Abstract
Luffa cylindrica L. is a cash crop which has important health, medicinal and industrial value, but no high saturation genetic map has been constructed owing to a lack of efficient markers. Furthermore, no genes were reportedly responsible for CMV resistance in Luffa spp. Specific length amplified fragment sequencing (SLAF-seq) is a valuable tool for large-scale discovery of markers and genetic mapping. The present study reported the construction of a high-density genetic map and the mapping of CMV resistant genes by using an F2 population of 130 individuals and their two inbred line parents. A total of 271.01 Mb pair-end reads were generated. 100,077 high-quality SLAFs were detected, and 7404 of them were polymorphic. Finally, 3701 of the polymorphic markers were selected for genetic map construction, and 13 linkage groups were generated. The map spanned 1518.56 cM with an average distance of 0.41 cM between adjacent markers. Based on the newly constructed high-density map, one gene located on chromosome 1 (100.072–100.457 cM) was identified to regulate CMV resistance in L. cylindrica. A gag-polypeptide of LTR copia-type retrotransposon was predicted as the candidate gene responsible for CMV resistance in L. cylindrica. The high-density genetic map and the CMV resistant gene mapped and predicted in this study will be useful in future research.
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included herein.
References
Oboh IO, Aluyor EO (2009) Luffa cylindrical-an emerging cash crop. Afr J Agric Res 4:684–688
Rabei S, Rizk RM, Khedr AHA (2013) Keys for and morphological character variation in some Egyptian cultivars of Cucurbitaceae. Genet Resour Crop Evol 60:1353–1364. https://doi.org/10.1007/s10722-012-9924-5
Prakash K, Pandey A, Radhamani J, Bisht IS (2013) Morphological variability in cultivated and wild species of Luffa (Cucurbitaceae) from India. Genet Resour Crop Evol 60:2319–2329. https://doi.org/10.1007/s10722-013-9999-7
Dairo FAS, Aye PA, Oluwasola TA (2007) Some functional properties of loofah gourd (Luffa cylindrical L., M. J. Roem) seed. J Food Agric Environ 5:97–101
Fernandes LCB, Cordeiro LAV, Soto-Blanco B (2010) Luffa acutangula Roxb. tea promotes developmental toxicity to rats. J Anim Vet Adv 9:1255–1258
Shang LH, Li CM, Yang ZY, Che DH, Cao JY, Yu Y (2012) Luffa echinata Roxb. induces human colon cancer cell (HT-29) death by triggering the mitochondrial apoptosis pathway. Molecules 17:5780–5794
Jamwal M, Sharma N (2015) Reproductive efficiency of two Luffa species-factors affecting low reproductive rate in meiotically stable Luffa acutangula (L.) Roxb. Nucleus 58:59–65
Papanicolaou GC, Psarra E, Anastasiou D (2015) Manufacturing and mechanical response optimization of epoxy resin/Luffa cylindrical composite. J Appl Polym Sci 132:41992. https://doi.org/10.1002/app.41992
Shahidi A, Jalilnejad N, Jalilnejad E (2015) A study on adsorption of cadmium(II) ions from aqueous solution using Luffa cylindrical. Desalin Water Treat 53:3570–3579
Cui J, Cheng J, Wang G, Tang X, Wu Z, Lin M, Li L, Hu K (2015) QTL analysis of three flower-related traits based on an interspecific genetic map of Luffa. Euphytica 202:45–54. https://doi.org/10.1007/s10681-014-1208-z
Wu H, He X, Gong H, Luo S, Li M, Chen J, Zhang C, Yu T, Huang W, Luo J (2016) Genetic linkage map construction and QTL analysis of two interspecific reproductive isolation traits in sponge gourd. Front Plant Sci 7:980. https://doi.org/10.3389/fpls.2016.00980
Zhang T, Ren X, Zhang Z, Ming Y, Yang Z, Hu J, Li S, Wang Y, Sun S, Sun K, Piao F, Sun Z (2020) Long-read sequencing and de novo assembly of the Luffa cylindrica (L.) Roem. genome. Mol Ecol Resour 20:511–519. https://doi.org/10.1111/1755-0998.13129
Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Jiang C, Guan N, Ma C, Zeng H, Xu C, Song J, Huang L, Wang C, Shi J, Wang R, Zheng X, Lu C, Wang X, Zheng H (2013) SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS ONE 8:e58700. https://doi.org/10.1371/journal.pone.0058700
Zhang Y, Wang L, Xin H, Li D, Ma C, Ding X, Hong W, Zhang X (2013) Construction of a high-density genetic map for sesame based on large scale marker development by specific length amplified fragment (SLAF) sequencing. BMC Plant Biol 13:141
Li B, Tian L, Zhang J, Huang L, Han F, Yan S, Wang L, Zheng H, Sun J (2014) Construction of a high-density genetic map based on large-scale markers developed by specific length amplified fragment sequencing (SLAF-seq) and its application to QTL analysis for isoflavone content in Glycine max. BMC Genomics 15:1086
Qi Z, Huang L, Zhu R, Xin D, Liu C, Han X, Jiang H, Hong W, Hu G, Zheng H, Chen Q (2014) A high-density genetic map for soybean based on specific length amplified fragment sequencing. PLoS ONE 9:104871
Zhang J, Zhang Q, Cheng T, Yang W, Pan H, Zhong J, Huang L, Liu E (2015) High-density genetic map construction and identification of a locus controlling weeping trait in an ornamental woody plant (Prunus mume Sieb. et Zucc). DNA Res 22:183–191. https://doi.org/10.1093/dnares/dsv003
Wei Q, Wang Y, Qin X, Zhang Y, Zhang Z, Wang J, Li J, Lou Q, Chen J (2014) An SNP-based saturated genetic map and QTL analysis of fruit-related traits in cucumber using specific-length amplified fragment (SLAF) Sequencing. BMC Genomics 15:1158. https://doi.org/10.1186/1471-2164-15-1158
Xu X, Xu R, Zhu B, Yu T, Qu W, Lu L, Xu Q, Qi X, Chen X (2015) A high-density genetic map of cucumber derived from specific length amplified fragment sequencing (SLAF-seq). Front Plant Sci 5:768. https://doi.org/10.3389/fpls.2014.00768
Jiang B, Liu W, Xie D, Peng Q, He X, Lin Y, Liang Z (2015) High-density genetic map construction and gene mapping of pericarp color in wax gourd using specific-locus amplified fragment (SLAF) sequencing. BMC Genomics 16:1035. https://doi.org/10.1186/s12864-015-2220-y
He Y, Yuan W, Dong M, Han Y, Shang F (2017) The first genetic map in sweet osmanthus (Osmanthus fragrans Lour.) using specific locus amplified fragment sequencing. Front Plant Sci 8:1621. https://doi.org/10.3389/fpls.2017.01621
Jacquemond M (2012) Chapter 13 - Cucumber mosaic virus. Adv Virus Res 84:439–504
Rani A, Jansirani P, Rabindran R (2017) Screening and identification of ridge gourd [Luffa acutangula (L.) Roxb] genotypes against Cucumber mosaic virus (CMV) tolerance. Int J Curr Microbiol App Sci 6:119–127. https://doi.org/10.20546/ijcmas.2017.603.013
Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018. https://doi.org/10.1073/pnas.81.24.8014
Munshi AD, Panda B, Mandal B, Bisht IS, Rao ES, Kumar R (2008) Genetics of resistance of cucumber mosaic virus in Cucumis sativus var. hardwickii R. Alef Euphytica 164:501–507. https://doi.org/10.1007/s10681-008-9741-2
Bos L (1982) Crop losses caused by viruses. Crop Prot 1:263–282
Yao M, Li N, Wang F, Ye Z (2013) Genetic analysis and identification of QTLs for resistance to cucumber mosaic virus in chili pepper (Capsicum annuum L.). Euphytica 193:135–145. https://doi.org/10.1007/s10681-013-0953-8
Kent WJ (2002) BLAT-the BLAST-like alignment tool. Genome Res 12:656–664. https://doi.org/10.1101/gr.229202
Liu D, Ma C, Hong W, Huang L, Liu M, Liu H, Zeng H, Deng D, Xin H, Song J, Xu C, Sun X, Hou X, Wang X (2014) Construction and analysis of high-density linkage map using high-throughput sequencing data. PLoS ONE 9:e98855. https://doi.org/10.1371/journal.pone.0098855
Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl. Springer, New York
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Maucelli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652
West MAL, van Leeuwen H, Kozik A, Kliebenstin DJ, Doerge RW, St Clair DA, Michelmore RW (2006) High-density haplotyping with microarray-based expression and single feature polymorphism markers in Arabidopsis. Genome Res 16:787–795. https://doi.org/10.1101/gr.5011206
Takahashi H, Miller J, Nozaki Y, Sukamto TM, Shah J, Hase S, Ikegami M, Ehara Y, Dinesh-Kumar SP (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J 32:655–667
Seo YS, Rojas MR, Lee JY, Lee SW, Jeon JS, Ronald P, Lucsa WJ (2006) Gilbertson RL. A viral resistance gene from common bean functions across plant families and is up-regulated in a non-virus-specific manner. PNAS 103:11856–11861
Kang WH, Hoang NH, Yang HB, Kwon JK, Jo SH, Seo JK, Kim KH, Choi D, Kang BC (2010) Molecular mapping and characterization of a single dominant gene controlling CMV resistance in peppers (Capsicum annuum L.). Theor Appl Genet 120:1587–1596. https://doi.org/10.1007/s00122-010-1278-9
Yoshii M, Nishikiori M, Tomita K, Yoshioka N, Kozuka R, Naito S, Ishikawa M (2004) The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J Virol 78:6102–6111
Caranta C, Pflieger S, Lefebvre V, Daubèze AM, Thabuis A, Palloix A (2002) QTLs involved in the restriction of cucumber mosaic virus (CMV) long-distance movement in pepper. Theor Appl Genet 104:586–591
Valkonen JPT, Watanabe KN (1999) Autonomous cell death, temperature sensitivity and the genetic control associated with resistance to cucumber mosaic virus (CMV) in diploid potatoes (Solanum spp). Theor Appl Genet 99:996–1005
Karchi Z, Cohen S, Govers A (1975) Inheritance of resistance to Cucumber Mosaic virus in melons. Phytopathology 65:479–481
Dogimont C, Leconte L, Périn C, Thabuis A, Lecoq H, Pitrat M (2000) Identification of QTLs contributing to resistance to different strains of cucumber mosaic cucumovirus in melon. Acta Hort 510:391–398
Guiu-Aragonés C, Monforte AJ, Saladié M, Corrêa RX, Garcia-Mas J, Martín-Hernández AM (2014) The complex resistance to cucumber mosaic cucumovirus (CMV) in the melon accession PI161375 is governed by one gene and at least two quantitative trait loci. Mol Breeding 34:351–362
Caranta C, Palloix A, Lefebvre V, Daubèze AM (1997) QTLs for a component of partial resistance to cucumber mosaic virus in pepper: restriction of virus installation in host-cells. Theor Appl Genet 94:431–438. https://doi.org/10.1007/s001220050433
Nono-Wondim R, Gebre-Selassie K, Palloix A, Pochard E, Marchoux G (1993) Study of multiplication of cucumber mosaic virus in susceptible and resistant Capsicum annuum lines. Ann Appl Biol 122:49–56
Dufour O, Palloix A, Gebre-Selassie K, Pochard E, Marchoux G (1989) The distribution of cucumber mosaic virus in resistant and susceptible plants of pepper. Can J Bot 67:655–660
Diaz-Pendon JA, Truniger V, Nieto C, Garcia-mas J, Bendahmane A, Aranda MA (2004) Advances in understanding recessive resistance to pant viruses. Mol Plant Pathol 5:223–233. https://doi.org/10.1111/j.1364-3703.2004.00223.x
Mazier M, Flamain F, Nicolaï M, Sarnette V, Caranta C (2011) Knockdown of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS ONE 6:e29595
Rodríguez-Hernández AM, Gosalvez B, Sempere RN, Burgos L, Aranda MA, Truniger V (2012) Melon RNA interference (RNAi) lines silenced for Cm-eIF4E show broad virus resistance. Mol Plant Pathol 13:755–763
Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17:1140–1153
Requena A, Simón-Buela L, Salcedo G, García-Arenal F (2006) Potential involvement of a cucumber homolog of phloem protein 1 in the long-distance movement of Cucumber mosaic virus particles. Mol Plant Microbe Interact 19:734–746
Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43:403–434
Moreau-mhiri C, Morel JB, Audeon C, Ferault M, Grandbastien MA, Lucas H (1996) Regulation of expression of the tobacco Tnt1 retrotransposon in heterologous species following pathogen-related stresses. Plant J 9:409–419
Acknowledgements
This study was funded by the National Natural Science Foundation of China (Grant No. 31501778). We thank Dr. Jeroen A. Berg for valuable suggestions during the preparation of the manuscript. We also acknowledge the reviewers for their constructive comments to improve the manuscript. We would give thanks to Biomarker Technologies Co., Ltd., Beijing for technical support in bioinformatics. Also we would like to thank Biomics (Beijing) Biotech Co. Ltd for providing technical support for the RNA-seq data. The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
Funding
This study was funded by the National Natural Science Foundation of China (Grant No. 31501778).
Author information
Authors and Affiliations
Contributions
LL designed, performed, analyses and drafted the experiments. With valuable suggestions by SX as well as technical assistance by LZ and LX. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary file1 (JPG 279 kb)
Number of SLAF markers in each of eight segregation patterns.
Supplementary file2 (JPG 140 kb)
Distribution of all mapped SNP markers on all individuals. The X-axes indicate individual F2 plants. The Y-axes indicate the distribution of all mapped markers.
Supplementary file3 (PDF 1796 kb)
Haplotype map of the genetic map. Green represents ʻP1-21ʼ, blue represent ʻP2-16ʼ, gray represents missing data, and red indicates heterozygosity. The two columns represent the genotype of an individual. Rows correspond to genetic markers.
Supplementary file4 (PDF 419 kb)
Heat map of the genetic map. Each cell represents the recombination rate of two markers. Yellow indicates a lower recombination rate and purple indicates a higher one.
Rights and permissions
About this article
Cite this article
Lou, L., Su, X., Liu, X. et al. Construction of a high-density genetic linkage map and identification of gene controlling resistance to cucumber mosaic virus in Luffa cylindrica (L.) Roem. based on specific length amplified fragment sequencing. Mol Biol Rep 47, 5831–5841 (2020). https://doi.org/10.1007/s11033-020-05652-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-020-05652-8