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Department of Taxonomy, Institute for Plant Genetics and Crop Plant Research (IPK), D-06466 Gatersleben, Germany
Received for publication March 10, 1998. Accepted for publication September 23, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Alliaceae • Allium altaicum; • A. fistulosum; • domestication • noncoding cpDNA • phylogenetic analysis • random amplified polymorphic DNA • restriction fragment length polymorphism analysis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Haishima, Kato, and Ikehashi, 1993). Two types can be distinguished on the basis of their use as vegetables and are sometimes taxonomically treated as two subspecies: subsp. fistulosum with four varieties, grown for its pseudostems, and subsp. caespitosum (Makino) Kaz. with three varieties, grown for pseudostems and leaf blades (Kasakova, 1978
).
Allium altaicum Pall., the wild bunching onion (called butun in Siberia), was discovered in 1735 near Lake Baikal by Steller (1740)
. About 40 yr later, the species was found again in the Altai mountains and described under its valid name by Pallas (1773)
. The frost-resistant bulbs of A. altaicum are gathered in Siberia and Mongolia and are locally used as condiment and vegetable comparable to the bulb onion (A. cepa L.). Due to the great morphological similarity between the two species, Allium altaicum is proposed to be the nearest wild relative of the bunching onion and is still common in Southern Siberia and Mongolia (Hanelt, 1985
; Friesen, 1987
, 1988
, 1995
).
In spite of their overall similarity, the two taxa are easily distinguished by some morphological characters. Allium altaicum possesses a well-developed bulb with a red-brown tunic, whereas A. fistulosum forms a poorly developed bulb, normally with a white tunic, with a diameter hardly exceeding that of the pseudostem. The other morphological characters often adduced to differentiate the two species such as length and diameter of pedicels or density of the umbel are not unequivocal differences. Karyotypes of A. altaicum and A. fistulosum are very similar (Derjagin and Jordansky, 1971
; Inada and Endo, 1994
). Interspecific hybridization between these two Allium species occurs easily and hybrids show a high pollen and seed fertility (Inada and Iwasa, 1983
; Nishitani, 1984
).
The origin of A. fistulosum is uncertain and several different hypotheses have been proposed. De Candole (1883)
followed Ledebour (1830)
and Regel (1875)
in the opinion that the wild species, A. altaicum, is the direct progenitor of A. fistulosum, which originated in Siberia. Prochanov (1930)
and Li (1970)
suspected that both taxa originated in northern China from an unknown (extinct) ancestor, so that A. altaicum is the sister group to A. fistulosum instead of its progenitor. Havey (1992)
, in a study of maternal phylogenies within Allium section Cepa, found A. altaicum to be paraphyletic after the exclusion of A. fistulosum, which together form the sister group to A. cepa and A. vavilovii M. Pop. et Vved. Conversely, a restriction fragment length polymorphism (RFLP) analysis of the nuclear genome with cDNA probes (Bradeen and Havey, 1995
) revealed A. fistulosum to be paraphyletic in relation to A. altaicum with a weak sister-group relationship of both to A. galanthum Kar. et Kir. Van Raamsdonk, Smiech, and Sandbrink (1997)
found A. altaicum and A. fistulosum to be closest relatives in an analysis of mostly morphological characters and proposed the paraphyly of A. altaicum with respect to A. fistulosum on the basis of random amplified polymorphic DNA (RAPD) data. Sister groups to the two taxa were A. galanthum/A. pskemense B. Fedt. in their morphological analysis and A. roylei Stearn in the analysis of the RAPD data. A completely different hypothesis was published recently by Dubouzet, Shinoda, and Murata (1997)
who used dot blot hybridization with RAPD probes and found A. galanthum to be the sister taxon of A. fistulosum. Allium altaicum in this analysis is the closest relative of both taxa. Due to small within-species samples in most of these studies no safe conclusions about a monophyletic or polyphyletic origin of A. fistulosum could be drawn.
In the framework of a phylogenetic analysis of the entire genus Allium we analyzed A. altaicum and A. fistulosum in more detail to obtain insight into the mode of evolution of the crop species. To do this we used two different molecular marker systems and several accessions of the two taxa representing the known morphological and geographical variation. For the investigation of interspecific relationships we conducted a RFLP analysis of polymerase chain reaction (PCR) amplified DNA fragments (Arnold, Buckner, and Robinson, 1991
; Liston, 1992
) from rapidly evolving regions of the chloroplast genome. This method allows a rapid screening of large numbers of taxa for phylogenetically informative characters (Mes et al., 1997
). It makes use of universal PCR primer sets designed by Taberlet et al. (1991)
and Demesure, Sodzi, and Petit (1995)
for the amplification of noncoding parts of the chloroplast genome. The primers anneal to highly conserved gene sequences flanking variable spacers and introns. Sequences of noncoding parts of the chloroplast genome are widely used in systematic studies at lower taxonomic ranks due to high levels of sequence variation (e.g., Morton and Clegg, 1993
; Hodges and Arnold, 1994
; van Ham et al., 1994
; Downie, Katz-Downie, and Cho, 1996
; Kelchner and Clark, 1997
).
For studies in closely related groups the amount of variation found even in noncoding cpDNA might be too small for analyses of large numbers of accessions or for taxa that originated only recently. To circumvent this problem we used RAPD data (Welsh and McClelland, 1990
; Williams et al., 1990
). RAPD analyses reveal even small genetic differences, since a large part of the nuclear genome will be scanned, as can be seen by mapping studies of segregating markers in a wide variety of plant families (e.g., Rieseberg et al., 1993
; Bachmann and Hombergen, 1996
; Byrne et al., 1997
; Emebiri et al., 1997
; Lawson, Lunde, and Mutschler, 1997
; Powell et al., 1997
; Serquen, Bacher, and Staub, 1997
). Another advantage of this method is that it is less expensive and can be performed more rapidly than most other methods (Morell et al., 1995
). However, RAPD techniques have some limitations, such as low reproducibility of some bands and the uncertain homology of comigrating fragments in gel electrophoresis (Van de Zande and Bijlsma, 1994
; Harris, 1995
; Pillay and Kenny, 1995
; Rieseberg, 1996
). Most of the limitations of RAPD analysis can be overcome by carefully adjusting the reaction and detection conditions (Bachmann, 1997
; Colosi and Schaal, 1997
; Friesen and Klaas, 1998
) and generating large data sets where the phylogenetic signal outweighs the noise produced by nonhomologous fragments.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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RFLP analysis of cpDNA
For a RFLP analysis of A. altaicum, A. fistulosum, and five outgroup species the five following noncoding regions of the chloroplast DNA were PCR amplified (Demesure, Sodzi, and Petit, 1995
; Tsumura et al., 1995
) in 50-µL reaction volumes and digested with restriction enzymes: psaA-trnS and trnC-trnD were digested with AluI, AvaI, BanII, BglII, DdeI, DraI, HindIII, HinfI, MspI, NsiI, and TruI; trnK and trnT-trnD with AluI, BglII, ClaI, DdeI, DraI, EcoRI, HaeIII, MspI, and SspI; psbC-trnS with HaeIII and HindIII. Phylogenetically informative restriction site mutations and length variations were scored and compiled into a binary data matrix. When restriction site homology was unclear, the restriction sites were mapped by double digests. Generalized parsimony analysis was performed with PAUP 3.1.1 (Swofford, 1993
) using the heuristic search option, MULPARS, ACCTRAN, TBR branch-swapping, 200 random addition sequences, and a stepmatrix with a gain/loss ratio of 1.3:1 for restriction sites (Albert, Mishler, and Chase, 1992
). Indels and inversions were not weighted. A bootstrap analysis was performed with 500 resamples. Allium oschaninii, most distantly related to the ingroup (Havey, 1992
; Bradeen and Havey, 1995
; Pollner, unpublished data), was specified as the outgroup taxon.
RAPD analysis
Two RAPD analyses were conducted: one including the five outgroup species together with two accessions of A. altaicum and one of A. fistulosum and a second including all accessions of A. altaicum and A. fistulosum together with the outgroup A. oschaninii. Amplification was carried out in 25-µL reaction volume, using ten arbitrary ten-basepair (bp) primers (A04, AA17, AB04, AC19, C05, G02, G13, G19, D01, and D03) obtained from Operon Technologies, Alameda, California. The amplification conditions were optimized according to Friesen and Klaas (1998)
. One-third of the reaction mixtures was separated on 1.5% agarose gels in 0.5x TBE, followed by staining with ethidium bromide (Sambrook, Fritsch, and Maniatis, 1989
). Clearly visible RAPD bands (Fig. 2) were scored manually for presence (1) or absence (0) from enlarged photographs of the gels. Differing band intensities were not taken into account to avoid errors introduced by competition among priming sites during the initial rounds of PCR (Bachmann, 1997
). Only bands reproducible in two independent amplification reactions were included in the data analyses. From the resulting 1/0 data matrices pairwise genetic distances were calculated using the Jaccard coefficient. Finally, phenograms were prepared with the neighbor-joining cluster analysis (Saitou and Nei, 1987
) of the genetic distances. The neighbor-joining method was used because it is less sensitive for unequal mutation rates on different branches than UPGMA (Swofford et al., 1996
). The genetic distance matrix of the A. altaicum/A. fistulosum group was also subjected to a principal co-ordinate analysis (PCA). From the distances, new independent axial co-ordinates, which represent most of the variability of the original data, were calculated. The taxa were then plotted as points in a three-dimensional continuous space defined by the first three co-ordinates. These calculations were done in the NTSYS-PC program, version 1.8 (F. J. Rohlf, 1993; distributed by Exeter Software, New York).
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350 bp downstream from primer trnS. To get insight into the sequence composition of the spacer flanking the indel region without sequencing the entire length of the spacer by primer walking we used an adapter-mediated sequencing strategy. DNA of a 50-µL PCR reaction was incubated with 12 U EcoRI in 1x KGB buffer (McClelland et al., 1988
) at 37°C. After 1 h 3 units T4 DNA Ligase, 1 µL 10 mmol/L ATP, 10 pmol EcoRI-adapter, fitting the EcoRI ends without restoring the restriction site (Vos et al., 1995
), were added, and the tube was filled to a final reaction volume of 100 µL with water, resulting in a 0.5x KGB buffer concentration, which is sufficient for both enzymes. After 3 h at 37°C the enzymes were inactivated by heating the reaction mixture to 90°C for 10 min. The DNA fragments were electrophoretically separated in a 1.5% agarose gel, and the larger fragment (2.2 kb), containing the indel, was eluted in 100 µL TE with a QIAquick Gel Extraction Kit (Qiagen, Hilden, Germany). The fragment was reamplified with the primers Eco+0 (corresponding to the EcoRI-adapter; Vos et al., 1995
) and trnS and again gel purified. Fifty nanograms dsDNA and primers Eco+0 and trnS were used in cycle sequencing reactions with the Rhodamine Dye Terminator Kit (Applied Biosystems Inc., Foster City, California), according to the recommendations of the manufacturer. Sequence detection was performed on an ABI 377 DNA sequencer. Two additional Allium specific sequencing primers (Eco-381: 5'-CTTTATCCATAGAATATAGTAKGTAGGC-3' and trnS-580: 5'-TACGAATAATTCCGACAACTTCAGG-3') were developed and used as internal primers to sequence the entire 2.2-kb fragment in four accessions (two A. altaicum and two A. fistulosum). The overlapping sequences of the analyzed taxa were combined in consensus sequences and manually aligned.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Downie, Katz-Downie, and Cho, 1996
; Kelchner and Clark, 1997
). The DNA sequences showed that the length mutation differentiating A. fistulosum from the other taxa in the analysis consists of a 19-bp repeat, resulting from a duplication in A. fistulosum. The second mutation, autapomorphic for A. fistulosum accession All515, is a 21-bp DNA duplication.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, thus contradicting results of Bradeen and Havey (1995)
with respect to monophyly and Dubouzet, Shinoda, and Murata (1997)
concerning the progenitor of the crop species. Bradeen and Havey (1995)
included up to eight accessions of A. altaicum/A. fistulosum in their analyses, resulting in phenograms that might indicate multiple origins of A. fistulosum from A. altaicum or vice versa. These results did not allow the authors to draw safe conclusions about the relationship of the two species. Studies of Havey (1992)
and van Raamsdonk, Smiech, and Sandbrink (1997)
found a close relationship between the two taxa, but due to small sample sizes no decisions about a monophyletic or polyphyletic origin could be made. The sister-group relationship of A. galanthum with A. fistulosum found by Dubouzet, Shinoda, and Murata (1997)
could not be confirmed in our study and was never mentioned in the other analyses cited. Our chloroplast DNA data agree with data from Havey (1992)
in showing A. altaicum to be the closest relative of A. fistulosum, and A. vavilovii and A. galanthum in a clade together with the former. The analysis of RAPD data (Fig. 4), as well as other studies based on RAPD (van Raamsdonk, Smiech, and Sandbrink, 1997
) and nuclear data (Bradeen and Havey, 1995
), which might be better comparable to the method used by Dubouzet, Shinoda, and Murata, found only distant relations between A. galanthum and A. fistulosum. During our survey of the origin of the bunching onion we found a possible explanation for these inconsistencies in different studies of Allium section Cepa. When we included all available accessions of the two species in a preliminary examination, we obtained nearly unstructured data with some A. altaicum clustering together with A. fistulosum and vice versa, leading to the conclusion that both taxa are polyphyletic. A close investigation of all ‘misplaced" accessions showed that they had come to the living collection via seed exchange from freely interpollinating populations in botanical gardens. Excluding all garden material from the analysis resulted in the strong polarization of the two taxa as shown above, allowing the recognition of A. fistulosum as a monophyletic unit within a paraphyletic A. altaicum. As an example for a ‘wrong" accession we included Tax1503 (A. fistulosum from Botanical Garden, Chorog, Tadjikistan) in this analysis, which contains an A. altaicum chloroplast type. F1 hybrids between the two species normally exhibit predominantly morphological characters of the maternal parent (Kokoreva and Jurjeva, 1987
) so that pollen-mediated introgression is difficult to detect morphologically. Also, A. altaicum and A. fistulosum can best be distinguished by subterranean characters, which might easily result in erroneously labelled plants when the two species were grown together and propagation by seeds is not prevented. This facilitates chloroplast capture (as in Tax1503) via repeated backcrosses to one parent and might also explain the postulated sister-group relationship of A. fistulosum to A. galanthum (Dubouzet, Shinoda, and Murata, 1997
) because both species are interfertile (van Raamsdonk, Wietsma, and de Vries, 1992
) and garden material was used in the analysis (J. G. Dubouzet, Hokkaido Agricultural Station, Sapporo, personal communication).
Whereas, apart from the study of Dubouzet, Shinoda, and Murata (1997)
, the close relationship of A. altaicum and A. fistulosum seems well supported, the nearest relatives of these species are uncertain. Both marker systems used here, as well as the study of Havey (1992)
, revealed a position of A. vavilovii (Figs. 3, 4) close to the ingroup taxa but suggest conflicting hypotheses about the placement of the other species. It was not the aim of this study to analyze the entire section Cepa, but additional different topologies in the studies of Bradeen and Havey (1995)
and van Raamsdonk, Smiech, and Sandbrink (1997)
, led us to the conclusion that the phylogeny of Allium section Cepa is still unresolved.
The monophyletic origin of A. fistulosum makes this taxon an additional example for the hypothesis that most cultivated species resulted from single domestication events and subsequently spread into their presently inhabited areas (Zohary, 1996
). The monophyly of A. fistulosum was revealed by the analysis of noncoding cpDNA and of RAPDs (Figs. 3, 5). A 19-bp insertion in the psaA-trnS intergenic spacer characterizes all accessions of A. fistulosum and clearly distinguishes it from the other taxa in the analysis. DNA sequencing of the mutated region (Fig. 7, insertion I) showed that two partly overlapping inverted repeat sequences flanking the insert allow the formation of two different stem/loop secondary structures: a small hairpin with six paired bases or alternatively a short 4-bp stem with a larger loop. As in other species where inverted repeat sequences flank deletions (von Stein and Hachtel, 1988
; van Ham et al., 1994
) or inversions (Kelchner and Wendel, 1996
; Blattner, unpublished data), they might also be involved in duplication and insertion of the duplicated DNA string adjacent to its pattern in A. fistulosum. The second insertion/duplication in the only European accession (All515) of A. fistulosum (Fig. 7, insertion II) appears to be comparable to insertion I in the possibility of forming a secondary structure. The two mirrored parts of the sequence might point to an additional mechanism of sequence evolution in noncoding DNA.
Within A. fistulosum no differences could be detected by the RFLP analysis of the chloroplast genome fragments, which is not surprising taking into account that only few variable positions (six point mutations representing 0.25%) exist, as shown by sequencing part of the psaA-trnS spacer. The RAPD data analyses revealed intraspecific variation within A. fistulosum. Three accessions from Japan (K6173-6175) exhibit the largest variability (Fig. 6) and occur in a position basal to the remaining accessions analyzed (Fig. 5). Compared with A. altaicum the cultivated accessions of A. fistulosum show less diversity in the RAPD bands, which agrees with isozyme data (Maass, 1997
). This also supports the conclusion that domestication has been localized and has involved a severe genetic bottleneck (Zohary, 1996
). New variation arises slowly via mutations or interbreeding with wild relatives, which explains the fact that only one mutation in the chloroplast genome and two RAPD fragments unique to A. fistulosum could be found. An analysis of a larger number of accessions of A. fistulosum, including an increased number of Japanese and Chinese genotypes, may reveal more intraspecific variation and result in slightly different intraspecific relationships within A. fistulosum. However, even a larger sample of accessions should not substantially alter the result, as the A. fistulosum accessions investigated by us are representative of the most divergent morphological groups of the species.
It is interesting that in the RAPD analysis (Figs. 5,6) two of the southernmost accessions of A. altaicum (Tax1667 and Tax1691 from Mongolia, Fig. 1), are the closest relatives of the A. fistulosum accessions. This result points to a possible origin of A. fistulosum in northern China as proposed by Prochanov (1930)
for the hypothetical progenitor of both species and would contradict the view of De Candole (1883)
who postulated Siberia as the area of domestication of the bunching onion. The inclusion of additional accessions of A. fistulosum from China might have elucidated this point. In our analysis Japanese material of the bunching onion (K6174, Fig. 4) is genetically closer to A. altaicum than the accession from China (K0433).
Our reconstruction of the origin of A. fistulosum raises the question why a bulbless plant has been bred for the use of pseudostems or leaves from a progenitor that possessed a well-developed and widely used bulb. One possible solution to this problem can be seen in the fact that some specimens of A. altaicum were found growing in scree and sometimes, if covered with gravel, develop elongated and etiolated pseudostems, which could be a starting point for domestication of a leek-like vegetable.
The results of our work show that relatively fast-evolving cpDNA regions allow phylogenetic analyses in closely related species. The RFLP data permit us in this case to detect species boundaries, while subspecific groupings were not easily resolved by this method (Fig. 3). One exception was a group of five accessions of A. altaicum (Tax1425 to Tax3400, including the hybrid Tax1503, in Fig. 3) that possessed a different chloroplast type with a 100-bp deletion in region trnC-trnD. The main advantage of the method, i.e., suitability for screening large numbers of accessions very rapidly, works well in comparisons among species. At the population level it may miss most of the small amount of divergence as can be seen from the sequence comparison of the psaA-trnS spacer. In this case DNA sequencing has the advantage of finding more mutations and permitting the detailed analysis of sequence evolution (base substitution, inversion, or insertion/deletion).
RAPD analysis detects large amounts of differences even in closely related taxa and, at least if detection conditions are adjusted very carefully, can find reliable phylogenetic signal even above the species level (Fig. 4; van Raamsdonk, Smiech, and Sandbrink, 1997
). The neighbor-joining analysis of genetic distances of the RAPD data resulted in a phenogram that closely reflected the results of PCA. In particular, the multivariate analysis of RAPD data with PCA clearly distinguishes three groups in the A. altaicum/A. fistulosum species complex (Fig. 6). Allium altaicum and A. fistulosum are separated and three A. altaicum accessions from the Altai occur apart from the remaining plants investigated. It is interesting in this respect that the two groups in A. altaicum correspond to two life forms of A. altaicum. A detailed investigation of A. altaicum by Grankina et al. (1986)
revealed that this species exhibits two ecologically and morphologically different forms in the Altai mountains. One of these forms, represented in our analyses by three accessions (Tax5149, Tax5559, and Tax5561), possesses abruptly pointed, broad leaves and mostly a single thick stem and is widespread only on rocky terrain in the Altai mountains. The other life form (represented by the remaining accessions of A. altaicum in our analysis) shows gradually pointed leaves and usually more than one stem and is common in the entire inhabited area of the species, growing in wetter habitats. Between two populations of the two life forms occurring at a distance of 2 km in the Altai mountains, one of the authors (N. Friesen) found morphologically intermediate individuals, growing in ecologically intermediate habitats. The RAPD differences found between the two groups led us to the conclusion that the obvious morphological difference is not a plastic reaction to environmental conditions but characterizes two phylogenetically distinct populations of A. altaicum.
As a result of the inconsistencies between our analysis and previously published studies, which, in our opinion, might mostly be caused by the inclusion of unrecognized hybrid plants, we would recommend using only plants from wild populations or vegetatively propagated material of such plants for studies in groups with high interfertility. Even a careful morphological determination of plants can fail to detect hybridization when backcrosses to one of the parents have occurred. Inconclusive results were obtained not only within A. altaicum/A. fistulosum, but relationships throughout section Cepa are somewhat different in studies published from different working groups. Whereas it is common knowledge that gene trees do not have to be identical with the species tree (Maddison, 1997
), so that phylogenetic hypotheses partly depend on the marker systems used, comparable methods should produce congruent results. In this study as well as in the studies of Dubouzet, Shinoda, and Murata (1997)
and van Raamsdonk, Smiech, and Sandbrink (1997)
RAPD-based markers led to different phylogenies. Apart from methodological problems of RAPD analyses this as well might be a result of the inclusion of concealed hybrids in some of these studies.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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