Construction of a high density SNP linkage map of kelp (Saccharina japonica) by sequencing Taq I site associated DNA and mapping of a sex determining locus

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Zhang, Ning ^a   Zhang, Linan ^b   Tao, Ye ^c   Guo, Li ^a   Sun, Juan ^b   Li, Xia ^b   Zhao, Nan ^b   Peng, Jie ^b   Li, Xiaojie ^b   Zeng, Liang ^c   Chen, Jinsa ^c   Yang, Guanpin ^a  

^a OCEAN UNIVERSITY OF CHINA   (China)

^b Shandong Oriental Ocean Sci tech Co Ltd   (China)

^c Majorbio Pharm Technology Co Ltd   (China)

Author keywords

Kelp; Linkage map; RAD; Saccharina japonica; Sex determining locus; SNP

Indexed keywords

GENOMIC DNA; MICROSATELLITE DNA; TCGA-SPECIFIC TYPE II DEOXYRIBONUCLEASES; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE;

ALLELE; ARTICLE; CLONE; DNA SEQUENCE; GAMETOPHYTE; GENE LOCUS; GENE MAPPING; GENETIC ANALYSIS; GENETIC DISTANCE; GENETIC LINKAGE; GENETIC VARIABILITY; GENOTYPE; HIGH THROUGHPUT SEQUENCING; KELP; MICROSATELLITE MARKER; NONHUMAN; RESTRICTION SITE; SEX CHROMOSOME; SEX DETERMINATION PROCESS; SEX DETERMINING LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; BINDING SITE; CHROMOSOME MAP; FLOWER; GENETICS; GENOTYPING TECHNIQUE; METABOLISM; QUANTITATIVE TRAIT LOCUS;

BRYOPHYTA; FILICOPHYTA; LAMINARIA JAPONICA; PHAEOPHYCEAE; VOLVOX;

BINDING SITES; CHROMOSOME MAPPING; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; GENETIC LINKAGE; GENOTYPING TECHNIQUES; GERM CELLS, PLANT; KELP; MICROSATELLITE REPEATS; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SEQUENCE ANALYSIS, DNA; SEX DETERMINATION PROCESSES;

EID: 84928252670     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1371-1     Document Type: Article

References (99)

1. Bartsch I, Wiencke C, Bischof K, Buchholz CM, Buck BH, Eggert A, et al. The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol. 2008;43:1-86.
2. Lane CE, Mayes C, Druehl LD, Saunders GW. A multi-gene molecular investigation of the kelp (Laminariales, Phaeophyceae) supports substantial taxonomic re-organization. J Phycol. 2006;42:493-512.
3. Li XJ, Liu JL, Cong YZ, Qu SC, Zhang ZZ, Dai HL, et al. Breeding and trial cultivation of Dongfang no.3, a hybrid of Laminaria gametophyte clones with a more than intraspecific less than interspecific relationship. Aquaculture. 2008;280:76-80.
4. Li XJ, Cong YZ, Yang GP, Shi YY, Qu SC, Li ZL, et al. Trait evaluation and trial cultivation of Dongfang no. 2, the hybrid of a male gametophyte clone of Laminaria longissima (Laminariales, Phaeophyta) and a female one of L. japonica. J Appl Phycol. 2007;19:139-51.
5. Zhang QS, Tang XX, Cong YZ, Qu SC, Luo SJ, Yang GP. Breeding of an elite Laminaria variety 90-1 through inter-specific gametophyte crossing. J Appl Phycol. 2007;19:303-11.
6. Kraan S. Mass-cultivation of carbohydrate rich macroalgae, a possible solution for sustainable biofuel production. Mitig Adapt Strat Glob Chang. 2013;18:27-46.
7. Wargacki AJ, Leonard E, Win MN, Regitsky DD, Santos CNS, Kim PB, et al. An engineered microbial platform for direct biofuel production from brown macroalgae. Science. 2012;335:308-13.
8. Takeda H, Yoneyama F, Kawai S, Hashimoto W, Murata K. Bioethanol production from marine biomass alginate by metabolically engineered bacteria. Energy Environ Sci. 2011;4:2575-81.
9. Gao K, McKinley KR. Use of macroalgae for marine biomass production and CO2 remediation: a review. J Appl Phycol. 1994;6:45-60.
10. Fang TC, Wu CY, Jiang BY, Li JJ, Ren GZ. The breeding of a new breed of Haidai (Laminaria japonica Aresch.) and its preliminary genetic analysis. Acta Botanica Sinica. 1962;10:197-209 (in Chinese with English abstract).
11. Roesijadi G, Jones SB, Snowden-Swan LJ, Zhu Y. Macroalgae as a biomass feedstock: a preliminary analysis, PNNL-19944. Richland, WA: Pacific Northwest National Laboratory; 2010.
12. Li J, Yuan L. Hybrid rice: genetics, breeding, and seed production. In: Janick J, editor. Plant breeding reviews. Volume 17. Oxford: John Wiley & Sons, Inc; 2010. p. 15-158.
13. Scoggan J, Zhuang Z, Wang F. Culture of Kelp (Laminaria japonica) in China, RAS/86/024. Qingdao, China: Yellow Sea Fisheries Research Institute; 1989. p. 1989.
14. Zhou Z, Li D, Wu C, Liu H. Laminaria gametophyte clone culture and its application in sporeling cultivation. Acta Oceanologica Sinica. 2000;19:89-95.
15. Zhang QS, Qu SC, Cong YZ, Luo SJ, Tang XX. High throughput culture and gametogenesis induction of Laminaria japonica gametophyte clones. J Appl Phycol. 2008;20:205-11.
16. Xu B, Zhang QS, Qu SC, Cong YZ, Tang XX. Introduction of a seedling production method using vegetative gametophytes to the commercial farming of Laminaria in China. J Appl Phycol. 2009;21:171-8.
17. Tseng CK, Sun KY, Wu CY. On the cultivation of Haitai (Laminaria japonica Aresch.) by summering young sporophytes at low temperature. Acta Botanica Sinica. 1955;4:255-64 (in Chinese with English abstract).
18. Forbord S, Skjermo J, Arff J, der Handå A, Reitan KI, Bjerregaard R, et al. Development of Saccharina latissima (Phaeophyceae) kelp hatcheries with year-round production of zoospores and juvenile sporophytes on culture ropes for kelp aquaculture. J Appl Phycol. 2012;24:393-9.
19. Pang S, Lüning K. Breaking seasonal limitation: year-round sporogenesis in the brown alga Laminaria saccharina by blocking the transport of putative sporulation inhibitors. Aquaculture. 2004;240:531-41.
20. Qin S, Jiang P, Tseng CK. Molecular biotechnology of marine algae in China. Hydrobiologia. 2004;512:21-6.
21. Zhou LR, Dai JX, Shen SD. An improved chromosome preparation from male gametophyte of Laminaria japonica (Heterokontophyta). Hydrobiologia. 2004;512:141-4.
22. Liu Y, Bi YH, Gu JG, Li LH, Zhou ZG. Localization of a female-specific marker on the chromosomes of the brown seaweed Saccharina japonica using fluorescence in situ hybridization. PLoS One. 2012;7:e48784.
23. Liu Y, Bi YH, Zhou ZG. Karyological observation on Saccharina japonica chromosomes stained with DAPI. J Fisheries China. 2012;36:50-4 (in Chinese with English abstracy).
24. Gu JG, Sun YP, Liu Y, Bi YH, Zhou ZG. Sex identification and genetic variation of Saccharina (Phaeophyta) gametophytes as revealed by inter-simple sequence repeat (ISSR) markers. J Appl Phycol. 2014;26:635-46.
25. Li J, Pang SJ, Liu F, Shan TF, Gao SQ. Spermatozoid life-span of two brown seaweeds, Saccharina japonica and Undaria pinnatifida, as measured by fertilization efficiency. Chinese J Oceanol Limnol. 2013;31:774-81.
26. Pang SJ, Jin ZH, Sun JZ, Gao SQ. Temperature tolerance of young sporophytes from two populations of Laminaria japonica revealed by chlorophyll fluorescence measurements and short-term growth and survival performances in tank culture. Aquaculture. 2007;262:493-503.
27. Ye S, Dhillon S, Ke X, Collins AR, Day IN. An efficient procedure for genotyping single nucleotide polymorphisms. Nucleic Acids Res. 2001;29:E88-8.
28. Drabovich AP, Krylov SN. Identification of base pairs in single-nucleotide polymorphisms by MutS protein-mediated capillary electrophoresis. Anal Chem. 2006;78:2035-8.
29. Li F, Niu B, Huang Y, Meng Z. Application of high-resolution DNA melting for genotyping in lepidopteran non-model species: Ostrinia furnacalis (Crambidae). PLoS One. 2012;7:e29664.
30. Tripathi N, Hoffmann M, Willing EM, Lanz C, Weigel D, Dreyere C. Genetic linkage map of the guppy, Poecilia reticulata, and quantitative trait loci analysis of male size and color variation. Proc R Soc B Biol Sci. 2009;276:2195-208.
31. Griffin TJ, Smith LM. Genetic identification by mass spectrometric analysis of single nucleotide polymorphisms: Ternary encoding of genotypes. Analytical Chemistr. 2000;72:3298-302.
32. Duan XR, Yue W, Liu LB, Li ZP, Li YL, He FC, et al. Single-nucleotide polymorphism (SNP) genotyping using cationic conjugated polymers in homogeneous solution. Nat Protoc. 2009;4:984-91.
33. Akond M, Liu S, Schoener L, Anderson JA, Kantartzi SK, Meksem K, et al. A SNP-based genetic linkage map of soybean using the SoyS-NP6K Illumina Infinium BeadChip Genotyping Array. J Plant Genome Sci. 2013;2013(1):80-9.
34. Raman H, Dalton-Morgan J, Diffey S, Raman R, Alamery S, Edwards D, et al. SNP markers-based map construction and genome-wides linkage analysis in Brassica napus. Plant Biotechnol J. 2014; doi: 10.1111/ pbi.12186.
35. Fu Y, Springer NM, Ying K, Yeh CT, Iniguez AL, Richmond T, et al. High-resolution genotyping via whole genome hybridizations to microarrays containing long oligonucleotide probes. PLoS One. 2010;5:e14178.
36. Miller MR, Atwood TS, Eames BF, Eberhart JK, Yan YL, Postlethwait JH, et al. RAD marker microarrays enable rapid mapping of zebrafish mutations. Genome Biol. 2007;8:R105.
37. Royo JL, Hidalgo M, Ruiz A. Pyrosequencing protocol using a universal biotinylated primer for mutation detection and SNP genotyping. Nat Protoc. 2007;2:1734-9.
38. Wang H, Elbein SC. Detection of allelic imbalance in gene expression using pyrosequencing. Methods Mol Biol. 2007;373:157-75.
39. Foley BR, Rose CG, Rundle DE, Leong W, Moy GW, Burton RS, et al. A gene-based SNP resource and linkage map for the copepod Tigriopus californicus. BMC Genomics. 2011;12:568.
40. Yamamoto K, Narukawa J, Kadono-Okuda K, Nohata J, Sasanuma M, Suetsugu Y, et al. Construction of a single nucleotide polymorphism linkage map for the silkworm, Bombyx mori, based on bacterial artificial chromosome end sequences. Genetics. 2006;173:151-61.
41. Hiremath PJ, Kumar A, Penmetsa RV, Farmer A, Schlueter JA, Chamarthi SK, et al. Large-scale development of cost-effective SNP marker assays for diversity assessment and genetic mapping in chickpea and comparative mapping in legumes. Plant Biotechnol J. 2012;10:716-32.
42. Bradley KM, Breyer JP, Melville DB, Broman KW, Knapik EW, Smith JR. An SNP-based linkage map for zebrafish reveals sex determination loci. Genes Genomes Genetics. 2011;1:3-9.
43. Hubert S, Higgins B, Borza T, Bowman S. Development of a SNP resource and a genetic linkage map for Atlantic cod (Gadus morhua). BMC Genomics. 2010;11:191.
44. Kenta S, Sachiko I, Hideki H, Erika A, Hiroyuki F, Daniel J, et al. SNP Discovery and linkage map construction in cultivated tomato. DNA Res. 2010;17:381-91.
45. Rashmi G, Sarwar A, Ganga J, Aamiir Waseem K, Shalu C, Mukesh J, et al. High-throughput SNP discovery and genotyping for constructing a saturated linkage map of chickpea (Cicer arietinum L.). DNA Res. 2012;19:357-73.
46. Shi YY, Sun LX, Huang ZY, Wu XB, Zhu YQ, Zheng HJ, et al. A SNP based high-density linkage map of Apis cerana reveals a high recombination rate similar to Apis mellifera. PLoS One. 2013;8:e76459.
47. Garvin MR, Saitoh K, Gharrett AJ. Application of single nucleotide polymorphisms to non-model species: A technical review. Mol Ecol Resour. 2010;10:915-34.
48. Altshuler D, Pollara VJ, Cowles CR, van Etten WJ, Baldwin J, Linton L, et al. An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature. 2000;407:513-6.
49. Willing EM, Hoffmann M, Klein JD, Weigel D, Dreyer C. Paired-end RAD-seq for de-novo assembly and marker design without available reference. Bioinformatics. 2011;27:2187-93.
50. Sánchez CC, Smith TPL, Wiedmann RT, Vallejo RL, Salem M, Yao JB, et al. Single nucleotide polymorphism discovery in rainbow trout by deep sequencing of a reduced representation library. BMC Genomics. 2009;10:559.
51. Miller MR, Dunham JP, Amores A, Cresko WA, Johnson EA. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res. 2007;17:240-8.
52. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One. 2008;3:e3376.
53. Baxter SW, Davey JW, Johnston JS, Shelton AM, Heckel DG, Jiggins CD, et al. Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism. PLoS One. 2011;6:e19315.
54. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One. 2012;7:e37135.
55. Gamble T, Zarkower D. Identification of sex-specific molecular markers using restriction site-associated DNA sequencing. Mol Ecol Resour. 2014;14:902-13.
56. Recknagel H, Elmer KR, Meyer A. A hybrid genetic linkage map of two ecologically and morphologically divergent midas cichlid fishes (Amphilophus spp.) obtained by massively parallel DNA sequencing (ddRADSeq). Genes Genomes Genetics. 2013;3:65-74.
57. Ma XF, Jensen E, Alexandrov N, Troukhan M, Zhang LP, Thomas-Jones S, et al. High resolution genetic mapping by genome sequencing reveals genome duplication and tetraploid genetic structure of the diploid Miscanthus sinensis. PLoS One. 2012;7:e33821.
58. Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH. Genome evolution and meiotic maps by massively parallel DNA sequencing: Spotted gar, an outgroup for the teleost genome duplication. Genetics. 2011;188:799-808.
59. O'Rourke SM, Yochem J, Connolly AA, Price MH, Carter L, Lowry JB, et al. Rapid mapping and identification of mutations in Caenorhabditis elegans by restriction site-associated DNA mapping and genomic interval pull-down sequencing. Genetics. 2011;189:767-78.
60. Anderson JL, Mari AR, Braasch I, Amores A, Hohenlohe P, Batzel P, et al. Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics. PLoS One. 2012;7:e40701.
61. Yu H, Xie W, Li J, Zhou F, Zhang Q. A whole-genome SNP array (RICE6K) for genomic breeding in rice. Plant Biotechnol J. 2014;12:28-37.
62. Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, et al. Characterization of polyploid wheat genomic diversity using a high-density 90 000 single nucleotide polymorphism array. Plant Biotechnol J. 2014;12:787-96.
63. Li F, Wang X, Liu J, Fu W, Duan D, Yang Y. Genetic mapping of the Laminaria japonica (Laminarales, Phaeophyta) using amplified fragments lengthpolymorphism markers. J Phycol. 2009;45:1228-33.
64. Yang G, Sun Y, Shi Y, Zhang L, Guo S, Li B, et al. Construction and characterization of a tentative amplified fragment length polymorphism-simple sequence repeat linkage map of Lamianria (Lamianrials, Phaeophyta). J Phycol. 2009;45:873-8.
65. Li Y, Yang Y, Liu J, Wang X, Gao T, Duan D. Genetic mapping of Laminaria japonica and L. longissima using amplified fragment length polymorphism markers in a "two-way pseudo-testcross" strategy. J Integr Plant Biol. 2007;49:392-400.
66. Zhang LN, Peng J, Li XJ, Liu YL, Cui CJ, Wu H, et al. Development of 27 trinucleotide microsatellite markers for Saccharina japonica using next generation sequencing technology. Conserv Genetics Resourc. 2014;6:341-4.
67. Liu F, Wang F, Duan D. EST-SSR markers derived from Laminaria digitata and its transferable application in Saccharina japonica. J Appl Phycol. 2012;24:501-5.
68. Liu F, Wang X, Yao J, Fu W, Duan D. Development of expressed sequence tag-derived microsatellite markers for Saccharina (Laminaria) japonica. J Appl Phycol. 2010;22:109-11.
69. Shi Y, Yang G, Liu Y, Liao M, Li X, Cong Y. Development of 18 polymorphic microsatellite DNA markers of Laminaria japonica (Phaeophyceae). Mol Ecol Notes. 2007;7:620-2.
70. Liu F, Shao Z, Zhang H, Liu J, Wang X, Duan D. QTL mapping for frond length and width in Laminaria japonica Aresch (Laminarales, Phaeophyta) using AFLP and SR. Marine Biotechnol. 2010;12:386-94.
71. Liu F, Yao J, Wang X, Repnikova A, Galanin DA, Duan D. Genetic diversity and structure within and between wild and cultivated Saccharina japonica (Laminariales, Phaeophyta) revealed by SSR markers. Aquaculture. 2012;358-359:139-45.
72. Li B, Shi Y, Yang G, Che S, Li X, Cong Y. Microsatellite DNA variation of the gametophyte clones isolated from introduced Laminaria japonica (Phaeophyta) and L. lonngissima of China and varieties derived from them. J Integr Plant Biol. 2008;50:352-9.
73. Li X, Yang G, Shi Y, Cong Y, Che S, Qu S, et al. Prediction of the heterosis of Laminaria hybrids with the genetic distance between their parental gametophyte clones. J Appl Phycol. 2008;20:1097-102.
74. Cock JM, Sterck L, Rouze P, Scornet D, Allen AE, Amoutzias G, et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature. 2010;465:617-21.
75. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH. Stacks: Building and genotyping loci de novo from short-read sequences. Genes Genomes Genetics. 2011;1:171-82.
76. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 2010;6:e1000862.
77. van Ooijen JW. Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Gen Res (Cambridge). 2011;93:343-9.
78. van Ooijen JW, Voorrips RE. JoinMap: software for the calculation of genetic linkage maps, version 3.0. Wageningen, The Netherlands: Plant Research International; 2001.
79. Voorrips RE. MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered. 2002;93:77-8.
80. Fishman L, Kelly AJ, Morgan E, Willis JH. A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics. 2001;159:1701-16.
81. Chakravarti A, Lasher LK, Reefer JE. A maximum likelihood method for estimating genome length using genetic linkage data. Genetics. 1991;128:175-82.
82. Zhang L, Yang G, Guo S, Wei Q, Zou G. Construction of a genetic linkage map for silver carp (Hypophthalmichthys molitrix). Anim Genet. 2010;41:523-30.
83. Zhou X, Xia Y, Ren X, Chen Y, Huang L, Huang S, et al. Construction of a SNP-based genetic linkage map in cultivated peanut based on large scale marker development using next-generation double digest restriction site associated DNA sequencing (ddRADseq). BMC Genomics. 2014;15:351.
84. Zhang J, Boualem A, Bendahmane A, Ming R. Genomics of sex determination. Curr Opin Plant Biol. 2014;18:110-6.
85. Houston P, Simon PJ, Broach JR. The Saccharomyces cerevisiae recombination enhancer biases recombination during interchromosomal mating-type switching but not in interchromosomal homologous recombination. Genetics. 2004;166:1187-97.
86. Aryal R, Ming R. Sex determination in flowering plants: Papaya as a model system. Plant Sci. 2014;217-218:56-62.
87. h chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci U S A. 2012;109:13710-5.
88. Gschwend AR, Yu Q, Tong EJ, Zeng F, Han J, VanBuren R, et al. Rapid divergence and expansion of the X chromosome in papaya. Proc Natl Acad Sci U S A. 2012;109:13716-21.
89. de Hoff PL, Ferris P, Olson BJSC, Miyagi A, Geng S, Umen JG. Species and population level molecular profiling reveals cryptic recombination and emergent asymmetry in the dimorphic mating locus of C. reinhardtii. PLoS Genet. 2013;9:e1003724.
90. Goodenough U, Lin H, Lee J-H. Sex determination in Chlamydomonas. Semin Cell Dev Biol. 2007;18:350-61.
91. Umen JG. Evolution of sex and mating loci: an expanded view from Volvocine algae. Curr Opin Microbiol. 2011;14:634-41.
92. Ferris P, Olson BJSC, de Hoff PL, Douglass S, Casero D, Prochnik S, et al. Evolution of an expanded sex-determining locus in Volvox. Science. 2010;238:351-4.
93. Telgmann-Rauber A, Jamsari A, Kinney MS, Pires JC, Jung C. Genetic and physical maps around the sex-determining M-locus of the dioecious plant asparagus. Molecular Genetics & Genomics. 2007;278:221-34.
94. Yamato KT, Ishizaki K, Fujisawa M, Okada S, Nakayama S, Fujishita M, et al. Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proc Natl Acad Sci U S A. 2007;104:6472-7.
95. McDaniel SF, Willis JH, Shaw AJ. A linkage map reveals a complex basis for segregation distortion in an interpopulation cross in the moss Ceratodon purpureus. Genetics. 2007;176:2489-500.
96. Frenkel J, Vyverman W, Pohnert G. Pheromone signaling during sexual reproduction in algae. Plant J. 2014;79:632-44.
97. Lane CE, Archibald JM. The eukaryotic tree of life: Endosymbiosis takes its TOL. Trends Ecol Evol. 2008;23:268-75.
98. Koonin EV. The incredible expanding ancestor of eukaryotes. Cell. 2010;140:606-8.
99. Ahmed S, Cock JM, Pessia E, Luthringer R, Cormier A, Robuchon M, et al. A haploid system of sex determination in the brown alga Ectocarpus sp. Curr Biol. 2014;24:1945-57.