Evidence of an additional centre of apple domestication in Iran, with contributions from the Caucasian crab apple Malus orientalis Uglitzk. to the cultivated apple gene pool.

Caucasus Iran apple climate crop-wild gene flow domestication fruit tree introgression

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
11 2022
Historique:
revised: 08 07 2022
received: 28 03 2021
accepted: 09 08 2022
pubmed: 20 8 2022
medline: 28 10 2022
entrez: 19 8 2022
Statut: ppublish

Résumé

Divergence processes in crop-wild fruit tree complexes in pivotal regions for plant domestication such as the Caucasus and Iran remain little studied. We investigated anthropogenic and natural divergence processes in apples in these regions using 26 microsatellite markers amplified in 550 wild and cultivated samples. We found two genetically distinct cultivated populations in Iran that are differentiated from Malus domestica, the standard cultivated apple worldwide. Coalescent-based inferences showed that these two cultivated populations originated from specific domestication events of Malus orientalis in Iran. We found evidence of substantial wild-crop and crop-crop gene flow in the Caucasus and Iran, as has been described in apple in Europe. In addition, we identified seven genetically differentiated populations of wild apple (M. orientalis), not introgressed by the cultivated apple. Niche modelling combined with genetic diversity estimates indicated that these wild populations likely resulted from range changes during past glaciations. This study identifies Iran as a key region in the domestication of apple and M. orientalis as an additional contributor to the cultivated apple gene pool. Domestication of the apple tree therefore involved multiple origins of domestication in different geographic locations and substantial crop-wild hybridization, as found in other fruit trees. This study also highlights the impact of climate change on the natural divergence of a wild fruit tree and provides a starting point for apple conservation and breeding programmes in the Caucasus and Iran.

Identifiants

pubmed: 35984725
doi: 10.1111/mec.16667
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5581-5601

Informations de copyright

© 2022 John Wiley & Sons Ltd.

Références

Abdollahi, H. (2021). An illustrated review on manifestation of pome fruit germplasm in the historic miniatures of ancient Persia. Genetic Resources and Crop Evolution, 68(7), 2775-2791. https://doi.org/10.1007/s10722-021-01244-y
Allouche, O., Tsoar, A., & Kadmon, R. (2006). Assessing the accuracy of species distribution models: Prevalence, kappa and the true skill statistic (TSS). Journal of Applied Ecology, 43(6), 1223-1232.
Amirchakhmaghi, N., Yousefzadeh, H., Hosseinpour, B., Espahbodi, K., Aldaghi, M., & Cornille, A. (2018). First insight into genetic diversity and population structure of the Caucasian wild apple (Malus orientalis Uglitzk.) in the Hyrcanian forest (Iran) and its resistance to apple scab and powdery mildew. Genetic Resources and Crop Evolution, 65(4), 1255-1268. https://doi.org/10.1007/s10722-018-0611-z
Anderson, E. (2005). Plants, man, and life: Illustrated. Dover Publications. /z-wcorg/.
Aradhya, M., Velasco, D., Ibrahimov, Z., Toktoraliev, B., Maghradze, D., Musayev, M., Bobokashvili, Z., & Preece, J. E. (2017). Genetic and ecological insights into glacial refugia of walnut (Juglans regia L.). PLoS One, 12(10), e0185974.
Arroyo-García, R., Ruiz-García, L., Bolling, L., Ocete, R., López, M. A., Arnold, C., Ergul, A., Söylemezoğlu, G., Uzun, H. I., Cabello, F., Ibáñez, J., Aradhya, M. K., Atanassov, A., Atanassov, I., Balint, S., Cenis, J. L., Costantini, L., Goris-Lavets, S., Grando, M. S., … Martinez-Zapater, J. M. (2006). Multiple origins of cultivated grapevine (Vitis vinifera L. ssp. Sativa) based on chloroplast DNA polymorphisms. Molecular Ecology, 15(12), 3707-3714. https://doi.org/10.1111/j.1365-294X.2006.03049.x
Asanidze, Z., Akhalkatsi, M., Henk, A. D., Richards, C. M., & Volk, G. M. (2014). Genetic relationships between wild progenitor pear (Pyrus L.) species and local cultivars native to Georgia, South Caucasus. Flora: Morphology, Distribution, Functional Ecology of Plants, 209(9), 504-512. https://doi.org/10.1016/j.flora.2014.06.013
Bacles, C. F. E., & Jump, A. S. (2011). Taking a tree's perspective on forest fragmentation genetics. Trends in Plant Science, 16(1), 13-18. https://doi.org/10.1016/j.tplants.2010.10.002
Bai, X. N., & Spitkovsky, A. (2010). Uncertainties of modeling gamma-ray pulsar light curves using vacuum dipole magnetic field. Astrophysical Journal, 715(2), 1270-1281. https://doi.org/10.1088/0004-637X/715/2/1270
Bailey-Serres, J., Parker, J. E., Ainsworth, E. A., Oldroyd, G. E. D., & Schroeder, J. I. (2019). Genetic strategies for improving crop yields. Nature, 575(7781), 109-118. https://doi.org/10.1038/s41586-019-1679-0
Balaguer-Romano, R., Barea-Marquez, A., Ocaña-Calahorro, F. J., Gomez, J. M., Schupp, E. W., Zhang, J., & de Casas, R. R. (2021). The potential role of synzoochory in the naturalization of almond tree. Basic and Applied Ecology, 50, 97-106. https://doi.org/10.1016/j.baae.2020.11.004
Barbet-Massin, M., Jiguet, F., Albert, C. H., & Thuiller, W. (2012). Selecting pseudo-absence for species distribution models: How, where and how many? Methods in Ecology and Evolution, 3, 327-338. https://doi.org/10.1111/j.2041-210X.2011.00172.x
Besnard, G., Terral, J. F., & Cornille, A. (2018). 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/mcx145
Bina, H., Yousefzadeh, H., Ali, S. S., & Esmailpour, M. (2016). Phylogenetic relationships, molecular taxonomy, biogeography of Betula, with emphasis on phylogenetic position of Iranian populations. Tree Genetics and Genomes, 12(5), 1-17. https://doi.org/10.1007/s11295-016-1037-4
Bowe, P. (2004). Gardens of the Roman world. J. Paul Getty Museum. /z-wcorg/.
Brandenburg, J. T., Mary-Huard, T., Rigaill, G., Hearne, S. J., Corti, H., Joets, J., Vitte, C., Charcosset, A., Nicolas, S. D., & Tenaillon, M. I. (2017). Independent introductions and admixtures have contributed to adaptation of European maize and its American counterparts. PLoS Genetics, 13(3), e1006666-e1006630. https://doi.org/10.1371/journal.pgen.1006666
Breiman, L. (2001). Random Forests. Machine Learning, 45(1), 5-32. https://doi.org/10.1023/A:1010933404324
Browicz, K. (1969). Amygdalus. Flora Iranica, 66, 166-168.
Büttner, R. (2001). Malus. In P. Hanelt & Institute of Plant Genetics and Crop Plant Research (Eds.), Mansfelds Encyclopedia of Agricultural and Horticultural Crops (pp. 471-482). Springer.
Canepa, M. (2010). Distant displays of power: understanding cross-cultural interaction among the elites of Rome, Sasanian Iran, and Sui-Tang China. Ars Orientalis, 38, 121-154.
Castañeda-Álvarez, N. P., Khoury, C. K., Achicanoy, H. A., Bernau, V., Dempewolf, H., Eastwood, R. J., Guarino, L., Harker, R. H., Jarvis, A., Maxted, N., Müller, J. V., Ramirez-Villegas, J., Sosa, C. C., Struik, P. C., Vincent, H., & Toll, J. (2016). Global conservation priorities for crop wild relatives. Nature Plants, 2(4), 16022. https://doi.org/10.1038/nplants.2016.22
Cavalli-Sforza, L. L. (1998). The Chinese human genome diversity project. Proceedings of the National Academy of Sciences, 95(20), 11501-11503. https://doi.org/10.1073/pnas.95.20.11501
Chen, J., Li, L., Milesi, P., Jansson, G., Berlin, M., Karlsson, B., Aleksic, J., Vendramin, G. G., & Lascoux, M. (2019). Genomic data provide new insights on the demographic history and the extent of recent material transfers in Norway spruce. Evolutionary Applications, 12(8), 1539-1551. https://doi.org/10.1111/eva.12801
Chen, X., Cornille, A., An, H., Xing, L., Ma, J., Zhao, C., Wang, Y., Han, M., & Dong, Z. (2022). The East Asian wild apples, Malus baccata (L.) Borkh and Malus hupehensis (Pamp.) Rehder., are additional contributors to the genomes of cultivated European and Chinese varieties. Molecular Ecology, 1-15. https://doi.org/10.1111/mec.16485
Choi, J. Y., Platts, A. E., Fuller, D. Q., Hsing (邢禹依), Y.-I., Wing, R. A., & Purugganan, M. D. (2017). The rice paradox: Multiple origins but single domestication in asian rice. Molecular Biology and Evolution, 34(4), 969-979. https://doi.org/10.1093/molbev/msx049
Cornille, A., Antolín, F., Garcia, E., Vernesi, C., Fietta, A., Brinkkemper, O., Kirleis, W., Schlumbaum, A., & Roldán-Ruiz, I. (2019). A multifaceted overview of apple tree domestication. Trends in Plant Science, 24(8), 770-782. https://doi.org/10.1016/j.tplants.2019.05.007
Cornille, A., Feurtey, A., Gélin, U., Ropars, J., Misvanderbrugge, K., Gladieux, P., & Giraud, T. (2015). Anthropogenic and natural drivers of gene flow in a temperate wild fruit tree: A basis for conservation and breeding programs in apples. Evolutionary Applications, 8(4), 373-384. https://doi.org/10.1111/eva.12250
Cornille, A., Giraud, T., Bellard, C., Tellier, A., le Cam, B., Smulders, M. J. M., Kleinschmit, J., Roldan-Ruiz, I., & Gladieux, P. (2013). Post-glacial recolonization history of the European crabapple (Malus sylvestris Mill.), a wild contributor to the domesticated apple. Molecular Ecology, 22(8), 2249-2263.
Cornille, A., Gladieux, P., & Giraud, T. (2013). Crop-to-wild gene flow and spatial genetic structure in the closest wild relatives of the cultivated apple. Evolutionary Applications, 6(5), 737-748. https://doi.org/10.1111/eva.12059
Cornille, A., Gladieux, P., Smulders, M. J. M., Roldán-Ruiz, I., Laurens, F., le Cam, B., Nersesyan, A., Clavel, J., Olonova, M., Feugey, L., Gabrielyan, I., Zhang, X. G., Tenaillon, M. I., & 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.
Cornille, A., Giraud, T., Smulders, M. J. M., Roldán-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
Cullingham, C. I., Miller, J. M., Peery, R. M., Dupuis, J. R., Malenfant, R. M., Gorrell, J. C., & Janes, J. K. (2020). Confidently identifying the correct K value using the ΔK method: When does K = 2? Molecular Ecology, 29(5), 862-869. https://doi.org/10.1111/mec.15374
Curtis, J., Tallis, N., Andre-Salvini, B., André-Salvini, B., Museum, B., & Armbruster, B. (2005). Forgotten Empire: The World of Ancient Persia. University of California Press. Retrieved from. https://books.google.fr/books?id=kJnaKu9DdNEC
Decroocq, S., Cornille, A., Tricon, D., Babayeva, S., Chague, A., Eyquard, J. P., Karychev, R., Dolgikh, S., Kostritsyna, T., Liu, S., Liu, W., Geng, W., Liao, K., Asma, B. M., Akparov, Z., Giraud, T., & 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., Espíndola, A., Joly, H., Benoit, L., Brouck, E., & Arrigo, N. (2011). Gene flow among wild and domesticated almond species: Insights from chloroplast and nuclear markers. Evolutionary Applications, 5(4), 317-329.
Diez, C. M., Trujillo, I., Martinez-Urdiroz, N., Barranco, D., Rallo, L., Marfil, P., & Gaut, B. S. (2015). Olive domestication and diversification in the Mediterranean Basin. New Phytologist, 206(1), 436-447. https://doi.org/10.1111/nph.13181
Duan, N., Bai, Y., Sun, H., Wang, N., Ma, Y., Li, M., Wang, X., Jiao, C., Legall, N., Mao, L., Wan, S., Wang, K., He, T., Feng, S., Zhang, Z., Mao, Z., Shen, X., Chen, X., Jiang, Y., … Chen, X. (2017). Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nature Communications, 8(1). https://doi.org/10.1038/s41467-017-00336-7
Earl, D. A. (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359-361.
Estoup, A. 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 de La Societe 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.
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., Foll, M., & Petit, R. J. (2009). Genetic consequences of range expansions. Annual Review of Ecology, Evolution, and Systematics, 40(1), 481-501. https://doi.org/10.1146/annurev.ecolsys.39.110707.173414
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(3), 564-567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fallahi, E., Colt, W. M., Fallahi, B., & Chun, I.-J. (2002). The Importance of Apple Rootstocks on Tree Growth, Yield, Fruit Quality, Leaf Nutrition, and Photosynthesis with an Emphasis on ‘Fuji’. HortTechnology Horttech, 12(1), 38-44. https://doi.org/10.21273/HORTTECH.12.1.38
Fallahi, E., Fallahi, P., & Mahdavi, S. (2020). Ancient urban gardens of persia: Concept, history, and influence on other world gardens. HortTechnology Hortte, 30(1), 6-12. https://doi.org/10.21273/HORTTECH04415-19
Feurtey, A., Cornille, A., Shykoff, J. A., Snirc, A., & Giraud, T. (2017a). Crop-to-wild gene flow and its fitness consequences for a wild fruit tree: Towards a comprehensive conservation strategy of the wild apple in Europe. Evolutionary Applications, 10(2), 180-188. https://doi.org/10.1111/eva.12441
Fieldings, A. H., & Bell, J. F. (1997). A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation, 24, 38-49.
Fischer, A., & Schmidt, M. (1938). Wilde Kern-und Steinobstarten, ihre Heimat und ihre Bedeutung für die Entstehung der Kultursorten und die Züchtung. Der Züchter, 10(6), 157-167.
Flowers, J. M., Hazzouri, K. M., Gros-Balthazard, M., Mo, Z., Koutroumpa, K., Perrakis, A., Ferrand, S., Khierallah, H. S. M., Fuller, D. Q., Aberlenc, F., Fournaraki, C., & 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
Fontaine, M. C., Gladieux, P., Hood, M. E., & Giraud, T. (2013). History of the invasion of the anther smut pathogen on Silene latifolia in North America. New Phytologist, 198(3), 946-956. https://doi.org/10.1111/nph.12177
Forsline, P. L., Aldwinckle, H. S., Dickson, E. E., Luby, J. J., & Hokanson, S. C. (2003). Collection, maintenance, characterization, and utilization of wild apples of central Asia. In J. Janick (Ed.), Horticultural reviews: Wild apple and fruit trees of central Asia (Vol. 29, pp. 1-62). John Wiley & Sons, Inc..
Fuller, D. Q. (2018). Long and attenuated: Comparative trends in the domestication of tree fruits. Vegetation History and Archaeobotany, 27(1), 165-176. https://doi.org/10.1007/s00334-017-0659-2
Gabrielian, E. T., & Zohary, D. (2004). Wild relatives of food crops native to Armenia and Nakhichevan. Flora Mediterranea, 14, 5-80.
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., Díez, 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
George, J.-P., Konrad, H., Collin, E., Thevenet, J., Ballian, D., Idzojtic, M., Kamm, U., Zhelev, P., & Geburek, T. (2015). High molecular diversity in the true service tree (Sorbus domestica) despite rareness: Data from Europe with special reference to the Austrian occurrence. Annals of Botany, 115(7), 1105-1115. https://doi.org/10.1093/aob/mcv047
Gharghani, A., Zamani, Z., Talaie, A., Fattahi, R., Hajnajari, H., Oraguzie, N. C., Wiedow, C., & Gardiner, S. E. (2010). The role of Iran (Persia) in apple (Malus × domestica Borkh.) domestication, evolution and migration via the silk trade route. Acta Horticulturae, 859, 229-236.
Gharghani, A., Zamani, Z., Talaie, A., Oraguzie, N. C., Fatahi, R., Hajnajari, H., Wiedow, C., & Gardiner, S. E. (2009). Genetic identity and relationships of Iranian apple (Malus× domestica Borkh.) cultivars and landraces, wild Malus species and representative old apple cultivars based on simple sequence repeat (SSR) marker analysis. Genetic Resources and Crop Evolution, 56(6), 829-842.
Giesecke, T., Brewer, S., Finsinger, W., Leydet, M., & Bradshaw, R. H. W. (2017). Patterns and dynamics of European vegetation change over the last 15,000 years. Journal of Biogeography, 44(7), 1441-1456. https://doi.org/10.1111/jbi.12974
Groppi, A., Liu, S., Cornille, A., Decroocq, S., & Decroocq, D. (2021). Population genomics of apricots unravels domestication history and adaptive events. Nature Communications, 12, 3956.
Gros-Balthazard, M., & Flowers, J. M. (2021). A brief history of the origin of domesticated date palms. In J. M. Al-Khayri, S. M. Jain, & D. V. Johnson (Eds.), The Date Palm Genome, Vol. 1: Phylogeny, Biodiversity and Mapping (pp. 55-74). Springer International Publishing. https://doi.org/10.1007/978-3-030-73746-7_3
Hardy, O. J., & Vekemans, X. (2002). SPAGeDi: A versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes, 2(4), 618-620.
Harris, S. A., Robinson, J. P., & Juniper, B. E. (2002). Genetic clues to the origin of the apple. Trends in Genetics, 18(8), 426-430.
Hewitt, G. M. (1990). Divergence and speciation as viewed from an insect hybrid zone. Canadian Journal of Zoology, 68(8), 1701-1715. https://doi.org/10.1139/z90-251
Hewitt, G. M. (1996). Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58(3), 247-276. https://doi.org/10.1006/bijl.1996.0035
Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 359(1442), 183-195. https://doi.org/10.1098/rstb.2003.1388
Höfer, M., Flachowsky, H., Hanke, M.-V., Semënov, V., Šlâvas, A., Bandurko, I., Sorokin, A., & Alexanian, S. (2013). Assessment of phenotypic variation of Malus orientalis in the North Caucasus region. Genetic Resources and Crop Evolution, 60(4), 1463-1477. https://doi.org/10.1007/s10722-012-9935-2
Huson, D. H. (1998). SplitsTree: Analyzing and visualizing evolutionary data. Bioinformatics (Oxford, England), 14(1), 68-73.
Huson, D. H., & Scornavacca, C. (2012). Dendroscope 3: An interactive tool for rooted phylogenetic trees and networks. Systematic Biology, 61(6), 1061-1067.
Jezkova, T., Olah-Hemmings, V., & Riddle, B. R. (2011). Niche shifting in response to warming climate after the last glacial maximum: Inference from genetic data and niche assessments in the chisel-toothed kangaroo rat (Dipodomys microps). Global Change Biology, 17(11), 3486-3502. https://doi.org/10.1111/j.1365-2486.2011.02508.x
Jombart, T., & Ahmed, I. (2011). Adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics, 27(21), 3070-3071. https://doi.org/10.1093/bioinformatics/btr521
Kalinowski, S. T. (2011). The computer program STRUCTURE does not reliably identify the main genetic clusters within species: Simulations and implications for human population structure. Heredity, 106(4), 625-632.
Koskinen, M. T., Hirvonen, H., Landry, P. A., & Primmer, C. R. (2004). The benefits of increasing the number of microsatellites utilized in genetic population studies: An empirical perspective. Hereditas, 141(1), 61-67. https://doi.org/10.1111/j.1601-5223.2004.01804.x
Langenfeld, W. T. (1991). Apple trees. Morphological evolution, phylogeny, geography and systematics (p. 232). Riga (Zinatne).
Lascoux, M., Palmé, A. E., Cheddadi, R., & Latta, R. G. (2004). Impact of Ice Ages on the genetic structure of trees and shrubs. Philosophical Transactions of the Royal Society B: Biological Sciences, 359(1442), 197-207. https://doi.org/10.1098/rstb.2003.1390
Leroy, B., Bellard, C., Dubos, N., Colliot, A., Vasseur, M., Courtial, C., Bakkenes, M., Canard, A., & Ysnel, F. (2014). Forecasted climate and land use changes, and protected areas: The contrasting case of spiders. Diversity and Distributions, 20(6), 686-697. https://doi.org/10.1111/ddi.12191
Liang, Z., Duan, S., Sheng, J., Zhu, S., Ni, X., Shao, J., Liu, C., Nick, P., du, F., Fan, P., Mao, R., Zhu, Y., Deng, W., Yang, M., Huang, H., Liu, Y., Ding, Y., Liu, X., Jiang, J., … Dong, Y. (2019). Whole-genome resequencing of 472 Vitis accessions for grapevine diversity and demographic history analyses. Nature Communications, 10(1), 1190. https://doi.org/10.1038/s41467-019-09135-8
Liu, S., Cornille, A., Decroocq, S., Tricon, D., Chague, A., Eyquard, J., Liu, W. S., Giraud, T., & Decroocq, V. (2019). The complex evolutionary history of apricots: Species divergence, gene flow and multiple domestication events. Molecular Ecology, 28, 5299-5314. https://doi.org/10.1111/mec.15296
Loiselle, B. A., Sork, V. L., Nason, J., & Graham, C. (1995). Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany, 82(11), 1420-1425.
Mabry, M. E., Rowan, T. N., Pires, J. C., & Decker, J. E. (2021). Feralization: Confronting the complexity of domestication and evolution. Trends in Genetics, 37(4), 302-305. https://doi.org/10.1016/j.tig.2021.01.005
Meyer, R. S., Duval, A. E., & Jensen, H. R. (2012). Patterns and processes in crop domestication: An historical review and quantitative analysis of 203 global food crops. New Phytologist, 196(1), 29-48. https://doi.org/10.1111/j.1469-8137.2012.04253.x
Migicovsky, Z., Gardner, K. M., Richards, C., Thomas Chao, C., Schwaninger, H. R., Fazio, G., Zhong, G. Y., & Myles, S. (2021). Genomic consequences of apple improvement. Horticulture Research, 8(1), 9-13. https://doi.org/10.1038/s41438-020-00441-7
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
Monserud, R. A., & Leemans, R. (1992). Comparing global vegetation maps with the Kappa statistic. Ecological Modelling, 62(4), 275-293.
Myles, S., Boyko, A. R., Owens, C. L., Brown, P. J., Grassi, F., Aradhya, M. K., Prins, B., Reynolds, A., Chia, J. M., Ware, D., Bustamante, C. D., & Buckler, E. S. (2011). Genetic structure and domestication history of the grape. Proceedings of the National Academy of Sciences of the United States of America, 108(9), 3530-3535. https://doi.org/10.1073/pnas.1009363108
Nakhutsrishvili, G., Zazanashvili, N., Batsatsashvili, K., & Montalvo, C. S. (2015). Colchic and Hyrcanian forests of the Caucasus: Similarities, differences and conservation status. Flora Mediterranea, 25, 185-192.
Nei, M. (1987). Molecular Evolutionary Genetics. Columbia University Press. Retrieved from. https://books.google.es/books?id=UhRSsLkjxDgC
Oddou-Muratorio, S., & Klein, E. K. (2008). Comparing direct vs. Indirect estimates of gene flow within a population of a scattered tree species. Molecular Ecology, 17(11), 2743-2754.
Omasheva, M. Y., Flachowsky, H., Ryabushkina, N. A., Pozharskiy, A. S., Galiakparov, N. N., & Hanke, M.-V. (2017). To what extent do wild apples in Kazakhstan retain their genetic integrity? Tree Genetics & Genomes, 13(3), 52. https://doi.org/10.1007/s11295-017-1134-z
Parvizi, E., Keikhosravi, A., Naderloo, R., Solhjouy-Fard, S., Sheibak, F., & Schubart, C. D. (2019). Phylogeography of Potamon ibericum (Brachyura: Potamidae) identifies Quaternary glacial refugia within the Caucasus biodiversity hot spot. Ecology and Evolution, 9(8), 4749-4759. https://doi.org/10.1002/ece3.5078
Patocchi, A., Fernàndez-Fernàndez, F., Evans, K., Gobbin, D., Rezzonico, F., Boudichevskaia, A., Dunemann, F., Stankiewicz-Kosyl, M., Mathis-Jeanneteau, F., Durel, C. E., Gianfranceschi, L., Costa, F., Toller, C., Cova, V., Mott, D., Komjanc, M., Barbaro, E., Kodde, L., Rikkerink, E., … van de Weg, W. (2009). Development and test of 21 multiplex PCRs composed of SSRs spanning most of the apple genome. Tree Genetics and Genomes, 5(1), 211-223.
Patocchi, A., Frei, A., Frey, J. E., & Kellerhals, M. (2009). Towards improvement of marker assisted selection of apple scab resistant cultivars: Venturia inaequalis virulence surveys and standardization of molecular marker alleles associated with resistance genes. Molecular Breeding, 24(4), 337-347. https://doi.org/10.1007/s11032-009-9295-6
Petit, R. J., Bialozyt, R., Garnier-Géré, P., & Hampe, A. (2004). Ecology and genetics of tree invasions: From recent introductions to Quaternary migrations. Forest Ecology and Management, 197(1-3), 117-137. https://doi.org/10.1016/j.foreco.2004.05.009
Petit, R. J., & Hampe, A. (2006). Some evolutionary consequences of being a tree. Annual Review of Ecology, Evolution, and Systematics, 37(1), 187-214. https://doi.org/10.1146/annurev.ecolsys.37.091305.110215
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
Puechmaille, S. J. (2016). The program structure does not reliably recover the correct population structure when sampling is uneven: Subsampling and new estimators alleviate the problem. Molecular Ecology Resources, 16(3), 608-627. https://doi.org/10.1111/1755-0998.12512
Putman, A. I., & Carbone, I. (2014). Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecology and Evolution, 4(22), 4399-4428. https://doi.org/10.1002/ece3.1305
Qiu, J., Wang, L., Liu, M., Shen, Q., & Tang, J. (2011). An efficient and simple protocol for a PdCl2-ligandless and additive-free Suzuki coupling reaction of aryl bromides. Tetrahedron Letters, 52(48), 6489-6491. https://doi.org/10.1016/j.tetlet.2011.09.115
Raymond, M., & Rousset, F. (1995). An exact test for population differentiation. Evolution, 49(6), 1280-1283.
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
Rechinger, K. H. (1964). Flora Iranica, Akademische Druck-und Verlagsanstalt Graz (p. 549). University of Tehran, Iran.
Rousset, F. (2008). genepop'007: A complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8(1), 103-106.
Schmitt, T. (2007). Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology, 4, 1-13. https://doi.org/10.1186/1742-9994-4-11
Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139(1), 457-462. https://doi.org/10.1093/genetics/139.1.457
Soofi, M., Ghoddousi, A., Zeppenfeld, T., Shokri, S., Soufi, M., Jafari, A., Ahmadpour, M., Qashqaei, A. T., Egli, L., Ghadirian, T., Chahartaghi, N. R., Zehzad, B., Kiabi, B. H., Khorozyan, I., Balkenholm, N., & Waltert, M. (2018). Livestock grazing in protected areas and its effects on large mammals in the Hyrcanian forest, Iran. Biological Conservation, 217, 377-382. https://doi.org/10.1016/j.biocon.2017.11.020
Spengler, R. N. (2019a). Fruit from the Sands: The Silk Road Origins of the Foods We Eat. University of California Press. Retrieved from. https://books.google.fr/books?id=fr6SDwAAQBAJ
Spengler, R. N. (2019b). Origins of the apple: The role of megafaunal mutualism in the domestication of malus and rosaceous trees. Frontiers in Plant Science, 10, 617. https://doi.org/10.3389/fpls.2019.00617
Spengler, R. N., Chang, C., & Tourtellotte, P. A. (2013). Agricultural production in the Central Asian mountains: Tuzusai, Kazakhstan (410-150 b.c.). Journal of Field Archaeology, 38(1), 68-85. https://doi.org/10.1179/0093469012Z.00000000037
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.
Takezaki, N., & Nei, M. (2008). Empirical tests of the reliability of phylogenetic trees constructed with microsatellite DNA. Genetics, 178(1), 385-392. https://doi.org/10.1534/genetics.107.081505
Tardío, J., Arnal, A., & Lázaro, A. (2020). Ethnobotany of the crab apple tree (Malus sylvestris (L.) Mill., Rosaceae) in Spain. Genetic Resources and Crop Evolution., 68(2), 795-808. https://doi.org/10.1007/s10722-020-01026-y
Tarkhnishvili, D., Gavashelishvili, A., & Mumladze, L. (2012). Palaeoclimatic models help to understand current distribution of Caucasian forest species. Biological Journal of the Linnean Society, 105(1), 231-248. https://doi.org/10.1111/j.1095-8312.2011.01788.x
Teixeira, J. C., & Huber, C. D. (2021). The inflated significance of neutral genetic diversity in conservation genetics. Proceedings of the National Academy of Sciences, 118(10), e2015096118. https://doi.org/10.1073/pnas.2015096118
Thuiller, W., Georges, D., Engler, R., & Breiner, F. (2016). Biomod2: Ensemble platform for species distribution modeling. R package version 3.3-7.
Tian, F., Li, B., Ji, B., Zhang, G., & Luo, Y. (2009). Identification and structure-activity relationship of gallotannins separated from Galla chinensis. LWT - Food Science and Technology, 42(7), 1289-1295. https://doi.org/10.1016/j.lwt.2009.03.004
Vavilov, N. I. (1926). Studies on the origin of cultivated plants. Trudy Byuro Prikladnoi Botanike, 16, 139-245.
Vavilov, N. I. (1992). Origin and geography of cultivated plants. Cambridge University Press. CABDirect.
Vekemans, X., & Hardy, O. J. (2004a). New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology, 13(4), 921-935. https://doi.org/10.1046/j.1365-294X.2004.02076.x
Vercken, E., Fontaine, M. C., Gladieux, P., Hood, M. E., Jonot, O., & Giraud, T. (2010). Glacial refugia in pathogens: European genetic structure of anther smut pathogens on Silene latifolia and Silene dioica. PLoS Pathogens, 6(12), e1001229.
Volk, G. M., & Cornille, A. (2019). Genetic diversity and domestication history in pyrus. In The Pear Genome (pp. 51-62). Springer.
Volk, G. M., Richards, C. M., Reilley, A. A., Henk, A. D., Reeves, P. A., Forsline, P. L., & Aldwinckle, H. S. (2008). Genetic diversity and disease resistance of wild Malus orientalis from Turkey and Southern Russia. Journal of the American Society for Horticultural Science, 133(3), 383-389.
Vouillamoz, J. F., McGovern, P. E., Ergul, A., Söylemezoğlu, G., Tevzadze, G., Meredith, C. P., & Grando, M. S. (2006). Genetic characterization and relationships of traditional grape cultivars from Transcaucasia and Anatolia. Plant Genetic Resources, 4(2), 144-158. https://doi.org/10.1079/pgr2006114
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
Weir, B. S., & Cockerham, C. C. (1984). Estimating F-Statistics for the analysis of population structure. Evolution, 38(6), 1358-1370.
Wilson, G. A., & Rannala, B. (2003). Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163(3), 1177-1191. https://doi.org/10.1093/genetics/163.3.1177
Wu, J., Wang, Y., Xu, J., Korban, S. S., Fei, Z., Tao, S., Ming, R., Tai, S., Khan, A. M., Postman, J. D., Gu, C., Yin, H., Zheng, D., Qi, K., Li, Y., Wang, R., Deng, C. H., Kumar, S., Chagné, D., … Zhang, S. (2018). Diversification and independent domestication of Asian and European pears. Genome Biology, 19(1), 77. https://doi.org/10.1186/s13059-018-1452-y
Yousefzadeh, H., Hosseinzadeh Colagar, A., Tabari, M., Sattarian, A., & Assadi, M. (2012). Utility of ITS region sequence and structure for molecular identification of Tilia species from Hyrcanian forests. Iran. Plant Systematics and Evolution, 298(5), 947-961. https://doi.org/10.1007/s00606-012-0604-x
Zazanashvili, N., Sanadiradze, G., Garforth, M., Bitsadze, M., Manvelyan, K., Askerov, E., Mousavi, M., Krever, V., Shmunk, V., Kalem, S., & Devranoğlu Tavsel, S. (2020). Ecoregional conservation plan (ECP) for the caucasus 2020 edition. WWF, KfW.
Zeng, G., Zhang, J., Chen, Y., Yu, Z., Yu, M., Li, H., Liu, Z., Chen, M., Lu, L., & Hu, C. (2011). Relative contributions of archaea and bacteria to microbial ammonia oxidation differ under different conditions during agricultural waste composting. Bioresource Technology, 102(19), 9026-9032. https://doi.org/10.1016/j.biortech.2011.07.076
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, H.-X., Li, H.-Y., & Li, Y.-X. (2018). Identifying evolutionarily significant units for conservation of the endangered Malus sieversii using genome-wide RADseq data. Nordic Journal of Botany, 36(7), e01733. https://doi.org/10.1111/njb.01733

Auteurs

Hamid Bina (H)

Department of Forestry, Tarbiat Modares University, Noor, Iran.

Hamed Yousefzadeh (H)

Department of Environmental Science, Biodiversity Branch, Natural Resources Faculty, Tarbiat Modares University, Noor, Iran.

Anthony Venon (A)

Université Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, Gif-sur-Yvette, France.

Carine Remoué (C)

Université Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, Gif-sur-Yvette, France.

Agnès Rousselet (A)

Université Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, Gif-sur-Yvette, France.

Matthieu Falque (M)

Université Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, Gif-sur-Yvette, France.

Shadab Faramarzi (S)

Department of Plant Production and Genetics, Faculty of Agriculture, Razi University, Kermanshah, Iran.

Xilong Chen (X)

Université Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, Gif-sur-Yvette, France.

Jarkyn Samanchina (J)

Fauna & Flora International, Cambridge, UK.

David Gill (D)

Fauna & Flora International, Cambridge, UK.

Akylai Kabaeva (A)

Fauna & Flora International, Cambridge, UK.

Tatiana Giraud (T)

Ecologie Systematique Evolution, Universite Paris-Saclay, CNRS, AgroParisTech, Gif-sur-Yvette, France.

Batool Hosseinpour (B)

Department of Agriculture, Iranian Research Organization for Science and Technology (IROST), Institute of Agriculture, Tehran, Iran.

Hamid Abdollahi (H)

Temperate Fruits Research Centre, Horticultural Sciences Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran.

Ivan Gabrielyan (I)

Department of Palaeobotany, A. Takhtajyan Institute of Botany, Armenian National Academy of Sciences, Yerevan, Armenia.

Anush Nersesyan (A)

Department of Conservation of Genetic Resources of Armenian Flora, A. Takhtajyan Institute of Botany, Armenian National Academy of Sciences, Yerevan, Armenia.

Amandine Cornille (A)

Université Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE - Le Moulon, Gif-sur-Yvette, France.

Articles similaires

Humans Female Case-Control Studies Adult Breast Diseases
1.00
Iran Environmental Monitoring Seasons Ecosystem Forests
Iran Ecosystem Phylogeny Cupressus Conservation of Natural Resources
Humans Retrospective Studies Male Female Child

Classifications MeSH