Arch Virol DOI 10.1007/s00705-014-1996-4

ANNOTATED SEQUENCE RECORD

Complete genome sequence of Jacquemontia yellow mosaic virus, a novel begomovirus from Venezuela related to other New World bipartite begomoviruses infecting Convolvulaceae Elvira Fiallo-Olive´ • Dorys T. Chirinos • Francis Geraud-Pouey • Enrique Moriones Jesu´s Navas-Castillo



Received: 30 September 2013 / Accepted: 17 January 2014 Ó Springer-Verlag Wien 2014

Abstract The complete genome of a bipartite begomovirus (genus Begomovirus, family Geminiviridae) infecting Jacquemontia sp. (Convolvulaceae) in Venezuela has been cloned and sequenced. Sequence comparison and phylogenetic analysis have shown that it represents an isolate of a novel species with closest relatives being two New World bipartite begomoviruses that infect Convolvulaceae, Jacquemontia mosaic Yucatan virus and Merremia mosaic virus. The DNA-As of these begomoviruses, however, share only 77.0-78.4 % nucleotide sequence identity with the DNA-A of the isolate described here, for which a recombinant origin is suggested. Based on the symptoms observed in the field, the name Jacquemontia yellow mosaic virus (JacYMV) is proposed for this novel bipartite begomovirus.

The genus Begomovirus is by far the largest of the seven genera included in the family Geminiviridae of plant viruses [1, 3]. Begomoviruses have a circular singlestranded DNA (ssDNA) genome encapsidated in twinned quasi-icosahedral (geminate) virions, and most have a bipartite genome [3]. Both genome components, referred to as DNA-A and DNA-B, are of similar size (2.5–2.7 kb).

E. Fiallo-Olive´  E. Moriones  J. Navas-Castillo (&) Instituto de Hortofruticultura Subtropical y Mediterra´nea La Mayora, Universidad de Ma´laga-Consejo Superior de Investigaciones Cientı´ficas (IHSM-UMA-CSIC), Estacio´n Experimental La Mayora, Algarrobo-Costa 29750, Ma´laga, Spain e-mail: [email protected] D. T. Chirinos  F. Geraud-Pouey Universidad del Zulia, Maracaibo 2005, Zulia, Venezuela

The DNA-A virion-sense strand encodes the coat protein and the precoat V2 protein, the latter being absent in the New World begomoviruses. The DNA A complementarysense strand encodes the replication-associated protein (Rep), the transcriptional activator protein, the replication enhancer protein, and the C4 protein. DNA-B encodes the nuclear shuttle protein on the virion-sense strand and movement protein on the complementary-sense strand. Rep initiates viral DNA replication by binding to reiterated motifs (iterons) and by introducing a nick into the nonanucleotide TAATATT/AC within the intergenic region (IR). A common region (CR) located within the IR exhibits a high degree of sequence identity between genome components of each bipartite begomovirus. Begomoviruses are transmitted by the whitefly (Hemiptera: Aleyrodidae) Bemisia tabaci and many cause important emergent diseases in vegetable, tuber and fiber crops worldwide [12]. Convolvulaceae, also known as the morning-glory family, comprises 1600–1700 species grouped into 55–60 genera [13]. The family, while primarily tropical, is almost ubiquitous, with many genera endemic to individual continents. Ipomoea is the largest genus in the family, with over 500 species, and includes the sweet potato (Ipomoea batatas), the second most important root crop worldwide. Ipomoea spp. (including I. batatas) and Merremia spp. have been shown to be hosts to a unique group of begomoviruses, the sweepoviruses, which cluster separately from the major Old World and New World begomovirus clades that include most begomoviruses reported to date [2, 8]. In addition, Merremia sp. has been found to be infected in Puerto Rico by a typical New World bipartite begomovirus, Merremia mosaic virus (MerMV) (GenBank accession nos. for DNA-A AF068636, DQ644558 and DQ644557). MerMV isolates have also been found infecting tomato in Venezuela [11], and these were

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previously named ‘‘tomato mosaic leaf curl virus’’ [3]. Recently, a New World bipartite begomovirus, Jacquemontia mosaic Yucatan virus (JacMYuV), has been reported, isolated from a member of another genus of Convolvulaceae in Mexico, Jacquemontia pentantha (JQ821386). In the last few years, surveys were carried out throughout Venezuela, searching for wild plants exhibiting symptoms suggestive of begomoviral infection. In this work, we analyzed a Jacquemontia sp. plant (sample #1250) with yellow mosaic symptoms (Fig. 1A) collected in the state of Monagas on January 2009. Total DNA was extracted from one leaf [4] and used as a template for rolling-circle amplification (RCA) using u29 DNA polymerase (TempliPhi kit, GE Healthcare). The amplified DNA was digested with a set of restriction enzymes

A

B

C

100 97

97 MerMV AF068636 100 MerMV DQ644557

MerMV DQ644558 MerMV AY508991 ToYMLCV AY508993 ToGMoV EF501976

JacYMV KF661331

97 95 99 98

98 99

83 100

JacMYuV JQ821386 CabLCJV DQ178608 SiYMoV HQ822123 ToYLDV FJ174698 CoYSV DQ875868 BCMV JN848772 DLDV JN848773 PYMTV AF039031 EACMV AJ717542

0.05

Fig. 1 (A) Symptoms consisting of a bright yellow mosaic observed in the Jacquemontia sp. plant (sample #1250). (B) Similarity plot diagram made using the program SimPlot (200-nt scanning window and step size of 20 nt) comparing the nucleotide sequences of isolate VE:Mon 1250:09 of Jacquemontia yellow mosaic virus (JacYMV) described in this work with those of Jacquemontia mosaic Yucatan virus (JacMYuV) (JQ821386, blue continuous line) and Merremia mosaic virus (MerMV) (AY508991, red dashed line). Schematic representations of the recombinant fragments and genome organization are shown at the top and bottom of the figure, respectively. (C, D)

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(BamHI, EcoRI, NcoI and SacI). The only enzyme that yielded DNA fragments putatively corresponding to the complete genome components was BamHI. Cloning of the BamHI-digested RCA product into pBluescript II SK(?) (Stratagene) resulted in clones with inserts of ca. 2.6, 2.3 and 0.3 kbp. Inserts of selected clones were sequenced (Macrogen Inc., Seoul, South Korea). The 2.6-kbp fragment corresponded to a complete begomovirus DNA-B component. The 2.3-kbp and 0.3-kbp fragments were assembled and shown to correspond to a complete begomovirus DNA-A component. To confirm that the 2.3kbp and 0.3-kbp fragments were part of the same genomic component, a primer (MA1802, 5’- CAATTCTCCTAC GCCGGACTG-30 ) corresponding to a sequence within the 2.6-kbp fragment was designed and used for direct sequencing of the undigested RCA product. The sequence

D

93 95 100 96 81

100 100

CoYSV DQ875869 SiYMoV HQ822124 ToYLDV FJ999999 BCMV JQ283246 PYMTV AF039032 DLDV JN848774 JacMYuV JQ821387

JacYMV KF661332

63 54 100

CabLCJV DQ178609 ToYMLCV AY508994 MerMV AY508992 MerMV AY965899 100 MerMV DQ644559 78 MerMV DQ644560 EACMV AJ704949

0.05

Phylogenetic trees illustrating the relationship of JacYMV [VE:Mon 1250:09] DNA-A (C) and DNA-B (D) to other New World begomoviruses. The tree was constructed by the neighbour-joining method with the MEGA 5 program, and bootstrap values (1000 replicates) are shown for supported branches ([ 60 %). GenBank accession numbers are shown in the trees, and the begomovirus names are in Table 1. East Africa cassava mosaic virus (EACMV, AJ717542 and AJ704949) was used as an outgroup. The bar below each tree indicates 0.05 nucleotide substitutions per site

Genome sequence of Jacquemontia yellow mosaic virus Table 1 Percent nucleotide sequence identity of the DNA-A and DNA-B components of the isolate JacYMV [VE:Mon 1250:09] compared with the most closely related begomovirus isolates selected

after an initial BLAST search. The highest value for each component is shown in bold letters

Virus (acronym, GenBank accession nos.)

DNA-A

DNA-B

Merremia mosaic virus (MerMV, AY508991, AY508992)

78.4

69.2

Merremia mosaic virus (MerMV, AF068636, AY965899)

78.4

70.0

Merremia mosaic virus (MerMV, DQ644558, DQ644559)

78.4

69.9

Merremia mosaic virus (MerMV, DQ644557, DQ644560) Jacquemontia mosaic Yucatan virus (JacMYuV, JQ821386, JQ821387)

78.4 77.0

69.9 74.6

Potato yellow mosaic Trinidad virus (PYMTV, AF039031, AF039032)

76.9

68.9

Tomato yellow margin leaf curl virus (TYMLCV, AY508993, AY508994)

76.8

69.1

Tomato golden mottle virus (ToGMoV, EF501976)

76.7

NA

Datura leaf distortion virus (DLDV, JN848773, JN848774)

76.6

69.9

Tomato yellow leaf distortion virus (ToYLDV, FJ174698, FJ999999)

76.4

70.7

Corchorus yellow spot virus (CoYSV, DQ875868, DQ875869)

76.4

71.6

Sida yellow mottle virus (SiYMoV, HQ822123, HQ822124)

76.2

70.6

Bean chlorotic mosaic virus (BCMV, JN848772, JQ283246)

76.2

71.5

Cabbage leaf curl Jamaica virus (CabLCJV, DQ178608, DQ178609)

75.2

69.2

of 1100 nt that was obtained, covering the complete 0.3kbp fragment and adjacent genome regions, was 100% identical to the assembled DNA-A component (not shown). The BLAST program (http://www.ncbi.nlm.nih.gov/) was used to perform an initial sequence similarity search. Sequences were aligned with MUSCLE [5], and pairwise identity scores were calculated with SDT (Species Demarcation Tool) (http://web.cbio.uct.ac.za/SDT) as described previously [10]. The cloned genome showed the typical organization of New World bipartite begomoviruses. DNA-A (2611 nt, GenBank accession no. KF661331) showed the highest degree of nucleotide identity (78.4%) to the four isolates of MerMV available in public databases, and with JacMYuV (77.0%) (Table 1). DNA-B (2578 nt, KF661332) showed the highest degree of nucleotide sequence identity (74.6%) with JacMYuV (Table 1). Both components shared iterons that were identical in sequence and organization (not shown) in a CR that was 93.4% identical, thus confirming that they are a cognate pair. The nucleotide sequence identity of the DNA-A genome component to the most closely related begomoviruses was far below the 91% threshold recently approved as the begomovirus species demarcation criterion [6]. Therefore, in accordance with current taxonomic guidelines for the genus Begomovirus, the virus described here represents an isolate of a novel species for which we propose the name Jacquemontia yellow mosaic virus (JacYMV) (isolate [Venezuela:Monagas 1250:2009]). Phylogenetic analysis of both DNA-A and DNA-B carried out with MEGA 5 [14] clustered the JacYMV isolate together with JacMYuV (Fig. 1C, D). Similarity

plots generated using SimPlot (Version 3.5.1) [7] with the Kimura 2-parameter distance model suggested a recombinant nature for the JacYMV DNA-A (Fig. 1B), resulting from genetic exchange between JacMYuV and MerMV. In fact, a recombination analysis carried out with the RDP3 package (v.3. 42) with default settings [9], using an alignment generated with MUSCLE, confirmed the presence of recombination events involving two genome regions (nt 1136-1781 and 1890-162), putatively identifying JacMYuV as the major parent (blue continuous line, Fig. 1B) and MerMV (AY908991) (red dashed line, Fig. 1B) as the minor parent (highest probability with 3Seq, p = 1.867 9 10-21 and Chimaera, p = 4.220 9 10-09, respectively). The phylogenetic relationships and recombination between MerMV, JacMYuV and JacYMV illustrate the existence of a cluster of begomoviruses adapted to members of the family Convolvulaceae. It is noteworthy that the MerMV isolate, the putative minor parent of JacYVV, was found infecting tomatoes in Venezuela [11], thus suggesting a complex evolutionary history and epidemiology involving the transmission of begomoviruses between Convolvulacae species and tomato crops. This highlights the role of wild species as reservoirs for viruses which, under appropriate conditions, are readily able to jump to crops of economic importance. Acknowledgments This work was carried out in the frame of Network 111RT0433 from Fundacio´n CYTED. E. M. and J. N.-C. are members of the Research Group AGR-214, partially funded by the Consejerı´a de Economı´a, Innovacio´n y Ciencia, Junta de Andalucı´a, Spain (cofinanced by FEDER-FSE). We are grateful to Dr. Carolyn A. Owen for her help in English editing.

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Complete genome sequence of Jacquemontia yellow mosaic virus, a novel begomovirus from Venezuela related to other New World bipartite begomoviruses infecting Convolvulaceae.

The complete genome of a bipartite begomovirus (genus Begomovirus, family Geminiviridae) infecting Jacquemontia sp. (Convolvulaceae) in Venezuela has ...
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