ALA13_Pl5 Finland Plantago lanceolata


123

Pairw

ise

iden

tity

(%)

100 96 93 89

85

81 78 74 70 67 63

100

99

95

100

100

100

100

100

7771

65

100

100

100

99

100

87

100


0.00

0.05

0.10

0.15

0.20

10099989796959493929190898887868584838281807978777675747372717069686766656463626160Percentage identity

Prop

ortio

n of

per

cent

age

pairw

ise

iden

titie

sA

BFbSLCV [JX094280]FbSLCV [JX094281]

ALCV [KP732474]ALCV [KT214353]ALCV [KT214352]ALCV [KT214354]ALCV [KT214357]ALCV [KT214355]ALCV [KT214356]ALCV [KT214350]ALCV [KT214374]ALCV [KT214351]ALCV [KT214373]ALCV [KT214365]ALCV [KT214369]ALCV [KT214367]ALCV [KT214371]ALCV [KT214364]ALCV [KT214366]ALCV [KT214358]ALCV [KT214362]ALCV [KT214363]ALCV [KT214375]ALCV [KT214359]ALCV [KT214368]ALCV [KT214360]ALCV [KT214361]ALCV [KT214370]ALCV [KT214372]

EcmLV [KT214378]EcmLV [HF921459]

EcmLV [KT214381]EcmLV [KT214387]EcmLV [HF921460]EcmLV [KT214383]EcmLV [KT214377]EcmLV [KT214379]EcmLV [KT214376]EcmLV [KT214382]EcmLV [KT214380]EcmLV [KT214388]EcmLV [KT214385]EcmLV [KT214386]EcmLV [HF921477]EcmLV [KT214384]

PlLV [KT214389]PlLV [KT214390]

FbSL

CV [J

X094

280]

FbSL

CV [J

X094

281]

ALCV

[KP7

3247

4]AL

CV [K

T214

353]

ALCV

[KT2

1435

2]AL

CV [K

T214

354]

ALCV

[KT2

1435

7]AL

CV [K

T214

355]

ALCV

[KT2

1435

6]AL

CV [K

T214

350]

ALCV

[KT2

1437

4]AL

CV [K

T214

351]

ALCV

[KT2

1437

3]AL

CV [K

T214

365]

ALCV

[KT2

1436

9]AL

CV [K

T214

367]

ALCV

[KT2

1437

1]AL

CV [K

T214

364]

ALCV

[KT2

1436

6]AL

CV [K

T214

358]

ALCV

[KT2

1436

2]AL

CV [K

T214

363]

ALCV

[KT2

1437

5]AL

CV [K

T214

359]

ALCV

[KT2

1436

8]AL

CV [K

T214

360]

ALCV

[KT2

1436

1]AL

CV [K

T214

370]

ALCV

[KT2

1437

2]

EcmL

V [K

T214

378]

EcmL

V [H

F921

459]

EcmL

V [K

T214

381]

EcmL

V [K

T214

387]

EcmL

V [H

F921

460]

EcmL

V [K

T214

383]

EcmL

V [K

T214

377]

EcmL

V [K

T214

379]

EcmL

V [K

T214

376]

EcmL

V [K

T214

382]

EcmL

V [K

T214

380]

EcmL

V [K

T214

388]

EcmL

V [K

T214

385]

EcmL

V [K

T214

386]

EcmL

V [H

F921

477]

EcmL

V [K

T214

384]

PlLV

[KT2

1438

9]Pl

LV [K

T214

390]

Fig. 4 A. Distribution of pairwise nucleotide sequence identities of

47 known capulavirus genomes. B. Genome-wide pairwise identities

determined using SDT v1.2 [27] and a neighbor-joining phylogenetic

tree of capulavirus isolates. The tree is rooted with mastrevirus

genome sequences (not shown)


123

CCDaV and MMDaV will need to remain unassigned to

a genus until their respective vector species are identified

and/or it is confirmed that they form geminate particles.

New geminiviruses identified recently that needto be reviewed by ICTV

Apple geminivirus and grapevine geminivirus A

One AGmV complete genome isolated from an apple tree

in China (accession no. KM386645) [20] and thirteen

GGVA complete genomes isolated from grapevine in

China (KX570611), Hungary (KX570618), Israel

(KX618694), Japan (KX570610, KX570612, KX570613,

KX570615, KX570616, KX570617) and South Korea

(KX570607, KX570609, KX570614) group together, with

94% bootstrap support (Fig. 2). These viruses isolated from

woody plants contain the typical geminivirus-like

nanonucleotide motif TAATATTAC and display a dis-

tinctly geminivirus-like genome organisation. In addition,

these viruses are clearly recombinant, with a begomovirus-

like Rep (sharing 59-68% amino acid sequence identity)

and a divergent CP that is unlike that of any known

geminivirus.

The thirteen GGVA sequences share[97% identity. The

unique AGmV sequence and the thirteen GGVA sequences

share*63%genome-wide pairwise identity. TheRep andCP

sequences of theAGmVandGGVA isolates share*60%and

48% amino acid sequence identity, respectively, with one

another. The Rep proteins are most closely related to those of

begomoviruses, curtoviruses, topocuvirus and turncur-

toviruses, sharing 50-68% identity (Fig. 3). Although, based

Table 2 Details of virus isolates that have been assigned to the proposed species Grapevine red blotch virus within the genus Grablovirus

Grablovirus Accession no. Virus acronym Isolate Country Host

Grapevine red blotch virus KF147916 GRBV NY175 USA1 Vitis vinifera

KU564249 GRBV NY701 USA2 Vitis vinifera cv.Cabernet Sauvignon

JQ901105 GRBV JRT[456]17NOV10 USA3 Vitis vinifera

KC896623 GRBV CF214-1 USA Vitis vinifera

KC896625 GRBV Z1A-1 USA Vitis vinifera

KF137562 GRBV OR1a USA4 Vitis vinifera cv. Pinot noir

KF147917 GRBV NY135 USA5 Vitis vinifera

KF147918 GRBV NY137 USA5 Vitis vinifera

KF751708 GRBV NY147 USA3 Vitis vinifera cv. Pinot Noir

KP221559 GRBV 1 USA Vitis vinifera cv. Early Burgundy

KU564247 GRBV NY699 USA2 Vitis californica x Vitis vinifera hybrid


KU564250 GRBV NY702 USA2 Vitis vinifera cv. Merlot

KU564251 GRBV NY703 USA2 Vitis vinifera cv. Cabernet franc






JX559642 GRBV 3138-03 Canada Vitis vinifera

KC896624 GRBV CS337-1 USA Vitis vinifera

KF147915 GRBV NY271 USA Vitis vinifera

KU821056 GRBV SW6 South Korea Vitis vinifera

KC427993 GRBV GiGV-WA-RS USA Vitis vinifera

KC427994 GRBV GiGV-WA-DS USA Vitis vinifera

KC427995 GRBV GiGV-WA-MR USA Vitis vinifera cv. Merlot

KC427996 GRBV GiGV-WA-CF USA Vitis vinifera cv. Cabernet franc

US state: 1MD, 2CA, 3NY, 4OR, 5PA


123

on inferred Rep, AGmV and GGVA branch with bego-

moviruses, both viruses group separately from all other

geminiviruses, with 100% aLRT branch support (Fig. 2),

based on the inferred CP amino acid sequences.

AGmV and GGVA must also remain unassigned to a

genus until the vectors are identified and/or geminate par-

ticles are observed.

Concluding remarks

The past ten years have seen the establishment of five new

geminivirus genera, and the next ten will likely see many

more being established as metagenomics-based approaches

begin enabling the convenient and cost-effective discovery

of viruses in greater numbers from cultivated and non-

Pairw

ise

iden

tity

(%)

100

99

98

97

96

96

95

94

93

92

91

95

100

86

100

98


0.0

0.1

0.2

0.3

0.4

0.5

10099989796959493929190Percentage identity

Prop

ortio

n of

per

cent

age

pairw

ise

iden

titie

sA

B GBRV [JX559642]GBRV [JQ901105]GBRV [KC896625]GBRV [KC896623]GBRV [KU564255]GBRV [KF137562]GBRV [KF751708]GBRV [KP221559]GBRV [KU564247]GBRV [KU564248]GBRV [KU564250]GBRV [KU564254]GBRV [KU564251]GBRV [KU564252]GBRV [KU564253]GBRV [KU564256]GBRV [KC427993]GBRV [KC427994]GBRV [KC427995]GBRV [KC427996]GBRV [KF147916]GBRV [KF147915]GBRV [KU564249]GBRV [KC896624]GBRV [KU821056]GBRV [KF147917]GBRV [KF147918]

GBRV

[JX5

5964

2]GB

RV [J

Q901

105]

GBRV

[KC8

9662

5]GB

RV [K

C896

623]

GBRV

[KU5

6425

5]GB

RV [K

F137

562]

GBRV

[KF7

5170

8]GB

RV [K

P221

559]

GBRV

[KU5

6424

7]GB

RV [K

U564

248]

GBRV

[KU5

6425

0]GB

RV [K

U564

254]

GBRV

[KU5

6425

1]GB

RV [K

U564

252]

GBRV

[KU5

6425

3]GB

RV [K

U564

256]

GBRV

[KC4

2799

3]GB

RV [K

C427

994]

GBRV

[KC4

2799

5]GB

RV [K

C427

996]

GBRV

[KF1

4791

6]GB

RV [K

F147

915]

GBRV

[KU5

6424

9]GB

RV [K

C896

624]

GBRV

[KU8

2105

6]GB

RV [K

F147

917]

GBRV

[KF1

4791

8]

Fig. 5 A. Distribution of pairwise nucleotide sequence identities of

27 grablovirus genomes. B. Genome-wide pairwise identities deter-

mined using SDT v1.2 [27] and a neighbor-joining phylogenetic tree

of grablovirus isolates. The tree is rooted with mastrevirus genome

sequences (not shown)


123

cultivated plant host species [29, 32]. As well as illumi-

nating the actual diversity of geminiviruses and the role

played by recombination in their evolutionary history, such

approaches also have the potential to elucidate the full

range of geminivirus host and vector species. Knowing

where geminiviruses are found (especially in non-culti-

vated hosts where they may cause no obvious disease

symptoms) and how they are transmitted will not only

enable prediction of which geminiviruses could pose seri-

ous threats to agriculture but also provide a detailed view

of the actual role of geminiviruses in natural and disturbed

terrestrial ecosystems.

Disclaimer This article is based on the taxonomic proposal

2016.014a-iP.A.v2.Geminiviridae_2gen.pdf, which has been consid-

ered and approved by the Executive Committee (EC) of the ICTV.

A.V. and F.M.Z. are elected members of the ICTV EC. A.V., D.P.M.,

P.R., J.N.-C., E.M., A.I., R.W.B., R.R.-B. and F.M.Z. are current

members of the Geminiviridae study group of the ICTV.

Compliance with ethical standards

There are no conflicts of interest; the research did not involve human

participants or animals. The data used for the analyses in this

manuscript are publicly available in GenBank.

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