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Review Global warming and sexual plant reproduction Afif Hedhly1,2, José I. Hormaza2 and Marı́a Herrero1 1 2 Departamento de Pomologı́a, Estación Experimental de Aula Dei, CSIC, Zaragoza, 50059, Spain Estación Experimental la Mayora, CSIC, Málaga, 29760, Spain The sexual reproductive phase in plants might be particularly vulnerable to the effects of global warming. The direct effect of temperature changes on the reproductive process has been documented previously, and recent data from other physiological processes that are affected by rising temperatures seem to reinforce the susceptibility of the reproductive process to a changing climate. But the reproductive phase also provides the plant with an opportunity to adapt to environmental changes. Understanding phenotypic plasticity and gametophyte selection for prevailing temperatures, along with possible epigenetic changes during this process, could provide new insights into plant evolution under a global-warming scenario. Consequences of global climate change An increasing body of evidence indicates that global climate change is taking place and that it will have important effects on biological processes over the next decades. The expected climate changes include, among other factors, an increase in average temperatures, an increase in atmospheric CO2 concentrations and an alteration of rainfall regimes [1]. Although the reasons behind global warming are still controversial, its adverse consequences are clear and of increasing concern worldwide. Observed changes in phenotypic traits of different plant and animal species indicate that natural populations are responding to this change [2]. Indeed, global warming has been shown to affect species ecology, ranging from effects on geographical distribution, phenology or species interaction to extinction risks (reviewed in Ref. [3]). In agricultural systems, the fertilizing effect of increasing CO2 concentration and the consequent increase in yield dominated early conclusions [4]; however, the lower than previously thought crop response to CO2 [5] and its interaction with other factors, such as rising temperatures, is changing the view of climate change effects in crop plants and in modelling strategies [6]. Nonetheless, current estimates indicate that the moderate increase in temperature forecasted for the first half of this century might result in an increase in average yields in temperate and high latitude regions, whereas yield would be reduced in semi-arid and tropical regions [7]. The additional warming forecasted for the second half of the century would have a negative effect on yield in all regions, although the forecasts are variable depending on the crop and the geographical area. Reports are already showing a negative effect of climate change on yield in Corresponding author: Hedhly, A. ([email protected]). 30 some crop species [8,9]. Respiration and photosynthesis [10] have been proposed as the main physiological processes affected by temperature and CO2 increases. However, the acclimation registered in such processes [11,12], the spatial–temporal heterogeneity of the climate change and the threshold responses of some plant developmental stages suggest that additional processes are also affected [6]. Little is known, however, on the actual effect that changes in temperature might have on the different plant developmental stages. Here, we discuss the effect of temperature change on the reproductive phase from an ecological, agricultural and physiological perspective, and we evaluate the potential implications of the forecasted global warming on this phase. Effects of increasing temperatures on the sexual plant reproductive phase We believe that three main points support the idea that the reproductive phase is a good candidate to be affected by climate change: (i) the events of irregular and reduced cropping; (ii) the forecasted change in temperature mainly in the spring, during the flowering season of many plant species; and (iii) the available information on the direct effect of temperature stress on the reproductive phase. (i) The processes that take place during the reproductive phase are determinant for final production in crop species cultivated by their seeds and/or fruits. The effect of high temperatures on the reproductive phase seems to be more pronounced in plant species that are at the limit of their cultivation range and, consequently, highly sensitive to short episodes of extreme temperatures [13]. A characteristic of global climatic change is the increase in the frequency of extreme temperatures, which are likely to reduce crop fertility and yield [6,7,14]. Possible yield increases due to CO2 enrichment might not offset the negative effects of high temperatures on reproductive processes, particularly if high temperatures coincide with sensitive stages of reproductive development [6,15]. Recent examples of the effect of global warming on yield include a 17% reduction in corn (Zea mays) and soybean (Glycine max [L.] Merr.) grain yields in the US Midwest [8] and a 15% reduction in rice (Oryza sativa) grain yield in the Philippines [9] for each 1 8C increase in temperature during the growing season. In fact, a recent modelling of extreme high temperatures forecasts a reduction of premium grapevine production in the US by 81% at the end of 1360-1385/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2008.11.001 Available online 4 December 2008 Review the 21st century [16]. The mechanisms underlying these effects are still unknown but, as outlined above, some evidence points to the reproductive phase as a potentially sensitive stage. High temperatures are likely to shorten the growing cycle of many crop species and, during some developmental stages, such as the reproductive phase, most crops are only able to tolerate narrow temperature changes, which, if exceeded, can reduce seed set and thus yield [14]. (ii) In some regions, mainly at higher latitudes, temperatures during the spring – when blooming of many crop plants takes place – are changing rapidly. In fact, the pronounced increase in temperature experienced so far has been mainly registered in late-winter and early-spring [17–19]. Indeed, for biological and agricultural systems, the timing and frequency of extreme temperature events could be more important than the increase in mean temperatures [16]. Likewise, the most recent best estimates of global average surface air warming range from 1.8 8C for the lowincrease scenario (with a range of predictions from 1.1 8C to 2.8 8C) to 4.0 8C for the high-increase scenario (with a range of predictions from 2.4 8C to 6.4 8C) at the end of the 21st century, and warming is expected to be greatest over land and at higher northern latitudes [1]. Besides the well-documented effect of winter–springtime temperature on the advancement of flowering time [2,3], subsequent reproductive processes, which are known to be sensitive to temperature stress, will necessarily be affected in these changing conditions. Irregular production in warm springs can indeed be explained by an effect of temperature on the reproductive phase (e.g. [20]). Thus, based on the narrow threshold responses during flowering time and the projected increase in extreme events, more data on spatiotemporal temperature climatic variation and their overlap with sensitive developmental stages such as flowering is needed for better modelling of future effects of global warming [6]. (iii) Before the current worldwide concern over global warming, information had built up showing that temperature stress affects the reproductive process. The response varies depending on the plant species, but both male and female functions are affected, along with the reproductive process itself. Due to the role that temperature has in crop adaptation and expansion to new latitudes, studies have mainly concentrated on cultivated and economically important annual crop species, in which the reproductive phase seems to be recurrently affected by temperature and is considered among the most sensitive stages of the plant life cycle [21]. In the different experiments performed, the stress was generally applied simultaneously to several different developmental stages, and this seemed to affect the final product. However, this approach misses developmental-stage-specific responses, which seem to be uncoupled and not necessary additive [6,22]. Thus, a better estimation of the effect of temperature could be obtained by studying the sensitive stages independently and then Trends in Plant Science Vol.14 No.1 integrating those effects into the whole plant response. In this sense, evaluation of temperature stress on the sexual reproductive process could be separated into three consecutive and interdependent developmental stages (Figure 1): gamete development, the progamic phase from pollination to fertilization and postzygotic early embryo development. In the next sections we will discuss the available data that deal with the effect of temperature variation on sexual plant reproduction, from gamete development to the beginning of the next plant generation. Gamete development High temperature stress during gamete development has been shown to affect plant reproduction with immediate and long-term effects. Some immediate effects on the female gametes mediated through flower production and their viability have been recorded [23,24]. However, probably because it is easier to handle, most of the work has concentrated on the male function. Thus, the quantity and morphology of pollen, anther dehiscence and pollen wall architecture, as well as the chemical composition and metabolism of pollen [15,24–26], have been shown to be affected by high temperatures. All these effects could alter male fitness by reducing the available amount of pollen and could also – if the pollen limitation is severe –indirectly limit female fitness by reducing the number of seeds sired. However, given the great amounts of pollen produced in most plant species, small variations in temperature, although inducing an effect, are not expected to produce very dramatic effects in terms of reproductive output. More subtle, but perhaps more important, is the effect that the temperature during pollen development seems to have on pollen performance. Although the range of temperature tolerance threshold is highly variable between species, mild increases in temperature negatively affect characteristics such as pollen viability [26,27], pollen germinative ability [24,28,29], pollen tube growth rate [29] and seed and fruit set [25,27]. Several studies across a range of unrelated genera on the effect of diverse biotic and abiotic factors during pollen development indicate that selection among developing microgametophytes has an effect beyond the gametophytic generation by altering the composition and performance of the next sporophytic generation [30–32], and temperature stress is one of the factors governing selection [29]. Thus, it seems that temperature variation during pollen development can alter pollen performance and that this effect might lead to changes in the genetic frequencies of the next sporophytic generation. But the extent to which this might be a general phenomenon remains to be explored. From pollination to fertilization Considering uniform and optimum conditions during gamete development, temperature variation during the postpollination–prezygotic stage affects both male and female functions, as well as the interaction between the two. The two main effects on the postpollination–prezygo31 Review Trends in Plant Science Vol.14 No.1 Figure 1. Temperature stress experienced during gamete development (blue), the postpollination–prezygotic stage (red) and the postzygotic stage (green) alters these stages (large coloured arrows) and also has long-lasting consequences on subsequent stages (small coloured arrows). Some processes warrant further investigation, such as how temperature stress at a given level might affect stress response at a different level (red question marks) or the nature of the reported transmitted effects for each stress level (green question marks). Gametophytic and sporophytic stages are shown with yellow and blue background colours, respectively. tic stage are (i) the acceleration or retardation of the whole process and (ii) the potential influence of the prevailing temperatures on pollen selection. Male–female synchrony for successful mating On the male side, temperature affects the quantity of pollen that succeeds in germinating [33,34], as well as the rate of pollen tube growth along the reproductive tract. John T. Buchholz and Albert F. Blakeslee [35] were the first to show an effect of high temperature on pollen tube growth rate in Datura stramonium L. Since then, data from both herbaceous [34,36] and woody plant species [37– 39] suggest that an acceleration of pollen tube growth under high temperatures and a slowing-down under low temperatures seem to be a general phenomenon. Although relatively less attention has been paid to the female counterpart, an effect of temperature on the female side has also been put forward. High temperatures accelerate overall female development, whereas low temperatures slow it down. Thus, high temperatures accelerate stigma and ovule development, reducing the duration for which they are receptive to pollen and pollen tubes, whereas low temperatures prolong both stigmatic receptivity and ovule longevity [40,41], extending the receptivity 32 period. Consequently, temperature stress seems to have a complementary effect on the male and female counterparts, accelerating or slowing down the reproductive process. However, this idea is true only within a given range of temperature, that to which a particular genotype is adapted, and exceeding this range might be detrimental to the reproductive process due to the shortening of the female receptive time. This might have severe consequences for the reproductive output, inducing low seed and/or fruit set [15,20,27,28]. Male–female synchrony seems to be a prerequisite for successful mating in plants [42], and fertilization occurs when the two gametes are at the same phase of the cell cycle [43]. Also a reduction in female receptivity might jeopardize pollination, especially under suboptimal pollinator activity, which can also be affected by changing environmental conditions. Pollination failure in insect-pollinated crops is of rising worldwide concern because weather change in spring can cause the uncoupling of insect cycles and flowering phenology [44]. Pollen competition and selection Temperature might also affect pollen selection during the progamic phase. The existence of pollen selection has caused some controversy (Box 1). During the reproductive Review Box 1. Hallmarks in pollen selection theory At the beginning of the 20th century, John T. Buchholz [70] was among the first to address what he called developmental selection, the potential evolutionary consequences, for both gymnosperms and angiosperms, of selection among male gametophytes represented by pollen tubes. J.B.S. Haldane [71] noted the ‘serious overcrowding’ of pollen grains in the stigma, which makes pollen competition likely. In 1979, David L. Mulcahy [45] synthesized these findings and integrated them in a hypothesis to explain the rise of angiosperms. He proposed that insect pollination and closed carpels, which are characteristics of primitive angiosperms, might intensify gametophytic competition and selection. In this way, flowering plants might take advantage of sexual recombinants while eliminating poorly functioning haploid individuals. Thanks to the correlation between pollen tube growth rate and performance of the next generation, he stated that the effect of gametophytic selection is not limited to the haploid generation and could influence the next sporophytic generation. This is further supported by the overlap in gene expression between the gametophytic and sporophytic phases. Since then the gametophytic competition and selection hypothesis has faced some questioning. First, owing to technical limitations, the finding of overlap in gene expression was initially based on data from few genes. However, with the help of high-throughput technology, we now know that the overlap of expression patterns is extensive [72]. Second, for gametophytic competition to occur, there must be more pollen grains in the stigma than ovules to be fertilized. Because the first results were obtained in cultivated plants, a question arose about the occurrence and magnitude of pollen surplus in natural systems. However, pollen surplus was also registered in natural populations [73]. Third, the genetic variation of pollen tube growth rate versus plastic response, reflecting environmental and nutritional conditions during development, provided another challenge. The key to gametophytic competition and selection – and its potential evolutionary implication – is the existence of genetic additive variation. This subject has been addressed [74], but variation in pollen tube growth could also be explained as the after-effects of gametophyte developmental conditions [32]. Fourth, because pollen performance is related to fitness and fitness is exposed to natural selection, we would expect genes controlling pollen performance to have been fixed during the evolutionary process. However, mechanisms such as male–female and genotype–environment interactions result in the modulation of pollen performance depending on the female genotype and the environmental factors and, consequently, variability for pollen performance can be maintained [30]. However, an additional question still needs to be addressed. So far, there is no direct evidence at the cellular and molecular levels of male–male competition or female choice, and works are generally based on indirect evidence (e.g. [75]). The only advance in this field comes from interspecific crosses, in which pollen tube paternity analysis revealed that conspecific fertilization precedence was mediated by favourable or unfavourable male–female interactions [76]; results are lacking at the intraspecific level. Further work is needed not only to give further support to the theory of pollen selection but also to mark the boundaries between genetically based variation in pollen competition (with respect to the plastic behaviour of pollen tubes in response to prezygotic differential provision of pollen grains) and selective postzygotic embryo abortion. Currently, non-random fertilization is widely accepted in plants, whereas both male competition and female choice are becoming unifying concepts of mate choice in plants and animals. Recent advances in molecular biology are revealing additional nonmendelian segregations during sexual plant reproduction, and these discoveries could answer some old questions that could not be addressed with traditional genetic approaches. process, an intense pollen competition that seems to be the substrate for gametophytic selection takes place in the pistil [45]. The first evidence for differential selection at the gametophytic level in response to low temperature Trends in Plant Science Vol.14 No.1 stress was demonstrated in cultivated and wild tomato (Lycopersicon esculentum Mill. and Lycopersicon hirsutum Humb. and Bonpl.) [46]. After mixed pollinations using pollen from genotypes with a differential temperature adaptation, a different paternity contribution occurred depending on the prevailing temperatures during the reproductive process. Later work demonstrated that cold tolerance was determined by genes expressed in the pollen genome [47] and that selection at the gametophytic level correlates to root elongation capacity under the same conditions [48]. Similar results were obtained in several unrelated plant species and confirmed a genotype– temperature interaction for pollen performance and for siring success [38,49]. Recent studies in sweet cherry (Prunus avium L.), a woody perennial species that promotes intense pollen competition, show that temperature affects pollen tube dynamics and, as a consequence, influences the proportion of pollen tubes that succeed in reaching the ovary [33]. Similarly, a clear genotype–temperature interaction that reflects climatic adaptation of the pollen donor has been observed [39]. More work needs to be done in different plant species, but these results suggest a natural selection of the best-adapted pollen tubes to the prevailing temperature during the reproductive phase. Future findings will contribute to the understanding of rapid adaptation to temperature and the rapid emergence of landraces that are well-adapted to new latitudes. Postzygotic stage Target oriented experiments analysing the effect of temperature stress at the postzygotic level are scarce. However, the study of the relative importance of preversus postzygotic temperature variation (15 8C nights/ 20 8C days and 20 8C nights/26 8C days at both stages) on offspring fitness and performance in field experiments in Plantago lanceolata L. [50] showed a major effect of postzygotic variation on offspring fitness. Higher temperature increased offspring fitness by 50%; furthermore, genotype-specific responses for seed germination, flowering time and spikelet production were observed. Likewise, in Norway spruce (Picea abies [L.] Karst.), cold and warm environments experienced during zygotic embryogenesis and seed maturation advanced and delayed, respectively, several progeny adaptive traits, such as bud set, cold acclimation in the autumn and dehardening and flushing in spring [51], and the changes last for at least two growing seasons [52]. Similar postfertilization effects have been registered in Arabidopsis thaliana, under both high and low temperatures [53]. Interestingly, the registered progeny hardening in P. abies was suggested to reflect temperature-induced epigenetic changes during embryo development and seed maturation. Taking all these effects together, it seems that the sexual phase in flowering plants is an active developmental process subjected to different selective forces. Heat stress affects male and female gametogenesis, pollen–pistil interaction and embryo development. Moreover, the three processes interact and have a bearing on each other. Finally, in addition to observed effects on reproductive output, the genetic composition, phenology of adaptive traits and fitness of the next generation might also be 33 Review influenced. From this perspective, we will discuss in the next sections both the ecological and evolutionary implications of global warming. Immediate implications The immediate effects of global warming are already observable, both in natural populations and in agricultural systems. These effects mainly concern: (i) the early onset of sexual reproductive development; (ii) higher or lower reproductive output, depending on the regions and species under study; and (iii) the expansion of crop plants and shifts in geographic distribution of natural populations towards higher latitudes. Early flowering in response to higher temperatures [2] is actually an advancement of the whole reproductive process that could potentially alter plant–pollinator interaction and subsequent reproductive stages; the effect of global change on plant phenology has been extensively reviewed elsewhere (e.g. Ref. [54]). The second immediate effect is the reproductive output. Although the dominant picture of the effect of global warming is an extension of the growing season and an increase in yield in some species and regions [1], the forecasted increase in the frequency of exposure to extreme temperatures and to short episodes of heat waves, changes in frost frequency and heat-induced shortening of developmental phases [6,14,55] are likely to cause irregular cropping. Current data indicate that temperature stress experienced during gamete development, the progamic phase and embryo development reduce final seed and fruit set. Different tools are available for investigating the cause further. First, determining the weak steps of the process provides a frame for disentangling the causes of erratic crops. These studies have the advantage that they do not require high technology because simple methods are available for evaluating both stigma and ovule receptivity, as well as pollen germination and pollen tube behaviour and their influence on the subsequent fruit set. Second, enough genetic variability is still present within many crops to enable the selection of new cultivars for new situations. Interestingly, this genetic variability has been previously selected and conserved owing to the adaptation of the different crops to different habitats and latitudes. A third expected immediate effect is plant migration. This can already be observed in natural populations (reviewed in Ref. [3]) and is expected to happen in agricultural systems (e.g. [16]). Geographical displacement of some crops might represent an advantage for higher latitude regions, opening the possibility for new crops not previously grown in those locations. However, this might represent a problem with socio-economical implications at lower latitudes, where most developing and undeveloped countries are located and where local populations can be highly dependant on specific crops, the disappearance of which could cause food shortages. Again, the search for new genotypes adapted to the changing environmental conditions might be an alternative. Long-term evolutionary and ecological implications The evolutionary implications of climate change in plants have received less attention than in animals. The best way 34 Trends in Plant Science Vol.14 No.1 to forecast the potential evolutionary implications of climate change is to learn from past experience, such as the different climate changes over the Quaternary period (the last 2.6 million years of geological time). During the Quaternary, sparse speciation events have been registered in plants, unlike in mammals [56]. However, the finding that abundant genetic differentiation has taken place during the Quaternary within different populations of the same plant species gives support for rapid evolutionary adaptation processes [57]. Clinal variation in physiological, phenological and fitness traits in relation to latitudinal or altitudinal climate gradients is the best example of such differentiation [58–60]. Furthermore, common garden experiments show that most tree and herbaceous plant species comprise a series of populations adapted to their respective local environments [57]. Thus, the palaeoecological idea that species, if climate change is outside their tolerance limits, will have to shift their geographic distribution or, alternatively, face extinction has been reviewed, and it has been argued that plant migration actually occurs via evolutionary adaptive processes [57,60]. However, the mechanisms underlying these adaptive processes are not yet well understood. Plant reproduction, together with death, represent two basic processes of population dynamics [61]. Thus, if climate change could modulate sexual plant reproduction, the consequences could be far reaching. Global change is already affecting animal sexual reproduction, leading to potential ecological and evolutionary implications [62]. In plants, genetic variation in fitness has been reported to be elicited by spatial climate variation. Thus, it is plausible that climate change might cause adaptive evolution of fitness-related traits [60]. Consequently, if climate change can modulate sexual plant reproduction, which strongly contributes to fitness, it is tempting to speculate that the sexual reproductive phase will have an important role in these adaptive processes. In the light of new progress in plant response to temperature stress during the sexual phase, two important players, gametophytic selection and phenotypic plasticity, seem to adjust plant behaviour against stress across generations, influencing the pace and direction of evolutionary processes. Both processes have been proposed as underlying mechanisms of variation in pollen performance and siring success [30–32]. Gametophytic selection under temperature stress can affect the rate of response to selection. Evolution of a life-history pattern is, indeed, not only dependent on genetic variation, which has been demonstrated for pollen performance and siring success (Box 1), but also on the environment in which selection takes place [50]. As detailed above, genotype–temperature interaction has been reported for pollen tube growth and for siring success. Furthermore, the finding that this selection could reflect the origin and adaptation of the pollen-producing sporophyte [39,46] is undoubtedly important for the dynamics of population genetic structure [63]. Phenotypic plasticity, defined as the ability of a genotype to adjust its developmental programs in response to environmental fluctuation [64], is important in terms of withstanding a changing environment and species evolutionary dynamics. It can accelerate or slow down the impact of environmental factors on population dynamics, might underlie ecological Review success in new habitats, can influence the direction of the response to selection [64] and has been interpreted also as a means of maintenance of genetic variability in pollen performance [32]. Perspectives The susceptibility of the reproductive phase to environmental stress also hides the strength of providing an opportunity for change by means of gametophytic selection and phenotypic plasticity. The possibility that gametophytic selection might favour the best-adapted genotypes to prevailing temperatures is an attractive hypothesis that warrants further investigation, and it could explain plants’ rapid adaptation to different temperatures while maintaining variability. Although the literature on pollen competition and selection is abundant (Box 1), the molecular mechanisms underpinning this selection are still to be analysed. Phenotypic plasticity is, however, experiencing a renewed interest and, although the precise mechanisms behind phenotypic plasticity are still to be deciphered, epigenetic mechanisms have been reported to be involved [65], suggesting that the epigenetic machinery might be superimposed on DNA sequence variation-based transgeneration effects. Incipient results show parent-of-origin upand downregulation of some progeny genes in P. abies [51] and A. thaliana [53]. These memory effects, potentially epigenetic in nature [51], are a consequence of temperature stress during embryo development. When they are generated in this way (i.e. in somatic cells), epigenetic marks are stable through mitosis and in some cases, such as flowering time in Arabidopsis [66], they are reset in each generation. However, to have evolutionary implications, these effects have to be transmitted to the subsequent generations through the male and/or female gametophytes. Interestingly, recent findings reveal that epigenetic marks can be often heritable over generations through DNA methylation [67,68]. Thus, although epigenetic modulation of embryo development could be important for adjusting the phenotype of the progeny, the prezygotic stages in which gamete development takes place in plants can be the key step for transgenerational effects. Furthermore, unlike in animals, in plants male and female gametophytes are exposed structures, which potentially makes them especially susceptible to environmental stress [69]. Thus, understanding epigenetic dynamics in plants, from the commitment of a sporophytic cell to be a germline to embryo development, will undoubtedly help to clarify potential temperature-stress-sensitive stages and, ultimately, heritable stress-induced epigenetic effects. Work aimed at elucidating the extent of gametophytic selection and epigenetic machinery in modulating plant constitution between generations and their interaction with environmental stresses will provide a better understanding and projection of ecological evolutionary dynamics under the current scenario of increasing temperatures. Acknowledgements Financial support for this work was provided by the Spanish Ministry of Education and Science (project grants AGL2006-13529-C02-01 and AGL2007-60130/AGR) and by the Diputación General de Aragón through the ‘Grupo Consolidado de la Comunidad Autónoma de Aragón, A-43’. A.H. was supported by ‘Juan de la Cierva’ and JAE-doc grants. Trends in Plant Science Vol.14 No.1 References 1 Intergovernmental Panel on Climate Change (2007) Summary for policymakers. In Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Solomon, S. et al., eds), Cambridge University Press 2 Menzel, A. et al. (2006) European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12, 1–8 3 Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 4 Long, S.P. et al. 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