Chromosome-scale genome assembly of Cucumis hystrix—a wild species interspecifically cross-compatible with cultivated cucumber

Xiaodong Qin , Zhonghua Zhang , Qunfeng Lou , Lei Xia , Ji Li , Mengxue Li , Junguo Zhou , Xiaokun Zhao , Yuanchao Xu , Qing Li , Shuqiong Yang , Xiaqing Yu , Chunyan Cheng , Sanwen Huang , Jinfeng Chen

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 40

PDF (1490KB)
Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :40 DOI: 10.1038/s41438-021-00475-5
Article
research-article
Chromosome-scale genome assembly of Cucumis hystrix—a wild species interspecifically cross-compatible with cultivated cucumber
Author information +
History +
PDF (1490KB)

Abstract

Cucumis hystrix Chakr. (2n = 2x = 24) is a wild species that can hybridize with cultivated cucumber (C. sativus L., 2n = 2x = 14), a globally important vegetable crop. However, cucumber breeding is hindered by its narrow genetic base. Therefore, introgression from C. hystrix has been anticipated to bring a breakthrough in cucumber improvement. Here, we report the chromosome-scale assembly of C. hystrix genome (289 Mb). Scaffold N50 reached 14.1 Mb. Over 90% of the sequences were anchored onto 12 chromosomes. A total of 23,864 genes were annotated using a hybrid method. Further, we conducted a comprehensive comparative genomic analysis of cucumber, C. hystrix, and melon (C. melo L., 2n = 2x = 24). Whole-genome comparisons revealed that C. hystrix is phylogenetically closer to cucumber than to melon, providing a molecular basis for the success of its hybridization with cucumber. Moreover, expanded gene families of C. hystrix were significantly enriched in “defense response,” and C. hystrix harbored 104 nucleotide-binding site–encoding disease resistance gene analogs. Furthermore, 121 genes were positively selected, and 12 (9.9%) of these were involved in responses to biotic stimuli, which might explain the high disease resistance of C. hystrix. The alignment of whole C. hystrix genome with cucumber genome and self-alignment revealed 45,417 chromosome-specific sequences evenly distributed on C. hystrix chromosomes. Finally, we developed four cucumber– C. hystrix alien addition lines and identified the exact introgressed chromosome using molecular and cytological methods. The assembled C. hystrix genome can serve as a valuable resource for studies on Cucumis evolution and interspecific introgression breeding of cucumber.

Cite this article

Download citation ▾
Xiaodong Qin, Zhonghua Zhang, Qunfeng Lou, Lei Xia, Ji Li, Mengxue Li, Junguo Zhou, Xiaokun Zhao, Yuanchao Xu, Qing Li, Shuqiong Yang, Xiaqing Yu, Chunyan Cheng, Sanwen Huang, Jinfeng Chen. Chromosome-scale genome assembly of Cucumis hystrix—a wild species interspecifically cross-compatible with cultivated cucumber. Horticulture Research, 2021, 8 (1) : 40 DOI:10.1038/s41438-021-00475-5

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Joseph John, K. et al. On the taxonomic status, occurrence and distribution of Cucumis hystrix Chakrav. and Cucumis muriculatus Chakrav. (Cucurbitaceae) in India. Genet. Resour. Crop Evol. 65, 1687-1698 (2018).

[2]

Chen, J. et al. Successful interspecific hybridization between Cucumis sativus L. and C. hystrix Chakr. Euphytica 96, 413-419 (1997).

[3]

Chen, J. et al. Some disease resistance tests in Cucumis hystrix and its progenies from interspecific hybridization with cucumber. Progress in Cucurbit Genetics and Breeding Research Proceedings of Cucurbitaceae 2004, the 8th EUCARPIA Meeting on Cucurbit Genetics and Breeding, 189-196 (Olomouc, 2004).

[4]

Qian, C. et al. Several photosynthetic characters of the synthetic species Cucumis hytivus Chen & Kirkbride under weak light condition. Plant Physiol. Commun. 38, 336-338 (2002).

[5]

Zhuang, F. et al. Responses of seedlings of Cucumis hytivus and progenies to low temperature. JNAU 25, 27-30 (2002).

[6]

Qi, J. et al. A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat. Genet. 45, 1510-1515 (2013).

[7]

S. D, T. & S. R., M. Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277, 1063—1066 (1997).

[8]

Zamir, D. Improving plant breeding with exotic genetic libraries. Nat. Rev. Genet. 2, 983-989 (2001).

[9]

Govindaraj, M. et al. Importance of genetic diversity assessment in crop plants and its recent advances: an overview of its analytical perspectives. Genet. Res. Int. 2015, 1-14 (2015).

[10]

Dempewolf, H. et al. Past and future use of wild relatives in crop breeding. Crop Sci. 57, 1070-1082 (2017).

[11]

Zhou, X. et al. Molecular analysis of introgression lines from Cucumis hystrix Chakr. to C. sativus L. Sci. Hortic. 119, 232-235 (2009).

[12]

Delannay, I. Y. et al. Backcross Introgression of the Cucumis hystrix Genome Increases Genetic Diversity in U.S. Processing Cucumber. J. Am. Soc. Hortic. Sci. 135, 351-361 (2010).

[13]

Chen, F. et al. The Sequenced Angiosperm Genomes and Genome Databases. Front Plant Sci. 9, 418 (2018).

[14]

Huang, S. et al. The genome of the cucumber, Cucumis sativus L. Nat. Genet. 41, 1275-1281 (2009).

[15]

Garcia—Mas, J. et al. The genome of melon (Cucumis melo L.). Proc. Natl Acad. Sci. USA. 109, 11872-11877 (2012).

[16]

Zhuang, F. et al. Taxonomic relationships of a rare Cucumis species (C. hystrix Chakr.) and its interspecific hybrid with cucumber. HortScience 41, 571-574 (2006).

[17]

Ghebretinsae, A. G. et al. Relationships of cucumbers and melons unraveled: Molecular phylogenetics of Cucumis and related genera (Benincaseae, Cucurbitaceae). Am. J. Bot. 94, 1256-1266 (2007).

[18]

Renner, S. S. et al. Phylogenetics of Cucumis (Cucurbitaceae): Cucumber (C. sativus) belongs in an Asian/Australian clade far from melon (C. melo). BMC Evol. Biol. 7, 58 (2007).

[19]

Sebastian, P. et al. Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. Proc. Natl Acad. Sci. USA 107, 14269-14273 (2010).

[20]

Zhang, Y. et al. Chromosomal structures and repetitive sequences divergence in Cucumis species revealed by comparative cytogenetic mapping. BMC Genomics 16, 730 (2015).

[21]

Han, Y. et al. Chromosome—specific painting in Cucumis Species using bulked oligonucleotides. Genetics 200, 771-779 (2015).

[22]

Li, D. et al. Syntenic relationships between cucumber (Cucumis sativus L.) and melon (C. melo L.) chromosomes as revealed by comparative genetic mapping. BMC Genomics 12, 396 (2011).

[23]

Wendel, J. F. & Doyle, J. J. in Molecular Systematics of Plants II: DNA Sequencing (eds Soltis, D. E., Soltis, P. S. & Doyle, J. J. ) 265-296 (Springer US, 1998).

[24]

Rokas, A. et al. Genome—scale approaches to resolving incongruence in molecular phylogenies. Nature 425, 798-804 (2003).

[25]

Nakhleh, L. Computational approaches to species phylogeny inference and gene tree reconciliation. Trends Ecol. Evol. 28, 719-728 (2013).

[26]

Som, A. Causes, consequences and solutions of phylogenetic incongruence. Brief. Bioinform. 16, 536-548 (2015).

[27]

Yang, L. et al. Next—generation sequencing, FISH mapping and synteny—based modeling reveal mechanisms of decreasing dysploidy in Cucumis. Plant J. 77, 16-30 (2014).

[28]

Weisenfeld, N. I. et al. Direct determination of diploid genome sequences. Genome Res. 27, 757-767 (2017).

[29]

Simão, F. A. et al. BUSCO: Assessing genome assembly and annotation completeness with single—copy orthologs. Bioinformatics 31, 3210-3212 (2015).

[30]

Wang, Y. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49 (2012).

[31]

Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).

[32]

Thornton, J. W. & DeSalle, R. Gene family evolution and homology: genomics meets phylogenetics. Annu. Rev. Genomics Hum. Genet. 1, 41-73 (2000).

[33]

Demuth, J. P. & Hahn, M. W. The life and death of gene families. BioEssays N. Rev. Mol. Cell. Dev. Biol. 31, 29-39 (2009).

[34]

Guo, Y.—L. Gene family evolution in green plants with emphasis on the origin and evolution of Arabidopsis thaliana genes. Plant J. Cell Mol. Biol. 73, 941-951 (2013).

[35]

Sahm, A. et al. PosiGene: automated and easy—to—use pipeline for genome—wide detection of positively selected genes. Nucleic Acids Res. 45, e100 (2017).

[36]

Kandoth, P. K. et al. The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates the expression of a large number of stress— and defense—related genes in degenerating feeding cells. Plant Physiol. 155, 1960-1975 (2011).

[37]

Jin, J. et al. Arabidopsis peroxidase AtPRX53 influences cell elongation and susceptibility to Heterodera schachtii. Plant Signal. Behav. 6, 1778-1786 (2011).

[38]

Dhar, N. et al. An Arabidopsis DISEASE RELATED NONSPECIFIC LIPID TRANSFER PROTEIN 1 is required for resistance against various phytopathogens and tolerance to salt stress. Gene 753, 144802 (2020).

[39]

Kourelis, J. & van der Hoorn, R. A. L. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30, 285-299 (2018).

[40]

Li, P. et al. RGAugury: a pipeline for genome—wide prediction of resistance gene analogs (RGAs) in plants. BMC Genomics 17, 852 (2016).

[41]

McHale, L. et al. Plant NBS—LRR proteins: adaptable guards. Genome Biol. 7, 212 (2006).

[42]

Marone, D. et al. Plant nucleotide binding site—leucine—rich repeat (NBS—LRR) genes: active guardians in host defense responses. Int. J. Mol. Sci. 14, 7302-7326 (2013).

[43]

Meyers, B. C. et al. Genome—wide analysis of NBS—LRR—encoding genes in Arabidopsis. Plant Cell 15, 809-834 (2003).

[44]

Monosi, B. et al. Full—genome analysis of resistance gene homologues in rice. Theor. Appl. Genet. Theor. Angew. Genet. 109, 1434-1447 (2004).

[45]

Leister, D. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet. 20, 116-122 (2004).

[46]

Singh, A. K. & Yadava, K. S. An analysis of interspecific hybrids and phylogenetic implications in Cucumis (Cucurbitaceae). Plant Syst. Evol. 147, 237-252 (1984).

[47]

Naranjo, T. The use of homoeologous pairing in the identification of homoeologous relationships in Triticeae. Hereditas 116, 219-223 (1992).

[48]

Rieseberg, L. H. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16, 351-358 (2001).

[49]

Meyer, R. S. & Purugganan, M. D. Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 840-852 (2013).

[50]

Zhao, G. et al. A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat. Genet. 51, 1607-1615 (2019).

[51]

Varshney, R. K. et al. Harvesting the promising fruits of genomics: applying genome sequencing technologies to crop breeding. PLOS Biol. 12, e1001883 (2014).

[52]

Crossa, J. et al. Genomic selection in plant breeding: methods, models, and perspectives. Trends Plant Sci. 22, 961-975 (2017).

[53]

Zhong, S. et al. High—throughput Illumina strand—specific RNA sequencing library preparation. Cold Spring Harb. Protoc. 2011, 940-949 (2011).

[54]

Liu, B. et al. Estimation of genomic characteristics by analyzing k—mer frequency in de novo genome projects. Preprint at https://arxiv.org/abs/1308.2012 (2020).

[55]

Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PloS One 9, e112963 (2014).

[56]

Chen, S. et al. fastp: an ultra—fast all—in—one FASTQ preprocessor. Bioinforma. Oxf. Engl. 34, i884-i890 (2018).

[57]

Zimin, A. V. et al. The MaSuRCA genome assembler. Bioinformatics 29, 2669-2677 (2013).

[58]

Koren, S. et al. Canu: scalable and accurate long—read assembly via adaptive k—mer weighting and repeat separation. Genome Res 27, 722-736 (2017).

[59]

English, A. C. et al. Mind the gap: upgrading genomes with Pacific Biosciences RS long—read sequencing technology. PloS One 7, e47768 (2012).

[60]

Boetzer, M. et al. Scaffolding pre—assembled contigs using SSPACE. Bioinforma. Oxf. Engl. 27, 578-579 (2011).

[61]

Leggett, R. M. et al. NextClip: an analysis and read preparation tool for Nextera Long Mate Pair libraries. Bioinformatics 30, 566-568 (2014).

[62]

Schuler, G. D. Sequence mapping by electronic PCR. Genome Res 7, 541-550 (1997).

[63]

Tang, H. et al. ALLMAPS: robust scaffold ordering based on multiple maps. Genome Biol. 16, 3 (2015).

[64]

Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows—Wheeler transform. Bioinforma. Oxf. Engl. 25, 1754-1760 (2009).

[65]

Kim, D. et al. Graph—based genome alignment and genotyping with HISAT2 and HISAT—genotype. Nat. Biotechnol. 37, 907-915 (2019).

[66]

Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA—seq reads. Nat. Biotechnol. 33, 290-295 (2015).

[67]

Majoros, W. H. et al. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene—finders. Bioinformatics 20, 2878-2879 (2004).

[68]

Hoff, K. J. & Stanke, M. Predicting genes in single genomes with AUGUSTUS. Curr. Protoc. Bioinforma. 65, e57 (2019).

[69]

Korf, I. Gene finding in novel genomes. BMC Bioinforma. 5, 59 (2004).

[70]

Birney, E. GeneWise and genomewise. Genome Res 14, 988-995 (2004).

[71]

Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVi—denceModeler and the program to assemble spliced alignments. Genome Biol. 9, R7 (2008).

[72]

Marçais, G. et al. MUMmer4: a fast and versatile genome alignment system. PLoS Comput. Biol. 14, e1005944 (2018).

[73]

Cock, P. J. A. et al. NCBI BLAST+ integrated into Galaxy. GigaScience 4, 39 (2015).

[74]

Zhang, Z. et al. ParaAT: a parallel tool for constructing multiple protein—coding DNA alignments. Biochem. Biophys. Res. Commun. 419, 779-781 (2012).

[75]

Zhang, Z. et al. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. GPB 4, 259-263 (2006).

[76]

De Bie, T. et al. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269-1271 (2006).

[77]

Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post—analysis of large phylogenies. Bioinformatics 30, 1312-1313 (2014).

[78]

Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).

[79]

Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).

[80]

Nguyen, L.—T. et al. IQ—TREE: a fast and effective stochastic algorithm for estimating maximum—likelihood phylogenies. Mol. Biol. Evol. 32, 268-274 (2015).

[81]

Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res. 47, W256-W259 (2019).

[82]

Wu, H. et al. A high—quality sponge gourd (Luffa cylindrica) genome. Hortic. Res. 7, 1-10 (2020).

[83]

Cui, J. et al. Whole—genome sequencing provides insights into the genetic diversity and domestication of bitter gourd (Momordica spp.). Hortic. Res. 7, 1-11 (2020).

[84]

Zhao, Q. et al. Oligo—painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis × hytivus with dysploid parental karyotypes. BMC Plant Biol. 19, 471 (2019).

[85]

Wang, Y. et al. Identification of all homoeologous chromosomes of newly synthetic allotetraploid Cucumis × hytivus and its wild parent reveals stable subgenome structure. Chromosoma 126, 713-728 (2017).

[86]

Bi, Y. et al. Flexible chromosome painting based on multiplex PCR of oligonucleotides and its application for comparative chromosome analyses in Cucumis. Plant J. 102, 178-186 (2020).

PDF (1490KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/