Abstract
The complete nuclear ribosomal DNA (nrDNA) cistron sequence of Pyropia yezoensis has been sequenced, of which each unit is composed of the intergenic spacer (IGS), the small-subunit (SSU) ribosomal RNA (rRNA) gene, the internal transcribed spacer 1 (ITS1), the 5.8S rRNA gene, the internal transcribed spacer 2 (ITS2), and the large-subunit (LSU) rRNA gene. This cistron occurs in tandem repeats that can number in 100s to 1000s. Furthermore, in the analysis of the sequence data, we determined that introns were present in the small-subunit rRNA genes, for which the exon sequences (1834 bp) are almost identical. The intron numbers ranging from zero to two in the small-subunit rRNA genes are different between multiple individuals. However, the full length of the large-subunit rRNA genes is 4770 bp without any introns, and the 5.8S rRNA gene is 159 bp. Moreover, the 5′ and 3′ terminal sequences of the genic regions of the ribosomal cistron are extremely conservative even among various species in red alga. In addition, the range for ITS1 is 371–372 bp and for ITS2 is 532 to 535 bp. The IGS is 5984 bp in length and possesses upstream direct repeats, downstream repeats, and middle inverted repeats that make sequencing untoward. This is the first time that the complete nucleotide of the IGS region of P. yezoensis has been sequenced. The provision of the full length of nrDNA cistron will offer useful information to be widely utilized for identification, taxonomic relationships, and phylogenies in red algae.
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Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Alvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434
Appels R, Honeycutt RL (1986) rDNA: evolution over a billion years. In: Dutta SK (ed) DNA systematics, vol 2. CRC Press, Boca Raton, pp 81–135
Blouin NA, Brodie JA, Grossman AC, Xu P, Brawley SH (2011) Porphyra: a marine crop shaped by stress. Trends Plant Sci 16:29–37
Brodie J, Hayes PK, Barker GL, Irvine LM, Bartsch I (1998) A reappraisal of Porphyra and Bangia (Bangiophycidae, Rhodophyta) in the Northeast Atlantic based on the rbcL-rbcS intergenic spacer. J Phycol 34:1069–1074
Broom JE, Jones WA, Hill DF, Knight GA, Nelson WA (1999) Species recognition in New Zealand Porphyra using 18S rDNA sequencing. J Appl Phycol 11:421–428
Cech TR (1988) Conserved sequences and structures of group I introns: building an active site for RNA catalysis—a review. Gene 73:259–271
Chen CS, Xie CT, Ji DH, Liang Y, Zhao LM (2010) Molecular divergence and application of the ITS-5.8S rDNA and RUBISCO spacer in Porphyra haitanensis Chang et Zheng (Bangiales, Rhodophyta). Aquacult Int 18:1045–1060
Dai XJ, OU LJ, Li WJ, Liang MZ, Chen LB (2008) Analysis of rDNA intergenic spacer (IGS) sequences in Oryza sativa L. and their phylogenetic implications. Acta Agron Sinica 34:1569–1573
Dover GA (1987) DNA turnover and the molecular clock. J Mol Evol 26:47–58
Erting L, Daugbjerg N, Pedersen PM (2004) Nucleotide diversity within and between four species of Laminaria (Phaeophyceae) analysed using partial LSU and ITS rDNA sequences and AFLP. Eur J Phycol 39:243–256
Gall LL, Saunders GW (2007) A nuclear phylogeny of the Floridephyceae (Rhodophyta) inferred from combined EF2, small subunit and large subunit ribosomal DNA: establishing the new red algal subclass Corallinophycidae. Mol Phylogenet Evol 43:1118–1130
Gall LL, Saunders GW (2010) DNA barcoding is a powerful tool to uncover algal diversity: a case study of the Phyllophoraceae (Gigartinales, Rhodophyta) in the Canadia flora. J Phycol 46:374–389
Harper JT, Saunders GW (2001) The application of sequences of the ribosomal cistron to the systematics and classification of the florideophyte red algae (Florideophyceae, Rhodophyta). Cah Biol Mar 42:25–38
He LW, Zhu JY, Lu QQ et al (2013) Genetic similarity analysis within Porphyra yezoensis blades developed from both conchospores and blade archeospores using AFLP. J Phycol 49:517–522
Hu ZM, Liu FL, Shao ZR, Yao JT, Duan DL (2010) NrDNA internal transcribed spacer revealed molecular diversity in strains of red seaweed Porphyra yezoensis and genetic insights for commercial breeding. Genet Resour Crop Evol 57:791–799
Iwasaki H (1961) The life-cycle of Porphyra tenera in vitro. Biol Bull 121:173–187
Kunimoto M, Kito H, Kaminishi Y, Mizukami Y, Murase N (1999a) Molecular divergence of the ssu rRNA gene and internal transcribed spacer 1 in Porphyra yezoensis (Rhodophyta). J Appl Phycol 11:211–216
Kunimoto M, Kito H, Yamamoto Y, Cheney DP, Kaminishi Y, Mizukami Y (1999b) Discrimination of Porphyra species based on small subunit ribosomal RNA gene sequence. J Appl Phycol 11:203–209
Li YY, Shen SD, He LH, Xu P, Wang GC (2009) Sequence analysis of the ITS region and 5.8S rDNA of Porphyra haitanensis. Chinese J Oceanol Limnol 27:493–501
Li YY, Shen SD, He LH, Xu P, Lu S (2010) Sequence analysis of rDNA intergenic spacer (IGS) of Porphyra haitanensis. J Appl Phycol 22:187–193
Matsuyama-Serisawa K, Yamamoto M, Fujishita M, Endo H, Serisawa Y, Tabata S, Kawano S, Saga N (2007) DNA content of cell nucleus in the macroalga, Porphyra yezoensis (Rhodophyta). Fish Sci 73:738–740
Milstein D, de Oliveira MC (2005) Molecular phylogeny of Bangiales (Rhodophyta) based on small subunit rDNA sequencing: emphasis on Brazilian Porphyra species. Phycologia 44:212–221
Müller KM, Cannone JJ, Gutell RR, Sheath RG (2001) A structural and phylogenetic analysis of the group IC1 introns in the order Bangiales (Rhodophyta). Mol Biol Evol 18:1654–1667
Naidoo K, Steenkamp ET, Coetzee MP, Wingfield MJ, Wingfield BD (2013) Concerted evolution in the ribosomal RNA cistron. PLOS One 8:e59355
Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, Satomi M et al (2013) The first symbiont-free genome sequence of marine red alga, susabi-nori (Pyropia yezoensis). Plos One 8:1–11
Nelson WA, Broom JE, Farr TJ (2001) Four new species of Porphyra (Bangiales, Rhodophyta) from the New Zealand region described using traditional characters and 18S rDNA sequences data. Cryptogam Algol 22:263–284
Niwa K, Kato A, Kobiyama A, Kawai H, Aruga Y (2008) Comparative study of wild and cultivated Porphyra yezoensis (Bangiales, Rhodophyta) based on molecular and morphological data. J Appl Phycol 20:261–270
Niwa K, Iida S, Kato A, Kawai H, Kikuchi N, Kobiyama A, Aruga Y (2009) Genetic diversity and introgression in two cultivated species (Porphyra yezoensis and Porphyra tenera) and closely related wild species of Porphyra (Bangiales, Rhodophyta). J Phycol 45:493–502
Onkendi EM, Moleleki LN (2013) Detection of Meloidogyne enterolobii in potatoes in South Africa and phylogenetic analysis based on intergenic region and mitochondrial DNA sequences. Eur J Plant Pathol 136:1–5
Parvaresh M, Talebi M, Sayed-Tabatabaei BE (2014) Molecular characterization of ribosomal DNA intergenic spacer (IGS) region in pomegranate (Punica granatum L.). Plant Syst Evol 300:899–908
Patwary MU, Sensen CW, MacKay RM, van der Meer JP (1998) Nucleotide sequences of small-subunit and internal transcribed spacer regions of nuclear rRNA genes support the autonomy of some genera of the Gelidiales (Rhodophyta). J Phycol 34:299–305
Ragan MA, Bird CJ, Rice EL, Singh RK (1993) The nuclear 18S ribosomal RNA gene of the red alga Hildenbrandia rubra contains a group I intron. Nucleic Acids Res 21:16
Saga N, Kitade Y (2002) Porphyra: a model plant in marine sciences. Fish Sci 68(Suppl):1075–1078
Sahoo D, Tang XR, Yarish C (2002) Porphyra—the economic seaweed as a new experimental system. Curr Sci 83:1313–1316
Saunders GW, Lehmkuhl KV (2005) Molecular divergence and morphological diversity among four cryptic species of Plocamium (Plocamiales, Florideophyceae) in northern Europe. Eur J Phycol 40:293–312
Saunders GW, Moore TE (2013) Refinements for the amplification and sequencing of red algal DNA barcode and RedTol phylogenetic markers: a summary of current primers, profiles and strategies. Algae 28:31–43
Sutherland JE, Lindstrom SC, Nelson WA, Brodie J, Lynch MDJ, Hwang MS, Choi H-G, Miyata M, Kikuchi N, Oliveira MC, Farr T, Neefus C, Mols-Mortensen A, Milstein D, Müller KM (2011) A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J Phycol 47:1131–1151
Worheide G, Nichols SA, Goldberg J (2004) Intragenomic variation of the rDNA internal transcribed spacers in sponges (Phylum Porifera): implications for phylogenetic studies. Mol Phylogenet Evol 33:816–830
Yang J, Wang Q, Liu MH, An LJ (1999) A simple method for extracting total DNA of seaweeds. Biotechnol 9:39–42
Zimmer EA, Martin SL, Beverley SM, Kan YW, Wilson AC (1980) Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proc Natl Acad Sci U S A 77:2158–2162
Acknowledgments
This work was supported by the National Natural Science Foundation of China (Project No. 31270256, No. 31272664) and the National “863” Project (Project No. 2012 AA10A 406-6). The authors are grateful to Dr. Kirsten M. Müller, University of Waterloo, for her suggestions in the manuscript.
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Xingchen Li and Yuan He contributed equally to this study.
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Li, X., Xu, J., He, Y. et al. The complete nuclear ribosomal DNA (nrDNA) cistron sequence of Pyropia yezoensis (Bangiales, Rhodophyta). J Appl Phycol 28, 663–669 (2016). https://doi.org/10.1007/s10811-015-0522-8
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DOI: https://doi.org/10.1007/s10811-015-0522-8