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J. Phycol. 53, 32–43 (2017) © 2016 Phycological Society of America DOI: 10.1111/Jpy.12472

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J. Phycol. 53, 32–43 (2017) © 2016 Phycological Society of America DOI: 10.1111/Jpy.12472 J. Phycol. 53, 32–43 (2017) © 2016 Phycological Society of America DOI: 10.1111/jpy.12472 ANALYSIS OF THE COMPLETE PLASTOMES OF THREE SPECIES OF MEMBRANOPTERA (CERAMIALES, RHODOPHYTA) FROM PACIFIC NORTH AMERICA1 Jeffery R. Hughey2 Division of Mathematics, Science, and Engineering, Hartnell College, 411 Central Ave., Salinas, California 93901, USA Max H. Hommersand Department of Biology, University of North Carolina at Chapel Hill, CB# 3280, Coker Hall, Chapel Hill, North Carolina 27599- 3280, USA Paul W. Gabrielson Herbarium and Department of Biology, University of North Carolina at Chapel Hill, CB# 3280, Coker Hall, Chapel Hill, North Carolina 27599-3280, USA Kathy Ann Miller Herbarium, University of California at Berkeley, 1001 Valley Life Sciences Building 2465, Berkeley, California 94720-2465, USA and Timothy Fuller Division of Mathematics, Science, and Engineering, Hartnell College, 411 Central Ave., Salinas, California 93901, USA Next generation sequence data were generated occurring south of Alaska: M. platyphylla, M. tenuis, and used to assemble the complete plastomes of the and M. weeksiae. holotype of Membranoptera weeksiae, the neotype Key index words: Ceramiales; Delesseriaceae; holo- (designated here) of M. tenuis, and a specimen type; Membranoptera; Northeast Pacific; phylogenetic examined by Kylin in making the new combination systematics; plastid genome; plastome; rbcL M. platyphylla. The three plastomes were similar in gene content and length and showed high gene synteny to Calliarthron, Grateloupia, Sporolithon, and Vertebrata. Sequence variation in the plastome Freshwater and Rueness (1994) were the first to coding regions were 0.89% between M. weeksiae and use gene sequences to address species-level taxo- M. tenuis, 5.14% between M. weeksiae and nomic problems in the Florideophyceae. Since then, M. platyphylla, and 5.18% between M. tenuis and other investigators have analyzed nuclear, plastid, M. platyphylla. We were unable to decipher the and mitochondrial DNA markers to resolve both complete mitogenomes of the three species due to higher level and species-level problems in red algae. low coverage and structural problems; however, we The major limitation of current markers is the assembled and analyzed, the cytochrome oxidase I, requirement for complete or nearly complete DNA II, and III loci and found that M. weeksiae and sequences to infer phylogenetic relationships. M. tenuis differed in sequence by 1.3%, M. weeksiae Although this is not an issue with fresh or silica gel- and M. platyphylla by 8.4%, and M. tenuis and dried material that contains large amounts of intact M. platyphylla by 8.1%. Evaluation of standard nucleic acids, DNA from historically important marker genes indicated that sequences from the herbarium specimens, including type specimens, is rbcL, RuBisCO spacer, and CO1 genes closely degraded and present only in low concentrations approximated the pair-wise genetic distances (Hughey and Gabrielson 2012). The correct applica- observed between the plastomes of the three tion of any name requires genetic analysis of type species of Membranoptera. A phylogenetic tree based material (Hughey et al. 2001, 2002, Gabrielson on rbcL sequences showed that M. tenuis and 2008a,b, Gabrielson et al. 2011, Lindstrom et al. M. weeksiae were sister taxa. Short rbcL sequences 2011, 2015a,b, Martone et al. 2012, Hind et al. were obtained from type specimens of M. dimorpha, 2014a,b, 2015, Sissini et al. 2014, Adey et al. 2015, M. multiramosa, and M. edentata and confirmed their Hernandez-Kantun et al. 2015, van der Merwe et al. conspecificity with M. platyphylla. The data support 2015). In these studies, however, targeted PCR the recognition of three species of Membranoptera methods were used to acquire small hypervariable sequences, which due to their length are not suit- 1Received 3 December 2015. Accepted 12 August 2016. 2Author for correspondence: e-mail: [email protected]. able for phylogenetic analysis. Hughey et al. (2014) Editorial Responsibility: C. Lane (Associate Editor) proposed a solution to the limitation of working 32 COMPLETE PLASTOMES OF MEMBRANOPTERA 33 with degraded DNA by analyzing the plastid and mitochondrial genomes from 12 archival herbarium MATERIALS AND METHODS specimens (including nine type specimens) of Ban- DNA extractions and PCR. DNA was isolated from herbar- giaceae using next generation sequencing method- ium specimens at Hartnell College following the precaution- ologies. Herein, we extended this methodology to ary contamination guidelines outlined by Hughey and closely and more distantly related species of North- Gabrielson (2012) and the protocol in Lindstrom et al. east Pacific florideophytes in the genus Membra- (2011). Silica gel-preserved contemporary specimens were processed at the University of North Carolina, Chapel Hill noptera Stackhouse (Delesserioideae, Delesseriaceae) following the protocol in Hughey et al. (2001). DNA from to evaluate the efficacy of plastid markers, particu- herbarium type and nontype specimens was PCR amplified larly the most commonly used marker rbcL. using the primer pair F753 (Freshwater and Rueness 1994) On the basis of morpho-anatomical characters, and R900 (50-GCGAGAATAAGTTGAGTTACCTG-30) follow- Gabrielson et al. (2012) recognized six species of ing the thermocycling methods in Lindstrom et al. (2011). Membranoptera in the Northeast Pacific: M. dimorpha This primer pair represents nucleotide positions 774–895 of N.L.Gardner (type locality: Neah Bay, Clallam the rbcL gene. Silica gel-preserved material was amplified with primer pairs F57/R753 and F753/RrbcS (Freshwater and County, Washington, USA); M. multiramosa Rueness 1994) based on the protocols in Hughey et al. N.L.Gardner (type locality: Moss Beach, San Mateo (2001). County, California, USA); M. platyphylla (Setchell & Phylogenetic analysis. Alignment of the rbcL sequences was N.L.Gardner) Kylin (type locality: Pleasant Beach, accomplished using the G-INS-1 Progressive Method in Kitsap County, Washington, USA); M. spinulosa MAFFT (Katoh and Standley 2013). Maximum likelihood (Ruprecht) Kuntze (syntype localities: Sea of analysis of the 13 Membranoptera sequences (Table 1) was per- Okhotsk and St. Paul Island, Bering Sea); M. tenuis formed using RAxML (Stamatakis 2014) with 1,000 bootstrap replicates and default parameters in Galaxy (Giardine et al. Kylin (type locality: Canoe Island, San Juan 2005, Blankenberg et al. 2010, Goecks et al. 2010) with Phy- County, Washington, USA, dredged 10–20 m codrys rubens (Linnaeus) Batters as the outgroup. Sequences depth); and M. weeksiae N.L.Gardner (type locality: of Grinnellia americana (C.Agardh) Harvey, Delesseria sanguinea Pacific Grove, Monterey County, California, USA). (Hudson) J.V.Lamouroux, Cumathamnion sympodophyllum They queried the distinctions between M. tenuis M.J.Wynne & K. Daniels, and C. decipiens (J.Agardh) and M. weeksiae and among M. multiramosa, M.J.Wynne & G.W.Saunders were included in the analysis for phylogenetic context. Bayesian analysis was executed with M. platyphylla, and M. spinulosa. Recently, on the MrBayes 3.2.1 (Huelsenbeck et al. 2001, Ronquist and basis of their analyses of mitochondrial cytochrome Huelsenbeck 2003) using the search parameters in Lindstrom oxidase 1 (COI-5P), nuclear internal transcribed et al. (2015a). The phylogenetic trees were visualized with spacers (ITS), large subunit of the ribosomal cis- TreeDyn 198.3 at Phylogeny.fr (Dereeper et al. 2008). tron (LSU), and RUBISCO large subunit (rbcL) Genomics. Genomic libraries were constructed following DNA sequences, Wynne and Saunders (2012) rec- the protocol outlined in Hughey et al. (2014) that was devel- ognized only one species, M. platyphylla, distributed oped by the High-Throughput Genomics Center (Seattle, Washington, USA). The genomic analysis was performed from British Columbia, Canada to central Califor- using standard Illumina 36 base pairs (bp) paired-end nia. All but two of their samples came from British sequencing methods. Data were assembled with default de Columbia, one from Monterey County, California novo settings in CLC Cell 4.3.0 (â2015 CLC bio, a QIAGEN and another identified as M. weeksiae from Boiler Company, Valencia, California, USA) and Velvet 1.2.08 (Zer- Bay, Oregon, USA (GenBank rbcL sequence- bino and Birney 2008) on the Bio-Linux platform (Field AF257384). et al. 2006) following the assembly steps in Hughey et al. (2014). The M. weeksiae plastome was assembled by perform- Our preliminary analysis of Membranoptera rbcL ing a Standard Nucleotide Blast search of the assembly con- sequences from northern Washington (San Juan tigs against the complete plastid genomes of Calliarthron County) to San Diego, California indicated the pres- tuberculosum (Postels & Ruprecht) E.Y.Dawson (GenBank ence of three species. To determine the correct accession KC153978), Grateloupia taiwanensis S.M.Lin & application of names and to compare rbcL H.Y.Liang (KC894740), and Chondrus crispus Stackhouse sequences with those of the entire plastid genome (HF562234). The 13 resulting contigs were oriented and as a diagnostic marker for red algal species, we joined via targeted PCR and direct Sanger sequencing. The plastid genomes of M. platyphylla and M. tenuis were assem- sequenced the plastomes from the holotype of bled by aligning the contigs from M. platyphylla and M. weeksiae, the neotype of M. tenuis collected by N. M. tenuis to the M. weeksiae plastome using a Standard L. Gardner in the absence of the type collection at Nucleotide Blast
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