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Ecology |
2Department of Botany and Ecology and Evolution, 437 Hesler Biology, University of Tennessee, Knoxville, Tennessee 37996 USA
Received for publication February 23, 2004. Accepted for publication January 20, 2005.
ABSTRACT
Thigmomorphogenesis refers to the widespread ability of sessile organisms to modify their morphology in response to a variety of mechanical stimulations, from direct contact with the stem by insects or other plants to flexure caused by wind, water, or snow. In this paper we investigated the differences in the reaction norms to wind exposure of seven species of the Brassicaceae that constitute a well-studied complex of known phylogenetic relationships. The goals included the characterization of differences between allopolyploids and their parental species and the comparison of wild and fast-cycling accessions within each species. We found statistically significant variation for plasticity among species or accessions for several characters, but the majority of the phenotypic variance was accounted for by overall (across-environment) differences among species and accessions and not by variation in plasticity. Allopolyploids displayed an array of behaviors when compared to their parents, from co-dominance to complete dominance to exceeding both parental means. Furthermore, fast-cycling plants showed distinct features from their wild relatives, suggesting that wild populations should be included with artificially selected lines in ecological studies. We proposed further steps to gain a more comprehensive understanding of thigmomorphogenetic responses, by integrating current research on the molecular bases of thigmomorphogenesis with insights into the ecology and evolution of plants exposed to wind.
Key Words: Brassica • phenotypic plasticity • Raphanus • thigmomorphogenesis • wind
Studies of phenotypic plasticity that consider phylogenetic relationships among taxa have the potential to shed light onto a variety of evolutionary responses to changes in the environment (Doughty, 1995
; Schlichting and Pigliucci, 1998
). Closely related species have been found to differ in their trait means, but not in patterns of plasticity (e.g., Pigliucci et al., 1999
). Alternatively, resemblance among species in their plasticities may reflect habitat similarity rather than phylogenetic relationships (Valladares et al., 2000
). Analyses of a particular kind of phylogenetic relationship—that between allopolyploid taxa and their parental diploid species—have found noticeably consistent patterns of phenotypic differentiation, in which hybrid or allopolyploid species most commonly show trait means and plasticities intermediate between those of the putative parental taxa (e.g., Repka et al., 1999
; Johnson et al., 2001
; Schranz and Osborn, 2004
). However, comparisons between lineages within a species, specifically between laboratory-selected lines and wild collections of annual Brassicaceae, have found that plasticities may differ between these sets of populations that have recent shared heritage (e.g., Pigliucci and Byrd, 1998
).
Plants that live in open fields and along roadsides may face environmental heterogeneity for a variety of habitat characteristics. An understudied component of the evolutionary ecology of plants growing in open habitats is phenotypic response to wind. Plants in open habitats are generally exposed to heterogeneous wind conditions, and wind responses are especially notable as altitude increases on mountains or with increasing proximity to the ocean. Phenotypic changes associated with wind exposure have been interpreted as generalized stress responses, examined from morphological and physiological points of view (e.g., Telewski and Pruyn, 1998
). Across life forms (from herbs to trees) phenotypic responses to wind or touch (thigmomorphogenesis) are generally similar, manifesting themselves most commonly as reduced stature and increased thickening of the stem (e.g., Jaffe and Forbes, 1993
; Cordero, 1999
), which in turn may confer resistance to other stresses (e.g., Biddington, 1986
; van Emden et al., 1990
). Pigliucci (2002)
found that Arabidopsis thaliana ecotypes exposed to sustained winds displayed genetic variation for phenotypic plasticity, though this was limited to branch number, possibly because of the rosette growth form (near the ground and hence less exposed to wind) of Arabidopsis thaliana. In agricultural systems, touch response has been investigated for some time (e.g., Biddington and Dearman, 1985
), and results have been used commercially to condition seedlings to withstand the physical stress associated with transplanting. However, little is known about the evolution of touch response despite its ubiquitousness, and this phenomenon may even confound ecological studies of plasticity to other environmental factors, if the investigator is not aware that simple repeated mechanical stimulation can affect—sometimes dramatically— several aspects of the plant's phenotype (e.g., Cahill et al., 2002
).
Expectations of the manner in which plants respond to wind are generally formulated for morphological traits and are often derived from general trends observed across taxa. For example, it is known that with increasing chance of flexure, stem diameter and root-to-shoot ratios tend to increase, whereas height and leaf area decrease (Telewski and Pruyn, 1998
; Cordero, 1999
). Cipollini (1999)
found similar patterns for morphological characters in Brassica napus, while simultaneously demonstrating that life history and fitness characters are also plastic in response to stem flexure. He showed that anthesis is delayed and flower number is reduced under stem flexure conditions and that all examined traits respond linearly to the dose. Cellular or molecular-level studies suggest that there may be underlying mechanistic similarities in hormone and/or gene action across taxa in response to wind or touch (Xu et al., 1995
; Smalle and van der Straeten, 1997
; Johnson et al., 1998
; Mussig et al., 2000
), perhaps reflecting a widespread and potentially phylogenetically ancient type of phenotypic plasticity.
In this paper, we investigate whether there are measurable differences in touch response among closely related species of Brassica and whether such differences may yield insights into the evolution of a generalized phenotypic response to mechanical stimulation. The genus Brassica includes several allopolyploid species (Thorman et al., 1994
; Warwick and Black, 1997
) that have persisted for a long time in nature, with ample time for selection to operate on aspects of their reaction norms (Pigliucci, 2001
). We characterize the manner in which multiple allopolyploid and parental species of Brassica respond to variation in wind exposure, an important component of their native habitat, particularly as these taxa occupy agricultural, coastal, and mountainous habitats. Members of the genus Brassica have an erect growth form and are rapidly becoming a model system in molecular genetics (e.g., Potter et al., 1999
; Lan and Paterson, 2000
), as well as evolutionary studies (e.g., Meyer, 2000
; Williams and Conner, 2001
). We examined several closely related species—three hybrid derived allopolyploid taxa, their diploid parentals, and a close relative of the group, Raphanus sativus, from both field-collected seed as well as rapid-cycling lines. The second component of this paper is a comparison of rapid-cycling laboratory lines with field populations of the same species. Rapid-cycling laboratory lines have been developed particularly for genetic studies and have undergone selection for early flowering under greenhouse settings in which wind exposure is often consistent and minimal. In contrast, field populations are likely from open disturbed sites and have evolved in heterogeneous wind environments. We utilized the different ecological histories of the laboratory and field lines to specifically compare field populations from heterogeneous wind environments (where we expect the evolution and maintenance of phenotypic plasticity for traits associated with wind response) and laboratory lines that have been exposed to generally constant wind environments (and for which we expect no plasticity to these conditions). We specifically examined traits that have been shown to respond to wind in other species.
We were interested in studying phenotypic plasticity to wind conditions at two levels of genetic differentiation: comparisons among populations characterized by different histories within a given species and comparisons within a phylogenetic framework between allopolyploids and their putative parentals. We asked the following questions: Are accessions including rapid-cycling and wild-collected populations of Brassica phenotypically plastic to increased wind exposure? Are rapid-cycling and wild populations different in their trait means? We hypothesized that rapid-cycling Brassica should have lower plasticity and trait means for morphological and life history traits compared to their wild-collected counterparts, due to the recent strong artificial selection for early flowering imposed on the rapid-cycling genotypes regardless of local environmental conditions (see Pigliucci and Byrd, 1998
, for evidence for this type of scenario concerning the laboratory lines Landsberg and Columbia of Arabidopsis thaliana, also a member of the Brassicaceae). Are allopolyploid species more similar in their trait means and plasticities to one parent than to the other, or do allopolyploids have intermediate phenotypes? Or do allopolyploids show phenotypes that trespass the range of variation encompassed by their parentals, possibly indicating the effects of complex (epistatic) genetic interactions? We have prior evidence that trait relationships between allopolyploids and their parental taxa are complex when examined under benign greenhouse conditions (Murren et al., 2002
), and we investigated here whether these complexities persist across wild populations and across multiple environmental conditions.
MATERIALS AND METHODS
We studied the evolution of touch response using six members of the genus Brassica: B. napus, B. nigra, B. carinata, B. oleracea, B. rapa, and B. juncea, as well as Raphanus sativus, a group for which a robust phylogenetic hypothesis is available (Galloway et al., 1998
; Koch et al., 2001
; and references therein). These species represent a hybrid complex in which the diploid parental species of the allopolyploid B. juncea are B. nigra and B. rapa, those of the allopolyploid B. carinata are B. nigra and B. oleracea, and those of the allopolyploid B. napus are B. rapa and B. oleracea (Fig. 1, Williams, 1989
; Song et al., 1990
). For each species, we utilized three accessions: one accession was a Wisconsin Fast Plants fast-cycling line, while the other two accessions were wild-collected seed from the native range of the species, obtained from the United States Department of Agriculture (USDA), the North Central Region Plant Introduction System (NCRPIS), the Centre for Genetic Resources in the Netherlands (CGN), and the Gottingen Botanical Gardens, Germany. Brassica rapa populations were collected from Turkey (USDA, #PI20911) and Poland (NCRPIS, #PI311723); B. oleracea populations were from Germany (USDA, #PI435900) and France (CGN, #14113); B. juncea accessions were collected from Germany (Gottingen, #712) and China (NCRIPS, #21719AMES); B. nigra populations were from Germany (USDA, #PI209782) and Turkey (USDA, #PI169057); B. napus seeds were from Great Britain (CGN, #14115) and France (USDA, #PI469791); B. carinata populations were from Kenya (NCRIPS, #19181) and Ethiopia (NCRIPS, #193459); and R. sativus accessions were from Germany (USDA, #PI209791) and Turkey (USDA PGRU, #PI169619). We chose accessions that spanned the native natural geographic ranges of the species and whose accession notes in the germplasm centers categorized the collections as natural wild populations. The geographic range of the populations and open areas in which they were found were consistent with natural variation in their wind environments and allowed us multiple points of contrast for each species with the rapid-cycling lines. Limitations of available greenhouse space constrained the number of populations that we could utilize as representative native populations.
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Seeds for a total of 630 individuals were planted on 28 February 2001. Five replicates were planted per block per treatment per species per collection combination. To minimize edge effects, during the course of the experiment, trays within chambers were carefully rotated multiple times to randomize as much as possible. Most plants were harvested at senescence. At harvest, plants were measured for height, stem diameter, leaf number, and stem biomass (as a measure of fitness), traits identified in previously published research to be associated with wind response. Biomass and overall reproductive success are often highly correlated (e.g., Murren et al., 2002
). Because no fruit were produced by these species in a greenhouse setting, stem biomass was used as a fitness measure. Stem diameter was measured above the first true leaf on the main stem. Leaf number was the total number of leaves produced on the plant. Stem biomass was collected after drying to a constant mass with all leaves and roots removed. Remaining plants were harvested and measured on 14 July 2001.
Statistical analyses
An analysis of variance (ANOVA; SAS, 1990
) model was developed to study the traits described. The ANOVA model accounted for: (1) overall genetic differentiation among species (species effect); (2) overall genetic differentiation between accessions (effect of collections, nested within species); (3) plasticity (treatment effect); (4) genetic differentiation for plasticity among species (species-by-treatment interaction); (5) genetic differentiation between collections within species (collection-by-treatment interaction); (6) microenvironmental effects within the greenhouse (block). Block was considered a random effect, whereas all other effects were considered fixed, because we were interested in the specific species and accessions (particularly the rapid-cycling ones). For each trait, the treatment effect was tested over the block-by-treatment interaction, unless the latter was nonsignificant, in which case the model error was utilized (Sokal and Rohlf, 1995
). To account for differences in time to first flower, separate regression models were conducted for each trait and the residuals of these models were utilized in the analysis of variance. Stem diameter and biomass were log transformed, and leaf number was square-root transformed to meet the assumptions of the regression model (Sokal and Rohlf, 1995
). For each species, collection, treatment, and trait combination, we determined the 95% confidence intervals around the trait means to examine biologically and statistically interesting differences, as well as to identify the overall patterns of reaction norms in response to wind.
To compare means and plasticities of fast-cycling with wild-collected accessions we performed another set of analyses of variance. The first model examined differences between the two accession types and included all species. A second model including block, accession type, treatment, and accession type by treatment were completed individually by species. The accession type was considered a fixed effect. Transformations and residuals were used as described previously. To compare allopolyploids and the parental taxa, we performed another pair of analyses of variance. In these analyses, B. nigra, B. rapa, and B. oleracea were the parental species. Brassica juncea, B. carinata, and B. napus were the allopolyploids. Raphanus sativus was omitted from this analysis. In the simple one-way ANOVA, only species categorization was utilized. The more complex model included block, treatment, species categorization, and treatment-by-species categorization interaction. Species categorization was considered as a fixed effect, and other transformations and residuals were the same as above.
RESULTS
The analysis of variance revealed that species were significantly different for all four traits examined and that these same traits were also significantly heterogeneous among collections (Table 1). There was a significant treatment effect on leaf number, stem diameter, and stem biomass, but not plant height. We uncovered few statistically significant interaction terms: treatment-by-species and treatment-by-collection for stem biomass and treatment-by-species for leaf number and stem diameter (Table 1). Interestingly, however, the relative importance of the various sources of variation (as judged by the proportion of MS explained or by the ranking of the F ratios) varied among traits. Block accounted for microenvironmental variation observed in the greenhouse, and we quantified significant differences between the blocks. In the cases of stem biomass and especially leaf number, species and collections within species accounted for the majority of the variance. However, variance in stem diameter was explained largely by differences among collections, while variance in height was accounted for mostly by differences among species (Table 1).
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In order to examine both the differences among collections (within species) and the effects elicited by the wind treatments (and corresponding interactions), we plotted the reaction norms of each accession for each trait (Fig. 3). The most general pattern emerging from these graphs, in agreement with the ANOVA results reported before, is that the treatments seemed to have a relatively minor effect on most accessions, yet there were several notable exceptions: the B. oleracea rapid-cycling line produced many more leaves in response to increasing wind conditions (Fig. 3a); one of the B. nigra, one of the R. sativus, both B. rapa wild collections, as well as the B. juncea fast line produced much thicker stems when exposed to wind, though the response was elicited mostly by the high wind condition (Fig. 3c). One of the B. carinata wild accessions reacted exactly in the opposite fashion, steadily decreasing its stem biomass with increasing wind (Fig. 3d).
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Wind-induced responses are a subset of the broader ensemble of "thigmo mechanisms" (Jaffe et al., 2002
) that have allowed plants to develop a wide array of adaptations mediated by the ability to sense and appropriately react to mechanical stimuli. The phenotypic responses to wind appear to be particularly important for species that grow in environments such as open areas of agricultural fields, roadsides, and meadows. Indeed, mechanically induced plasticity is widespread even outside of the plant kingdom (e.g., in fungi) and probably represents a major contribution to the success of sessile organisms (Jaffe and Forbes, 1993
; Jaffe et al., 2002
). Jaffe and Forbes (1993)
pointed out that, while the most spectacular mechanically induced responses are found under high levels of air or water turbulence, it is clear that sessile species are exposed to some degree of air or water movement in all but the most restricted laboratory conditions. This makes thigmomorphogenesis one of the most widespread and yet relatively little studied types of phenotypic plasticity (Pigliucci, 2001
). Additionally, as agricultural fields comprise the habitat for crop, natural, and weedy Brassica and as plants in these settings often experience strong wind to the point of falling over (lodging), the understanding of the ecological genetics of wind response may also have important agricultural implications for yield and weed management (e.g., see Cleugh et al., 1998
).
In this paper we set out to investigate phenotypic differentiation and plasticity for four traits known to be involved in thigmomorphogenetic responses by examining these questions in a phylogenetic framework of an allopolyploid and diploid complex of closely related species within the family Brassicaceae. In particular, we asked whether our natural and fast-cycling accessions of the seven species considered were phenotypically plastic for a variety of traits to mechanical stimulation induced by increasing duration of wind. Previous studies with another species of Brassicaceae (Arabidopsis thaliana) indicated that rapid-cycling genotypes may behave in a substantially different fashion from their close wild relatives (Pigliucci and Byrd, 1998
).
Within this phylogenetic framework, we also investigated the patterns of phenotypic similarity or dissimilarity between pairs of parental species and their allopolyploids, asking whether the phenotypes of the latter were intermediate between those of the parents, displayed partial or total dominance of one parent, or even exceeded the range of phenotypic values found in the parents—possibly indicating strong epistatic interactions. Our previous work with the same set of species (Murren et al., 2002
) indicated the presence of a complex mix of all these possibilities, although that study was conducted under a single greenhouse condition.
Plasticity to wind exposure of wild and rapid-cycling accessions
Our results show a statistically significant effect of the wind treatments on three of the four characters (the exception being plant height) and some variation for plasticity among species (stem biomass) or among accessions within species (stem biomass and leaf number). However, the phenotypic variance explained by these effects was relatively small when compared to that accounted for by the species and collection main effects in the ANOVA model. Our examination of the reaction norm plots confirmed the results from the analysis of variance: while some accessions showed clear responses to the environmental gradient, most were relatively insensitive to the variation in wind intensity. Interestingly, the qualitative pattern of the response was not at all uniform among accessions: for example, some genotypes increased their stem biomass with increasing wind conditions—mostly responding to the long wind treatment rather than the short one—but at least one genotype clearly reacted in exactly the opposite fashion. In another instance, Raphanus sativus reaction norm for stem diameter appeared clearly plastic, but it peaked at the intermediate level of wind exposure.
Across other systems, results tend to be heterogeneous as well: Cipollini (1999)
, using stem flexure with a bamboo rod in Brassica napus (one of the species we studied), found an essentially linear dose dependency of characters including plant height, root biomass, and stem diameter. Our accessions of B. napus, on the other hand, hardly responded to increasing exposure to constant wind. Interestingly, Cipollini (1999)
found that the thigmomorphogenetic response came with a potential reproductive cost, because his plants delayed anthesis and produced fewer flowers when exposed to mechanical stimulation. Pigliucci (2002)
found that exposure to wind resulted in a rearrangement of the phenotypic correlations of several (but not all) of the studied populations of Arabidopsis thaliana, so that the plants produced a bushy phenotype in response to wind. Such a phenotypic syndrome was largely driven by changes in the degree of branching of the inflorescence, which had a direct effect on plant's fecundity.
Work by Smith and Ennos (2003)
in Helianthus annuus may lend additional insight into the heterogeneity of the results obtained by different investigators. They discuss the obvious fact that when different species are used the plasticities reflect the past evolutionary history and current ecological conditions idiosyncratic to each species. They found that plants exposed to stem flexure reacted in a different, and indeed opposite, way to plants subjected to air flow. Specifically, wind increased plant height and stem hydraulic conductivity, while at the same time reducing stem rigidity and strength. Flexure did exactly the opposite, revealing a trade-off between mechanical flexibility and hydraulic capability. The fact that the study by Cipollini (1999)
and our study obtained different results while utilizing the same species, B. napus, may be explained, at least in part, by the flexure/air flow trade-off identified by Smith and Ennor (2003)
, as Cipollini (1999)
investigated the effects of direct stem flexure, while we addressed simulated wind exposure on trait expression. This is certainly a viable hypothesis that could be addressed by further studies of Brassica napus.
Of additional note is the finding that the reaction norms of the fast-cycling accessions tended to be different from those of their wild relatives for all traits except stem biomass. While these differences were not due to accession-level variation in phenotypic plasticity, the across-environment character means were clearly distinct. The fast-cycling plants conformed to an across-species syndrome of reduced leaf production, increased height, and decreased stem diameter. The combination of the last two traits explains why we found no difference between fast-cycling and wild plants in stem biomass: what the fast-cycling plants gained in stem biomass by increasing height they lost by thinning the stem. Although selection of other wild populations may have lead to different specific trait values and plasticities, the consistent pattern across all species is strong evidence that artificial selection in the rapid-cycling lines lead to divergent trait values across environments from wild populations chosen at random.
Pigliucci and Byrd (1998)
have suggested that lines that evolved under laboratory conditions, and in particular selected for a fast life cycle for experimental genetics, will be characterized by phenotypic syndromes that logically result from such selection regimes. Data presented here follow this suggestion; the differences in trait means we observed between wild and rapid-cycling accessions of Brassica were consistent even after variation in flowering time was taken into account. This makes such fast-cycling plants poor representatives of the phenotypic range of their wild relatives, something that needs to be considered seriously by ecologists and evolutionary biologists in light of the increasingly widespread use of specific lines designed for genetics and molecular biology being used for studies of a more ecological or evolutionary type. It increasingly appears that the study of an array of species or populations that are phylogenetically closely related to established lines would be the most useful. Such an approach will retain the advantages afforded by the molecular and developmental insights into the basic biology of the model systems, while also providing an array of ecologically and evolutionarily interesting taxa.
Differences between allopolyploids and their diploid parents
Patterns of phenotypic relationships between allopolyploids and their parents were not consistent across the species studied (see also Murren et al., 2002
). Using leaf number, we detected examples of almost exactly intermediate phenotypes in the allopolyploid (B. juncea), of allopolyploid phenotypes clearly exceeding the means of both parents (B. carinata), and of almost complete dominance of one parent (B. napus).
Indeed, of the 12 possible comparisons (three allopolyploid taxa, four characters), the outcomes were almost equally split, with three cases of intermediate phenotype, five of allopolyploids exceeding both parents, and four of clear dominance by one parent. Curiously, stem diameter was the only trait displaying only a pattern of dominance by one parent. Considering that the allopolyploid taxa are established biological species, which have undergone a great degree of independent evolution after the initial hybridization event, the variety of patterns that we found are consistent with the diverse ecological and evolutionary paths of each species (see also Schranz and Osborn, 2004
, for evidence of de novo variation in newly resynthesized Brassica polyploid and diploid taxa). If any simpler or more consistent pattern between allopolyploids and parental species is to be expected, this will be in cases of recent or continuous hybridization, before natural selection and other evolutionary causal factors have time to shift the genetic constitution of the hybrid polyploids.
The only other study of the effect of recent hybridization on thigmomorphogenesis of which we are aware was conducted by Pruyn et al. (2000)
on two recently derived Populus trichocarpa x P. deltoides hybrids—a situation in which more clear-cut patterns of phenotypic differentiation between hybrids and parentals may have been expected. The authors used stem flexure as the inducer of mechanical stimulation. They found some interesting differences, because they were able to produce a stem that was more tolerant to flexure and because both the mechanical properties of the stem and the allometric pattern of growth were altered. Unfortunately, these authors did not compare the hybrids with either parental species.
Concluding remarks
The study of thigmomorphogenesis has been pursued so far on two parallel, and almost independent, tracks. On the one hand, researchers have quantified the response in individual species under a set of controlled conditions, usually either stem flexure by direct mechanical means or exposure to wind (see earlier references). Here, we examined species and collections from across a geographical range that experienced heterogeneous wind conditions. On the other hand, the mechanistic study of the hormonal (e.g., Emery et al., 1994
; Sunohara et al., 2002
), and especially lower-level molecular (among recent examples: Shimmen, 2001
; Fasano et al., 2002
; Gutierrez et al., 2002
; Iliev et al., 2002
; Shepherd et al., 2002
) bases of touch response plasticity has been conducted primarily on model systems and largely in Arabidopsis.
Two of the gaps in our understanding of touch-response plasticity, therefore, deal with the ecological and evolutionary levels of analyses. From an ecological standpoint, we need field research on the effects of thigmomorphogenesis on the reproductive success of plants in natural populations or in agricultural settings in which wind can have an important effect on crop yield (e.g., Cleugh et al., 1998
). Additionally, studies of variation of traits both through development and across environments will lead to insights into the observed differences between rapid-cycling and wild populations, and together these studies would allow us to further connect the results of the controlled-condition studies to nature. From an evolutionary point of view, we need both additional studies of the degree of quantitative genetic variation for touch-response plasticity within natural populations and interspecific studies within a phylogenetic context to examine the evolution of the response.
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1 The authors thank Warren Denning and Ryan Jacobs for help with the construction of wind environments and with data collection in the greenhouse. We also thank Ken McFarland for his extensive assistance as greenhouse manager. 
3 E-mail: murrenc{at}cofc.edu
. Present address: Department of Biology, College of Charleston, 58 Coming Street Room 214, Charleston SC 29424
4 Present address: Department of Ecology and Evolution, State University of New York at Stonybrook, 650 Life Science Boulevard Stony Brook, New York 11794 USA
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