The complex evolutionary history of apricots: Species divergence, gene flow and multiple domestication events.
ABC-RF (random forest)
admixture
domestication
gene flow
introgression
model testing
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
received:
19
02
2019
revised:
28
10
2019
accepted:
31
10
2019
pubmed:
5
11
2019
medline:
17
6
2020
entrez:
3
11
2019
Statut:
ppublish
Résumé
Domestication is an excellent model to study diversification and this evolutionary process can be different in perennial plants, such as fruit trees, compared to annual crops. Here, we inferred the history of wild apricot species divergence and of apricot domestication history across Eurasia, with a special focus on Central and Eastern Asia, based on microsatellite markers and approximate Bayesian computation. We significantly extended our previous sampling of apricots in Europe and Central Asia towards Eastern Asia, resulting in a total sample of 271 cultivated samples and 306 wild apricots across Eurasia, mainly Prunus armeniaca and Prunus sibirica, with some Prunus mume and Prunus mandshurica. We recovered wild Chinese species as genetically differentiated clusters, with P. sibirica being divided into two clusters, one possibly resulting from hybridization with P. armeniaca. Central Asia also appeared as a diversification centre of wild apricots. We further revealed at least three domestication events, without bottlenecks, that gave rise to European, Southern Central Asian and Chinese cultivated apricots, with ancient gene flow among them. The domestication event in China possibly resulted from ancient hybridization between wild populations from Central and Eastern Asia. We also detected extensive footprints of recent admixture in all groups of cultivated apricots. Our results thus show that apricot is an excellent model for studying speciation and domestication in long-lived perennial fruit trees.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5299-5314Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Ai, P. F., Zhen, Z. J., & Jin, Z. Z. (2011). Genetic diversity and relationships within sweet kernel apricot and related Armeniaca species based on sequence-related amplified polymorphism markers. Biochemical Systematics and Ecology, 39(4-6), 694-699. https://doi.org/10.1016/j.bse.2011.05.026
Aradhya, M., Velasco, D., Ibrahimov, Z., Toktoraliev, B., Maghradze, D., Musayev, M., … Preece, J. E. (2017). Genetic and ecological insights into glacial refugia of walnut (Juglans regia L.). PLoS ONE, 12(10), e0185974. https://doi.org/10.1371/journal.pone.0185974
Bailey, C. H., & Hough, L. F. (1975). Apricots. In J. M. Janick (Ed.), Advances in fruit breeding (pp. 367-384). West Lafayette, IN: Purdue University Press.
Beer, R., Kaiser, F., Schmidt, K., Arnmann, B., Carraro, G., Grisa, E., & Tinner, W. (2008). Vegetation history of the walnut forests in Kyrgyzstan (Central Asia): Natural or anthropogenic origin? Quaternary Science Reviews, 27(5-6), 621-632. https://doi.org/10.1016/j.quascirev.2007.11.012
Belfanti, E., Silfverberg-Dilworth, E., Tartarini, S., Patocchi, A., Barbieri, M., Zhu, J., … Sansavini, S. (2004). The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proceedings of the National Academy of Sciences of the United States of America, 101(3), 886-890. https://doi.org/10.1073/pnas.0304808101
Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., & Bonhomme, F. (2004). GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Retrieved from http://www.genetix.univ-montp2.fr/genetix/genetix.htm
Besnard, G., El Bakkali, A., Haouane, H., Baali-Cherif, D., Moukhli, A., & Khadari, B. (2013). Population genetics of Mediterranean and Saharan olives: Geographic patterns of differentiation and evidence for early generations of admixture. Annals of Botany, 112(7), 1293-1302. https://doi.org/10.1093/aob/mct196
Besnard, G., Terral, J.-F., & Cornille, A. (2017). On the origins and domestication of the olive: A review and perspectives. Annals of Botany, 121(3), 385-403. https://doi.org/10.1093/aob/mcy002
Bourguiba, H., Audergon, J.-M., Krichen, L., Trifi-Farah, N., Mamouni, A., Trabelsi, S., … Khadari, B. (2012). Loss of genetic diversity as a signature of apricot domestication and diffusion into the Mediterranean Basin. BMC Plant Biology, 12(49), 1471-2229. https://doi.org/10.1186/1471-2229-12-49
Breiman, L. (2001). Random forests. Machine Learning, 45(1), 5-32. https://doi.org/10.1023/A:1010933404324
Chen, H. Y. (2009). A buddhist classification of animals and plants in early Tang times. Journal of Asian History, 43(1), 31-51.
Chin, S. W., Shaw, J., Haberle, R., Wen, J., & Potter, D. (2014). Diversification of almonds, peaches, plums and cherries - molecular systematics and biogeographic history of Prunus (Rosaceae). Molecular Phylogenetics and Evolution, 76, 34-48. https://doi.org/10.1016/j.ympev.2014.02.024
Collard, B. C., & Mackill, D. J. (2008). Marker-assisted selection: An approach for precision plant breeding in the twenty-first century. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363(1491), 557-572. https://doi.org/10.1098/rstb.2007.2170
Cornille, A., Giraud, T., Smulders, M. J., Roldan-Ruiz, I., & Gladieux, P. (2014). The domestication and evolutionary ecology of apples. Trends in Genetics, 30(2), 57-65. https://doi.org/10.1016/j.tig.2013.10.002
Cornille, A., Gladieux, P., Smulders, M. J. M., Roldán-Ruiz, I., Laurens, F., Le Cam, B., … Giraud, T. (2012). New insight into the history of domesticated apple: Secondary contribution of the European wild apple to the genome of cultivated varieties. PLOS Genetics, 8(5), e1002703. https://doi.org/10.1371/journal.pgen.1002703
Decroocq, S., Cornille, A., Tricon, D., Babayeva, S., Chague, A., Eyquard, J. P., … Decroocq, V. (2016). New insights into the history of domesticated and wild apricots and its contribution to Plum pox virus resistance. Molecular Ecology, 25(19), 4712-4729. https://doi.org/10.1111/mec.13772
Delplancke, M., Alvarez, N., Benoit, L., Espindola, A., I Joly, H., Neuenschwander, S., & Arrigo, N. (2013). Evolutionary history of almond tree domestication in the Mediterranean basin. Molecular Ecology, 22(4), 1092-1104. https://doi.org/10.1111/mec.12129
Earl, D. A., & Vonholdt, B. M. (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359-361. https://doi.org/10.1007/s12686-011-9548-7
Estoup, A., Jarne, P., & Cornuet, J. M. (2002). Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Molecular Ecology, 11(9), 1591-1604. https://doi.org/10.1046/j.1365-294X.2002.01576.x
Estoup, A., Raynal, L., Verdu, P., & Marin, J. M. (2018). Model choice using Approximate Bayesian Computation and Random Forests: Analyses based on model grouping to make inferences about the genetic history of Pygmy human populations. Journal of the Société Française de Statistique, 159(3), 167-190.
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14(8), 2611-2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier, L., & Foll, M. (2011). fastsimcoal: A continuous-time coalescent simulator of genomic diversity under arbitrarily complex evolutionary scenarios. Bioinformatics, 27(9), 1332-1334. https://doi.org/10.1093/bioinformatics/btr124
Excoffier, L., & Lischer, H. E. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3), 564-567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Flowers, J. M., Hazzouri, K. M., Gros-Balthazard, M., Mo, Z., Koutroumpa, K., Perrakis, A., … Purugganan, M. D. (2019). Cross-species hybridization and the origin of North African date palms. Proceedings of the National Academy of Sciences of the United States of America, 116(5), 1651-1658. https://doi.org/10.1073/pnas.1817453116
Francois, O., & Durand, E. (2010). Spatially explicit Bayesian clustering models in population genetics. Molecular Ecology Resources, 10(5), 773-784. https://doi.org/10.1111/j.1755-0998.2010.02868.x
Garza, J. C., & Williamson, E. G. (2001). Detection of reduction in population size using data from microsatellite loci. Molecular Ecology, 10(2), 305-318. https://doi.org/10.1046/j.1365-294x.2001.01190.x
Gaut, B. S., Diez, C. M., & Morrell, P. L. (2015). Genomics and the contrasting dynamics of annual and perennial domestication. Trends in Genetics, 31(12), 709-719. https://doi.org/10.1016/j.tig.2015.10.002
Geuna, F., Toschi, M., & Bassi, D. (2003). The use of AFLP markers for cultivar identification in apricot. Plant Breeding, 122(6), 526-531. https://doi.org/10.1111/j.1439-0523.2003.00897.x
Goldstein, D. B., Linares, A. R., Cavallisforza, L. L., & Feldman, M. W. (1995). An evaluation of genetic distances for use with microsatellite loci. Genetics, 139(1), 463-471.
Gros-Balthazard, M., Galimberti, M., Kousathanas, A., Newton, C., Ivorra, S., Paradis, L., … Wegmann, D. (2017). The discovery of wild date palms in Oman reveals a complex domestication history involving centers in the Middle East and Africa. Current Biology, 27(14), 2211-2218.e8. https://doi.org/10.1016/j.cub.2017.06.045
Gross, B. L., & Olsen, K. M. (2010). Genetic perspectives on crop domestication. Trends in Plant Science, 15(9), 529-537. https://doi.org/10.1016/j.tplants.2010.05.008
Hartl, D. L., & Clark, G. C. (1997). Principles of population genetics. Sunderland, MA: Sinauer Associates Inc. Publishers.
Hazzouri, K. M., Flowers, J. M., Visser, H. J., Khierallah, H. S. M., Rosas, U., Pham, G. M., … Purugganan, M. D. (2015). Whole genome re-sequencing of date palms yields insights into diversification of a fruit tree crop. Nature Communications, 6, 8824. https://doi.org/10.1038/ncomms9824
He, T. M., Chen, X. S., Xu, Z., Gao, J. S., Lin, P. J., Liu, W., … Wu, Y. (2007). Using SSR markers to determine the population genetic structure of wild apricot (Prunus armeniaca L.) in the Ily Valley of West China. Genetic Resources and Crop Evolution, 54(3), 563-572. https://doi.org/10.1007/s10722-006-0013-5
Hormaza, J., Yamane, H., & Rodrigo, J. (2007).Apricot.In K. Chittaranjan (Ed.), Fruits and nuts (pp. 171-187). Berlin, Germany: Springer.
Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23(2), 254-267. https://doi.org/10.1093/molbev/msj030
Iwata, H., Kato, T., & Ohno, S. (2000). Triparental origin of Damask roses. Gene, 259(1-2), 53-59. https://doi.org/10.1016/S0378-1119(00)00487-X
Jakobsson, M., & Rosenberg, N. A. (2007). CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23(14), 1801-1806. https://doi.org/10.1093/bioinformatics/btm233
Kostina, K. (1960). The use of varietal resources of apricots for breeding. Trudy Nikitskogo Botanicheskogo Sada, 40, 45-63.
Kostina, K. (1964). Application of phytogeographical method to apricot classification. Trudy Nikitskogo Botanicheskogo Sada, 37.
Kovach, M. J., & McCouch, S. R. (2008). Leveraging natural diversity: Back through the bottleneck. Current Opinion in Plant Biology, 11(2), 193-200. https://doi.org/10.1016/j.pbi.2007.12.006
Larson, G., Piperno, D. R., Allaby, R. G., Purugganan, M. D., Andersson, L., Arroyo-Kalin, M., … Fuller, D. Q. (2014). Current perspectives and the future of domestication studies. Proceedings of the National Academy of Sciences of the United States of America, 111(17), 6139-6146. https://doi.org/10.1073/pnas.1323964111
Ledbetter, C. A. (2008). Apricots. In J. F. Hancock (Ed.), Temperate fruit crop breeding: Germplasm to genomics (pp. 39-82). Berlin, Germany: Springer Science & Business Media.
Li, M., Zhao, Z., & Miao, X. J. (2014). Genetic diversity and relationships of apricot cultivars in North China revealed by ISSR and SRAP markers. Scientia Horticulturae, 173, 20-28. https://doi.org/10.1016/j.scienta.2014.04.030
Li, M., Zhao, Z., Miao, X., & Zhou, J. (2013). Genetic diversity and population structure of Siberian apricot (Prunus sibirica L.) in China. International Journal of Molecular Sciences, 15(1), 377-400. https://doi.org/10.3390/ijms15010377
Li, X., Wang, Y., Wang, B., Wang, C., Shangguan, L., Huang, Z., & Fang, J. (2010). Genetic relationships between fruiting and flowering mei (Prunus mume) cultivars using SNP markers. Journal of Horticultural Science & Biotechnology, 85(4), 329-334. https://doi.org/10.1080/14620316.2010.11512676
Ligges, U., & Mächler, M. (2002). Scatterplot3d - An R package for visualizing multivariate data. Retrieved from https://EconPapers.repec.org/RePEc:zbw:sfb475:200222
Liorzou, M., Pernet, A., Li, S., Chastellier, A., Thouroude, T., Michel, G., … Grapin, A. (2016). Nineteenth century French rose (Rosa sp.) germplasm shows a shift over time from a European to an Asian genetic background. Journal of Experimental Botany, 67(15), 4711-4725. https://doi.org/10.1093/jxb/erw269
Liu, M. P., Du, H. Y., Zhu, G. P., Fu, D. L., & Tana, W. Y. (2015). Genetic diversity analysis of sweet kernel apricot in China based on SSR and ISSR markers. Genetics and Molecular Research, 14(3), 9722-9729. https://doi.org/10.4238/2015.August.19.4
Martin, G., Carreel, F., Coriton, O., Hervouet, C., Cardi, C., Derouault, P., … D'Hont, A. (2017). Evolution of the banana genome (Musa acuminata) is impacted by large chromosomal translocations. Molecular Biology and Evolution, 34(9), 2140-2152. https://doi.org/10.1093/molbev/msx164
McCouch, S., Baute, G. J., Bradeen, J., Bramel, P., Bretting, P. K., Buckler, E., … Zamir, D. (2013). Agriculture: Feeding the future. Nature, 499(7456), 23-24. https://doi.org/10.1038/499023a
Meirmans, P. G., & Van Tienderen, P. H. (2004). GENOTYPE and GENODIVE: Two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes, 4(4), 792-794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
Meyer, R. S., & Purugganan, M. D. (2013). Evolution of crop species: Genetics of domestication and diversification. Nature Reviews Genetics, 14(12), 840-852. https://doi.org/10.1038/nrg3605
Miller, A. J., & Gross, B. L. (2011). From forest to field: Perennial fruit crop domestication. American Journal of Botany, 98(9), 1389-1414. https://doi.org/10.3732/ajb.1000522
Nagaraju, J., Kathirvel, M., Kumar, R. R., Siddiq, E. A., & Hasnain, S. E. (2002). Genetic analysis of traditional and evolved Basmati and non-Basmati rice varieties by using fluorescence-based ISSR-PCR and SSR markers. Proceedings of the National Academy of Sciences of the United States of America, 99(9), 5836-5841. https://doi.org/10.1073/pnas.042099099
Neophytou, C. (2014). Bayesian clustering analyses for genetic assignment and study of hybridization in oaks: Effects of asymmetric phylogenies and asymmetric sampling schemes. Tree Genetics & Genomes, 10(2), 273-285. https://doi.org/10.1007/s11295-013-0680-2
Peakall, R., & Smouse, P. E. (2012). GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 28(19), 2537-2539. https://doi.org/10.1093/bioinformatics/bts460
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. Journal of Heredity, 90(4), 502-503. https://doi.org/10.1093/jhered/90.4.502
Pollegioni, P., Woeste, K. E., Chiocchini, F., Olimpieri, I., Tortolano, V., Clark, J. O., … Malvolti, M. E. (2014). Landscape genetics of Persian walnut (Juglans regia L.) across its Asian range. Tree Genetics & Genomes, 10(4), 1027-1043. https://doi.org/10.1007/s11295-014-0740-2
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945-959.
Pudlo, P., Marin, J. M., Estoup, A., Cornuet, J. M., Gautier, M., & Robert, C. P. (2016). Reliable ABC model choice via random forests. Bioinformatics, 32(6), 859-866. https://doi.org/10.1093/bioinformatics/btv684
Purugganan, M. D., & Fuller, D. Q. (2009). The nature of selection during plant domestication. Nature, 457(7231), 843-848. https://doi.org/10.1038/nature07895
Raynal, L., Marin, J. M., Pudlo, P., Ribatet, M., Robert, C. P., & Estoup, A. (2019). ABC random forests for Bayesian parameter inference. Bioinformatics, 35(10), 1720-1728. https://doi.org/10.1093/bioinformatics/bty867
Rehder, A. (Ed.) (1940). Manual of cultivated trees and shrubs hardy in North America: Exclusive of the subtropical and warmer temperate regions. New York, NY: Macmillan Company.
Riaz, S., Boursiquot, J. M., Dangl, G. S., Lacombe, T., Laucou, V., Tenscher, A. C., & Walker, M. A. (2013). Identification of mildew resistance in wild and cultivated Central Asian grape germplasm. BMC Plant Biology, 13(1), 149. https://doi.org/10.1186/1471-2229-13-149
Rosenberg, N. A. (2004). DISTRUCT: A program for the graphical display of population structure. Molecular Ecology Notes, 4(1), 137-138. https://doi.org/10.1046/j.1471-8286.2003.00566.x
Spengler, R. N., Maksudov, F., Bullion, E., Merkle, A., Hermes, T., & Frachetti, M. (2018). Arboreal crops on the medieval Silk Road: Archaeobotanical studies at Tashbulak. PLoS ONE, 13(8), e0201409. https://doi.org/10.1371/journal.pone.0201409
Szpiech, Z. A., Jakobsson, M., & Rosenberg, N. A. (2008). ADZE: A rarefaction approach for counting alleles private to combinations of populations. Bioinformatics, 24(21), 2498-2504. https://doi.org/10.1093/bioinformatics/btn478
Tanksley, S. D., & McCouch, S. R. (1997). Seed banks and molecular maps: Unlocking genetic potential from the wild. Science, 277(5329), 1063-1066. https://doi.org/10.1126/science.277.5329.1063
Vähä, J. P., & Primmer, C. R. (2006). Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Molecular Ecology, 15(1), 63-72. https://doi.org/10.1111/j.1365-294X.2005.02773.x
Vavilov, N. I. (1930). Wild progenitors of the fruit trees of Turkistan and the Caucasus and the problem of the origin of fruit trees. Reports and Proceedings of the 9th International Horticultural Congress, 27-286.
Vavilov, N. I. (1951). Phytogeographic basis of plant breeding. The origin, variation, immunity and breeding of cultivated plants (tr. K.S. Chester). Chronica Botanica, 13, 366.
Velasco, D., Hough, J., Aradhya, M., & Ross-Ibarra, J. (2016). Evolutionary genomics of peach and almond domestication. G3 (Bethesda), 6(12), 3985-3993. https://doi.org/10.1534/g3.116.032672
Verde, I., Abbott, A. G., Scalabrin, S., Jung, S., Shu, S., Marroni, F., … Rokhsar, D. S. (2013). The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nature Genetics, 45(5), 487-494. https://doi.org/10.1038/ng.2586
Voss-Fels, K. P., Stahl, A., & Hickey, L. T. (2019). Q&A: Modern crop breeding for future food security. BMC Biology, 17(1), 18. https://doi.org/10.1186/s12915-019-0638-4
Wang, Z., Kang, M., Liu, H., Gao, J., Zhang, Z., Li, Y., … Pang, X. (2014). High-level genetic diversity and complex population structure of Siberian apricot (Prunus sibirica L.) in China as revealed by nuclear SSR markers. PLoS ONE, 9(2), e87381. https://doi.org/10.1371/journal.pone.0087381
Wegmann, D., Leuenberger, C., Neuenschwander, S., & Excoffier, L. (2010). ABCtoolbox: A versatile toolkit for approximate Bayesian computations. BMC Bioinformatics, 11(1), 116. https://doi.org/10.1186/1471-2105-11-116
Wincker, P. (2013). Genomics and fruit crop selection. Nature Genetics, 45(1), 9-10. https://doi.org/10.1038/ng.2498
Wright, S. (1949). The genetical structure of populations. Annals of Eugenics, 15(1), 323-354. https://doi.org/10.1111/j.1469-1809.1949.tb02451.x
Wu, G. A., Terol, J., Ibanez, V., López-García, A., Pérez-Román, E., Borredá, C., … Talon, M. (2018). Genomics of the origin and evolution of Citrus. Nature, 554(7692), 311-316. https://doi.org/10.1038/nature25447
Yazbek, M., & Oh, S. H. (2013). Peaches and almonds: Phylogeny of Prunus subg. Amygdalus (Rosaceae) based on DNA sequences and morphology. Plant Systematics and Evolution, 299(8), 1403-1418. https://doi.org/10.1007/s00606-013-0802-1
Yu, Y., Fu, J., Xu, Y., Zhang, J., Ren, F., Zhao, H., … Xie, H. (2018). Genome re-sequencing reveals the evolutionary history of peach fruit edibility. Nature Communications, 9(1), 5404. https://doi.org/10.1038/s41467-018-07744-3
Yuan, J. H., Cornille, A., Giraud, T., Cheng, F. Y., & Hu, Y. H. (2014). Independent domestications of cultivated tree peonies from different wild peony species. Molecular Ecology, 23(1), 82-95. https://doi.org/10.1111/mec.12567
Zaurov, D. E., Molnar, T. J., Eisenman, S. W., Ford, T. M., Mavlyanova, R. F., Capik, J. M., … Goffreda, J. C. (2013). Genetic resources of apricots (Prunus armeniaca L.) in Central Asia. HortScience, 48, 681-691. https://doi.org/10.21273/hortsci.48.6.681
Zeinalabedini, M., Khayam-Nekoui, M., Grigorian, V., Gradziel, T. M., & Martinez-Gomez, P. (2010). The origin and dissemination of the cultivated almond as determined by nuclear and chloroplast SSR marker analysis. Scientia Horticulturae, 125(4), 593-601. https://doi.org/10.1016/j.scienta.2010.05.007
Zhang, H., Mittal, N., Leamy, L. J., Barazani, O., & Song, B. H. (2017). Back into the wild-Apply untapped genetic diversity of wild relatives for crop improvement. Evolutionary Applications, 10(1), 5-24. https://doi.org/10.1111/eva.12434
Zhang, Q. P., Liu, D. C., Liu, S., Liu, N., Wei, X., Zhang, A. M., & Liu, W. S. (2014). Genetic diversity and relationships of common apricot (Prunus armeniaca L.) in China based on simple sequence repeat (SSR) markers. Genetic Resources and Crop Evolution, 61(2), 357-368. https://doi.org/10.1007/s10722-013-0039-4
Zhang, Q., Zhang, H. E., Sun, L., Fan, G., Ye, M., Jiang, L., … Cheng, T. (2018). The genetic architecture of floral traits in the woody plant Prunus mume. Nature Communications, 9(1), 1702. https://doi.org/10.1038/s41467-018-04093-z
Zhao, P., Zhou, H.-J., Potter, D., Hu, Y.-H., Feng, X.-J., Dang, M., … Woeste, K. (2018). Population genetics, phylogenomics and hybrid speciation of Juglans in China determined from whole chloroplast genomes, transcriptomes, and genotyping-by-sequencing (GBS). Molecular Phylogenetics and Evolution, 126, 250-265. https://doi.org/10.1016/j.ympev.2018.04.014
Zhebentyayeva, T. N., Reighard, G. L., Lalli, D., Gorina, V. M., Krska, B., & Abbott, A. G. (2008). Origin of resistance to plum pox virus in Apricot: What new AFLP and targeted SSR data analyses tell. Tree Genetics & Genomes, 4(3), 403-417. https://doi.org/10.1007/s11295-007-0119-8
Zheng, Y., Crawford, G. W., & Chen, X. (2014). Archaeological evidence for peach (Prunus persica) cultivation and domestication in China. PLoS ONE, 9(9), e106595. https://doi.org/10.1371/journal.pone.0106595
Zhisheng, A., Kutzbach, J. E., Prell, W. L., & Porter, S. C. (2001). Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature, 411(6833), 62-66. https://doi.org/10.1038/35075035
Zhu, R., Zhang, B., Cai, C., & Wang, Z. (2016). The food of song. In A social history of Medieval China (pp. 74-76). Cambridge, UK: Cambridge University Press.