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2 Department of Biology, James Madison University, Harrisonburg, Virginia 22807 USA; and 3 Integrative Biology Section, School of Biological Sciences, University of Texas, Austin, Texas 78712 USA
Received for publication May 18, 1999. Accepted for publication August 9, 1999.
ABSTRACT
The phylogenetic relationships of Silphium and subtribe Engelmanniinae were examined using DNA sequence data. The internal transcribed spacer (ITS) region and the external transcribed spacer (ETS) region were sequenced for 39 specimens representing the six genera of subtribe Engelmanniinae (Berlandiera, Chrysogonum, Dugesia, Engelmannia, Lindheimera, and Silphium), plus five additional genera identified as closely related to the Engelmanniinae by chloroplast DNA restriction site analysis, and three outgroups. Phylogenetic analysis supported the monophyly of Silphium with Lindheimera as sister. Silphium can be divided into two sections based upon two well-supported clades that correspond to root type and growth form. These results also supported the expansion of subtribe Engelmanniinae to include Balsamorhiza, Borrichia, Rojasianthe, Vigethia, and Wyethia. We hypothesize that subtribe Engelmanniinae originated in Mesoamerica and later radiated to the United States. We suggest that the cypsela complex, which is present in Berlandiera, Chrysogonum, Engelmannia, and Lindheimera, arose only once and was subsequently lost in Silphium.
Key Words: Asteraceae • Engelmanniinae • external transcribed spacer • Heliantheae • internal transcribed spacer • molecular phylogeny • Silphium.
Silphium L., commonly known as rosin-weed, is a member of the sunflower family Asteraceae. The genus is primarily distributed in the eastern United States with a small part of its range extending into Canada. Small (1933)
recognized 33 species of Silphium, which he divided into five sections (Composita, Dentata, Integrifolia, Laciniata, and Perfoliata) based upon leaf, stem, capitulum, and phyllary morphology. Perry (1937)
included 23 species in her revision of Silphium. Cronquist (1980)
, as part of the Asteraceae volume for the Vascular Flora of the Southeastern United States, revised Silphium to include 15 species. Since these treatments, only one additional species of Silphium has been described, Silphium wasiotense Medley (1989)
from Kentucky and Tennessee. Medley hypothesized that S. wasiotense is most closely related to S. brachiatum and S. mohrii, which would place it in sect. Dentata.
Silphium, because of its carbonized cypselae and paleate receptacles, is a member of the mostly Neotropical tribe Heliantheae. Traditionally, the genus has been classified in subtribe Melampodiinae Lessing because its capitula have functionally staminate disc florets. Stuessy (1973)
treated subtribe Melampodiinae as an artificial taxon and suggested that several genera, including Silphium, should be removed. In 1977, Stuessy erected subtribe Engelmanniinae to accommodate Silphium, the North American genera Berlandiera DC., Lindheimera A. Gray & Engelm., Chrysogonum L., and Engelmannia A. Gray ex Nutt., and the central Mexican endemic Dugesia A. Gray. According to Stuessy, all members of this subtribe share functionally staminate disc florets, radially flattened ray cypselae, and alternate leaves. All genera but Silphium and Dugesia have a distinctive cypsela complex that is composed of a ray cypsela attached to the subtending phyllary, two to four paleae, and two to four adjacent disc florets. Robinson (1981)
placed the Engelmanniinae within his concept of subtribe Ecliptinae, which he characterized by genera with blackened, nonstriate cypselae, strongly blackened anthers, and lack of well-developed patterns of colored resin in disc corollas. Molecular studies based on chloroplast DNA (cpDNA) restriction site data revealed a polyphyletic subtribe Ecliptinae (Kim, Jansen, and Turner, 1990
; Panero and Jansen, 1997
; Panero, Jansen, and Clevinger, 1999
). Karis (1993)
and Karis and Ryding (1994)
, based upon morphological cladistic analysis, resurrected subtribe Engelmanniinae. Panero, Jansen, and Clevinger (1999)
included three members of the Engelmanniinae in their study. They found that Chrysogonum, Engelmannia, and Silphium form a monophyletic group together with two western United States genera, Balsamorhiza Nutt. and Wyethia Nutt., the North American coastal genus Borrichia Adans., the Mexican genus Vigethia W. A. Webber, and the Mesoamerican genus Rojasianthe Standl. and Steyerm. Given these results, they hypothesized a Mesoamerican origin for the members of this clade with the monotypic genera Rojasianthe, Vigethia, and Dugesia as paleoendemic relicts isolated in the mountains of Mexico and the other genera representing the radiation of the lineage into the temperate regions of the eastern and western United States. The affinity of the Engelmanniinae with Balsamorhiza, Borrichia, and Wyethia was also confirmed by Urbatsch and Jansen (1995)
and Urbatsch (1997)
.
The purpose of this study was to construct a phylogeny of subtribe Engelmanniinae using nucleotide sequence data from the Internal Transcribed Spacer (ITS) and the External Transcribed Spacer (ETS) regions of nuclear ribosomal DNA (nrDNA) that would allow us to (1) examine the monophyly and circumscription of Silphium and its sections; (2) evaluate whether the Engelmanniinae should be expanded to include Balsamorhiza, Borrichia, Rojasianthe, Vigethia, and Wyethia; (3) evaluate the hypothesis of a Mesoamerican origin of the Engelmanniinae; and (4) examine the evolution of the cypsela complex.
MATERIALS AND METHODS
Sampling
Sequences of the ITS and ETS regions were obtained for 39 specimens (Table 1) representing the six genera of the subtribe Engelmanniinae (Berlandiera, Chrysogonum, Dugesia, Engelmannia, Lindheimera, and Silphium), and the five genera (Balsamorhiza, Borrichia, Rojasianthe, Vigethia, and Wyethia) that were identified as being closely related to the Engelmanniinae using cpDNA restriction site analysis (Panero, Jansen, and Clevinger, 1999
). Within Silphium 14 species were sampled. Podachaenium Benth., Squamopappus R. K. Jansen, N. A. Harriman, & Urbatsch, and Verbesina L. were chosen as the outgroups based upon cpDNA restriction site analysis (Panero, Jansen, and Clevinger, 1999
). The history of the subtribal classification of these genera according to Stuessy (1977)
, Robinson (1981)
, and Karis and Ryding (1994)
is outlined in Table 2.
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and purified by ultracentrifugation with cesium chloride/ethidium bromide gradients (Sambrook, Fritsch, and Maniatis, 1989
). Double-stranded DNAs of the entire ITS region and 383–460 bases of the 3' end of the ETS region were amplified directly by polymerase chain reaction (PCR). Originally, primers ITS4 and ITS5 (White et al., 1990
) were used for the amplification of the ITS region. Later a modified ITS5 (Downie and Katz-Downie, 1996
) was substituted for ITS5. Primers 18S-ETS and ETS-Hel-1 (Baldwin and Markos, 1998
) were used for the amplification of the ETS region. PCR protocol for the ITS began with an initial 4-min denaturation at 95°C, 45 s annealing at 48°C, and 1 min primer extension at 72°C, followed by 32 cycles with 1 min denaturation at 95°C, 45 s (2 s were added in each subsequent cycle) annealing at 48°C, and 1 min primer extension at 72°C. The reaction was terminated with an 8 min final extension at 72°C and then held at 10°C. PCR protocol for the ETS followed Baldwin and Markos (1998)
. PCR products were purified using filter centrifugation (Ultrafree-MC filter units, 30 000 nominal molecular weight limit—NMWL, Millipore Corporation, Bedford, Massachusetts, USA). DNAs were sequenced at the Automated Sequencing Facility, Plant Research Laboratories, Michigan State University, and the DNA Analysis Laboratory, Institute for Cellular and Molecular Biology, University of Texas at Austin. The ITS region was sequenced in both directions using the same primers used for amplification. In cases where these primers did not provide adequate sequences, the ITS was then sequenced using the internal primers, ITS2 and ITS3 (White et al., 1990
). The ETS region was sampled only from the 3 end with the 18S-ETS primer.
Sequence analysis
Proofreading and editing were performed on a Macintosh Computer using the program Sequencher 3.0 (Gene Codes Corporation, Ann Arbor, Michigan, USA). Alignments were made using the program Clustal X (Thompson et al., 1997
) with the default settings. Afterwards it was necessary to make some manual adjustments to the alignment. We did not include the 5.8S subunit in the ITS data set because sequence data for it were incomplete for the taxa that were sequenced using the internal primers. The 39 sequences reported in this study are available from GenBank (accession numbers AF171947–AF172063).
Phylogenetic analysis
The ITS and ETS data sets were first analyzed separately and then in combination. The combinability of the ITS and ETS sequences was assessed using the partition-homogeneity test (Farris et al., 1994, 1995
) in PAUP* 4.0b1 (Swofford, 1999
). Maximum parsimony analyses were conducted using a Power Macintosh 7200/120 with 32 MB of RAM and PAUP* 4.0b1. Given the large size of the data set, heuristic searches used the Tree Bisection Reconstruction (TBR) option with MULPARS and ACCTRAN optimization. The amount of support for the branches was assessed using 100 bootstrap replicates (Felsenstein, 1985
) with ten random additions per replicate using TBR and MULPARS.
RESULTS
Phylogenetic analysis of ITS and ETS
The length of ITS 1 in the taxa surveyed varied from 242 to 261 bp and the length of ITS 2 varied from 222 to 228 bp. The ITS1 data set included a 10-bp indel that was absent in Silphium asperrimum, S. asteriscus, S. brachiatum, S. gracile, S. mohrii, S. radula, and S. trifoliatum. All other indels in the ITS data set were three or fewer base pairs long. The ITS data set contained 216 invariable nucleotide positions and 280 variable nucleotide positions, of which 198 were phylogenetically informative. The parsimony analysis resulted in two shortest trees of 588 steps, a consistency index (CI) of 0.602 (excluding autapomorphies), and a retention index (RI) of 0.713. The length of the 3' region of the ETS in the taxa surveyed varied from 383 to 460 bp, including a 70-bp indel that was present in the outgroups but absent in all other taxa. All other indels in the ETS data set were either 1 or 2 bp long. The ETS data set contained 240 invariable nucleotide positions and 232 variable nucleotide positions, of which 146 were phylogenetically informative. The parsimony analysis resulted in 36 shortest trees of 495 steps, a CI of 0.593, and a RI of 0.823. Gaps were treated as missing data because it was found that when they were coded the topology of the tree did not change. Comparison of the strict consensus tree for each analysis can be found in Fig. 1.
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Analysis of combined data
The partition-homogeneity test results indicated that the ETS and ITS data sets were compatible (P = 0.09). Simultaneous analysis of the ETS and ITS data resulted in one most parsimonious tree (Fig. 2). It had a length of 1093, consistency index of 0.591 (excluding autapomorphies), and a retention index of 0.793. The ETS, ITS and cpDNA data sets (using only the 11 taxa that appeared in all three data sets) were found to be incompatible (P = 0.026).
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In the ITS analysis the Silphium clade had an unresolved basal trichotomy, but in the ETS and ITS + ETS analyses the genus was fully resolved into two main clades. These two clades corresponded to the morphological characters of root type and growth form. The clade containing S. asperrimum, S. asteriscus, S. brachiatum, S. gracile, S. integrifolium, S. mohrii, S. perfoliatum, S. radula, S. trifoliatum, and S. wasiotense was characterized by fibrous roots and a caulescent form. This was strongly supported by ten changes and a bootstrap of 100 in the ETS analysis and 11 changes and a bootstrap of 99 in the combined analysis. The clade containing S. albiflorum, S. compositum, S. laciniatum, and S. terebinthinaceum was characterized by tap roots and a tendency for a scapose inflorescence with a prominent basal rosette. It was strongly supported by three changes and a bootstrap of 90 in the ETS analysis. The support was weaker in the combined analysis with four changes and a bootstrap of only 69.
The fibrous-root clade of Silphium was further resolved into two clades. Silphium asperrimum, S. asteriscus, S. brachiatum, S. gracile, S. mohrii, S. radula, and S. trifoliatum formed a clade that was strongly supported in all analyses. This clade was supported by seven changes and a bootstrap of 100 in the combined data set. In the ITS data set it was also defined by a 10-bp deletion. Within this clade there was very little resolution of relationships between the species and varieties. The other clade contained S. integrifolium, S. perfoliatum, and S. wasiotense. It was strongly supported in the combined analysis by four changes and a bootstrap of 90. Silphium wasiotense was sister to S. perfoliatum rather than to S. mohrii and S. brachiatum as Medley (1989)
suggested. This was strongly supported in the combined analysis by four changes and a bootstrap of 98.
Within the taproot-clade, the Texas endemic Silphium albiflorum was derived from the widespread S. laciniatum. This was strongly supported in the combined analysis by eight changes and a bootstrap of 100. Fisher (1959)
and Fisher and Speer (1978)
hypothesized that S. terebinthinaceum var. pinnatifidum is a hybrid between S. terebinthinaceum and S. laciniatum. In our analysis Silphium terebinthinaceum var. pinnatifidum was sister to S. terebinthinaceum var. terebinthinaceum rather than to S. laciniatum.
Only two of the five sections of Small (1933)
were monophyletic in our analyses. These sections were Perfoliata, which is monotypic, and Laciniata, which contains only two species. Furthermore, sect. Laciniata was embedded within sect. Composita in the ETS and combined analyses. The clade containing sect. Dentata also included two species, S. asperrimum and S. mohrii from sect. Integrifolia.
Engelmanniinae
The six genera that Stuessy (1977)
placed in the Engelmanniinae did not form a monophyletic clade in our analyses. However, in the ETS analysis, the four genera (Berlandiera, Chrysogonum, Engelmannia, and Lindheimera) that have cypsela complexes together with Silphium formed a weakly supported clade with six changes and a bootstrap of 29. In the ITS analysis, Engelmannia was absent from this clade. If the data were constrained to include Engelmannia, however, the resulting most parsimonious trees were only two steps longer. The purported sixth member of the Engelmanniinae, Dugesia, was not sister to these genera in any of the analyses. Instead, nested between Dugesia and the rest of the Engelmanniinae were Balsamorhiza, Borrichia, Rojasianthe, Wyethia, and Vigethia. In all analyses Silphium, which lacks the cypsela complex, was derived from the taxa having it. Dugesia, a monotypic endemic genus from Central Mexico, was sister to Rojasianthe, a monotypic genus from southern Mexico and Guatemala. This was supported by 33 changes and a bootstrap of 70 in the combined analysis. Balsamorhiza and Wyethia were strongly supported as sister taxa by 15 changes and a bootstrap of 92 in the combined analysis.
DISCUSSION
Utility of the ETS region
Results of a phylogenetic analysis of the ITS region provided resolution between the genera of subtribe Engelmanniinae, but the sequences lacked sufficient variability to resolve relationships within Silphium. By sequencing a second spacer, the ETS region, we were able to strengthen the support for relationships between genera of the Engelmanniinae as well as resolve relationships among the species of Silphium. Our analysis supported Baldwin and Markos's (1998)
assertion that the ETS region can be useful in studies of young lineages in which the ITS region lacks sufficient variation.
Silphium
Our results supported the hypothesis that Lindheimera is the sister group of Silphium. They also supported the monophyly of Silphium, although the support for that was weak in the ITS analysis. Morphologically, Silphium and Lindheimera are quite distinct. Silphium differs from Lindheimera in being perennial and lacking the cypsela complex. Silphium has a base chromosome number of x = 7; Lindheimera has x = 8 (Settle, 1967
; Turner and Woodruff, 1993
).
Our results did not support the division of Silphium into the five sections as treated by Small (1933)
. Instead, we propose two sections based upon root type and growth form. One section will be formed from the clade containing S. asperrimum, S. asteriscus, S. brachiatum, S. gracile, S. integrifolium, S. mohrii, S. perfoliatum, S. radula, S. trifoliatum, and S. wasiotense. Small placed these species in sect. Dentata, Integrifolia, and Perfoliata. These taxa all have fibrous root systems and a caulescent growth form. Because this section contains S. asteriscus, the type species of the genus, the section must be called Silphium rather than Integrifolia, Perfoliata, or Dentata. The other section will be formed from the clade containing S. albiflorum, S. compositum, S. laciniatum, and S. terebinthinaceum. Small placed these genera in sects. Composita and Laciniata. These taxa all have tap roots and a tendency for a scapose inflorescence with prominent basal rosettes. Our results suggested that Small's sect. Laciniata evolved from within his sect. Composita, and therefore we propose that this clade retain the name sect. Composita.
Section Silphium
Our results supported two major clades within sect. Silphium. One clade contains S. integrifolium, S. perfoliatum, and S. wasiotense. Medley (1989)
hypothesized that his new species S. wasiotense is closely related to S. brachiatum and S. mohrii. All three of these species are geographically restricted to the southeastern United States. Our results, however, suggest that S. wasiotense is sister to the geographically widespread species S. perfoliatum. Both species have opposite leaves, but the leaves of S. wasiotense are petiolate, whereas the leaves of S. perfoliatum are connate-perfoliate. The second clade contains S. asperrimum, S. asteriscus, S. brachiatum, S. gracile, S. mohrii, S. radula, and S. trifoliatum. There was very little resolution among these species. Our current monographic study is exploring the morphological relationships of the species in this clade to determine whether there should be circumscriptional and nomenclatural changes. It appears that there is much introgression and/or phenotypic plasticity among these species, with the exceptions of the Appalachian endemics, S. brachiatum and S. mohrii.
Section Composita
Three of the members of this section, Silphium albiflorum, S. laciniatum, and S. terebinthinaceum, have 15–30 ray florets per capitulum; the other member S. compositum has 6–15 florets per capitulum. Our results supported the hypothesis that the reduction of ray floret number evolved once in sect. Composita. Furthermore, our results support that the Texan endemic S. albiflorum evolved from the widespread species S. laciniatum. Silphium albiflorum differs from all other Silphium spp. in having white disc and ray corollas and a short stature; its leaf shape is nearly identical to that of S. laciniatum. Two varieties of S. terebinthinaceum were sampled. Dr. Richard Fisher and his students (Fisher 1959
; Fisher and Speer, 1978
) hypothesized that var. pinnatifidum is the result of a hybridization of var. terebinthinaceum and S. laciniatum. Our results supported a close affinity of var. pinnatifidum to var. terebinthinaceum. To clarify whether hybridization has been involved in the evolution of S. terebinthinaceum var. pinnatifidum future studies should include sampling a chloroplast marker for these species and varieties.
Engelmanniinae
The Engelmanniinae was circumscribed by Stuessy (1977)
to include Berlandiera, Chrysogonum, Dugesia, Engelmannia, Lindheimera, and Silphium. Panero, Jansen, and Clevinger (1999)
concluded from their analysis of cpDNA restriction site data that the subtribe should be expanded to include the North American genera Balsamorhiza, Borrichia, Vigethia, and Wyethia and the Mesoamerican monospecific genus Rojasianthe. In no modern classification scheme for tribe Heliantheae have Balsamorhiza, Borrichia, Rojasianthe, Vigethia, and Wyethia been allied to the genera in Stuessy's Engelmanniinae (Table 2). Our results, based on nrDNA, concurred with the expanded concept of Engelmanniinae that Panero, Jansen, and Clevinger (1999)
suggest. These genera have previously never been allied to Stuessy's Engelmanniinae because they lack the cypsela complex, have fertile disc florets, and their cypselae are mostly quadrate. Furthermore Rojasianthe differs from all these genera in having a well-developed pappus and neutral ray florets. The one characteristic that all of these five genera do share with Stuessy's Engelmanniinae is foliaceous phyllaries.
Panero, Jansen, and Clevinger (1999)
suggested a Mesoamerican origin for subtribe Engelmanniinae. Our results based upon a more thorough sampling concurred with that hypothesis. The three outgroups, Podachaenium, Squamopappus, and Verbesina, used in this study are found in Mesoamerica and although Verbesina is found as far north as Canada its centers of diversity are Mexico and the Andes of South America (Panero and Jansen, 1997
). The two most basal genera of the Engelmanniinae are the monotypic genera Dugesia and Rojasianthe, the former of central Mexico and the latter of southern Mexico and Guatemala. We hypothesize that Dugesia and Rojasianthe represent paleoendemic relicts that evolved before the lineage spread north adapting to significantly different habitats. The coastal genus Borrichia and the northern Mexican genus Vigethia were the first to split off followed by radiations of Balsamorhiza and Wyethia into the western United States and Berlandiera, Chrysogonum, Engelmannia, Lindheimera, and Silphium into the eastern United States.
Based upon our results we hypothesize that Silphium is derived from the genera that have the distinctive cypsela complex. The most parsimonious interpretation of these results is that the cypsela complex evolved once and was subsequently lost in Silphium. We are currently studying the development of the capitulum in Silphium using electron microscopy to investigate whether any remnant of the cypsela complex is present during the initial states of the development of the ray and adjacent disc florets.
Traditionally, Balsamorhiza, Vigethia, and Wyethia, because of their similar cypsela morphology and large heads with foliaceous phyllaries, have been considered closely related (Weber, 1943, 1946
). Our results strongly supported Balsamorhiza and Wyethia as sister taxa, but Vigethia‘s relationship with them was unclear. In our analysis and that of Panero, Jansen, and Clevinger (1999)
, Vigethia was not placed near any one genus, indicating that there has been considerable divergence of Vigethia from the rest of the genera of the Engelmanniinae.
In conclusion, we propose that Silphium be divided into two sections, Silphium and Composita, which are circumscribed morphologically based upon root type and growth form. We also propose that subtribe Engelmanniinae be expanded to include: Balsamorhiza, Berlandiera, Borrichia, Chrysogonum, Dugesia, Engelmannia, Lindheimera, Rojasianthe, Silphium, Vigethia, and Wyethia.
FOOTNOTES
1 The authors thank Lowell and Mary Amick, Curtis Clevinger, Myra Miller, Anne Plovanich, Alan Risk, Sarah Simmons, and Dan Skein for field and/or lab assistance, John Bain, Doug Goldman, Jan Saunders, and Edward Schilling for providing leaf material or DNA, Robert Jansen, Edward Schilling, and Beryl Simpson for their review of the manuscript, and the curators of the following herbaria for the loan of specimens: F, FLAS, GH, IA, LL, LSU, MICH, MO, MSC, NCU, NY, OS, TENN, TEX, US, and USCH. Support for some aspects of this study was provided by grants from the Graduate School and Department of Botany at Michigan State University. This paper represents a portion of a doctoral dissertation by the first author submitted to the Department of Botany at the University of Texas at Austin. 
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 R. Acevedo-Rosas, K. Cameron, V. Sosa, and S. Pell A molecular phylogenetic study of Graptopetalum (Crassulaceae) based on ETS, ITS, RPL16, and TRNL-F nucleotide sequences Am. J. Botany, July 1, 2004; 91(7): 1099 - 1104. [Abstract] [Full Text] [PDF]
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G. D. Hoggard, P. J. Kores, M. Molvray, and R. K. Hoggard The phylogeny of Gaura (Onagraceae) based on ITS, ETS, and trnL-F sequence data Am. J. Botany, January 1, 2004; 91(1): 139 - 148. [Abstract] [Full Text] [PDF]
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A. J. Moore and L. Bohs An ITS phylogeny of Balsamorhiza and Wyethia (Asteraceae: Heliantheae) Am. J. Botany, November 1, 2003; 90(11): 1653 - 1660. [Abstract] [Full Text] [PDF]
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L. E. Urbatsch, R. P. Roberts, and V. Karaman Phylogenetic evaluation of Xylothamia, Gundlachia, and related genera (Asteraceae, Astereae) based on ETS and ITS nrDNA sequence data Am. J. Botany, April 1, 2003; 90(4): 634 - 649. [Abstract] [Full Text] [PDF]
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 J. F. Tooker, W. A. Koenig, and L. M. Hanks Altered host plant volatiles are proxies for sex pheromones in the gall wasp Antistrophus rufus PNAS, November 26, 2002; 99(24): 15486 - 15491. [Abstract] [Full Text] [PDF]
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