Genetic Structure of a Worldwide Germplasm Collection of Prunus armeniaca L. Reveals Three Major Diffusion Routes for Varieties Coming From the Species' Center of Origin
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
32523597
PubMed Central
PMC7261834
DOI
10.3389/fpls.2020.00638
Knihovny.cz E-resources
- Keywords
- Approximate Bayesian Computation, Prunus armeniaca L., SSR markers, apricot, core collection, diversity pattern, history of diffusion, population structure,
- Publication type
- Journal Article MeSH
The characterization of the largest worldwide representative data set of apricot (Prunus armeniaca L.) germplasm was performed using molecular markers. Genetic diversity and structure of the cultivated apricot genetic resources were analyzed to decipher the history of diffusion of this species around the world. A common set of 25 microsatellite markers was used for genotyping a total of 890 apricot accessions in different collections from the center of origin to the more recent regions of apricot culture. Using a Bayesian model-based clustering approach, the apricot genotypes can be structured into five different genetic clusters (FST = 0.174), correlated with the geographical regions of origin of the accessions. Accessions from China and Central Asia were clustered together and exhibited the highest levels of diversity, confirming an origin in this region. A loss of genetic diversity was observed from the center of origin to both western and eastern zones of recent apricot culture. Altogether, our results revealed that apricot spread from China and Central Asia, defined as the center of origin, following three major diffusion routes with a decreasing gradient of genetic variation in each geographical group. The identification of specific alleles outside the center of origin confirmed the existence of different secondary apricot diversification centers. The present work provides more understanding of the worldwide history of apricot species diffusion as well as the field of conservation of the available genetic resources. Data have been used to define an apricot core collection based on molecular marker diversity which will be useful for further identification of genomic regions associated with commercially important horticultural traits through genome-wide association studies to sustain apricot breeding programs.
Department of Fruit Growing Faculty of Horticulture Mendel University Lednice Czechia
Dipartimento di Scienze Agrarie Alimentari e Agro Ambientali Università di Pisa Pisa Italy
INRA Centre PACA UR 1052 GAFL Montfavet France
INRA Centre PACA UR 629 URFM Avignon France
Liaoning Institute of Pomology Yingkou City China
National Agriculture and Food Research Organization Institute of Fruit Tree Science Tsukuba Japan
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Aranzana M. J., Garcia-Màs J., Carbo J., Arùs P. (2002). Development and variability analysis of microsatellite markers in peach. Plant Breed. 121 87–92.
Barthe S., Binelli G., Herault B., Scotti-Saintagne C., Sabatier D., Scotti I. (2017). Tropical rainforests that persisted: inferences from the Quaternary demographic history of eight tree species in the Guiana shield. Mol. Ecol. 26 1161–1174. 10.1111/mec.13949 PubMed DOI
Beaumont M., Zhang W., Balding D. J. (2002). Approximate Bayesian computation in population genetics. Genetics 162 2025–2035. 10.1089/cmb.2018.0217 PubMed DOI PMC
Belkhir K., Borsa P., Chikhi L., Raufaste N., Bonhomme F. (2004). GENETIX 4.05, Logiciel sous Windows TM pour la Génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171. Montpellier: Université de Montpellier II.
Besnard G., El Bakkali A., Haouane H., Baali-Cherif D., Moukhli A., Khadari B. (2013a). Population genetics of Mediterranean and Saharan olives: geographic patterns of differentiation and evidence for early generations of admixture. Ann. Bot. 112 1293–1302. 10.1093/aob/mct196 PubMed DOI PMC
Besnard G., Khadari B., Navascués M., Fernandez-Mazuecos M., El Bakkali A., Arrigo N., et al. (2013b). The complex history of the olive tree: from Late Quaternary diversification of Mediterranean lineages to primary domestication in the northern Levant. Proc. R. Soc. B 280:20122833. 10.1098/rspb.2012.2833 PubMed DOI PMC
Bourguiba H., Audergon J. M., Krichen L., Trifi-Farah N., Mamouni A., Trabelsi S., et al. (2012b). Loss of genetic diversity as a signature of apricot domestication and diffusion into the Mediterranean Basin. BMC Plant Biol. 12:49. 10.1186/1471-2229-12-49 PubMed DOI PMC
Bourguiba H., Audergon J. M., Krichen L., Trifi-Farah N., Mamouni A., Trabelsi S., et al. (2012a). Genetic diversity and differentiation of grafted and seed propagated apricot (Prunus armeniaca L.) in the Maghreb region. Sci. Hort. 142 7–13.
Bourguiba H., Khadari B., Krichen L., Trifi-Farah N., Mamouni A., Trabelsi S., et al. (2013). Genetic relationships between local North African apricot (Prunus armeniaca L.) germplasm and recently introduced varieties. Sci. Hortic. 152 61–69.
Campoy J. A., Lerigoleur-Balsemin E., Christmann H., Beauvieux R., Girollet N., Quero-Garcia J. (2016). Genetic diversity, linkage disequilibrium, population structure and construction of a core collection of Prunus avium L. landraces and bred cultivars. BMC Plant Biol. 16:49. 10.1186/s12870-016-0712-9 PubMed DOI PMC
Cao K., Zheng Z., Wang L., Liu X., Zhu G., Fang W., et al. (2014). Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol. 15:415. 10.1186/s13059-014-0415-1 PubMed DOI PMC
Cipriani G., Lot G., Huang W. G., Marrazzo M. T., Peterlunger E., Testolin R. (1999). AC/GT and AG/CT microsatellite repeats in peach (Prunus persica L. Batsch) isolation, characterization and cross-species amplification in Prunus. Theor. Appl. Genet. 99 65–72. PubMed
Cornuet J. M., Luikart G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144 2001–2014. PubMed PMC
Cornuet J.-M., Pudlo P., Veyssier J., Dehne-Garcia A., Gautier M., Leblois R., et al. (2014). DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30 1187–1189. 10.1093/bioinformatics/btt763 PubMed DOI
Decroocq S., Cornille A., Tricon D., Babayeva S., Chague A., Eyquard J. P. (2016). New insights into the history of domesticated and wild apricots and its contribution to Plum pox virus resistance. Mol. Ecol. 25 4712–4729. 10.1111/mec.13772 PubMed DOI
Denham T., Barton H., Castillo C., Crowther A., Dotte-Sarout E., Florin S. A., et al. (2020). The domestication syndrome in vegetatively propagated field crops. Ann. Bot. 125 581–597. 10.1093/aob/mcz212 PubMed DOI PMC
Di Rienzo A., Peterson A. C., Garza J. C., Valdes A. M., Slatkin M., Freimer N. B. (1994). Mutation processes of simple-sequence repeat loci in human populations. Proc. Natl. Acad. Sci. U.S.A. 91 3166–3170. 10.1073/pnas.91.8.3166 PubMed DOI PMC
Dirlewanger E., Cosson P., Tavaud M., Aranzana M., Poizat C., Zanetto A., et al. (2002). Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.). Theor. Appl. Genet. 105 127–138. 10.1007/s00122-002-0867-7 PubMed DOI
Earl D. A., VonHoldt B. M. (2012). Structure Harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Cons. Genet. Res. 4 359–361.
Evanno G., Regnaut S., Goudet J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14 2611–2620. 10.1111/j.1365-294X.2005.02553.x PubMed DOI
Faust M., Surányi D., Nyujtó F. (1998). Origin and dissemination of apricot. Hort. Rev. 22 225–266.
Felsenstein J. (2008). PHYLIP: Phylogeny Inference Package. Seattle, WA: USA Department of Genome Sciences and Department of Biology.
Gaut B. S., Diez C. M., Morrell P. L. (2015). Genomics and the contrasting dynamics of annual and perennial domestication. Trends Genet. 31 709–719. 10.1016/j.tig.2015.10.002 PubMed DOI
Glaubitz J. C. (2004). CONVERT: a user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol. Ecol. Resour. 4 309–310.
Goudet J. (2003). Fstat (ver. 2.9.4), a Program to Estimate and Test Population Genetics Parameters. Available online at: http://www.unil.ch/izea/softwares/fstat.html
Hagen L. S., Chaib J., Fady B., Decroocq V., Bouchet J. P., Lambert P., et al. (2004). Genomic and cDNA microsatellites from apricot (Prunus armeniaca L.). Mol. Ecol. Notes 4 742–745. PubMed
Hagen L. S., Khadari B., Lambert P., Audergon J. M. (2002). Genetic diversity in apricot revealed by AFLP markers: species and cultivars comparisons. Theor. Appl. Genet. 105 298–305. 10.1007/s00122-002-0910-8 PubMed DOI
Haouane H., El Bakkali A., Moukhli A., Tollon C., Santoni S., Oukable A. (2011). Genetic structure and core collection of the World Olive Germplasm Bank of Marrakech: towards the optimised management and use of Mediterranean olive genetic resources. Genetica 139 1083–1094. 10.1007/s10709-011-9608-7 PubMed DOI PMC
He T. M., Chen X. S., Xu Z., Gao J. S., Lin P. J., Liu W., et al. (2007). Using SSR markers to determine the population genetic structure of wild apricot (Prunus armeniaca L.) in the Ily Valley of West China. Genet. Resour. Crop Evol. 54 563–572.
Hudson R. R. (1990). Gene genealogies and the coalescent process. Oxford Surveys Evol. Biol. 7 1–44.
Jakobsson M., Rosenberg N. A. (2007). CLUMPP: cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23 1801–1806. 10.1093/bioinformatics/btm233 PubMed DOI
Kato S., Iwata H., Tsumura Y., Mukai Y. (2011). Genetic structure of island populations of Prunus lannesiana var. speciosa revealed by chloroplast DNA, AFLP and nuclear SSR loci analyses. J. Plant Res. 124 11–23. 10.1007/s10265-010-0352-3 PubMed DOI
Kim K. W., Chung H. K., Cho G. T., Ma H., Chandrabalan D. (2007). PowerCore: a program applying the advanced M strategy with a heuristic search for establishing core sets. Bioinformatics 23 2155–2162. 10.1093/bioinformatics/btm313 PubMed DOI
Kostina K. F. (1964). “Application the phytogeographical method to apricot classification (in Russian),” in Proceedings (Trudi) of the Nikita Botanical Gardens Vol 24, Moscow.
Linhart Y. B., Grant M. C. (1996). Evolutionary significance of local genetic differentiation in plants. Ann. Rev. Ecol. Syst. 27 237–277.
Liu S., Cornille A., Decroocq S., Tricon D., Chague A., Eyquard J.-P. (2019). The complex evolutionary history of apricots: species divergence, gene flow and multiple domestication events. Mol. Ecol. 28 5299–5314. 10.1111/mec.15296 PubMed DOI
Luikart G., Allendorf F. C., Cornuet J. M., Sherwin W. B. (1998). Distortion of allele frequency distributions provides a test for recent population bottlenecks. J. Hered. 89 238–247. 10.1093/jhered/89.3.238 PubMed DOI
Mamouni A., El Bakkali A., Lambert P., Krichen L., Oukabli A., Audergon J. M. (2014). Bottleneck and gene flow effects impact the genetic structure of seed-propagated apricot populations in Moroccan oasis agroecosystems. Plant Genet. Resour. 12 215–225.
Mariette S., Wong Jun Tai F., Roch G., Barre A., Chague A., Decroocq S., et al. (2016). Genome-wide association links candidate genes to resistance to Plum Pox Virus in apricot (Prunus armeniaca). New Phytol. 209 773–784. 10.1111/nph.13627 PubMed DOI
Miller A. J., Gross B. L. (2011). From forest to field: perennial fruit crop domestication. Am. J. Bot. 98 1389–1414. 10.3732/ajb.1000522 PubMed DOI
Myles S., Boyko A. R., Owens C. L., Brown P. J., Grassi F., Aradhya M. K., et al. (2011). Genetic structure and domestication history of the grape. Proc. Natl. Acad. Sci. U.S.A. 108 3530–3535. 10.1073/pnas.1009363108 PubMed DOI PMC
Nei M. (1972). Genetic distance between populations. Am. Nat. 106 283–292.
Peakall R., Smouse P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28 2537–2539. 10.1093/bioinformatics/bts460 PubMed DOI PMC
Pedryc A., Szabolcs R., Herman R., Krska B., Hegedüs A., Halász J. (2009). Genetic diversity of apricot revealed by a set of SSR markers from linkage group G1. Sci. Hortic. 121 19–26.
Perrier X., Jacquemoud-Collet J. P. (2006). DARwin Software. Available online at: http://darwin.cirad.fr/darwin (accessed April 26, 2019).
Pickrell J. K., Pritchard J. K. (2012). Inference of population splits and mixtures from genome wide allele frequency data. PLoS Genet. 8:e1002967. 10.1371/journal.pgen.1002967 PubMed DOI PMC
Piry S., Luikart G., Cornuet J. M. (1999). Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 90 502–503.
Pritchard J. K., Stephens M., Donnelly P. (2000). Inference of population structure using multilocus genotype data. Genetics 155 945–959. 10.1111/j.1471-8286.2007.01758.x PubMed DOI PMC
Raymond M., Rousset F. (1995a). An exact test for population differentiation. Evolution 49 1283–1286. PubMed
Raymond M., Rousset F. (1995b). GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86 248–249.
Razifard H., Ramos A., Della Valle A. L., Bodary C., Goetz E., Manser E. J., et al. (2020). Evidence for complex domestication history of the cultivated tomato in Latin America. Mol. Biol. Evol. 37 1118–1132. 10.1093/molbev/msz297 PubMed DOI PMC
Romero C., Pedryc A., Muñoz V., Llácer G., Badenes M. L. (2003). Genetic diversity of different apricot geographical groups determined by SSR markers. Genome 46 244–252. 10.1139/g02-128 PubMed DOI
Rosenberg N. A. (2004). DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes 4 137–138.
Rousset F. (2008). Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Res. 8 103–106. 10.1111/j.1471-8286.2007.01931.x PubMed DOI
Testolin R., Marrazzo T., Cipriani G., Quarta R., Verde I., Dettori M. T. (2000). Microsatellite DNA in Peach (Prunus persica L. Batsch) and its use in fingerprinting and testing the genetic origin of cultivars. Genome 43 512–520. PubMed
Urrestarazu J., Denancé C., Ravon E., Guyader A., Guisnel R., Feugey L. (2016). Analysis of the genetic diversity and structure across a wide range of germplasm reveals prominent gene flow in apple at the European level. BMC Plant Biol. 16:130. 10.1186/s12870-016-0818-0 PubMed DOI PMC
Van Inghelandt D., Melchinger A. E., Lebreton C., Stich B. (2010). Population structure and genetic diversity in a commercial maize breeding program assessed with SSR and SNP markers. Theor. Appl. Genet. 120 1289–1299. 10.1007/s00122-009-1256-2 PubMed DOI PMC
Van Oosterhout C., Hutchinson W. F., Wills D. P. M., Shipley P. (2004). Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4 535–538.
Vavilov N. I. (1951). The origin, variation, immunity and breeding of cultivated plants. Soil Sci. 72:482.
Weir B. S., Cockerham C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38 1358–1370. PubMed
Xiang Y., Huang C.-H., Hu Y., Wen J., Li S., Yi T., et al. (2016). Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Mol. Biol. Evol. 34 262–281. 10.1093/molbev/msx093 PubMed DOI PMC
Yamamoto T., Mochida K., Imai T., Shi Y. Z., Ogiwara T., Hayashi T. (2002). Microsatellite markers in peach [Prunus persica (L.) Batsch] derived from an enriched genomic and cDNA libraries. Mol. Ecol. Notes 2 298–301.
Yeh F. C., Yang R., Boyle T. (1999). POPGENE: Microsoft Windows-based Freeware for Population Genetic Analysis. Release 1.31. Edmonton: University of Alberta.
Zehdi-Azouzi S., Cherif E., Moussouni S., Gros-Balthazard M., Naqvi S. A., Ludena B., et al. (2015). Genetic structure of the date palm (Phoenix dactylifera) in the Old World reveals a strong differentiation between eastern and western populations. Ann. Bot. 116 101–112. 10.1093/aob/mcv132 PubMed DOI PMC
Zhang J., Chen T., Wang Y., Chen Q., Sun B., Luo Y., et al. (2018). Genetic diversity and domestication footprints of Chinese cherry [Cerasus pseudocerasus (Lindl.) G.Don] as revealed by nuclear microsatellites. Front. Plant Sci. 9:238. 10.3389/fpls.2018.00238 PubMed DOI PMC
Zhebentyayeva T. N., Ledbetter C., Burgos L., Llácer G. (2012). “Apricots,” in Handbook of Plant Breeding. Fruit Breeding, Vol. 8 eds Badenes M. L., Byrne D. H. (New York, NY: Springer; ), 415–458.
Zhebentyayeva T. N., Reighard G. L., Gorina V. M., Abbott A. G. (2003). Simple sequence repeat (SSR) for assessment of genetic variability in apricot germplasm. Theor. Appl. Genet. 106 435–444. 10.1007/s00122-002-1069-z PubMed DOI
Zhebentyayeva T. N., Reighard G. L., Lalli D. A., Gorina V. M., Krška B., Abbott A. G. (2008). Origin of resistance to plum pox virus in Apricot: what new AFLP and targeted SSR data analyses tell. Tree Genet. Genomes 4 403–417.
Zohary D., Hopf M., Weiss E. (2012). Domestication of Plants in the Old World: the Origin and Spread of Cultivated Plants in Southwest Asia, Europe, and the Mediterranean Basin, 4th Edn Oxford: Oxford University Press.
