Molecular comparative analysis of component 1 (DNA-R) of an … · 2017. 2. 11. · ARTICLE Molecular comparative analysis of component 1 (DNA-R) of an Egyptian isolate of banana

Journal of Genetic Engineering and Biotechnology (2012) 10, 55–65

Academy of Scientific Research & Technology andNational Research Center, Egypt

Journal of Genetic Engineering and Biotechnology

www.elsevier.com/locate/jgeb

ARTICLE

Molecular comparative analysis of component 1 (DNA-R)

of an Egyptian isolate of banana bunchy top nanovirus

isolated from banana aphid (Pentalonia nigronervosa)

Shimaa M. Abdel-Salama,*, M.U. Dahot

b, A.S. Sadik

c,d

a Department of Botany, University College for Women (Arts, Science and Education), Ain Shams University, Cairo, Egyptb Institute of Genetic Engineering and Biotechnology, Sindh University, Jamshoroo, Pakistanc Department of Agricultural Microbiology, Faculty of Agriculture, Ain Shams University, Cairo, Egyptd Department of Biology, Faculty of Science, Taif University, Taif, Saudi Arabia

Received 27 July 2011; revised 1 May 2012; accepted 5 May 2012Available online 5 June 2012

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E-

16

Pr

Pe

ht

KEYWORDS

Banana bunchy top virus

(BBTV);

Banana aphid (Pentalonia

nigronervosa);

Replicase gene;

Molecular characterization;

Nucleotide sequence

Corresponding author. Addr

llege forWomen (Arts, Scienc

smaa Fahmy St., Heliopolis,

obile: +20 2 0100 6208264.

mail address: dr.shsalam@gm

87-157X ª 2012 Academy

oduction and hosting by Els

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Abstract We are reporting a molecular comparative analysis of component 1 BBTV-DNA-R of an

Egyptian isolate of (BBTV) and 30 different geographical isolates. DNA was extracted from BBTV-

infected adult banana aphids collected from El-Qalubia Governorate, Egypt. Using specific primers

the BBTV-DNA-R was amplified, cloned into a prokaryote vector, sequenced and a molecular com-

parative analysis of BBTV-DNA-R of this study and some overseas isolates of BBTV-infected

banana plants was determined. Results showed that the component 1 consists of 1108 nts and con-

tains a sequence of 69 nts representing the CR-SL of 31 nts. A CR-M (90 nts) at the position (972–

1062) characterized with GC-rich sequence from nts 76 to 90 (average of 80% G + C) was found.

Alignment results of BBTV DNA-R confirmed the presence of a number of conserved regions in all

isolates. Large ORF of 861 nts at position 102 to 962 in the virion sense were detected. The pre-

dicted protein of this ORF consisted of 286 amino acids and had a molecular weight of

33.8 kDa. The DNA-phylogenetic analysis showed a percent identity of 98.0 and 97.9 between

BBTV DNA-R and isolates of Pakistan (isolate TJ1) and Australia (isolate V1), respectively. The

rtment of Botany, University

cation),Ain ShamsUniversity,

ypt. Tel.: +20 2 02 37214660,

(S.M. Abdel-Salam).

ific Research & Technology.

. All rights reserved.

enter, Egypt.

003

lsevier

mailto:[email protected]

http://dx.doi.org/10.1016/j.jgeb.2012.05.003

http://dx.doi.org/10.1016/j.jgeb.2012.05.003

Table 1 BBTV isolates and accessi

studied isolate of Egyptian BBTV D

BBTV groups Overseas BBTV

Isolates

Asian Taiwan

V14

Vietnam

Veitnam1

Vietnam 2

JT7

bp5

bp26

Philippines

China

IG33

IJs11

South Pacific TJ1

mrep8

Mrep7

mrep9

Mrep2

Mrep3

mrep jav

Eta

Kan

Bi

India

India1

MY02

MY03

Fiji

Tonga

V1

V-1

56 S.M. Abdel-Salam et al.

similarities between the gene product of Egyptian BBTV DNA-R and the 30 overseas isolates ran-

ged from 93.7 to 99.0%. Differences in phylogenetic trees based on the entire sequence of BBTV

DNA-R, CR-M and amino acid sequences confirmed the existence of two taxonomic groups of

BBTV and the Egyptian isolate belongs to the south pacific group.

ª 2012 Academy of Scientific Research & Technology. Production and hosting by Elsevier B.V.

All rights reserved.

1. Introduction

Banana bunchy top virus (BBTV) of genus Babuvirus (familyNanoviridae) is the most dangerous banana viruses. Susceptible

host species are found in the family Musaceae [45,15]. The fol-lowing species were susceptible to experimental viral infection:Musa sapientum (cv. Cavendish) [6]. Experimentally infected

hosts mainly show symptoms of chlorosis, stunting and darkgreen streaks on the lower portion of the midrib and leaves.These streaks consist of a series of ‘‘dots’’ and short lines

‘‘dashes’’ often known as ‘‘Morse code’’ streaking. If fruit is pro-duced, hands may have distorted and twisted forms[41,51,43,12,14,32,42,39].

The virus can be best detected in phloem [41]. It is transmit-

ted by arthropods, insects of the order Hemiptera, family Aph-ididae; Pentalonia nigronervosa in a persistent manner [26]. Thevirus spreads in Africa Burundi, Gabon and Egypt [14] and

on numbers of the 30 overseas iso

NA-R (A) based on the nucleot

isolates

Accession # Lengths

compone

AF416468.1 1104

AB113660.1 1104

AF416479.1 1104

AF416474.1 1104

AF416478.1 1104

AB108458.1 1103

AB189067.1 1104

AB250955.1 1104

AF416469.1 1103

AY450396.1 1104

AB186924.1 1104

AB186926.1 1103

AY996562.2 1110

AM418539.1 1111

AM418535 1110

AM418537.1 1111

AM418534.1 1110

AM418536.1 1111

AM418538.1 1111

DQ656119.1 1111

DQ656118.1 1111

FJ605506.1 1111

AF416470.1 1111

DQ256267.1 1111

AB252640.1 1111

AB252641.1 1111

AF416466.1 1111

AF416467.1 1109

S56276.1 1111

EF095162.1 1110

occurs in Australia, Pacific Islands, the Philippines, and Tai-

wan [12,36,31,42,17].The virions consist of an 18–20 nm isometric non enveloped

capsid surrounding a segmented genome that consists of at least

six integral circular, single-stranded DNA components origi-nally named DNA-1–6 and recently renamed DNA-R, -U3, -S, -M, -C and –N, respectively according to their putative func-

tions [45]. The integral components were found in all isolatescollected around the world [9,30]. Each BBTV-associated com-ponent is �1.1 kb, and the transcripts have been mapped[18,7,8]. DNA-R encodes a replication initiation protein

(Rep), which later was shown to support the replication of othernon-Rep-encoding components and was found to be associatedwith a smaller internal gene in a +2 reading frame [24,7]. The

open reading frame (ORF) of DNA-U3 is not consistently pres-ent among characterized isolates, and the function of DNA-U3in BBTV infection is currently unknown. DNA-S encodes a

lates used in alignment and Sequence distance between them and

ide (nt), CR-M and the amino acid sequences (aa).

% Identities

of the

nt (nts)

Regions nt CR-M aa

Taiwan 90.0 30.3 94.1

Vietnam 91.5 33.7 94.1

90.6 36.0 93.7

90.4 37.1 93.7

89.3 36.0 94.1

Japan 90.4 31.5 94.4

89.8 32.6 94.4

89.9 31.5 94.4

Philippines 90.1 31.5 94.4

China 89.7 36.0 93.7

Indonesia 89.8 32.6 94.1

89.8 31.8 94.1

Pakistan 98.0 93.3 98.6

97.7 93.3 98.6

97.7 91.1 98.6

97.7 93.3 98.6

97.6 91.1 98.3

97.5 93.3 98.3

97.6 93.3 98.3

India 97.7 93.3 98.6

97.7 93.3 98.6

97.6 93.3 98.3

97.6 93.3 98.2

97.0 89.9 97.9

Myanmar 97.7 93.3 99.0

97.5 93.3 99.0

Fiji 97.4 93.3 97.9

Tonga 96.9 85.6 98.3

Australia 97.9 93.3 98.6

Taiwan 96.8 91.1 97.9

Figure 1 TAE agarose gel (1%) shows PCR amplification of

BBTV DNA-R of Egyptian isolate isolated from banana aphid.

Approximately 1.1 kb was amplified. Lanes, M: 1 kb ladder

(Promega); A: Egyptian isolate; P.C.: positive control; N.C.:

negative control (PCR with no DNA template).

Figure 2 The nucleotide sequence of the Egyptian BBTV DNA-R fu

underlined at the beginning and the end of the ORF respectively. Th

accession No. HQ259074 in EMBL in Europe and the DNA Data Ba

1084-44 CR-SL 51

972-1062 CR-M 94

102-962 ORF 40

531-536 polyadenylation signal 32

Molecular comparative analysis of component 1 (DNA-R) 57

capsid protein [47], DNA-M and DNA-N encode possible

movement proteins [48], and DNA-C encodes a protein thatcan bind retinoblastoma and may be involved in host-cell-cyclemanipulation [4].

All BBTV integral components share a common genome

organization; all have a conserved major common region(CR-M) and stem–loop common region (CR-SL), a potentialTATA box 30 of the stem–loop, at least one major gene in

the virion sense and a polyadenylation signal associated witheach gene [7,8,10]. Several additional Reps have been reportedin BBTV but are confined to banana cultivated in Asia [25,9].

The existence of additional Reps may suggest opportunities fornanovirus evolution [16].

In this study, the nucleotide sequence of DNA-R of an Egyp-

tian isolate of BBTV amplified from the DNA extracts of theadults’ BBTV-infected banana aphid (P. nigronervosa) wasdetermined and a comparative analysis with the overseas BBTVisolates that of BBTV-infected plant materials was aimed.

ll length. The start codon and the possible termination signal were

is nucleotide sequence was submitted in the gene bank under the

nk of Japan.

-59 TATA box

1-946 polyadenylation sequence

3-531 internal ORF

-43, 1085-091 Putative iterons


2. Materials and methods

2.1. Nucleic acid extraction

Nucleic acid was extracted from BBTV-infected adults ofbanana aphid (P. nigronervosa) collected from El-Qalubia

Governorate, Egypt as described by Sadik and El-Karim [40].

2.2. Primers used

Two primers (F1: 50 TGA GAG GCT TCT TCC CAG GCGCAC ACC TTG and R1: TCT GCT TCA GAG AGC TTC

GTC 30) flanking the full length of BBTV-DNA-R were de-signed and generated from the sequences published by Hardinget al. [22]. (Gene Bank Accession # S56276).

Figure 4 Phylogenetic analysis of BBTV DNA-R full length

Figure 3 The stem-loop structure of BBTV DNA-R full length

of the Egyptian isolate. (Underlined numbers: indicate their

position).

2.3. PCR amplification of BBTV DNA-R and sequencing

PCR mixes comprised 50 pmol of each primer (F1 and R1),10 mM dNTPs, 1 U Taq DNA polymerase (Roche) and 1 llof total nucleic acid extract (100 ng/ll). The reaction mixeswere denatured at 94 �C for 5 min followed by 30 cycles of94 �C for 1 min, 55 �C for 1 min and 72 �C for 2 min followed

by 1 cycle of 72 �C for 7 min. The PCR product was then puri-fied using a High Pure PCR Purification kit (Roche), and wasdigested at 37 �C for 2 h with AvaII. The digested productswere purified using High Pure columns (Roche) and were li-

gated into pGEM�–T vector (Promega) at 4 �C overnightusing 2 U T4 DNA ligase (Roche) to form pRMAF1 plasmid.The ligations were then electroporated into Escherichia coli

JM109. Selected clones were sequenced using automatedsequencing and Big Dye Termination Cycle Sequencing ReadyReaction (PE Applied Biosystems).

2.4. Sequence analysis

The obtained DNA sequence was examined for similaritysearching using the basic local alignment search tool (BLASTversion of the national center for Biotechnology information(NCBI) http://www.ncbi.nlm.nih.gov/BLAST. The DNA se-

quences related to BBTV-DNA-R of 30 overseas isolates (Ta-ble 1) were collected and aligned with the nucleotide sequenceof the PCR insert in pRMAF1 plasmid using the DNA Star

Software Package (Expert Sequence Analysis Software,USA). DNA sequence was translated to protein using EditSeqprogram and then alignment using MegaAlign program was

done.

3. Results and discussion

There are two groups of BBTV, the South Pacific group (iso-lates from Australia, Burundi, Egypt, Fiji, India, Tonga andWestern Samoa) and the Asian group (Vietnam, Philippines

and Taiwan), based on sequence analysis of BBTV DNA-R

with the other isolates based on the nucleotide sequence.

http://www.ncbi.nlm.nih.gov/BLAST


[29,30] and BBTV-DNA-S-N [48]. These two groups differ by

an average of 9.6% (DNA-R), 11.86% (DNA-S) and 14.5%(DNA-N) over the entire nucleotide sequence with an averagedifference of 32% (DNA-R), 38.6% (DNA-S), and 27%(DNA-N) within the CR-M [29,30,48].

Results in Fig. 1 showed that the molecular size of theexamined BBTV DNA-R Egyptian isolate was found to be1.1 kb in length. This band was obtained in the positive

control, as well as, the BBTV-infected plants and was not de-

Figure 5 Alignment of nucleotide sequence of BBTV DNA-R CR-M

Egyptian BBTV DNA-R CR-M were hidden, while the others that di

tected in the negative control. A fragment of 1111 nts of an

Egyptian isolate was obtained Karan et al. [29]. The overseasBBTV DNA-R fragments were ranged in length from 1103to 1111 nts (Table 1). Fig. 2 representing the nucleotide se-quence of the obtained fragment.

On the sequence analysis, it was found that, the sequence ofthe full length of BBTV DNA-R contains a sequence of 69 ntsrepresented the common region (CR)-stem loop (SL) in which

a SL structure consisted of 31 nts has the sequence (TATTAT-

with 30 overseas isolates. The sequence nucleotides matches the

ffer from it were written in boxes.


TAC) was observed. This sequence is similar to that found in

all geminiviruses and contains the origin of replication for sin-gle-stranded DNA viruses [35]. (Figs. 2 and 3). This functionwas supposed to be due to the presence of iterated sequences(iterons) in the viral genome with sequence (GGGAC) occur-

ring as a tandem repeat on the virion-sense strand, 30 of thestem-loop (position 32–43 in the present study), and as a singleiteron on the complementary strand, 50 of the stem loop (1085–

1091) (Fig. 2). These iterons act as recognition sites for se-quence specific binding for the initiation proteins. Mutationin these sequences negatively affects Rep binding in vitro and

replication in vivo [23]. Findings of CR-SL sequence analysisin the present study agree with reports from Pakistan and In-dia [3,46]. The second CR was located at 50 of the CR-SL,

called the major CR-M (90 nts) at the position (972–1062)and characterized with GC-rich sequence from nts 76 to 90(average of 80% G+ C). CR-M was possessed to direct syn-thesis of primer that initiates the formation of the complimen-

tary strand of BBTV DNA component [13,20,21,43,11].A potential TATA box of nine nucleotides was identified

and located downstream from the SL sequence in a distance

of 41 nts with the nona nucleotide sequence (CTATAAATA)this box was found to locate before the start codon of anORF by 42 bases. This box is commonly found in the gene

promoters from 20 to 60 bp before the start of transcription,and any removing or altering in this sequence markedly re-duces the promoter activity [2].

Results also showed the presence of a large ORF of 861 nts,

started with the translation initiation codon ATG at position102–962 in the virion sense. In addition, one potential polyad-enylation signal (PAS) was found, associated with the 30 end of

the major ORF with 19 nts prior the stop codon. A GT-richregion contained the trinucleotide TTG located after thisPAS. Another internal ORF of 129 nts was observed inside

Figure 6 Phylogenetic analysis of BBTV DNA-R full length CR-

the main ORF which encode a protein of 42 aa with a molec-

ular weight of 5 kDa. This ORF was found to have a PASoverlapping the stop codon. No other ORFs were identifiedin the component in either the virion or complementary sensewhich had appropriately located potential TATA boxes and

polyadenylation signals. These findings came in line with pre-vious studies [28,7].

The nucleotide sequence of the Egyptian BBTV DNA-R

full length was compared with the nucleotide sequences of 30different geographical isolates of BBTV DNA-R belongingto the two groups, i.e. 12 from Asian group and 18 from South

Pacific group Table (1). The alignment of BBTV DNA-R withthese isolates confirmed the presence of a number of conservedregions in all isolates which are the CR-SL and CR-M. Addi-

tionally, the internal ORF was observed in all studied isolatesand the PAS and the GT-rich regions were conserved for boththe major ORF and the internal ORF. The same was observedin a study from Japan [17]. The phylogenetic analysis based on

the BBTV DNA-R nucleotides, CR-M and the predicted pro-tein sequences of the isolate under investigation and other 30isolates confirmed the categorization of BBTV isolates under

two groups, namely the Asian group and the South Pacificgroup in which The Egyptian isolate (A isolate) was foundto be grouped (Figs. 4, 6 and 9). Results are illustrated by

Fig. 6. The existence of two geographical groups of BBTVwas previously reported based on sequence variation inDNA-1(-R), DNA-6(-N), DNA-3(-S) and DNA-5(-C)[29,30,38,48,1] respectively.

Comparative analysis showed that the A isolate revealedhigh degree of homology to BBTV DNA-R sequences fromPakistan isolate (TJ1) and Australia (isolate V1), in a percent

identity of 98.0% and 97.9%, respectively. However, the low-est identity was obtained in comparison with an isolate fromVietnam with percent identity of 89.3%. Sequence comparison

M with 30 different isolates based on the nucleotide sequence.

Figure 7 Alignment of BBTV DNA-R full length of Egyptian isolates. Similar letters were hidden, while the others that differ from our

isolate (A) were written in shaded boxes. CR-Ms were outlined in the two boxes.


of replicase at amino acid level showed greater identity (97.9–99.0%) with South Pacific group and (93.7–94.4%) with Asiangroup, than the nucleotide sequences (Table 1).

The sequence variability between CR-M of the 30 isolateswas determined as shown in Fig. 5, which illustrates thealignment report of the thirty-one CR-Ms.

Figure 8 Amino acid sequence of the translated ORF of BBTV

DNA-R of the Egyptian isolate. The underlined sequence repre-

sents the d-NTP-binding motif.


Results in Table 1 demonstrated that the comparative anal-ysis of the CR-Ms. in which a maximum divergence of 6.7–

10.1% (mean of 8.4%) was observed between the Egyptian iso-

Table 2 Variations in amino acid sequence of BBTV rep protein b

Position South Pacific group

aa Propertie

16 T Theronine Neutral, p

17 T Theronine Neutral, p

25 I Isoleucine Aliphatic

78 S Serine Neutral, p

124 D Aspartic Acidic

143 M Methionine Neutral

153 R Arginine Basic

169 Q Glutamine Neutral, p

198 R Arginine Basic

231 D Aspartic Acidic

285 S Serine Neutral, p

Figure 9 Phylogenetic analysis of BBTV DNA-R full length wit

late and the South Pacific group (1st group) and 62.9–69.7%

(mean of 66.3%) with the Asian group (2nd group). Theseresults showed that CR-M revealed CR-SL to be highly con-served between all reported isolates, while as CR-M found tobe conserved within the same group but shows less identity

between members of South Pacific and Asian group. Similarresults were obtained before for BBTV DNA-S which indicatesthe important role of CR-M in the determination of the taxo-

nomic group of the BBTV isolates [48]. Furthermore a case ofgenome reassortment was observed in Taiwan V-1 isolate. Thesame was observed in case of the BBTV DNA-C full length of

this isolate [1]. This may suggest a concerted evolution in theCR-M of the Pacific or the Asian group [27]. Therefore, analignment analysis between our isolate and the fore-published

Egyptian isolates – Egypt 1 isolate with the accession numberAF416465.1 [29] and Egypt 2 isolate with the accession num-ber AF102780.1 – was performed (Fig. 7).

etween two groups of BBTV.

Asian group

s aa Properties

olar A Alanine Aliphatic

olar S Serine Neutral, polar

F Phenylalanine Aromatic


E Glutamic Acidic

L Leucine Aliphatic

K Lysine Basic

olar E glutamic Acidic

K Lysine Basic

E Glutamic Acidic


h thirty different isolates based on the amino acid sequences.

Figure 10 Alignment of amino acid sequence of Egyptian BBTV DNA-R ORF with thirty geographical isolates. The underlined

characters represent the d-NTP binding motif (183–188). Amino acids that match the amino acids of the Egyptian ORF predicted protein

were hidden, while the others that differ from it were written in boxes.


Interestingly we found that these two isolates have percent

identity of 100% between them while and after 15 years our iso-late showed 97.6% identity with them. In addition the

differences between these isolates and ours were found in 26

positions eight of them were found in the CR-M only (five dif-ferences and three deletions), i.e., 28.5% of the differences were


located in 8.1% of the full component. The divergence in the

similarities between the studied isolates in case of full lengthanalysis and CR-M (Table 1) reflects that the CR-M undergoesan independent evolution a distant from the full length.

The ORF of the Egyptian isolate (A) of BBTV DNA-R pre-

dicted protein was consisted of 286 amino acids and had amolecular weight of 33.8 kDa. The sequence analysis of thisprotein was illustrated in Fig. 8. In this sequence, the d-NTP

binding motif GGEGKT was observed in the position183–188 suggesting that it is a putative replicase protein [22].Rep proteins have been found to be associated with a variety

of plasmids of Gram-positive [49,44,19,33] and Gram-negativebacteria [50], single stranded DNA (ssDNA) and doublestranded DNA (dsDNA) phages [5] and viruses, including

the geminiviruses [34], all of which replicate via a rolling-circlemechanism [18,11].

The alignment report of the gene product of BBTV DNA-Rwas illustrated in Fig. 10. Results showed that the d-NTP bind-

ing motif was observed in all isolates (underlined letters). In 11positions, isolates belonging to south pacific group were foundto be different from Asian ones in the replacement of an amino

acid with another- except for the two Vietnam isolates (1 and 2)in positions 153, and 143 and 169, respectively (Table 2 andFig. 10). These variations were found to be unique for the group

and could be used as a distinguishable tool between the twogroups but further investigations need to be done in order to ap-prove this postulation and examine its effect on the properties ofthe protein. In addition our isolate was found to be unique in

three amino acid substitutions 47, 172 and 277, inwhich the ami-no acid Glutamic, Tyrosine/Histidine and Serine in the otherisolates were substituted with Alanine, Asparagine and Phenyl-

alanine in ours. These finding disagree with Islam et al., [37] whoobtained only one change in the amino acid sequence of Repli-case gene at position 95. The obtained changes in our isolate

can play a point of study to perform an interfering strategy forovercome the Egyptian isolate of the virus.

As a conclusion, from the present study the differences in

phylogenetic trees based on the entire sequence of BBTVDNA-R, CR-M and amino acid sequences of replicase protein,confirmed the existence of two taxonomic groups of BBTV andthe Egyptian isolate belongs to the south pacific group. Also

considering the fact that the CR-M region doesn’t encodefor any protein the recorded independent evolution may haveno effect on viral replication, but it reflects an evidence of pro-

gress taking place in the viral genome that may be a mecha-nism by which the virus can overcome the host defenses,change its pathogenicity or change its host on the long term

of evolution.

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Molecular comparative analysis of component 1 (DNA-R) of an … · 2017. 2. 11. · ARTICLE Molecular comparative analysis of component 1 (DNA-R) of an Egyptian isolate of banana