Selection footprints reflect genomic changes associated with breeding efforts in 56 cucumber inbred lines

Abstract

Cucumber selective breeding over recent decades has dramatically increased productivity and quality, but the genomic characterizations and changes associated with this breeding history remain unclear. Here, we analyzed the genome resequencing data of 56 artificially selected cucumber inbred lines that exhibit various phenotypes to detect trait-associated sequence variations that reflect breeding improvement. We found that the 56 cucumber lines could be assigned to group 1 and group 2, and the two groups formed a distinctive genetic structure due to the breeding history involving hybridization and selection. Differentially selected regions were identified between group 1 and group 2, with implications for genomic-selection breeding signatures. These regions included known quantitative trait loci or genes that were reported to be associated with agronomic traits. Our results advance knowledge of cucumber genomics, and the 56 selected inbred lines could be good germplasm resources for breeding.

References

[1] Huang, S. et al. The genome of the cucumber, Cucumis sativus L.. Nat. Genet. 41, 1275 (2009).

[2] Liu, B. et al. Silencing of the gibberellin receptor homolog, CsGID1a, affects locule formation in cucumber (Cucumis sativus) fruit. New Phytol. 210, 551-563 (2016).

[3] Qi, J. et al. A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat. Genet. 45, 1510 (2013).

[4] Che, G. & Zhang, X. Molecular basis of cucumber fruit domestication. Curr. Opin. Plant Biol. 47, 38-46 (2019).

[5] Staub, J. E., Robbins, M. D. & Wehner, T. C. in Vegetables I (eds Prohens, J. & Nuez, F.) 241-282 (Springer, 2008).

[6] Voss-Fels, K. P., Cooper, M. & Hayes, B. J. Accelerating crop genetic gains with genomic selection. Theor. Appl. Genet. 132, 669-686 (2019).

[7] Kozik, E. U. in Cucurbitaceae 2016, XIth Eucarpia Meeting on Cucurbit Genetics & Breeding, July 24-28, 2016, Warsaw, Poland. (Organizing Committee of Cucurbitaceae, 2016).

[8] Xu, Y. & Crouch, J. H. Marker-assisted selection in plant breeding: from publications to practice. Crop Sci. 48, 391-407 (2008).

[9] Fan, Z., Robbins, M. D. & Staub, J. E. Population development by phenotypic selection with subsequent marker-assisted selection for line extraction in cucumber (Cucumis sativus L.). Theor. Appl. Genet. 112, 843-855 (2006).

[10] Kooistra, E. Femaleness in breeding glasshouse cucumbers. Euphytica 16, 1-17 (1967).

[11] Sitterly, W. R. Breeding for disease resistance in cucurbits. Annu. Rev. Phytopathol. 10, 471-490 (1972).

[12] Yang, X. et al. Fine mapping of the uniform immature fruit color gene u in cucumber (Cucumis sativus L.). Euphytica 196, 341-348 (2014).

[13] Andeweg, J. & De, BruynJ. Breeding of non-bitter cucumbers. Euphytica 8, 13-20 (1959).

[14] Hufford, M.-B. et al. Comparative population genomics of maize domestication and improvement. Nat. Genet. 44, 808 (2012).

[15] Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961 (2010).

[16] Lam, H. M. et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 42, 1053 (2010).

[17] Mace, E. S. et al. Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum. Nat. Commun. 4, 2320 (2013).

[18] Duan, N. et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat. Commun. 8, 249 (2017).

[19] Guo, S. et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat. Genet. 45, 51 (2013).

[20] Pereira-Dias, L., Vilanova, S., Fita, A., Prohens, J. & Rodríguez-Burruezo, A. Genetic diversity, population structure, and relationships in a collection of pepper (Capsicum spp.) landraces from the Spanish centre of diversity revealed by genotyping-by-sequencing (GBS). Hort. Res. 6, 54 (2019).

[21] Huang, X. et al. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat. Genet. 44, 32 (2012).

[22] Wang, X. et al. The USDA cucumber (Cucumis sativus L.) collection: genetic diversity, population structure, genome-wide association studies, and core collection development. Hort. Res. 5, 64 (2018).

[23] Zheng, Y. et al. Cucurbit Genomics Database (CuGenDB): a central portal for comparative and functional genomics of cucurbit crops. Nucleic Acids Res. 47, D1128-D1136 (2018).

[24] Yang, X. et al. High-resolution mapping of the dull fruit skin gene D in cucumber (Cucumis sativus L.). Mol. Breed. 33, 15-22 (2014).

[25] Wang, Y.-L. et al. Identification and mapping of Tril, a homeodomain-leucine zipper gene involved in multicellular trichome initiation in Cucumis sativus. Theor. Appl. Genet. 129, 305-316 (2016).

[26] Yang, X. et al. Tuberculate fruit gene Tu encodes a C₂H₂ zinc finger protein that is required for the warty fruit phenotype in cucumber (Cucumis sativus L.) . Plant J. 78, 1034-1046 (2014).

[27] Yang, S. et al. A CsTu‐TS 1 regulatory module promotes fruit tubercule formation in cucumber. Plant Biotechnol. J. 17, 289-301 (2018).

[28] Guo, C. et al. Identification and mapping of ts (tender spines), a gene involved in soft spine development in Cucumis sativus. Theor. Appl. Genet. 131, 1-12 (2018).

[29] Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).

[30] Zhou, H., Alexander, D. & Lange, K. A quasi-Newton acceleration for high-dimensional optimization algorithms. Stat. Comput. 21, 261-273 (2011).

[31] Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425 (1987).

[32] Pickrell, J. K. & Pritchard, J. K. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (2012).

[33] Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239-2252 (2011).

[34] Hübner, S. et al. Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance. Nat. Plants 1, 54-62 (2018).

[35] Bo, K., Ma, Z., Chen, J. & Weng, Y. Molecular mapping reveals structural rearrangements and quantitative trait loci underlying traits with local adaptation in semi-wild Xishuangbanna cucumber (Cucumis sativus L. var. xishuangbannanesis Qi et Yuan). Theor. Appl. Genet. 128, 25-39 (2015).

[36] Pan, Y. et al. QTL mapping of domestication and diversifying selection related traits in round-fruited semi-wild Xishuangbanna cucumber (Cucumis sativus L. var. xishuangbannanesis). Theor. Appl. Genet. 130, 1531-1548 (2017).

[37] Liu, B. et al. A new grafted rootstock against root-knot nematode for cucumber, melon, and watermelon. Agron. Sustain Dev. 35, 251-259 (2015).

[38] Pavlidis, P., Živković, D., Stamatakis, A. & Alachiotis, N. SweeD: likelihood-based detection of selective sweeps in thousands of genomes. Mol. Biol. Evol. 30, 2224-2234 (2013).

[39] Xu, X. et al. Fine mapping of a dominantly inherited powdery mildew resistance major-effect QTL, Pm1. 1, in cucumber identifies a 41.1 kb region containing two tandemly arrayed cysteine-rich receptor-like protein kinase genes. Theor. Appl. Genet. 129, 507-516 (2016).

[40] Win, K. T., Vegas, J., Zhang, C., Song, K. & Lee, S. QTL mapping for downy mildew resistance in cucumber via bulked segregant analysis using next-generation sequencing and conventional methods. Theor. Appl. Genet. 130, 199-211 (2017).

[41] Lu, H. et al. QTL-seq identifies an early flowering QTL located near Flowering Locus T in cucumber. Theor. Appl. Genet. 127, 1491-1499 (2014).

[42] Tan, J. et al. A novel allele of monoecious (m) locus is responsible for elongated fruit shape and perfect flowers in cucumber (Cucumis sativus L.). Theor. Appl. Genet. 128, 2483-2493 (2015).

[43] Shang, Y. et al. Biosynthesis, regulation, and domestication of bitterness in cucumber. Science 346, 1084-1088 (2014).

[44] Purugganan, M. D. & Fuller, D. Q. The nature of selection during plant domestication. Nature 457, 843 (2009).

[45] Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv Prepr. arXiv 1303, 3997 (2013).

[46] Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).

[47] Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120 (2014).

[48] McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 9, 1297-1303 (2010).

[49] Browning, B. L. & Browning, S. R. Genotype imputation with millions of reference samples. Am. J. Hum. Genet. 98, 116-126 (2016).

[50] Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80-92 (2012).

[51] Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575 (2007).

[52] Alexander, D. H. & Lange, K. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinform. 12, 246 (2011).

[53] Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome res. 9, 1655-1664 (2009).

[54] Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156-2158 (2011).

[55] Zhang, C., Dong, S.-S., Xu, J.-Y., He, W.-M. & Yang, T.-L. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 10, 1786-1788 (2018).

[56] Foll, M. & Gaggiotti, O. E. A genome scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 2, 977-993 (2008).

[57] Nielsen, R. et al. Genomic scans for selective sweeps using SNP data. Genome Res. 15, 1566-1575 (2005).