Analysis of >3400 worldwide eggplant accessions reveals two independent domestication events and multiple migration-diversification routes.

Single Primer Enrichment Technology Solanum melongena domestication passport data single nucleotide polymorphism

Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
Dec 2023
Historique:
received: 13 12 2022
accepted: 26 08 2023
pubmed: 8 9 2023
medline: 8 9 2023
entrez: 8 9 2023
Statut: ppublish

Résumé

Eggplant (Solanum melongena) is an important Solanaceous crop, widely cultivated and consumed in Asia, the Mediterranean basin, and Southeast Europe. Its domestication centers and migration and diversification routes are still a matter of debate. We report the largest georeferenced and genotyped collection to this date for eggplant and its wild relatives, consisting of 3499 accessions from seven worldwide genebanks, originating from 105 countries in five continents. The combination of genotypic and passport data points to the existence of at least two main centers of domestication, in Southeast Asia and the Indian subcontinent, with limited genetic exchange between them. The wild and weedy eggplant ancestor S. insanum shows admixture with domesticated S. melongena, similar to what was described for other fruit-bearing Solanaceous crops such as tomato and pepper and their wild ancestors. After domestication, migration and admixture of eggplant populations from different regions have been less conspicuous with respect to tomato and pepper, thus better preserving 'local' phenotypic characteristics. The data allowed the identification of misclassified and putatively duplicated accessions, facilitating genebank management. All the genetic, phenotypic, and passport data have been deposited in the Open Access G2P-SOL database, and constitute an invaluable resource for understanding the domestication, migration and diversification of this cosmopolitan vegetable.

Identifiants

pubmed: 37682777
doi: 10.1111/tpj.16455
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1667-1680

Subventions

Organisme : Horizon 2020 G2P-SOL project
ID : 677379
Organisme : HORIZON EUROPE PRO-Grace
ID : 101094738

Informations de copyright

© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Acquadro, A., Barchi, L., Gramazio, P., Portis, E., Vilanova, S., Comino, C. et al. (2017) Coding SNPs analysis highlights genetic relationships and evolution pattern in eggplant complexes. PLoS One, 12, e0180774.
Alexander, D.H., Novembre, J. & Lange, K. (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655-1664.
ADMIXTOOLS 2. Available at: https://github.com/uqrmaie1/admixtools. Accessed on 11th February 2023
Arnoux, S., Fraïsse, C. & Sauvage, C. (2021) Genomic inference of complex domestication histories in three Solanaceae species. Journal of Evolutionary Biology, 34, 270-283.
Barchi, L., Acquadro, A., Alonso, D., Aprea, G., Bassolino, L., Demurtas, O. et al. (2019) Single primer enrichment technology (SPET) for high-throughput genotyping in tomato and eggplant germplasm. Frontiers in Plant Science, 10, 1005. Available from: https://doi.org/10.3389/fpls.2019.01005/full
Barchi, L., Pietrella, M., Venturini, L., Minio, A., Toppino, L., Acquadro, A. et al. (2019) A chromosome-anchored eggplant genome sequence reveals key events in Solanaceae evolution. Scientific Reports, 9, 11769.
Barchi, L., Rabanus-Wallace, M.T., Prohens, J., Toppino, L., Padmarasu, S., Portis, E. et al. (2021) Improved genome assembly and pan-genome provide key insights into eggplant domestication and breeding. The Plant Journal, 107, 579-596.
Cao, Y., Zhang, K., Yu, H., Chen, S., Xu, D., Zhao, H. et al. (2022) Pepper variome reveals the history and key loci associated with fruit domestication and diversification. Molecular Plant, 15, 1744-1758.
Chang, C.C., Chow, C.C., Tellier, L.C., Vattikuti, S., Purcell, S.M. & Lee, J.J. (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience, 4, 7.
Danecek, P., Auton, A., Abecasis, G., Albers, C.A., Banks, E., DePristo, M.A. et al. (2011) The variant call format and VCFtools. Bioinformatics, 27, 2156-2158.
Daunay, M.-C. (2008) Eggplant. In: Prohens, J. & Nuez, F. (Eds.) Vegetables II: Fabaceae, Liliaceae, Solanaceae, and Umbelliferae. New York: Springer, pp. 163-220.
Daunay, M.-C. & Janick, J. (2007) History and iconography of eggplant. Chronica Horticulturae, 47, 16-22.
Daunay, M.C., Lester, R.N., Gebhardt, C., Hennart, J.W. & Jahn, M. (2001) Genetic resources of eggplant (Solanum melongena) and allied species: a new challenge for molecular geneticists and eggplant breeders. In: van den Berg, R.G., Barendse, G.W.M., van der Weerden, G.M. & Mariani, C. (Eds.) Solanaceae V: advances in taxonomy and utilization. Nijmegen, The Netherlands: Nijmegen University Press, pp. 251-274.
Daunay, M.C.C. & Hazra, P. (2012) Eggplant. In: Hazra, P. & Peter, K.V. (Eds.) Handbook of vegetables. Houston: Springer, pp. 257-322.
Del Fabbro, C., Scalabrin, S., Morgante, M. & Giorgi, F.M. (2013) An extensive evaluation of read trimming effects on Illumina NGS data analysis. PLoS One, 8, e85024.
DePristo, M.A., Banks, E., Poplin, R., Garimella, K.V., Maguire, J.R., Hartl, C. et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics, 43, 491-498.
easySFS. Available at: https://github.com/isaacovercast/easySFS. Accessed on 22 March 2023
Ellstrand, N.C., Meirmans, P., Rong, J., Bartsch, D., Ghosh, A., de Jong, T.J. et al. (2013) Introgression of crop alleles into wild or weedy populations. Annual Review of Ecology, Evolution, and Systematics, 44, 325-345.
FAO. Available at: http://faostat3.fao.org/home/E.org/. Accessed on 25 October 2022
Felsenstein, J. (2005) PHYLIP (Phylogeny Inference Package). version 3.6.
Fitak, R.R. (2021) OptM: estimating the optimal number of migration edges on population trees using Treemix. Biology Methods and Protocols, 6, bpab017.
Fuks, D., Amichay, O., & Weiss, E. (2020). Innovation or preservation? Abbasid aubergines, archaeobotany, and the Islamic Green Revolution. Archaeological and Anthropological Sciences, 12, 50.
Gramazio, P., Prohens, J., Borràs, D., Plazas, M., Herraiz, F.J. & Vilanova, S. (2017) Comparison of transcriptome-derived simple sequence repeat (SSR) and single nucleotide polymorphism (SNP) markers for genetic fingerprinting, diversity evaluation, and establishment of relationships in eggplants. Euphytica, 213, 264.
Gramazio, P., Yan, H., Hasing, T., Vilanova, S., Prohens, J. & Bombarely, A. (2019) Whole-genome resequencing of seven eggplant (Solanum melongena) and one wild relative (S. incanum) accessions provides new insights and breeding tools for eggplant enhancement. Frontiers in Plant Science, 10, 1220.
Green, R.E., Krause, J., Briggs, A.W., Maricic, T., Stenzel, U., Kircher, M. et al. (2010) A draft sequence of the Neandertal genome. Science, 328, 710-722.
Harrison, R. (2017) Freezing seeds and making futures: endangerment, hope, security, and time in agrobiodiversity conservation practices. Culture, Agriculture, Food and Environment, 39, 80-89.
Herrero, J., Santika, B., Herrán, A., Erika, P., Sarimana, U., Wendra, F. et al. (2020) Construction of a high density linkage map in oil palm using SPET markers. Scientific Reports, 10, 9998.
Hoang, D.T., Chernomor, O., Haeseler, A.v., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35, 518-522.
Isshiki, S., Iwata, N. & Khan, M.M.R. (2008) ISSR variations in eggplant (Solanum melongena L.) and related solanum species. Scientia Horticulturae, 117, 186-190.
Knapp, S., Vorontsova, M.S. & Prohens, J. (2013) Wild relatives of the eggplant (Solanum melongena L.: Solanaceae): new understanding of species names in a complex group. PLoS One, 8, e57039.
Kopelman, N.M., Mayzel, J., Jakobsson, M., Rosenberg, N.A. & Mayrose, I. (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15, 1179-1191.
Langridge, P. & Waugh, R. (2019) Harnessing the potential of germplasm collections. Nature Genetics, 51, 200-201.
Lester, R. & Hasan, S. (1991) Origin and domestication of the brinjal egg-plant, Solanum melongena, from S. incanum, in Africa and Asia. Kew, Richmond: The Royal Botanic Gardens.
Lester, R.N. & Niakan, L. (1986) Origin and domestication of the scarlet eggplant, Solanum aethiopicum, from S. anguivi in Africa. In: D'Arcy, W.G. (Ed.) Solanaceae: Biology and systematics. New York: Columbia University Press, pp. 433-456.
Lewicki, T., Johnson, M. & Abrahamowicz, M. (1974) West African food in the Middle Ages: according to Arabic sources. Cambridge: Cambridge University Press.
Li, D., Qian, J., Li, W., Yu, N., Gan, G., Jiang, Y. et al. (2021) A high-quality genome assembly of the eggplant provides insights into the molecular basis of disease resistance and chlorogenic acid synthesis. Molecular Ecology Resources, 21, 1274-1286.
Li, H. (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv. Available from: http://arxiv.org/abs/1303.3997. Accessed on 13 June 2022
Liu, X. & Fu, Y.-X. (2020) Stairway Plot 2: demographic history inference with folded SNP frequency spectra. Genome Biology, 21, 280.
Maier, R., Flegontov, P., Flegontova, O., Changmai, P. & Reich, D. (2022) On the limits of fitting complex models of population history to genetic data. bioRxiv. 2022.05.08.491072. Available from: https://doi.org/10.1101/2022.05.08.491072
Malomane, D.K., Reimer, C., Weigend, S., Weigend, A., Sharifi, A.R. & Simianer, H. (2018) Efficiency of different strategies to mitigate ascertainment bias when using SNP panels in diversity studies. BMC Genomics, 19, 22.
Mangino, G., Arrones, A., Plazas, M., Pook, T., Prohens, J., Gramazio, P. et al. (2022) Newly developed MAGIC population allows identification of strong associations and candidate genes for anthocyanin pigmentation in eggplant. Frontiers in Plant Science, 13, 847789. Available from: https://doi.org/10.3389/fpls.2022.847789
Martin, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal, 17(1), 200.
Meyer, R.S., Bamshad, M., Fuller, D.Q. & Litt, A. (2014) Comparing medicinal uses of eggplant and related Solanaceae in China, India, and The Philippines suggests the independent development of uses, cultural diffusion, and recent species substitutions. Economic Botany, 68, 137-152.
Meyer, R.S., Karol, K.G., Little, D.P., Nee, M.H. & Litt, A. (2012) Phylogeographic relationships among Asian eggplants and new perspectives on eggplant domestication. Molecular Phylogenetics and Evolution, 63, 685-701.
Milanesi, M., Capomaccio, S., Vajana, E., Bomba, L., Garcia, J.F., Ajmone-Marsan, P. et al. (2017) BITE: an R package for biodiversity analyses. bioRxiv. Available from: https://www.biorxiv.org/content/10.1101/181610v1 [Accessed 6th December 2021].
Milner, S.G., Jost, M., Taketa, S., Mazón, E.R., Himmelbach, A., Oppermann, M. et al. (2019) Genebank genomics highlights the diversity of a global barley collection. Nature Genetics, 51, 319-326.
Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., Haeseler, A.v. et al. (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530-1534. Available from: https://doi.org/10.1093/molbev/msaa015
Page, A., Gibson, J., Meyer, R.S. & Chapman, M.A. (2019) Eggplant domestication: pervasive gene flow, feralization, and transcriptomic divergence. Molecular Biology and Evolution, 36, 1359-1372.
Patterson, N., Moorjani, P., Luo, Y., Mallick, S., Rohland, N., Zhan, Y. et al. (2012) Ancient admixture in human history. Genetics, 192, 1065-1093.
Peter, B.M. (2016) Admixture, population structure, and F-statistics. Genetics, 202, 1485-1501.
Pickrell, J.K. & Pritchard, J.K. (2012) Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics, 8, e1002967.
Plazas, M., AndÃojar, I., Vilanova, S., Gramazio, P., Herraiz, F.J. & Prohens, J. (2014) Conventional and phenomics characterization provides insight into the diversity and relationships of hypervariable scarlet (Solanum aethiopicum L.) and gboma (S. macrocarpon L.) eggplant complexes. Frontiers in Plant Science, 5, 318.
Prell, W.L. & Kutzbach, J.E. (1987) Monsoon variability over the past 150,000 years. Journal of Geophysical Research: Atmospheres, 92, 8411-8425.
Prohens, J., Blanca, J.M. & Nuez, F. (2005) Morphological and molecular variation in a collection of eggplants from a secondary center of diversity: implications for conservation and breeding. Journal of the American Society for Horticultural Science, 130, 54-63.
Sakata, Y. & Lester, R.N. (1997) Chloroplast DNA diversity in brinjal eggplant (Solanum melongena L.) and related species. Euphytica, 97, 295-301.
Sakata, Y., Nishio, T. & Matthews, P.J. (1991) Chloroplast DNA analysis of eggplant (Solanum melongena) and related species for their taxonomic affinity. Euphytica, 55, 21-26.
Särkinen, T., Bohs, L., Olmstead, R.G. & Knapp, S. (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evolutionary Biology, 13, 214.
Scaglione, D., Pinosio, S., Marroni, F. et al. (2019) Single primer enrichment technology as a tool for massive genotyping: a benchmark on black poplar and maize. Annals of Botany, 124(4), 543-552. Available from: https://doi.org/10.1093/aob/mcz054/5424191
Syfert, M.M., Castañeda-Álvarez, N.P., Khoury, C.K., Särkinen, T., Sosa, C.C., Achicanoy, H.A. et al. (2016) Crop wild relatives of the brinjal eggplant (Solanum melongena): poorly represented in genebanks and many species at risk of extinction. American Journal of Botany, 103, 635-651.
Tripodi, P., Rabanus-Wallace, M.T., Barchi, L. et al. (2021) Global range expansion history of pepper (Capsicum spp.) revealed by over 10,000 genebank accessions. Proceedings of the National Academy of Sciences of the United States of America, 118, e2104315118.
Vilanova, S., Alonso, D., Gramazio, P., Plazas, M., García-Fortea, E., Ferrante, P. et al. (2020) SILEX: a fast and inexpensive high-quality DNA extraction method suitable for multiple sequencing platforms and recalcitrant plant species. Plant Methods, 16, 110.
Villanueva, G., Rosa-Martínez, E., Şahin, A., García-Fortea, E., Plazas, M., Prohens, J. et al. (2021) Evaluation of advanced backcrosses of eggplant with Solanum elaeagnifolium introgressions under low N conditions. Agronomy, 11, 1770.
Vorontsova, M.S., Stern, S., Bohs, L. & Knapp, S. (2013) African spiny Solanum (subgenus Leptostemonum, Solanaceae): a thorny phylogenetic tangle. Botanical Journal of the Linnean Society, 173, 176-193.
Wang, J.-X., Gao, T.-G. & Knapp, S. (2008) Ancient Chinese literature reveals pathways of eggplant domestication. Annals of Botany, 102, 891-897.
Weese, T.L. & Bohs, L. (2010) Eggplant origins: out of Africa, into the orient. Taxon, 59, 49-56.
Wei, Q., Wang, J., Wang, W., Hu, T., Hu, H. & Bao, C. (2020) A high-quality chromosome-level genome assembly reveals genetics for important traits in eggplant. Horticulture Research, 7, 1-15.
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
Zheng, X., Levine, D., Shen, J., Gogarten, S.M., Laurie, C. & Weir, B.S. (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics, 28, 3326-3328.

Auteurs

Lorenzo Barchi (L)

DISAFA - Plant Genetics, University of Turin, Grugliasco, Torino, 10095, Italy.

Giuseppe Aprea (G)

ENEA, Casaccia Res Ctr, Via Anguillarese 301, Rome, 00123, Italy.

M Timothy Rabanus-Wallace (MT)

Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstr. 3, Seeland, OT Gatersleben, 06466, Germany.
Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, Australia.

Laura Toppino (L)

CREA, Research Centre for Genomics and Bioinformatics, Via Paullese 28, Montanaso Lombardo, LO 26836, Italy.

David Alonso (D)

Universitat Politècnica de València, Camino de Vera 14, Valencia, 46022, Spain.

Ezio Portis (E)

DISAFA - Plant Genetics, University of Turin, Grugliasco, Torino, 10095, Italy.

Sergio Lanteri (S)

DISAFA - Plant Genetics, University of Turin, Grugliasco, Torino, 10095, Italy.

Luciana Gaccione (L)

DISAFA - Plant Genetics, University of Turin, Grugliasco, Torino, 10095, Italy.

Emmanuel Omondi (E)

The World Vegetable Centre, Tainan City, Taiwan.

Maarten van Zonneveld (M)

The World Vegetable Centre, Tainan City, Taiwan.

Roland Schafleitner (R)

The World Vegetable Centre, Tainan City, Taiwan.

Paola Ferrante (P)

ENEA, Casaccia Res Ctr, Via Anguillarese 301, Rome, 00123, Italy.

Andreas Börner (A)

Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstr. 3, Seeland, OT Gatersleben, 06466, Germany.

Nils Stein (N)

Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstr. 3, Seeland, OT Gatersleben, 06466, Germany.
Department of Crop Sciences, Center for Integrated Breeding Research (CiBreed), Georg-August-University, Von Siebold Str. 8, Göttingen, 37075, Germany.

Maria José Díez (MJ)

Universitat Politècnica de València, Camino de Vera 14, Valencia, 46022, Spain.

Veronique Lefebvre (V)

INRAE, GAFL, Montfavet, F-84140, France.

Jérémy Salinier (J)

INRAE, GAFL, Montfavet, F-84140, France.
CIRAD La Réunion et Mayotte, UMR PVBMT Saint-Pierre, La Réunion, France.

Hatice Filiz Boyaci (HF)

Department of Horticulture, Faculty of Agriculture, University of Recep Tayyip Erdogan, Rize, Turkey.

Richard Finkers (R)

Wageningen University & Research WUR, Wageningen, The Netherlands.
GenNovation B.V., Wageningen, The Netherlands.

Matthijs Brouwer (M)

Wageningen University & Research WUR, Wageningen, The Netherlands.

Arnaud G Bovy (AG)

Wageningen University & Research WUR, Wageningen, The Netherlands.

Giuseppe Leonardo Rotino (GL)

CREA, Research Centre for Genomics and Bioinformatics, Via Paullese 28, Montanaso Lombardo, LO 26836, Italy.

Jaime Prohens (J)

Universitat Politècnica de València, Camino de Vera 14, Valencia, 46022, Spain.

Giovanni Giuliano (G)

ENEA, Casaccia Res Ctr, Via Anguillarese 301, Rome, 00123, Italy.

Classifications MeSH