Horticulture
| Open Access | Population Genomics of Eruca sativa Reveals a Dual Domestication History and Provides a Roadmap for Crop Improvement
Dr. Elena Petrova , Department of Plant and Microbial Biology, Wageningen University & Research, Wageningen, NetherlandsAbstract
Background: Arugula (Eruca sativa Mill.), a member of the Brassicaceae family, is a globally cultivated salad vegetable prized for its distinct pungent flavor and nutritional value. Despite its long history of cultivation, its precise geographic origins, domestication trajectory, and the genetic basis of key agronomic traits remain poorly understood. A comprehensive genomic investigation is essential to unravel its evolutionary history and accelerate modern breeding efforts.
Methods: We performed whole-genome resequencing on a diverse panel of 150 E. sativa accessions, encompassing wild relatives and cultivated landraces from across its native range. Using a high-quality single nucleotide polymorphism (SNP) dataset, we conducted population genetic analyses, including principal component analysis (PCA), phylogenetic reconstruction using IQ-TREE [27], and ancestry modeling with ADMIXTURE [2]. We inferred demographic history using Stairway Plot 2 [22] and identified signatures of selection by calculating population differentiation (Fst) and applying the cross-population composite likelihood ratio (XP-CLR) test [6].
Results: Our analyses revealed two major, distinct genetic clusters corresponding to Mediterranean/European and Asian gene pools, with limited admixture between them. This strong differentiation, supported by phylogenetic and
demographic modeling, points towards a dual domestication history. We identified hundreds of genomic regions bearing strong signatures of positive selection in cultivated accessions. Within these selective sweeps, we annotated candidate genes associated with critical agronomic traits, including flowering time, leaf morphology, and glucosinolate biosynthesis, which dictates flavor. Furthermore, we found evidence of selection on genes homologous to known domestication loci in other crop species.
Conclusion: This study provides the first robust, genome-wide evidence for a dual-origin model of arugula domestication. We have created a detailed map of genomic variation and identified key candidate genes underlying important agricultural traits. These findings not only clarify the evolutionary history of arugula but also provide a valuable genomic toolkit of markers and target genes to guide future crop improvement and breeding programs.
Keywords
Eruca sativa, Population Genomics, Domestication, Selective Sweep
References
Agrawal N, Gupta M, Banga SS, Heslop-Harrison JP. Identification of chromosomes and chromosome rearrangements in crop brassicas and Raphanus sativus: a cytogenetic toolkit using synthesized massive oligonucleotide libraries. Front Plant Sci. 2020;11:598039. https://doi.org/10.3389/FPLS.2020.598039.
Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19(9):1655–64. https://doi.org/10.1101/gr.094052.109.
Behr AA, Liu KZ, Liu-Fang G, Nakka P, Ramachandran S. pong: fast analysis and visualization of latent clusters in population genetic data. Bioinformatics. 2016;32(18):2817–23. https://doi.org/10.1093/bioinformatics/btw327.
Bell L, Wagstaff C. Rocket science: a review of phytochemical & health-related research in Eruca & Diplotaxis species. Food Chemistry: X. 2019;1:100002. https://doi.org/10.1016/j.fochx.2018.100002.
Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience. 2015;4(1):7. https://doi.org/10.1186/s13742-015-0047-8.
Chen H, Patterson N, Reich D. Population differentiation as a test for selective sweeps. Genome Res. 2010;20(3):393–402. https://doi.org/10.1101/gr.100545.109.
Dai L, Li X, Guan C, Zhong J. On ovary and embryo culture of hybrid between rapeseeds and Rocketsalad. J Hunan Agric Univ (Nat Sci). 2004;3:201–4.
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156–8. https://doi.org/10.1093/bioinformatics/btr330.
Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10(2):giab008. https://doi.org/10.1093/GIGASCIENCE/GIAB008.
Dong G, Du L, Yang L, Lu M, Qiu M, Li H, et al. Dispersal of crop-livestock and geographical-temporal variation of subsistence along the Steppe and Silk Roads across Eurasia in prehistory. Sci China Earth Sci. 2022;65(7):1187–210. https://doi.org/10.1007/s11430-021-9929-x.
Golkar P, Bakhtiari MA. Evaluation of genetic diversity in the world collection of Eruca sativa L. using oil content, fatty acids and molecular markers. Ind Crops Prod. 2020;148:112280. https://doi.org/10.1016/j.indcrop.2020.112280.
Greuter W, Burdet HM, Long G. Med-Checklist: a critical inventory of vascular plants of the circum-mediterranean countries, vol. 3. Geneva: OPTIMA and Conservatoire et Jardin botaniques; 2008.
Guijarro-Real C, Navarro A, Esposito S, Festa G, Macellaro R, Di Cesare C, et al. Large scale phenotyping and molecular analysis in a germplasm collection of rocket salad (Eruca vesicaria) reveal a differentiation of the gene pool by geographical origin. Euphytica. 2020;216(3):53. https://doi.org/10.1007/s10681-020-02586-x.
Hall M, Jobling J, Rogers G. Factors affecting growth of perennial wall rocket and annual garden rocket. Int J Veg Sci. 2012;18(4):393–411. https://doi.org/10.1080/19315260.2012.660565.
Hanelt P, Buttner R, Mansfeld R. Mansfeld’s encyclopedia of agricultural and horticultural crops (except ornamentals). Springer; 2001. https://doi.org/10.1007/978-3-540-30442-5.
Kang L, Qian L, Zheng M, Chen L, Chen H, Yang L, et al. Genomic insights into the origin, domestication and diversification of Brassica juncea. Nat Genet. 2021;53(9):1392–402. https://doi.org/10.1038/s41588-021-00922-y.
Kiefer C, Willing EM, Jiao WB, Sun H, Piednoel M, Humann U, et al. Interspecies association mapping links reduced CG to TG substitution rates to the loss of gene-body methylation. Nat Plants. 2019;5(8):846–55. https://doi.org/10.1038/s41477-019-0486-9.
Lan M. Dian Nan Ben Cao. 1959.
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60. https://doi.org/10.1093/bioinformatics/btp324.
Lidin OG. Tanegashima-the arrival of Europe in Japan. Routledge; 2003.
Liu H, Li Q, Xing Y. Genes contributing to domestication of rice seed traits and its global expansion. Genes. 2018. https://doi.org/10.3390/genes9100489.
Liu X, Fu YX. Stairway plot 2: demographic history inference with folded SNP frequency spectra. Genome Biol. 2020;21(1):280. https://doi.org/10.1186/s13059-020-02196-9.
Malinsky M, Matschiner M, Svardal H. Dsuite-fast D-statistics and related admixture evidence from VCF files. Mol Ecol Resour. 2021;21(2):584–95. https://doi.org/10.1111/1755-0998.13265.
Manichaikul A, Mychaleckyj JC, Rich SS, Daly K, Sale M, Chen WM. Robust relationship inference in genome-wide association studies. Bioinformatics. 2010;26(22):2867–73. https://doi.org/10.1093/bioinformatics/btq559.
Matsuzawa Y, Mekiyanon S, Kaneko Y, Bang SW, Wakui K, Takahata Y. Male sterility in alloplasmic Brassica rapa L. carrying Eruca sativa cytoplasm. Plant Breed. 1999;118(1):82–4.
Morales M, Janick J. Arugula: a promising specialty leaf vegetable. In: Janick J, Whipkey A, editors. n.d.
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. https://doi.org/10.1093/molbev/msu300.
Nothnagel T, Budahn H, Schrader O, Klocke E, editors. Intergeneric hybridization between Brassica oleracea and Eruca sativa. VI International Symposium on Brassicas and XVIII Crucifer Genetics Workshop 1005; 2012.
Olesen MH, Romme HA, Kampmann HH. Rucola plants with cytoplasmic male sterility (CMS). US8247655B2. Google; 2012.
Park JS, Park JH, Park YD. Construction of pseudomolecule sequences of Brassica rapa ssp. pekinensis inbred line CT001 and analysis of spontaneous mutations derived via sexual propagation. PLoS One. 2019;14(9):e0222283. https://doi.org/10.1371/journal.pone.0222283.
Pickrell JK, Pritchard JK. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 2012;8(11):e1002967. https://doi.org/10.1371/journal.pgen.1002967.
Pignone D, Gómez-Campo C. Eruca. Wild crop relatives: genomic and breeding resources. In: Kole C, editor. Springer; 2011. p. 149–60. https://doi.org/10.1007/978-3-642-21102-7.
R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2023.
Renfrew J, Sanderson H. Herbs and vegetables. In: Ghillean P, Mark N, editors. 2012.
RStudio Team. RStudio: Integrated Development for R. PBC, Boston, MA; 2020.
Sastry E. Taramira (Eruca sativa) and its improvement–a review. Agric Rev. 2003;24(4):235–49.
Sihag RC. Pollination ecology of rocket (Eruca vesicaria) in semi-arid Northwest India: native bees are the major pollinators. Ecologies. 2023;4(3):580–94. https://doi.org/10.3390/ecologies4030038.
Subramanian B, Gao S, Lercher MJ, Hu S, Chen WH. Evolview v3: a webserver for visualization, annotation, and management of phylogenetic trees. Nucleic Acids Res. 2019;47(W1):W270–5. https://doi.org/10.1093/nar/gkz357.
Sun W, Guan C, Meng Y, Liu Z, Zhang T, Li X, et al. Intergeneric crosses between Eruca sativa Mill. and Brassica species. Zuo Wu Xue Bao. 2005;1:36–42.
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide datasets. Nucleic Acids Res. 2019;47(D1):D607–13. https://doi.org/10.1093/nar/gky1131.
Traboulay DM. Columbus and Las Casas: the conquest and Christianization of America, 1492–1566. Maryland: University Press of America; 1994.
Wang Y, Chu P, Yang Q, Chang S, Chen J, Hu M, et al. Complete mitochondrial genome of Eruca sativa Mill. (Garden rocket). PLoS One. 2014;9(8):e105748. https://doi.org/10.1371/journal.pone.0105748.
Warwick SI, Gugel RK, Gómez-Campo C, James T. Genetic variation in Eruca vesicaria. Plant Genet Resour. 2007;5(3):142–53. https://doi.org/10.1017/S1479262107842675.
Xu G, Zhang X, Chen W, Zhang R, Li Z, Wen W, et al. Population genomics of Zea species identifies selection signatures during maize domestication and adaptation. BMC Plant Biol. 2022;22(1):72. https://doi.org/10.1186/s12870-022-03427-w.
Yaniv Z, editor. Tradition, uses and research on rocket in Israel. In: Rocket: a Mediterranean crop for the world. Legnaro (Padova); 1996.
Zafar-Pashanezhad M, Shahbazi E, Golkar P, Shiran B. Genetic variation of Eruca sativa L. genotypes revealed by agro-morphological traits and ISSR molecular markers. Ind Crops Prod. 2020;145:111992. https://doi.org/10.1016/j.indcrop.2019.111992
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