Construction of high-density genetic linkage map of Pyropia yezoensis (Bangiales, Rhodophyta) and identification of red color trait QTLs in the thalli

Abstract

Pyropia yezoensis is an important macroalga because of its extensive global distribution and economic importance. Color is an important trait in the thalli of P. yezoensis, it is also an effective marker to identify the hybridization in genetic breeding. In this study, a high-density genetic linkage map was constructed based on high-throughput single nucleotide polymorphism (SNP) markers, and used for analyzing the quantitative trait loci (QTLs) of red color trait in the thalli of P. yezoensis. The conchospore undergoes meiosis to develop into an ordered tetrad, and each cell has a haploid phenotype and can grow into a single individual. Based on this theory, F1 haploid population was used as the mapping population. The map included 531 SNP markers, 394.57 cM long on average distance of 0.74 cM. Collinear analysis of the genetic linkage map and the physical map indicated that the coverage between the two maps was 79.42%. Furthermore, QTL mapping identified six QTLs for the chromosomal regions associated with the red color trait of the thalli. The value of phenotypic variance explained (PVE) by an individual QTL ranged from 4.71%–63.11%. And QTL qRed-1-1, with a PVE of 63.11%, was considered the major QTL. Thus, these data may provide a platform for gene and QTL fine mapping, and marker-assisted breeding in P. yezoensis in the future.

This is a preview of subscription content, access via your institution.

References

  1. Brand A, Borovsky Y, Meir S, Rogachev I, Aharoni A, Paran I. 2012. pc8.1, a major QTL for pigment content in pepper fruit, is associated with variation in plastid compartment size. Planta, 235(3): 579–588, https://doi.org/10.1007/s00425-011-1530-9.

    Article  Google Scholar 

  2. Chai L G, Zhang J J, Lin G P, Wang Y, Xu F S. 2007. Construction of two DH populations and identification of chromosome ploidy in burley tobacco. Acta Tabacaria Sinica, 13(2): 33–37, https://doi.org/10.3321/j.issn:1004-5708.2007.02.007. (in Chinese with English abstract)

    Google Scholar 

  3. Cheema J, Dicks J. 2009. Computational approaches and software tools for genetic linkage map estimation in plants. Briefings in Bioinformatics, 10(6): 595–608, https://doi.org/10.1093/bib/bbp045.

    Article  Google Scholar 

  4. Chen J X, Zhou H, Gu Y, Xia D, Wu B, Gao G J, Zhang Q L, He Y Q. 2019. Mapping and verification of grain shape QTLs based on high-throughput SNP markers in rice. Molecular Breeding, 39(3): 42, https://doi.org/10.1007/s11032-019-0955-x.

    Article  Google Scholar 

  5. Cheng L R, Chen X C, Jiang C H, Ma B, Ren M, Cheng Y Z, Liu D, Geng R M, Yang A G. 2019. High-density SNP genetic linkage map construction and quantitative trait locus mapping for resistance to cucumber mosaic virus in tobacco (Nicotiana tabacum L.). The Crop Journal, 7(4): 539–547, https://doi.org/10.1016/j.cj.2018.11.010.

    Article  Google Scholar 

  6. Choi J K, Sa K J, Park D H, Lim S E, Ryu S H, Park J Y, Park K J, Rhee H I, Lee M, Lee J K. 2019. Construction of genetic linkage map and identification of QTLs related to agronomic traits in DH population of maize (Zea mays L.) using SSR markers. Genes & Genomics, 41(6): 667–678, https://doi.org/10.1007/s13258-019-00813-x.

    Article  Google Scholar 

  7. Danecek P, Auton A, Abecasis G, Albers C A, Banks E, DePristo M A, Handsaker R E, Lunter G, Marth G T, Sherry S T, McVean G, Durbin R, 1000 Genomes Project Analysis Group. 2011. The variant call format and VCFtools. Bioinformatics, 27(15): 2 156–2 158, https://doi.org/10.1093/bioinformatics/btr330.

    Article  Google Scholar 

  8. Davey J W, Hohenlohe P A, Etter P D, Boone J Q, Catchen J M, Blaxter M L. 2011. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Reviews Genetics, 12(7): 499–510, https://doi.org/10.1038/nrg3012.

    Article  Google Scholar 

  9. De Keyser E, Lootens P, Van Bockstaele E, De Riek J. 2013. Image analysis for QTL mapping of flower colour and leaf characteristics in pot azalea (Rhododendron simsii hybrids). Euphytica, 189(3): 445–460, https://doi.org/10.1007/s10681-012-0809-7.

    Article  Google Scholar 

  10. De Leon T B, Linscombe S, Subudhi P K. 2016. Molecular dissection of seedling salinity tolerance in rice (Oryza sativa L.) using a high-density GBS-based SNP linkage map. Rice, 9(1): 52, https://doi.org/10.1186/s12284-016-0125-2.

    Article  Google Scholar 

  11. Ding H C, Lv F, Wu H X, Yan X H. 2018. Selection and characterization of an improved strain produced by inter-species hybridization between Pyropia sp. from India and Pyropia haitanensis from China. Aquaculture, 491: 177–183, https://doi.org/10.1016/j.aquaculture.2018.03.015.

    Article  Google Scholar 

  12. Dirlewanger E, Cosson P, Howad W, Capdeville G, Bosselut N, Claverie M, Voisin R, Poizat C, Lafargue B, Baron O, Laigret F, Kleinhentz M, Arús P, Esmenjaud D. 2004. Microsatellite genetic linkage maps of myrobalan plum and an almond-peach hybrid—location of root-knot nematode resistance genes. Theoretical and Applied Genetics, 109(4): 827–838, https://doi.org/10.1007/s00122-004-1694-9.

    Article  Google Scholar 

  13. Fei X G, Wang S J, Lu S. 1998. Red Algae Cell Engineering Breeding and Seedling. Marine Biotechnology. Shandong Science and Technology Press, Jinan, China. p.7–26. (in Chinese)

    Google Scholar 

  14. Frett T J, Reighard G L, Okie W R, Gasic K. 2014. Mapping quantitative trait loci associated with blush in peach [Prunuspersica (L.) Batsch]. Tree Genetics & Genomes, 10(2): 367–381, https://doi.org/10.1007/s11295-013-0692-y.

    Article  Google Scholar 

  15. Ganal M W, Durstewitz G, Polley A, Bérard A, Buckler E S, Charcosset A, Clarke J D, Graner E M, Hansen M, Joets J, Le Paslier M C, McMullen M D, Montalent P, Rose M, Schön C C, Sun Q, Walter H, Martin O C, Falque M. 2011. A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS One, 6(12): e28334, https://doi.org/10.1371/journal.pone.0028334.

    Article  Google Scholar 

  16. He Y, Zhou W, Li J M, Shen S D. 2019. Study of mosaicism of Pyropia yezoensis. Marine Biology Research, 15(2): 150–158, https://doi.org/10.1080/17451000.2019.1605183.

    Article  Google Scholar 

  17. Heesch S, Cho G Y, Peters A F, Le Corguillé G, Falentin C, Boutet G, Coëdel S, Jubin C, Samson G, Corre E, Coelho S M, Cock J M. 2010. A sequence-tagged genetic map for the brown alga Ectocarpus siliculosus provides large-scale assembly of the genome sequence. New Phytologist, 188(1): 42–51, https://doi.org/10.1111/j.1469-8137.2010.03273.x.

    Article  Google Scholar 

  18. Hu Y M. 2006. The history and actuality of Porphyra’s breeding. Journal of Ningbo Institute of Education, 8(4): 22–26, https://doi.org/10.3969/j.issn.1009-2560.2006.04.007. (in Chinese with English abstract)

    Google Scholar 

  19. Huang L B, Yan X H. 2019. Construction of a genetic linkage map in Pyropia yezoensis (Bangiales, Rhodophyta) and QTL analysis of several economic traits of blades. PLoS One, 14(3): e0209128, https://doi.org/10.1371/journal.pone.0209128.

    Article  Google Scholar 

  20. Jiang H, Ding H C, Yan X H. 2018. Selection and characterization of an improved strain (A-18) by hybridization recombinant in Pyropia yezoensis (Bangiales, Rhodophyta). Acta Oceanologica Sinica, 40(2): 95–103, https://doi.org/10.3969/j.issn.0253-4193.2018.02.010. (in Chinese with English abstract)

    Google Scholar 

  21. Johnson R. 2003. Marker-assisted selection. In: Janick J ed. Plant Breeding Reviews. John Wiley & Sons, New York, p.293–309, https://doi.org/10.1002/9780470650240.ch13.

    Google Scholar 

  22. Kui L W, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie T K, Espley R V, Hellens R P, Allan A C. 2010. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biology, 10(1): 50, https://doi.org/10.1186/1471-2229-10-50.

    Article  Google Scholar 

  23. Kumawat G, Raje R S, Bhutani S, Pal J K, Mithra A S V C R, Gaikwad K, Sharma T R, Singh N K. 2012. Molecular mapping of QTLs for plant type and earliness traits in pigeonpea (Cajanus cajan L. Millsp.). BMC Genetics, 13(1): 84, https://doi.org/10.1186/1471-2156-13-84.

    Article  Google Scholar 

  24. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14): 1 754–1 760, https://doi.org/10.1093/bioinformatics/btp324.

    Article  Google Scholar 

  25. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics, 25(16): 2 078–2 079, https://doi.org/10.1093/bioinformatics/btp352.

    Article  Google Scholar 

  26. Li H, Hearne S, Bänziger M, Li Z, Wang J. 2010. Statistical properties of QTL linkage mapping in biparental genetic populations. Heredity, 105(3): 257–267, https://doi.org/10.1038/hdy.2010.56.

    Article  Google Scholar 

  27. Liu J, Shikano T, Leinonen T, Cano J M, Li M H, Merilä J. 2014. Identification of major and minor QTL for ecologically important morphological traits in three-spined sticklebacks (Gasterosteus aculeatus). Genes, Genomes, Genetics, 4(4): 595–604, https://doi.org/10.1534/g3.114.010389.

    Google Scholar 

  28. Liu K Y, Xu H, Liu G, Guan P F, Zhou X Y, Peng H R, Yao Y Y, Ni Z F, Sun Q X, Du J K. 2018. QTL mapping of flag leaf-related traits in wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 131(4): 839–849, https://doi.org/10.1007/s00122-017-3040-z.

    Article  Google Scholar 

  29. Liu M J, Huang L B, Yan X H. 2015. Isolation and characterization of the improved strain HW-4 by intraspecific hybridization in Pyropia yezoensis. Journal of Fishery Sciences of China, 22(1): 33–43, https://doi.org/10.3724/SP.J.1118.2015.00213. (in Chinese with English abstract)

    Google Scholar 

  30. Lowry D B, Taylor S H, Bonnette J, Aspinwall M J, Asmus A L, Keitt T H, Tobias C M, Juenger T E. 2015. QTLs for biomass and developmental traits in Switchgrass (Panicum virgatum). Bioenergy Research, 8(4): 1 856–1 867, https://doi.org/10.1007/s12155-015-9629-7.

    Article  Google Scholar 

  31. Ma L L, Guan Z R, Zhang Z T, Zhang X X, Zhang Y L, Zou C Y, Peng H W, Pan G T, Lee M, Shen Y O, Lübberstedt T. 2018. Identification of quantitative trait loci for leaf-related traits in an IBM Syn10 DH maize population across three environments. Plant Breeding, 137(2): 127–138, https://doi.org/10.1111/pbr.12566.

    Article  Google Scholar 

  32. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo M A. 2010. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20(9): 1 297–1 303, https://doi.org/10.1101/gr.107524.110.

    Article  Google Scholar 

  33. Migita S. 1967. Cytological studies on Porphyra yezoensis Ueda. Nagasaki University Bulletin of the Faculty of Fisheries, 24: 55–64, http://naosite.lb.nagasaki-u.ac.jp/dspace/handle/10069/31358.

    Google Scholar 

  34. Miura A, Shin J A. 1989. Crossbreeding in cultivars of Porphyra yezoensis (Bangiales, Rhodophyta)-Preliminary report. The Korean Journal of Phycology, 4(2): 207–211, https://link.springer.com/article/10.1023%2FA:1022998823920.

    Google Scholar 

  35. Mo H D. 2003. Look back and reflect on genetic researches of variation for quantitative traits: a challenge for quantitative genetics in post-genome ear. Journal of Yangzhou University (Agricultural and Life Sciences Edition), 24(2): 24–31. (in Chinese with English abstract)

    Google Scholar 

  36. Moose S P, Mumm R H. 2008. Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiology, 147(3): 969–977, https://doi.org/10.1104/pp.108.118232.

    Article  Google Scholar 

  37. Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, Satomi M, Fukuma Y, Shiwaku K, Tsujimoto A, Kobayashi T, Nakayama I, Ito F, Nakajima K, Sano M, Wada T, Kuhara S, Inouye K, Gojobori T, Ikeo K. 2013. The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS One, 8(3): e57122, https://doi.org/10.1371/journal.pone.0057122.

    Article  Google Scholar 

  38. Niwa K, Yamamoto T, Furuita H, Abe T. 2011. Mutation breeding in the marine crop Porphyra yezoensis (Bangiales, Rhodophyta): cultivation experiment of the artificial red mutant isolated by heavy-ion beam mutagenesis. Aquaculture, 314(1–4): 182–187, https://doi.org/10.1016/j.aquaculture.2011.02.007.

    Article  Google Scholar 

  39. Niwa K. 2010. Genetic analysis of artificial green and red mutants of Porphyra yezoensis Ueda (Bangiales, Rhodophyta). Aquaculture, 308(1–2): 6–12, https://doi.org/10.1016/j.aquaculture.2010.08.007.

    Article  Google Scholar 

  40. Ohme M, Kunifuji Y, Miura A. 1986. Cross experiments of the color mutants in Porphyra yezoensis Ueda. Journal of Applied Phycology, 34: 101–106, https://www.oalib.com/references/10851746.

    Google Scholar 

  41. Ohme M, Miura A. 1988. Tetrad analysis in conchospore germlings of Porphyra yezoensis (Rhodophyta, Bangiales). Plant Science, 57(2): 135–140, https://doi.org/10.1016/0168-9452(88)90079-9.

    Article  Google Scholar 

  42. Qing D J, Dai G X, Zhou W Y, Huang S S, Liang H F, Gao L J, Gao J, Huang J, Zhou M, Chen R T, Chen W W, Huang F K, Deng G F. 2019. Development of molecular marker and introgression of Bph3 into elite rice cultivars by marker-assisted selection. Breeding Science, 69(1): 40–46, https://doi.org/10.1270/jsbbs.18080.

    Article  Google Scholar 

  43. Randhawa M S, Bains N S, Sohu V S, Chhuneja P, Trethowan R M, Bariana H S, Bansal U. 2019. Marker assisted transfer of stripe rust and stem rust resistance genes into four wheat cultivars. Agronomy, 9(9): 497, https://doi.org/10.3390/agronomy9090497.

    Article  Google Scholar 

  44. Ribaut J M, De Vicente M C, Delannay X. 2010. Molecular breeding in developing countries: challenges and perspectives. Current Opinion in Plant Biology, 13(2): 213–218, https://doi.org/10.1016/j.pbi.2009.12.011.

    Article  Google Scholar 

  45. Shan T F, Pang S J, Li J, Li X, Su L. 2015. Construction of a high-density genetic map and mapping of a sex-linked locus for the brown alga Undaria pinnatifida (Phaeophyceae) based on large scale marker development by specific length amplified fragment (SLAF) sequencing. BMC Genomics, 16(1): 902, https://doi.org/10.1186/s12864-015-2184-y.

    Article  Google Scholar 

  46. Shen Y S, Yang Y, Xu E S, Ge X H, Xiang Y, Li Z Y. 2018. Novel and major QTL for branch angle detected by using DH population from an exotic introgression in rapeseed (Brassica napus L.). Theoretical and Applied Genetics, 131(1): 67–78, https://doi.org/10.1007/s00122-017-2986-1.

    Article  Google Scholar 

  47. Sitonik C A, Suresh L M, Beyene Y, Olsen M S, Makumbi D, Oliver K, Das B, Bright J M, Mugo S, Crossa J, Tarekegne A, Prasanna B M, Gowda M. 2019. Genetic architecture of maize chlorotic mottle virus and maize lethal necrosis through GWAS, linkage analysis and genomic prediction in tropical maize germplasm. Theoretical and Applied Genetics, 132(8): 2 381–2 399, https://doi.org/10.1007/s00122-019-03360-x.

    Article  Google Scholar 

  48. Sooriyapathirana S S, Khan A, Sebolt A M, Wang D C, Bushakra J M, Kui L W, Allan A C, Gardiner S E, Chagné D, Iezzoni A F. 2010. QTL analysis and candidate gene mapping for skin and flesh color in sweet cherry fruit (Prunus avium L.). Tree Genetics & Genomes, 6(6): 821–832, https://doi.org/10.1007/s11295-010-0294-x.

    Article  Google Scholar 

  49. Sun X W, Liu D Y, Zhang X F, Li W B, Liu H, Hong W G, Jiang C B, Guan N, Ma C X, Zeng H P, Xu C H, Song J, Huang L, Wang C M, Shi J J, Wang R, Zheng X H, Lu C Y, Wang X W, Zheng H K. 2013. SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One, 8(3): e58700, https://doi.org/10.1371/journal.pone.0058700.

    Article  Google Scholar 

  50. Sutherland J E, Lindstrom S C, Nelson W A, Brodie J, Lynch M D J, Hwang M S, Choi H G, Miyata M, Kikuchi N, Oliveira M C, Farr T, Neefus C, Mols-Mortensen A, Milstein D, Müller K M. 2011. A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). Journal of Phycology, 47(5): 1 131–1 151, https://doi.org/10.1111/j.1529-8817.2011.01052.x.

    Article  Google Scholar 

  51. Tao Y F, Liu Q C, Wang H H, Zhang Y J, Huang X Y, Wang B B, Lai J S, Ye J R, Liu B S, Xu M L. 2013. Identification and fine-mapping of a QTL, qMrdd1, that confers recessive resistance to maize rough dwarf disease. BMC Plant Biology, 13(1): 145, https://doi.org/10.1186/1471-2229-13-145.

    Article  Google Scholar 

  52. Van Ooijen J W, Kyazma B V. 2009. MapQTL 6: Software for the Mapping of Quantitative Trait Loci in Experimental Populations of Diploid Species. Kyazma BV, Wageningen, Netherlands.

    Google Scholar 

  53. Wang B B, Liu H, Liu Z P, Dong X M, Guo J J, Li W, Chen J, Gao C, Zhu Y B, Zheng X M, Chen Z L, Chen J, Song W B, Hauck A, Lai J S. 2018a. Identification of minor effect QTLs for plant architecture related traits using super high density genotyping and large recombinant inbred population in maize (Zea mays). BMC Plant Biology, 18(1): 17, https://doi.org/10.1186/s12870-018-1233-5.

    Article  Google Scholar 

  54. Wang C N, Qiao A H, Fang X F, Sun L, Gao P, Davis A R, Liu S, Luan F S. 2019. Fine mapping of lycopene content and flesh color related gene and development of molecular marker-assisted selection for flesh color in watermelon (Citrullus lanatus). Frontiers in Plant Science, 10: 1 240, https://doi.org/10.3389/fpls.2019.01240.

    Article  Google Scholar 

  55. Wang S J, Zheng Y Z, Ma L B, Xu P, Zhu J Y. 2000. Gamma-rays induction of mutation in conchocelis of Porphyra yezoensis. Chinese Journal of Oceanology and Limnology, 18(1): 47, https://doi.org/10.1007/BF02842541.

    Article  Google Scholar 

  56. Wang S, Basten C, Zeng Z. 2007. Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC.

    Google Scholar 

  57. Wang X L, Chen Z H, Li Q Y, Zhang J, Liu S, Duan D L. 2018b. High-density SNP-based QTL mapping and candidate gene screening for yield-related blade length and width in Saccharina japonica (Laminariales, Phaeophyta). Scientific Reports, 8(1): 13 591, https://doi.org/10.1038/s41598-018-32015-y.

    Article  Google Scholar 

  58. Xu D H, Sun R F, Zhang Y G, Yuan Y X, Kang J G, Wu J, Zhang H, Song X F, Li X N, Song Y M, Wang X W. 2007. Mapping and analysis of QTL related to leaf color in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Acta Horticulturae Sinica, 34(1): 99–104, https://doi.org/10.3321/j.issn:0513-353X.2007.01.020. (in Chinese with English abstract)

    Google Scholar 

  59. Xu K P, Yu X Z, Tang X H, Kong F N, Mao Y X. 2019. Organellar genome variation and genetic diversity of Chinese Pyropia yezoensis. Frontiers in Marine Science, 6: 756, https://doi.org/10.3389/fmars.2019.00756.

    Article  Google Scholar 

  60. Xu Y, Huang L, Ji D H, Chen C S, Zheng H K, Xie C T. 2015. Construction of a dense genetic linkage map and mapping quantitative trait loci for economic traits of a doubled haploid population of Pyropia haitanensis (Bangiales, Rhodophyta). BMC Plant Biology, 15(1): 228, https://doi.org/10.1186/s12870-015-0604-4.

    Article  Google Scholar 

  61. Yabu H, Tokida J. 1963. Mitosis in Porphyra. Hokkaido University Bulletin of the Faculty of Fisheries, 14(3): 131–136, https://eprints.lib.hokudai.ac.jp/dspace/bitstream/2115/23185/1/14(3)_P131-136.pdf.

    Google Scholar 

  62. Yabu H. 1969. Observation on chromosomes in some species of Porphyra. Hokkaido University Bulletin of the Faculty of Fisheries, 19(4): 239–243, https://link.springer.com/article/10.1007/s10811-007-9235-y.

    Google Scholar 

  63. Yan X H, Aruga Y 2000. Genetic analysis of artificial pigmentation mutants in Porphyra yezoensis Ueda (Bangiales, Rhodophyta). Phycological Research, 48(3): 177–187, https://doi.org/10.1046/j.1440-1835.2000.00203.x.

    Article  Google Scholar 

  64. Yan X H, Fujita Y, Aruga Y. 2000. Induction and characterization of pigmentation mutants in Porphyra yezoensis (Bangiales, Rhodophyta). Journal of Applied Phycology, 12(1): 69–81, https://doi.org/10.1023/A:1008129119065.

    Article  Google Scholar 

  65. Yan X H, Fujita Y, Aruga Y. 2004. High monospore-producing mutants obtained by treatment with MNNG in Porphyra yezoensis Ueda (Bangiales, Rhodophyta). Hydrobiologia, 512(1–3): 133–140, https://doi.org/10.1023/B:Hydr.0000020318.00749.2d.

    Article  Google Scholar 

  66. Yan X H, Liang Z Q, Song W L, Huang J, Ma P, Aruga Y 2005. Induction and isolation of artificial pigmentation mutants in Porphyra haitanensis Chang et Zheng (Bangiales, Rhodophyta). Journal of Fisheries of China, 29(2): 166–172, https://doi.org/10.3321/j.issn:1000-0615.2005.02.005. (in Chinese with English abstract)

    Google Scholar 

  67. Yang G P, Sun Y, Shi Y Y, Zhang L N, Guo S S, Li B J, Li X J, Li Z L, Cong Y Z, Zhao Y S, Wang W Q. 2009. Construction and characterization of a tentative amplified fragment length polymorphism-simple sequence repeat linkage map of Laminaria (Laminariales, Phaeophyta). Journal of Phycology, 45(4): 873–878, https://doi.org/10.1111/j.1529-8817.2009.00720.x.

    Article  Google Scholar 

  68. Yu Y, Zhang X J, Li F H, Xiang J H. 2011. Strategy of whole genomic selection breeding and its application prospect in aquaculture. Journal of Fishery Sciences of China, 18(4): 936–943, https://doi.org/10.3724/SP.J.1118.2011.00935. (in Chinese with English abstract)

    Article  Google Scholar 

  69. Zeng Z B. 1994. Precision mapping of quantitative trait loci. Genetics, 136(4): 1 457–1 468.

    Article  Google Scholar 

  70. Zhang W J, Lukaszewski A J, Kolmer J, Soria M A, Goyal S, Dubcovsky J. 2005. Molecular characterization of durum and common wheat recombinant lines carrying leaf rust resistance (Lr19) and yellow pigment (Y) genes from Lophopyrum ponticum. Theoretical and Applied Genetics, 111(3): 573–582, https://doi.org/10.1007/s00122-005-2048-y.

    Article  Google Scholar 

  71. Zhu H Q, Zhang X G, Xue Q Z. 2004. Developing practicable system of chromosomal doubling for the construction of doubled haploid population in tobacco. Molecular Plant Breeding, 2(5): 643–648, https://doi.org/10.3969/j.issn.1672-416X.2004.05.007. (in Chinese with English abstract)

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Fanna Kong or Yunxiang Mao.

Additional information

Supported by the National Natural Science Foundation of China (Nos. 41976146, 31672641), the Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (No. 2018SDKJ0302-4), the National Key R&D Program of China (No. 2018YFD0900106), and the Shandong Province Key Research and Development Program (No. 2019GHY112008)

Data Availability Statement

The data generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Xu, K., Tang, X. et al. Construction of high-density genetic linkage map of Pyropia yezoensis (Bangiales, Rhodophyta) and identification of red color trait QTLs in the thalli. J. Ocean. Limnol. (2021). https://doi.org/10.1007/s00343-020-0184-5

Download citation

Keyword

  • Pyropia yezoensis
  • high-density genetic linkage map
  • quantitative trait loci (QTL) mapping
  • F1 haploid population
  • red pigment variant