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Journal of Applied Phycology

, Volume 30, Issue 6, pp 3435–3443 | Cite as

Comparative genomics and systematics of Betaphycus, Eucheuma, and Kappaphycus (Solieriaceae: Rhodophyta) based on mitochondrial genome

  • Yue Li
  • Na Liu
  • Xumin Wang
  • Xianming Tang
  • Lei Zhang
  • Maria Dyah Nur Meinita
  • Guoliang Wang
  • Hongxin Yin
  • Yuemei Jin
  • Haiyang Wang
  • Cui Liu
  • Shan ChiEmail author
  • Tao LiuEmail author
  • Jing ZhangEmail author
8th Asian Pacific Phycological Forum

Abstract

Betaphycus Doty, Eucheuma J. Agardh, and Kappaphycus Doty (Solieriaceae, Gigartinales) are the three most commercially important seaweed genera that produce carrageenan. In the present study we provide mitogenomes of Betaphycus gelatinus, Eucheuma denticulatum and Kappaphycus alvarezii. The mitogenomes of these three species contain a set of 50 genes, including 24 protein-coding genes, 2 rRNA genes, and 24 tRNA genes. The mitogenome length ranges from 25,198 bp (Kappaphycus alvarezii) to 25,327 bp (Eucheuma denticulatum). As compared with the previous published mitogenomes of Florideophyceae species, only the species in Gelidiaceae and Pterocladiaceae have smaller mitochondrial genome size than these reported here. At the junction of two transcription units, we identified a stem-loop structure in six representative Gigartinales species, which is presumed to play an important role in the replication and transcription of mitochondrial genes. In Gigartinales the difference in gene order among the four Solieriaceae (B. gelatinus, E. denticulatum, K. alvarezii, K. striatus) and other two Gigartinales species (Chondrus crispus and Mastocarpus papillatus) can be explained by inversion of two tRNA genes. Collinearity analysis of the 12 mitochondrial genomes of Florideophyceae showed considerable sequence synteny across all the species compared, with the exception of a highly variable region between atp6 and rpl20 genes. Phylogenetic analyses based on 21 shared mitochondrial genes showed that the four Solieriaceae species form one clade (Solieriaceae clade). Within this clade, B. gelatinae is basal relative to the other three species. The genus Kappaphycus is more closely related to Eucheuma than Betaphycus.

Keywords

Collinearity analysis Mitochondrial genome Phylogenetic analyses Solieriaceae Stem-loop 

Notes

Funding

This work was supported by the China-ASEAN Maritime Cooperation Fund, by Public Science and Technology Research Funds Projects of Ocean (Grant No. 201405020), and by the Fundamental Research Funds for the Central Universities.

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References

  1. Bixler HJ (1996) Recent developments in manufacturing and marketing carrageenan. Hydrobiologia 326:35–57CrossRefGoogle Scholar
  2. Bonen L (1998) Mitochondrial genomes. Adv Genome Biol 5:415–461CrossRefGoogle Scholar
  3. Boo GH, Hughey JR, Miller KA, Boo SM (2016) Mitogenomes from type specimens, a genotyping tool for morphologically simple species: ten genomes of agar-producing red algae. Sci Rep 6:35337CrossRefGoogle Scholar
  4. Boore JL, Brown WM (1998) Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev 8:668–674CrossRefGoogle Scholar
  5. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716CrossRefGoogle Scholar
  6. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552CrossRefGoogle Scholar
  7. Clayton DA (1982) Replication of animal mitochondrial DNA. Cell 28:693–705CrossRefGoogle Scholar
  8. Conklin KY, Kurihara A, Sherwood AR (2009) A molecular method for identification of the morphologically plastic invasive algal genera Eucheuma and Kappaphycus (Rhodophyta, Gigartinales) in Hawaii. J Appl Phycol 21:691–699CrossRefGoogle Scholar
  9. Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14(7):1394–1403CrossRefGoogle Scholar
  10. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165CrossRefGoogle Scholar
  11. Dierckxsens N, Mardulyn P, Smits G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45:e18CrossRefGoogle Scholar
  12. Doty MS, Norris JN (1985) Eucheuma species (Solieriaceae, Rhodophyta) that are major sources of carrageenan. In: Abbott IA (ed) Taxonomy of economic seaweeds. California Sea Grant College Program, La Jolla, pp 47–61Google Scholar
  13. Dumilag RV, Liao LM, Lluisma AO (2014) Phylogeny of Betaphycus (Gigartinales, Rhodophyta) as inferred from COI sequences and morphological observations on B. philippinensis. J Appl Phycol 26:587–595CrossRefGoogle Scholar
  14. Fredericq S, Freshwater DW, Hommersand MH (1999) Observations on the phylogenetic systematics and biogeography of the Solieriaceae (Gigartinales, Rhodophyta) inferred from rbcL sequences and morphological evidence. Hydrobiologia 398:25–38CrossRefGoogle Scholar
  15. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT; Nucl Acids Symp Ser 41:95–98Google Scholar
  16. Heather JM, Chain B (2016) The sequence of sequencers: the history of sequencing DNA. Genomics 107:1–8CrossRefGoogle Scholar
  17. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefGoogle Scholar
  18. Leblanc C, Boyen C, Richard O, Bonnard G, Grienenberger JM, Kloareg B (1995) Complete sequence of the mitochondrial DNA of the rhodophyte Chondrus crispus (Gigartinales). Gene content and genome organization. J Mol Biol 250:484–495CrossRefGoogle Scholar
  19. Lim PE, Yang LE, Tan J, Meggs CA, Brodie J (2017) Advancing the taxonomy of economically important red seaweeds (Rhodophyta). Eur J Phycol 52:438–451CrossRefGoogle Scholar
  20. Lohse M, Drechsel O, Bock R (2007) OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 52:267–274CrossRefGoogle Scholar
  21. Ma PF, Zhang YX, Zeng CX, Guo ZH, Li DZ (2014) Chloroplast phylogenomic analyses resolve deep-level relationships of an intractable bamboo tribe Arundinarieae (Poaceae). Syst Biol 63:933–950CrossRefGoogle Scholar
  22. Martin WF, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41CrossRefGoogle Scholar
  23. Ng PK, Lin SM, Lim PE, Liu LC, Chen CM, Pai TW (2017) Complete chloroplast genome of Gracilaria firma (Gracilariaceae, Rhodophyta), with discussion on the use of chloroplast phylogenomics in the subclass Rhodymeniophycidae. BMC Genomics 18:40CrossRefGoogle Scholar
  24. Pereira L, Meireles F, Abreu HT, Ribeiro-Claro PJA (2015) A comparative analysis of carrageenans produced by underutilized versus industrially utilized macroalgae (Gigartinales, Rhodophyta). In: Kim S-K, Chojnacka K (eds) Marine algae extracts: processes, products, and applications. Wiley-VCH, Weinheim, pp 277–294Google Scholar
  25. Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:686–689CrossRefGoogle Scholar
  26. Sissini MN, Navarrete-Fernández TM, Murray EMC, Freese JM, Gentilhomme AS, Huber SR, Mumford TF, Hughey JR (2016) Mitochondrial and plastid genome analysis of the heteromorphic red alga Mastocarpus papillatus (C. Agardh) Kützing (Phyllophoraceae, Rhodophyta) reveals two characteristic florideophyte organellar genomes. Mitochondrial DNA B 1:676–677CrossRefGoogle Scholar
  27. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedPubMedCentralGoogle Scholar
  28. Sun YY, Luo D, Zhao C, Li W, Liu T (2011) DNA extraction and PCR analysis of five kinds of large seaweed under different preservation conditions. Mol Plant Breed 9:1680–1691Google Scholar
  29. Taanman JW (1999) The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta 1410:103–123CrossRefGoogle Scholar
  30. Tablizo FA, Lluisma AO (2014) The mitochondrial genome of the red alga Kappaphycus striatus (“Green Sacol” variety): complete nucleotide sequence, genome structure and organization, and comparative analysis. Mar Genomics 18:155–161CrossRefGoogle Scholar
  31. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  32. Tan J, Lim P-E, Phang S-M (2013) Phylogenetic relationship of Kappaphycus Doty and Eucheuma J. Agardh (Solieriaceae, Rhodophyta) in Malaysia. J Appl Phycol 25:13–29CrossRefGoogle Scholar
  33. Tirtawijaya G, Mohibbullah M, Meinita MDN, Moon IS, Hong Y-K (2016) The ethanol extract of the rhodophyte Kappaphycus alvarezii promotes neurite outgrowth in hippocampal neurons. J Appl Phycol 28:2515–2522CrossRefGoogle Scholar
  34. Vellai T, Takacs K, Vida G (1998) A new aspect to the origin and evolution of eukaryotes. J Mol Evol 46:499–507CrossRefGoogle Scholar
  35. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591CrossRefGoogle Scholar
  36. Yang EC, Kim KM, Kim SY, Lee J, Boo GH, Lee J-H, Nelson WA, Yi G, Schmidt WE, Fredericq S, Boo SM, Bhattacharya D, Yoon HS (2015) Highly conserved mitochondrial genomes among multicellular red algae of the Florideophyceae. Genome Biol Evol 7:2394–2406CrossRefGoogle Scholar
  37. Zhang L, Wang X, Qian H, Chi S, Liu C, Lui T (2012) Complete sequences of the mitochondrial DNA of the wild Gracilariopsis lemaneiformis and two mutagenic cultivated breeds (Gracilariaceae, Rhodophyta). PLoS One 7(6):e40241CrossRefGoogle Scholar
  38. Zuccarello GC, Critchley AT, Smith J, Sieber V, Lhonneur GB, West JA (2007) Systematics and genetic variation in commercial Kappaphycus and Eucheuma (Solieriaceae, Rhodophyta). In: Anderson R, Brodie J, Onsøyen E, Critchley AT (eds) Proceedings of the Eighteenth International Seaweed Symposium. Springer, Dordrecht, pp 417–425CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Yue Li
    • 1
  • Na Liu
    • 1
  • Xumin Wang
    • 2
  • Xianming Tang
    • 3
  • Lei Zhang
    • 1
  • Maria Dyah Nur Meinita
    • 4
  • Guoliang Wang
    • 2
  • Hongxin Yin
    • 1
  • Yuemei Jin
    • 1
  • Haiyang Wang
    • 1
  • Cui Liu
    • 1
  • Shan Chi
    • 1
    • 5
    Email author
  • Tao Liu
    • 1
    Email author
  • Jing Zhang
    • 6
    Email author
  1. 1.Laboratory of Genetics and Breeding of Marine Organisms, College of Marine Life SciencesOcean University of ChinaQingdaoChina
  2. 2.CAS Key Laboratory of Genome Sciences and Information, Beijing Key Laboratory of Genome and Precision Medicine Technologies, Beijing Institute of GenomicsChinese Academy of SciencesBeijingChina
  3. 3.Hainan Academy of Ocean and Fisheries SciencesHaikouChina
  4. 4.Faculty of Fisheries and Marine ScienceJenderal Soedirman UniversityPurwokertoIndonesia
  5. 5.Qingdao Haida BlueTek Biotechnology Co., LTDQingdaoChina
  6. 6.Qilu University of Technology, Shandong Academy of SciencesJinanChina

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