1 Department of Primary Industries and Fisheries, 80 Meiers Road, Indooroopilly, Queensland 4068, Australia
2 Department of Plant Biology, University of Minnesota, St Paul, MN 55108, USA
3 John Innes Centre, Colney Lane, Norwich NR4 7UH, UK
4 Department of Plant Pathology, University of Minnesota, St Paul, MN 55108, USA
Correspondence
Andrew D. W. Geering
andrew.geering{at}dpi.qld.gov.au
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers reported in this paper are AY189378AY189383, AY189384AY189392, AY189444AY189453, AY189393AY189400, AY189401AY189419, AY189420AY189435 and AY189436AY189443.
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INTRODUCTION |
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The banana is one of the oldest domesticated crops in the world and the majority of cultivars (cvs) have arisen by a process of traditional selection. The wild progenitors of the domesticated banana are Musa acuminata (A genome), Musa balbisiana (B genome), and to a much lesser extent, Musa schizocarpa (S genome) and Musa textilis/Musa maclayi (T genome) (Carreel et al., 2002; Daniells et al., 2001
). M. acuminata is morphologically very variable and up to nine different subspecies are recognized (Daniells et al., 2001
). Recent evidence suggests that parthenocarpy first arose in M. acuminata subsp. banksii and/or subsp. errans, two subspecies occurring in New Guinea and the Philippines, respectively (Carreel et al., 2002
). From there, primitive cultivated types were probably taken by humans to other parts of South-east Asia where other subspecies of M. acuminata occur, providing opportunities for intraspecific hybridization. The sweetness of dessert bananas is a trait of M. acuminata subsp. malaccensis and zebrina, two subspecies found in the Indonesian archipelago and Malay Peninsula (Bakry et al., 2001
; Carreel et al., 2002
). Finally, banana cultivation expanded north and westwards into the region stretching from southern China and northern Indochina to northern India, where M. balbisiana naturally occurs, resulting in interspecific hybridization and selection of an even greater diversity of cvs with improved drought and cold tolerance and disease resistance (Bakry et al., 2001
; Jones, 1999
).
Banana breeding programmes began in the 1920s, but despite several decades of research only a small number of cvs have been successfully commercialised (Bakry et al., 2001). One of the major constraints to international banana breeding efforts has been the Obino l'Ewai isolate of BSV, for which the name Banana streak Obino l'Ewai virus (BSOEV) is proposed (G. Harper & R. Hull, personal communication). Despite an apparent absence of virus particles in the parent lines used in the breeding programmes, hybrid progeny resulting from crosses between these lines are frequently infected with BSOEV, curtailing any further exploitation (Dahal et al., 1999
; Harper et al., 1999a
; Ndowora et al., 1999
). An integrated sequence with 99 % identity to BSOEV has been identified in one parent line, Musa AAB group cv. Obino l'Ewai (Harper et al., 1999b
; Ndowora et al., 1999
). This integrant consists of two segments of viral sequence, which together comprise the full complement of the virus genome, but these two segments are separated by a 6 kb scrambled region containing non-contiguous and inverted viral sequences. It is thought that infection in the hybrids arises following activation of this integrant. The current model for activation involves two homologous recombinations, leading to excision of the scrambled region and the joining of either end of the integrant to give rise to a circular molecule, the equivalent of the virus mini-chromosome (Ndowora et al., 1999
). A stimulus for these recombinations is tissue culture (Dallot et al., 2001
), a propagation practice used to multiply planting stock once a hybrid is made.
PCR using degenerate badnavirus-group primers amplifies badnavirus-related sequences from a broad range of banana cvs suggesting that most cvs contain integrated badnavirus sequences (A. D. W. Geering, unpublished results). However, BSV infection in Cavendish bananas (Musa AAA group, Cavendish subgroup), the most important bananas in world trade, is rare, despite propagation by tissue culture in large quantities for many years. In providing an explanation for this conundrum, Geering et al. (2001) showed that integrated BSOEV DNA is linked to M. balbisiana and is therefore absent from Cavendish bananas, which have a pure M. acuminata genetic background. However, Geering et al. (2001)
did show that Cavendish bananas contain a non-functional integrated badnavirus sequence which, in contrast to BSVOEV, was linked to M. acuminata.
In this study, we have investigated the diversity of integrated badnavirus sequences in banana. As cultivated bananas are parthenocarpic and frequently sterile, plants are vegetatively propagated and their genotypes have largely been preserved since the initial hybridization events. Consequently, in order to understand the diversity of integrated badnavirus sequences that occur in at least 500 different banana cvs that exist today (Jones, 1999), we have examined accessions of M. acuminata, M. balbisiana and M. schizocarpa, as well as, two landraces, cvs Klue Tiparot (Musa BAB group) and Obino l'Ewai (Musa AAB group).
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METHODS |
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PCR and cloning.
Badnavirus DNA was amplified using Badna-1A (5'-CTNTAYGARTGGYTNGTNATGCCNTTYGG-3') and Badna 4 (5'-TCCAYTTRCANAYNSCNCCCCANCC-3') primers, designed to conserved sequences in the reverse transcriptase/RNase H region of the badnavirus open reading frame (ORF) III. A 50 µl PCR mix contained 2 µl Elongase enzyme mix (Gibco-BRL), 1x Elongase reaction buffer, 400 nM each primer, 100 µM each dNTP and 1·6 mM MgSO4. Thermal cycling conditions were one cycle at 94 °C for 2 min, 30 cycles at 94 °C for 15 s, 52 °C for 30 s and 72 °C for 1 min, followed by one cycle at 72 °C for 5 min. The PCR product was gel-purified using a QIAEX II gel extraction kit, A-tailed with Taq DNA polymerase (Gibco-BRL) and then cloned into pCR-Script II using a TOPO TA cloning kit (Invitrogen) according to the manufacturer's instructions.
Restriction enzyme analysis of PCR clones and sequencing.
To screen for sequence variants, purified plasmid DNA was digested with a mixture of DdeI and EcoRI and the digests electrophoresed in a 2 % agarose gel in 0·5x Tris-borate-EDTA. Representatives from each restriction pattern group were then selected for sequencing. Sequencing was done using fluorescent dye terminators on an Applied Biosystems automatic sequencer.
Sequence analyses.
Searches of GenBank were done using BLASTN (Altschul et al., 1990). DNA sequences were aligned using CLUSTALX (Thompson et al., 1997
) and the alignment manually adjusted by using an amino acid sequence alignment as a guide. All phylogenetic and molecular evolutionary analyses were done using MEGA version 2.1 (Kumar et al., 2001
). A distance matrix was created using the Kimura two-parameter model and relationships deduced using the neighbour-joining method. A bootstrap consensus tree was generated from 1000 replicates. Rates of synonymous and non-synonymous substitution were estimated using the method of Nei & Gojobori (1986)
. All new sequences have been lodged in GenBank: Shiz2, Shiz3, Shiz25, Shiz14, Shiz23 and Shiz24 under accession numbers AY189378 to AY189383, respectively; Bank1, Bank10, Bank11, Bank13, Bank14, Bank17, Bank19, Bank6 and Bank8 under accession numbers AY189384 to AY189392, respectively; Cal12, Cal13, Cal1, Cal22, Cal27, Cal30, Cal34, Cal6, Cal8 and Cal22t under accession numbers AY189444 to AY189453, respectively; Mal10, Mal11, Mal15, Mal22, Mal26, Mal3, Mal6 and Mal8 under accession numbers AY189393 to AY189400, respectively; OBLE15, OBLE17, OBLE1, OBLE21, OBLE24, OBLE2, OBLE32, OBLE34, OBLE35, OBLE36, OBLE37, OBLE3, OBLE4, OBLE5, OBLE7, OBLE8, OBLE13t, OBLE1t and OBLE22t under accession numbers AY189401 to AY189419, respectively; Batu10, Batu19, Batu20, Batu21, Batu24, Batu25, Batu27, Batu2, Batu31, Batu34, Batu36, Batu4, Batu5, Batu6, Batu8 and Batu9 under accession numbers AY189420 to AY189435, respectively; PKW12, PKW16, PKW18, PKW23, PKW32, PKW36, PKW8 and PKW9 under accession numbers AY189436 to AY189443, respectively. Additional sequences used in analyses were (abbreviations and GenBank accession numbers in parentheses): Banana streak Cavendish virus (BSCavV, A.D.W. Geering, unpublished data); Banana streak Mysore virus (BSMysV, AF214005); Banana streak Goldfinger virus (BSGFV, A.D.W. Geering, unpublished data); Banana streak Imove virus (BSImV, A.D.W. Geering, unpublished data); BSOEV (AJ002234); Banana streak Uganda A virus (BSUgAV, G. Harper, unpublished data), Banana streak Uganda I virus (BSUgIV, G. Harper, unpublished data), Banana streak Uganda J virus (BSUgJV, G. Harper, unpublished data), Banana streak Uganda K virus (BSUgKV, G. Harper, unpublished data), Banana streak Uganda L virus (BSUgLV, G. Harper, unpublished data); Cacao swollen shoot virus (CSSV, L14546); Cassava vein mosaic virus (CsVMV, U20341); Citrus mosaic virus (CMBV, AF347695); Commelina yellow mottle virus (ComYMV, X52938); Dioscorea bacilliform virus (DBV, X94576 and X94581); Kalanchoe top-spotting virus (KTSV, AY180137); Rice tungro bacilliform virus isolate Chainat (RTBV-Ch, AF220561); RTBV isolate Ic (RTBV-Ic, AF113832); RTBV isolate G1 (RTBV-G1, AF113830); RTBV isolate Philippines (RTBV-Phil, X57924); RTBV isolate Serdang (RTBV-Serdang, AF076470); RTBV isolate West Bengal (RTBV-WB, AJ314596); Sugarcane bacilliform virus isolate Ireng Maleng (SCBV-IM, AJ277091); SCBV isolate Morocco (SCBV-M, M89923); Taro bacilliform virus (TaBV, AF357836).
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RESULTS |
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Rapid screening of PCR clones by restriction enzyme analysis
A method was developed to rapidly screen PCR clones for sequence variation by analysing restriction patterns following digestion with a combination of EcoRI, an enzyme that symmetrically excises the PCR fragment out of the vector, and DdeI, a 5-base cutter. An example of the restriction patterns obtained is shown in Fig. 1. This technique proved to be both informative and reliable in grouping clones with nearly identical sequences and differentiating significantly divergent sequences.
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To examine whether each of the sequences contained functional protein coding sequence, amino acid sequence translations were done (Table 2). Ninety-two clones were 544 bp long (excluding primer sequences), the expected size for a badnavirus, and 60 had an uninterrupted reading frame starting at nt 2. Seven clones (Bank11, Bank 17, Cal 27, KT32, OBLE34, PKW12 and Shiz23) had additions or deletions of 1 or 2 nt, leading to translational frameshifts. The clone Zeb2t, which was 588 bp long, contained two segments of sequence (nt 1246 and 292588) with at least 95 % identity to other variants of BEV 10 (e.g. Bank11, Mal8, Zeb3). However, the 45 bp of sequence separating these two segments had little similarity to any part of the badnavirus genome and was presumably Musa sequence. The clone Batu5, when compared with other variants of BEV 11, had deleted blocks of 14 and 6 nt, the first resulting in a translational frameshift. The additional length of the clone OBLE2 was due to the Badna 4 primer binding at a site 4 nt downstream of its normal position. Remaining clones with an interrupted reading frame had nucleotide substitutions leading to insertion of stop codons. Interestingly, sequences of the clones Batu27 and PKW32 were identical to that of BSImV in all but 1 nt position; both had an identical substitution at nt 442 (TGG to TGA), leading to insertion of a stop codon. This substitution was not present in the clone KT32, the other variant of BSImV isolated, but for reasons stated above, this clone also had an interrupted reading frame.
Phylogenetic analyses
Deduced relationships of the BEVs to a range of badnaviruses and closely related pararetroviruses are shown in Fig. 3. Strong bootstrap support was obtained for eight major clades of badnaviruses, of which the BEVs grouped in three (1, 3 and 5). Clades 1 and 5 were the largest and were further divided into six and eight subclades, respectively. Twelve of the 14 BEVs amplified from M. acuminata clustered in clade 1, and 11 of these specifically in subclades 1A and 1B. In comparison, all but one of the BEVs amplified from M. balbisiana were evenly distributed across subclades 1C to 1F and clades 3 and 5 (Table 2
). BSOEV, BSMysV and BSImV all clustered in clade 5 along with BSCavV, BSGfV and KTSV.
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DISCUSSION |
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To examine the basis of the diversity of the BEVs, rates of synonymous versus non-synonymous substitution were calculated. For each clade and subclade of BEVs, even those containing non-functional sequences, the kn/ks ratio was substantially less than one, suggesting that during the evolution of the sequences, the majority of non-synonymous mutations had been selectively removed, probably because they were highly deleterious to the functioning of the encoded protein, an essential protein in the replication cycle of a badnavirus. This result is consistent with the majority of nucleotide polymorphism arising when the BEVs were still free-living, and each of the 36 distinct BEVs probably represents an independent integration event. Although the presence of non-functional sequences suggests some sequence decay following integration, the amount of decay has been insufficient to remove the strong underlying signal of purifying selection. Also supporting the conclusion of minimal sequence decay, the length of the amplified DNA fragments was very uniform. The tendency for genes, once function has been lost, is for frameshift mutations to accumulate, as well for the rates of synonymous and non-synonymous substitution to reach equivalence (Bensasson et al., 2001; Page & Holmes, 1998
). Providing a contrast to the BEVs in Musa, the 21 geminivirus-related DNA (GRD) sequences integrated in the genomes of several Nicotiana spp. appear to stem from two independent integration events and the ancestral sequences have subsequently diverged as a result of genetic drift (Murad et al., 2004
).
In previous Southern hybridization studies, BSOEV and BSMysV have been linked to the B genome, and BEV 1 to the A genome (Geering et al., 2001, 2005
). Here, it has not been possible to make such linkages with the same certainty, as the absence of a BEV in a particular Musa genotype may simply reflect insufficient sampling of the PCR clones. Whilst acknowledging this caveat, some interesting trends were observed. No individual BEV was found in both M. acuminata and M. balbisiana, suggesting that integration occurred after separation of these species. M. acuminata is susceptible to infection by a broad range of badnaviruses, including BSOEV, BSMysV and BSImV (G. Harper, unpublished results; Geering et al., 2005
), precluding this as a reason for the absence of integrated DNA of these viruses in this species. Two BEVs were found in common between M. acuminata and M. schizocarpa. At this point of time, it is unclear whether this reflects integration of these BEVs prior to the separation of these species or, alternatively, there has been introgression of the BEVs in M. schizocarpa by plant hybridization or the BEVs independently integrated into the different Musa genomes. It should be noted that M. acuminata subsp. banksii and M. schizocarpa are sympatric in New Guinea and natural hybrids do occur (Carreel et al., 2002
).
Some BEVs were amplified from all subspecies of M. acuminata examined while others from only one or two subspecies. Using a Southern hybridization assay, Geering et al. (2001) were unable to detect BEV 1 in M. acuminata subsp. burmannicoides, apparently contradicting the results presented in this study. However, the variant of BEV 1 amplified from M. acuminata subsp. burmannicoides in this study (clone Cal12) had only 85·9 % nucleotide identity to the variant of BEV 1 amplified from cv. Williams (clone Wil1) by Geering et al. (2001)
, and the two sequences would not be expected to cross-hybridize under high stringency conditions.
As expected, A- and B-type BEVs were amplified from the AAB hybrid cv. Obino l'Ewai. However, surprisingly, no A-type BEVs were amplified from cv. Klue Tiparot, a BAB hybrid (Jenny et al., 1997; Carreel et al., 2002). Further examination of the BEV integration patterns in cv. Klue Tiparot may provide additional insights into the genetic background of this cultivar.
If it is assumed that the BEVs are molecular fossils' of viruses that existed in wild plant populations before plants were domesticated and traded, some predictions can be made about the prehistoric distributions of badnaviruses. BEVs from M. balbisiana showed the greatest diversity, suggesting a major radiation of badnaviruses in the region where M. balbisiana originated, which includes the Philippines and a broad zone stretching from southern China and northern Indochina to northern India (Jones, 1999). It is of significance that two of the three BEVs from M. acuminata grouping outside subclades 1A and 1B were from subsp. burmannicoides, a subspecies naturally occurring in Myanmar near India (Jones, 1999
). Otherwise, the diversity of BEVs in M. acuminata was very low, suggesting that badnaviruses were either not very common or diverse in places like Indonesia and the Malay Peninsula where M. acuminata originated (Jones, 1999
).
What evolutionary implications do the BEVs have for banana plants? The BEVs may confer a selective advantage upon the plant by contributing towards plant virus resistance through induction of transcriptional or post-transcriptional gene silencing of homologous sequences (Hull et al., 2000; Mette et al., 2002
). If this is so, it would provide a selection pressure for the maintenance of sequence integrity. The presence of multiple copies of a particular BEV may facilitate duplication of endogenous genes by homologous, unequal recombination, as is thought to be the case when a retrotransposon inserts on either side of an endogenous gene (White et al., 1994
). The presence of closely related endogenous badnavirus sequences at distant loci may also mediate larger scale chromosomal rearrangements through homologous recombination (Hughes & Coffin, 2001
). Insertion of a badnavirus promoter next to an endogenous plant gene may not only change its transcription levels, but also alter the tissue specificity of expression (Matzke et al., 2004
). Of importance to banana breeding programmes, endogenous virus sequences in addition to BSOEV may be able to be activated to give rise to infection. Of particular note, sequences nearly identical to BSImV and BSMysV have been found. Evidence from Nicotiana and Oryza suggests that endogenous pararetrovirus sequences are transcriptionally silenced through methylation, and it is possible that interspecific hybridization or the creation of polyploids during breeding may lead to the release of this silencing mechanism (Kunii et al., 2004
; Matzke et al., 2004
). Further work is required to characterize the BEVs to determine if they are capable of giving rise to an episomal virus genome.
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ACKNOWLEDGEMENTS |
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Received 7 May 2004;
accepted 5 November 2004.
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