Genetic diversity in European beech (Fagus sylvatica L.) seed stands in the Romanian Carpathians

Authors

  • Anna-Maria Szasz-Len University of Agri­cultural Sciences and Veterinary Medicine Cluj-Napoca, Calea Manastur 3-5, 400372 Cluj-Napoca, Romania
  • Monika Konnert Bavarian Office for Forest Seeding and Planting, 83317 Teisendorf, Sudetenlandstr. 23, Germany

DOI:

https://doi.org/10.15287/afr.2018.1019

Keywords:

Fagus sylvatica L., genetic diversity, genetic differentiation, seed stand, natural regeneration

Abstract

In Romania, European beech (Fagus sylvatica L.) is the most important broadleaved tree species. The goal of the present study was to determine the genetic diversity and differentiation in and between natural beech populations from the Romanian Carpathians and the transmission of the genetic diversity to the next generation. The populations analyzed were registered as seed stands. Genetic analysis was based on ten nuclear microsatellites. The highest amount of genetic variation was within populations, whereas genetic differentiation between populations was low. In the adult populations the mean number of alleles per locus varied from 8.0 to 10.9, the effective number from 8.3 to 9.6. Heterozygosity ranged from 0.637 to 0.750 with the mean of 0.681(±0.018). The overall genetic differentiation FST between populations averaged 0.014. Geographic patterns within this region were not detected. Regenerating these stands naturally has not implied a reduction in the genetic variation in the following generation. Allelic richness, genetic diversity and heterozygosity in adult stands and their natural regeneration is not significantly different. Inbreeding effects were not observed (F between -0.032 and 0.061). The results complete the knowledge on genetic variation of beech in Romania and give insides into the genetic diversity of beech seed stands. They can be helpful too for the delineation of provenance regions in the Romanian Carpathians.

References

Anonymous, 2016. Statistica activităților din silvicultură în anul 2015 [Statistics of Forestry Activities in 2015]. National Institute of Statistics, București.

Anonymous, 2010. Ordin nr. 1028 din 30/06/2010 privind aprobarea delimitării şi descrierii regiunilor de provenienţă pentru materialele de bază din care se obţin materiale forestiere de reproducere din categoriile “sursă identificată” şi “selecţionat”, pentru speciile de interes forestier din România [Order no. 1028 of 30/06/2010 approving delimitation and description of regions of provenance for base materials from which is obtained forest reproductive material of “source identified” and “selected” categories for forest species of interest in Romania]. Official Journal no. 617 of 01 September 2010.

Anonymous, 2011. Legea nr. 107/2011 privind comercializarea materialelor forestiere de reproducere. [Law no. 107/2011 on the marketing of forest reproductive material]. Monitorul Oficial no. 430 of 20 June 2011.

Anonymous, 2012. Catalogul Naţional al Materialelor de bază pentru producerea materialelor Forestiere de Reproducere [National Catalogue of Basic Materials for Production of Forest Reproductive Materials]. Edited by Ministry of Environment and Forestry, National Forest Administration – ROMSILVA and Institute of Forest Research and Management – ICAS, Editura Silvica, București.

Asuka Y., Tani N., Tsumura Y., Tomaru N., 2004. Development and characterization of microsatellite markers for Fagus crenata Blume. Molecular Ecology Notes 4: 101–103.

Behm A., Konnert M., 1999. Erhaltung forstlicher Genressourcen durch naturnahe Forstwirtschaft - eine reelle Chance? [Conservation of forest genetic resources through close to nature forestry - a real opportunity?] Mitteilungen der Bundesforschungsanstalt für Forst- und Holzwirtschaft . Hamburg 194: 215–235.

Buiteveld J., Vendramin G.G., Leonardi S., Kamer K., Geburek T., 2007. Genetic diversity and differentiation in European beech (Fagus sylvatica L.) stands varying in management history. Forest Ecology and Management 247(1-3): 98-106.

Burczyk J., DiFazio S.P., Adams, W.T., 2004. Gene flow in forest trees: how far do genes really travel?. Forest Genetics, 11(3/4): 179-192.

Carlsson J., 2008. Effects of microsatellite null alleles on assignment testing. Journal of Heredity. 99(6): 616-623.

Chapuis M.P., Estoup A., 2007. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24(3): 621–631.

Chapuis M.P., Lecoq M., Michalakis Y., Loiseau A., Sword G.A., Piry S., Estoup A., 2008. Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Molecular ecology, 17(16): 3640-3653.

Chybicki I.J., Burczyk J., 2009. Simultaneous estimation of null alleles and inbreeding coefficients, Journal of Heredity 100: 106-113.

Ciocîrlan E., 2014. Structura genetică în populații marginale de fag (Fagus sylvatica L.) din România – evaluări cu markeri moleculari [Genetic structure of marginal beech (Fagus sylvatica L.) populations in Romania – evaluations using molecular markers], PhD Thesis. Forestry Department. University Transilvania, Brașov.

Ciocîrlan E., Sofletea N., Ducci F., Curtu A.L., 2017. Patterns of genetic diversity in European beech (Fagus sylvatica L.) at the eastern margins of its distribution range. iForest-Biogeosciences and Forestry, 10(6): 916-922.

Comps B., Gömöry D., Letouzey J., Thiébaut B., Petit R.J., 2001. Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157(1): 389-397.

Comps B., Thiébaut B., Paule L., Merzeau D., Letouzey, J., 1990. Allozymic variability in beechwoods (Fagus sylvatica L.) over central Europe: spatial differentiation among and within populations. Heredity 65: 407-417.

Cremer E., Fussi B., Konnert M. 2014. Forstgenetische Untersuchungen für die Praxis am ASP [Genetic investigations for forest practice at the ASP]. AFZ/Der Wald 16: 20-23.

Cuguen J., Thiébaut B., Ntsiba F., Barrière G., 1985. Enzymatic variability of beech stands (Fagus sylvatica L.) on three scales in Europe: evolutionary mechanisms, in: Jacquard P. (Ed.) Genetic Differentiation and Dispersal in Plants, NATO ASI Series, vol. G5, pp. 17-39.

Dakin E.E., Avise J.C., 2004. Microsatellite null alleles in parentage analysis. Heredity, 93(5): 504-509.

De Lafontaine G., Ducousso A., Lefèvre S., Magnanou E., Petit R.J., 2013. Stronger spatial genetic structure in recolonized areas than in refugia in the European beech. Molecular Ecology 22(17): 4397-4412.

Doniţă N., Bândiu C., Biriş I., Stan D., Zolotovici GH., 1997. Harta forestieră a României [Romanian Forest Map]. RNP- ICAS Bucuresti.

Doniţă N., Chiriţă C.D., Stănescu, V. et al., 1980. Zonarea şi regionarea ecologică a pădurilor din R.S. România [Ecological forest zones of R.S. Romania]. ICAS Seria a II a, Redacţia de propagandă tehnică agricolă. Bucureşti, p. 83.

Dounavi A., Netzer F., Celepirovic N., Ivanković M., Burger J., Figueroa A.G., Schön S., Simon J., Cremer E., Fussi B., Konnert M., Rennenberg H., 2016. Genetic and physiological differences of European beech provenances (F. sylvatica L.) exposed to drought stress. Forest Ecology and Management, 361: 226-236.

Dow B.D., Ashley M.V., 1998. High levels of gene flow in bur oak revealed by paternity analysis using microsatellites. Journal of Heredity, 89(1): 62-70.

Dumolin S., Demesure B., Petit R.J., 1995. Inheritance of chloroplast and mitochondrial genomes in pedunculated oak investigated with an efficient PCR method. Theoretical and Applied Genetic 91: 1253-1256.

Earl D.A., von Holdt B.M., 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.

Enescu V., Doniţă N., Bândiu C., Contescu L., Chiriţă C.D., Roşu C., 1988. Zonele de recoltare a seminţelor forestiere din R.S. România [Forest seed harvesting zones of R.S. Romania], Min. Silviculturii, ICAS Seria a II a, Bucuresti, p. 60.

Evanno G., Regnaut S., Goudet J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular ecology 14: 2611–2620.

Excoffier L., Lischer H.E.L., 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564-567.

Falush D., Stephens M., Pritchard J.K., 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4): 1567-1587.

Falush D., Stephens M., Pritchard J.K., 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7(4): 574-578.

Feurdean A., 2005. Holocene forest dynamics in northwestern Romania. The Holocene 15(3): 435-446.

Gömöry D., Hynek V., Paule L., 1998. Delineation of seed zones for European beech (Fagus sylvatica L.) in the Czech Republic based on isozyme gene markers. In Annales des Sciences Forestières 55(4): 425-436.

Gömöry D., Longauer R., Paule L., Krajmerová D., Schmidtová J., 2010. Across-species patterns of genetic variation in forest trees of Central Europe. Biodiversity and Conservation 19(7): 2025-2038.

Gömöry D., Paule L., Brus R., Zhelev P., Tomovic Z., Gracan J., 1999. Genetic differentiation and phylogeny of beech on the Balkan Peninsula. Jourbal of Evolutive Biology 12: 746–754.

Gömöry D., Paule L., Shvadchak I.M., Popescu F., Sulkowska M., Hynek V., Longauer R., 2003. Spatial patterns of the genetic differentiation in European beech (Fagus sylvatica L.) at allozyme loci in the Carpathians and the adjacent regions. Silvae Genetica 52(2): 78-83.

Gömöry D., Vysny J., Comps B., Thiebaut B., 1992. Geographical patterns of genetic differentiation and diversity in European beech (Fagus sylvatica L.) populations in France. Biologia (Bratislava) 47: 571–579.

Goudet J., 2002. FSTAT: a computer program to calculate Fstatistics. Version 2.9.3.2. J Heredity 86: 485-486.

Hamrick J.L., Godt M.J.W., Sherman-Broyles S.L., 1992. Factors influencing levels of genetic diversity in woody plant species. New Forests 6: 95-124.

Hartl D.L., Clark A.G., 1997. Principles of Population Genetics 3rd Ed. Sunderland, Massachusetts: Sinauer Associates, Inc.

Hasenkamp N., Ziegenhagen B., Mengel C., Schulze L., Schmitt H.P., Liepelt S., 2011. Towards a DNA marker assisted seed source identification: a pilot study in European beech (Fagus sylvatica L.). European Journal of Forest Research 130(4): 513-519.

Hazler K., Comps B., Sugar I., Melovski L., Tashev A., Gracan J., 1997. Genetic structure of Fagus sylvatica L. populations in southeastern Europe. Silvae Genetica 46(4): 229-235.

Hosius B., Leinemann L., Konnert M., Bergmann F., 2006. Genetic aspects of forestry in the Central Europe. European Journal of Forest Research 125(4): 407-417.

Hurlbert S. H., 1971. The nonconcept of species diversity: a critique and alternative parameters. Ecology 52: 577–586.

Ißleib D., Krabel D., 2005. Untersuchungen genetischer Strukturen in Buchen-Beständen (Fagus sylvatica L.) des mittleren Erzgebirges. Teil 1: Isoenzym-Genmarker [Investigations of the genetic structure in beech stands (Fagus sylvatica L.) of the middle Ore Mountains. Part 1: Isoenzyme Gene Marker]. Forst und Holz 60:190-193.

Janssen A., 2000. Untersuchungen zur genetischen Variation der Buche in Hessen: der Einfluss von Ernteverfahren auf die genetische Struktur von Saatgut eines Buchenbestandes [Studies on the genetic variation of beech in Hessen: the influence of harvesting methods on the genetic structure of seeds of a beech stand]. Forschungsberichte der Hessischen Landesanstalt für Forsteinrichtung, Waldforschung und Waldökologie 27: 142.

Jump A.S., Penuelas J., 2007. Extensive spatial genetic structure revealed by AFLP but not SSR molecular markers in the wind-pollinated tree, Fagus sylvatica. Molecular Ecology 16: 925–936.

Kavaliauskas D., Fussi B., Westergren M., Aravanopoulos F., Finzgar D., Baier R., Alizoti P., Bozic G., Avramidou E., Konnert M., Kraigher H., 2018. The Interplay between Forest Management Practices, Genetic Monitoring, and Other Long-Term Monitoring Systems. Forests 9(3): 133.

Kempf M., Konnert M., 2016. Distribution of genetic diversity in Fagus sylvatica at the north-eastern edge of the natural range. Silva Fennica 50(4): article id 1663. DOI: 10.14214/sf.1663.

Kim Z.S., 1985. Viability selection at an allozyme locus during development in European Beech (Fagus sylvatica L.). Silvae Genetica 34(4-5): 181-186.

Kimura M., Crow J.F., 1964. The number of alleles that can be maintained in a finite population. Genetics 49: 725-738.

Konnert M., 1995. Investigations on the genetic variation of beech (Fagus sylvatica L.) in Bavaria. Silvae Genetica 44(5): 346-350.

Konnert M., 2010. Contribution of forest genetics for a sustainable forest management. Polska Akademia Umiejetnosci Prace Komisji Nauk Rolniczych, Lesnych I Weterynaryjnych Pau Nr. 13: 67–78.

Konnert M., Fady B., Gömöry D., A’hara S., Wolter F., Ducci F., Koskela J., Bozzano M., Maaten T., Kowalczyk J., 2015. Use and transfer of forest reproductive material in Europe in the context of climate change, European Forest Genetic Resources Programme (EUFORGEN), Bioversity International xvi, Rome, Italy, p. 75.

Konnert M., Hosius B., 2010. Contribution of forest genetics for a sustainable forest management. Forstarchiv 81(4): 170-174.

Konnert M., Ruetz W., 2001. Genetic variation of beech (Fagus sylvatica L.) provenances in an international beech provenance trial. Forest Genetics 8(3): 173-184.

Konnert M., Zanker Th., Böhm H., 2010. Die Douglasie im bayerischen Staatswald [Douglas-fir in the Bavarian State forest]. AFZ/Der Wald 10, 26-28.

Lander T.A., Oddou-Muratorio S., Prouillet-Leplat H., Klein E.K., 2011. Reconstruction of a beech population bottleneck using archival demographic information and Bayesian analysis of genetic data. Molecular Ecology 20: 5182–5196.

Leberg P.L., 2002. Estimating allelic richness: Effects of sample size and bottlenecks. Molecular Ecology 11: 2445–2449.

Lefévre S., Wagner S., Petit R.J., de Lafontaine G., 2012. Multiplexed microsatellite markers for genetic studies of beech. Molecular Ecology Resources 12(3): 484-491.

Leonardi S., Menozzi P., 1995. Genetic variability of Fagus sylvatica L. in Italy: the role of postglacial recolonization. Journal of Heredity 75: 35-44.

Liesebach H., 2012. Genotypisierung mit nuklearen Mikrosatellitenmarkern – Möglichkeiten der Datenauswertung am Beispiel von Buchenpopulationen (Fagus sylvatica L.) aus einem Herkunftsversuch [Genetic characterisation of beech populations (Fagus sylvatica L.) from a provenance trial with nuclear microsatellite markers]. Landbauforsch 62(4): 221-236.

Liesebach H., Eusmann P., Liesebach M., 2015. Verwandtschaftsbeziehungen innerhalb von Prüfgliedern in Herkunftsversuchen – Beispiel Buche (Fagus sylvatica L.) [Sibship structure in samples from a provenance trial – A case study in beech (Fagus sylvatica L.)]. Forstarchiv 86(6): 174-182.

Longauer R., Gömöry D., Paule L., Blada I., Popescu F., Mankovska B., Müller-Stark G., Schubert R., Percy K., Szaro R.C., Karnosky D.F., 2004. Genetic effects of air pollution on forest tree species of the Carpathian Mountains. Environmental Pollution 130: 85-92.

Longauer R., Gömöry D., Paule L., Karnosky D.F., Mankovska B., Müller-Stark G., Percy K., Szaro R., 2001. Selection effects of air pollution on gene pools of Norway spruce, European silver fir and European beech. Environmental Pollution 115: 405–411.

Magri D, Vendramin G.G., Comps B., Dupanloup I., Geburek T., Gömöry D., Latałowa M., Litt T., Paule L., Roure J.M., Tantau I., van der Knaap W.O., Petit R.J., de Beaulieu J.-L., 2006. A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytologist 171: 199-221.

Mantel N., 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27: 209-220.

Merzeau D., Comps B., Thiebaut B., Cuguen J., Letouzey J., 1994. Genetic structure of natural stands of Fagus sylvatica L. (beech). Heredity 72: 269–277.

Milescu I., Alexe A., Nicovescu H., Suciu P., 1967. Fagul [The European beech]. Editura Agro-Silvică. Bucureşti, p. 244.

Müller-Starck G., Starke R., 1993. Inheritance of isoenzymes in European beech (Fagus sylvatica L.), Journal of Heredity 84: 291-296.

Nascimento de Sousa S., Finkeldey R., Gailing, O., 2005. Experimental verification of microsatellite null alleles in Norway spruce (Picea abies [L.] Karst.): Implications for population genetic studies. Plant Molecular Biology Reporter 23(2): 113-119.

Nei M, Maruyama T, Chakraborty R (1975) Bottleneck effect and genetic variability in populations. Evolution 29: 1-10.

Nei M., 1972. Genetic distance between populations. American Naturalist 106: 283-392.

Oddou-Muratorio S., Vendramin G.G., Buiteveld J., Fady B., 2009. Population estimators or progeny tests: what is the best method to assess null allele frequencies at SSR loci? Conservation Genetics 10(5): 1343-1347.

Paffetti D., Travaglini D., Buonamici A., Nocentini S., Vendramin G.G., Giannini R., Vettori C., 2012. The influence of forest management on beech (Fagus sylvatica L.) stand structure and genetic diversity. Forest Ecology and Management 284: 34-44.

Pârnuţă Gh., Lorenţ A., Tudoroiu M., Petrilă M., 2010. Regiunile de provenienţă pentru materialele de bază din care se obţin materialele forestiere de reproducere din România [Regions of provenances of basic materials for forest reproductive material in Romania]. Editura Silvică, Bucureşti, 122 p.

Pârnuță Gh., Mihai G., Ștețca I., Petrila M., 2005. Aspecte noi privind stabilirea și delimitarea regiunilor de proveniență pentru materialele forestiere de reproducere din România [New aspects regarding description and demarcation of the regions of provenance for the Romanian Forest Reproductive Materials]. Anale ICAS 48: 27-43.

Pastorelli R., Smulders M.J.M., Van’t Westende W.P.C., Vorman B., Giannini R., Vettori C., Vendramin G.G., 2003. Characterization of microsatellite markers in Fagus sylvatica L. and Fagus orientalis Lipsky. Molecular Ecology Notes 3: 76-78.

Paule L., 1995. Gene conservation in European beech (Fagus sylvatica L.). Forest Genetics 2(3): 161-170.

Paule L., Gömöry D., Longauer R., Krajmerova D., 2002. Patterns of genetic diversity distribution in three main Central European montane tree species: Picea abies Karst., Abies alba Mill. and Fagus sylvatica L. Lesnícky časopis 47(2): 153–163.

Peakall R., Smouse P.E., 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics (Oxford, England) 28: 2537–2539.

Petit R.J., Aguinagalde I., de Beaulieu J.L., Bittkau C., Brewer S., Cheddadi R., Ennos R., Fineschi S., Grivet D, Lascoux M., Mohanty A., Müller-Stark G., Demesure-Musch B., Palme A., Martin J.P., Rendell S., Vendraminn G.G., 2003. Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300: 1563-1565.

Popescu F., Postalache D., 2009. Markeri ADNcp [cpDNA markers]. In: Georgeta Mihai (ed.), Surse de seminţe testate pentru principalele specii de arbori forestieri din România [Tested seed sources for the main forest tree species from Romania]. Editura Silvica, București, pp. 208, 215, 220.

Pritchard J.K., Stephens M., Donnelly P., 2000. Inference of population structure using multilocus genotype data. Genetics 155(2): 945-959.

Rajendra K.C., Seifert S., Prinz K., Gailing O., Finkeldey R., 2014. Subtle human impacts on neutral genetic diversity and spatial patterns of genetic variation in European beech (Fagus sylvatica). Forest Ecology and Management 319: 138-149.

Stănescu V., 1979. Dendrologie [Dendrology]. Editura Didactică și Pedagogică, București, p. 267.

Starke R., 1996. Genetische Aspekte der Reproduction der Buche (Fagus sylvatica L.) unter Berücksichtigung waldbaulicher Gegebenheiten. Berichte des Forschungszentrums Waldökosysteme, Reihe A, Bd. 135, pp. 103.

Sulkowska M., Gömöry D., Paule L., 2012. Genetic diversity of European beech in Poland estimated on the basis of isoenzyme analyses. Folia Forestalia Polonica 54 series A: 48–55.

Szasz-Len A.M., 2016. Evaluarea diversității genetice a fagului european (Fagus sylvatica L.) în arborete surse de semințe din Munții Carpați [Evaluation of genetic diversity of European beech (Fagus sylvatica L.) in seed source stands in the Carpathian Mountains]. USAMV Cluj-Napoca, Ph.D. Thesis, pp. 174.

Takezaki N., Nei M., Tamura K., 2014. POPTREEW: Web version of POPTREE for constructing population trees from allele frequency data and computing some other quantities. Molecular Biology and Evolution 31(6): 1622-1624.

Tanaka K., Tsumura Y., Nakamura T., 1999. Development and polymorphism of microsatellite markers for Fagus crenata and the closely related species, F. japonica. Theoretical and Applied Genetics 99: 11-15.

Tanţău I., Feurdean A., de Beaulieu J.L., Reille M., Fărcaş S., 2011. Holocene vegetation history in the upper forest belt of the Eastern Romanian Carpathians. Palaeogeography, Palaeoclimatology, Palaeoecology 309(3-4): 281-290.

Tanţău I., Reille M., de Beaulieu J.L., Fărcaş S., 2006. Late Glacial and Holocene vegetation history in the southern part of Transylvania (Romania): pollen analysis of two sequences from Avrig. Journal of Quaternary Science 21(1): 49-61.

Tanţău I., Reille M., de Beaulieu J.L., Fărcaş S., Brewer S., 2009. Holocene vegetation history in Romanian Subcarpathians. Quaternary Research 72(2): 164-173.

Tröber U., Brandes E., 2004. Genetic structures of adult European beech (Fagus sylvatica) stands and the corresponding natural regeneration in the middle Ore Mountains – Pt 1: Isoyzme gene markers. In: Fürst C. (ed.), Sustainable Methods and Ecological Processes of a Conversion of Pure Norway Spruce and Scots Pine stands into Ecologically Adapted Mixed Stands. Forstwissenschaftliche Beiträge Tharandt 20: 121-130.

Van Oosterhout C., Hutchison W.F., Wills D.P.M., Shipley P., 2004. Micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

Vornam B., Decarli N., Gailing O., 2004. Spatial distribution of genetic variation in a natural beech stand (Fagus sylvatica L.) based on microsatellite markers. Conservation Genetics 5: 561-570.

Weir B.S., Cockerham C.C., 1984. Estimating F-Statistics for the analysis of population structure. Evolution 38(6): 1358-1370.

Ziehe M., Vornam B., Müller-Starck G., Turok J., Hattemer H.-H., Maurer W.D., Tabel W., 2002. Genetische Struktur der Buche in Rheinland-Pfalz [Genetic structure of beech in Rhineland-Palatinate]. Mitteilungen aus der Forschungsanstalt für Waldökologie und Forstwirtschaft Rheinland-Pfalz 49: 99-119.

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2018-07-03

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