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Rhodophyta) Based on Carposporophyte Development and Molecular Data

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Rhodophyta) Based on Carposporophyte Development and Molecular Data Botanica Marina 2017; 60(5): 515–532 Jeong Chan Kang, Mi Yeon Yang and Myung Sook Kim* Neoharaldiophyllum, a new genus of Delesseriaceae (Rhodophyta) based on carposporophyte development and molecular data DOI 10.1515/bot-2017-0003 Received 9 January, 2017; accepted 20 April, 2017; online first 22 Introduction June, 2017 Zinova (1981) established the genus Haraldiophyllum Abstract: The new genus Neoharaldiophyllum J.C. Kang et based on three species of Nitophyllum (i.e. Nitophyllum M.S. Kim belonging to the tribe Myriogrammeae, subfam- bonnemaisonii Greville [=Myriogramme bonnemaisonii ily Phycodryoideae of the Delesseriaceae, is described. Kylin], N. mirabile Kylin and N. versicolor Harvey). The This new genus consists of four species, namely Neoharal- three species had been mentioned by Kylin (1934, 1956) as diophyllum udoense (M.S. Kim et J.C. Kang) gen. et comb. having the same pattern of procarp development but differ nov. from Jeju Island Korea as the type species, Neoharal- from those of the generitype species Nitophyllum punc- diophyllum nottii (R.E. Norris et M.J. Wynne) J.C. Kang et tatum (Stackhouse) Greville. Kylin (1925, 1934) described M.S. Kim comb. nov. from the Hood Canal, Mason County, that the procarp in the three species has two sterile-cell Washington, USA, Neoharaldiophyllum mirabile (Kylin) groups, whereas that of N. punctatum has a single sterile- J.C. Kang et M.S. Kim comb nov. from Canoe Island, San cell group. He also noted that the two pericentral cells cut Juan County, Washington, USA, and Neoharaldiophyl- off from the fertile central cell in the procarp are borne lum erosum (Harvey) J.C. Kang et M.S. Kim comb. nov. perpendicular to the longitudinal axis of the frond in the from Garden Island, Western Australia. The morphologi- three species, while they are arranged in parallel with cal traits of the new genus are very similar to the genera the axis in N. punctatum. These two major differences Haraldiophyllum and Myriogramme in terms of the veg- between the three species and N. punctatum became the etative and reproductive structures. There are differences primary basis for establishing the genus Haraldiophyl- among the three genera in the developmental patterns lum by Zinova (1981). At that time, she designated Haral- of the carposporophyte: the primary gonimoblast cells diophyllum bonnemaisonii (Kylin) Zinova from Atlantic of Neoharaldiophyllum are prostrate on the floor cells of Europe as generitype species. Among the three species, the cavity of the cystocarp and fuse together secondarily, N. versicolor is currently regarded as a taxonomic synonym whereas in the two other genera they remain free without of Drachiella heterocarpa (Chauvin ex Duby) Maggs et a secondary incorporation with the floor cells; the car- Hommersand (Wynne 2014, Guiry and Guiry 2016). In the posporangia of Myriogramme are borne in short chains same study, Zinova (1981) established another new genus, terminating the gonimoblast filaments, while those in Hideophyllum, based on Myriogramme yezoensis Yamada the other two genera are borne as solitary structures. The et Tokida from Hokkaido, Japan. molecular phylogenies based on rbcL and LSU sequences The morphological traits of Haraldiophyllum are strongly support the significance of the developmental known to be very similar to those of Myriogramme Kylin patterns of the carposporophyte and support the separa- and Hideophyllum Zinova in terms of habit, thallus struc- tion of Neoharaldiophyllum from Haraldiophyllum in the ture, morphology of spermatangial and tetrasporan- tribe Myriogrammeae. gial sori, and composition of procarp (i.e. with anterior cover-cell group and two sterile-cell groups). However, Keywords: cystocarp structure; Delesseriaceae; molecular Haraldiophyllum differs from the two other genera in that phylogeny; Neoharaldiophyllum gen. nov.; taxonomy. it has single terminally borne carposporangia, while the other genera produce short chains of carposporangia *Corresponding author: Myung Sook Kim, Department of Biology, on the gonimoblast filaments (Zinova 1981, Maggs and Jeju National University, Jeju 690-756, Korea; and Research Institute Hommersand 1993, Hommersand and Fredericq 1997a, for Basic Sciences, Jeju National University, Jeju 690-756, Korea, e-mail: [email protected] Lin et al. 2007, Wynne 2014). Another important charac- Jeong Chan Kang and Mi Yeon Yang: Department of Biology, Jeju ter of Haraldiophyllum could be observed in the cystocarp, National University, Jeju 690-756, Korea that is, the incorporation of the fusion cell with the floor 516 J.C. Kang et al.: Neoharaldiophyllum gen. nov. cells in the cavity of the cystocarp (Zinova 1981, Maggs and desiccant for DNA extraction, and the samples for mor- Hommersand 1993, Millar 1994, Millar and Huisman 1996, phological observation were preserved in 5% formalin/ Hommersand and Fredericq 1997a, Lin et al. 2007, Wynne seawater. Voucher specimens were deposited in the her- 2014). barium of Jeju National University (JNUB, Jeju, Korea) While only seven species of Haraldiophyllum have and the National Institute of Biological Resources (NIBR, been recognized to date, they are scattered across Atlantic Incheon, Korea). Europe, the northern Pacific America, the north-western Sections for morphological examination were cut Pacific region and the southern hemisphere (Wynne 2014, by hand using razor blades or with bench-top freezing Guiry and Guiry 2016). In the north-western Pacific region, microtome (MFS no. 222; Nippon Optical Works, Tokyo, Nam and Kim (1996) initially recorded H. bonnemaisonii Japan). Materials were stained with Wittmann’s (1965) based on specimens from the southern coast of Korea, aceto-iron-hematoxylin-chloral hydrate and mounted and the second species, namely Haraldiophyllum udoense in 50% Hoyer’s mounting medium, or stained with 1% [“udoensis”] from Jeju Island, was described by Kim and aniline blue acidified with 1% HCl and mounted in 40% Kang (2011). As H. udoense was described based on tet- corn syrup solution (Lin et al. 2007). Images were cap- rasporic plants, the morphological features of female and tured using a G7x digital camera (Canon, Tokyo, Japan) male reproductive structures are still unknown. attached to an SZ2-ILST dissecting microscope (Olympus, To investigate their distribution and confirm the game- Tokyo, Japan); anatomical images were captured with a tophytic reproductive structures, we collected the species BX 43 microscope (Olympus, Tokyo, Japan) equipped with along the coast of the Korean peninsula, and gametan- an EOS 600 D digital camera (Canon, Tokyo, Japan). gial plants were successfully collected from several sites Total genomic DNA was extracted from specimens from the western and southern coasts of Korea including with a DNeasy Plant Mini kit (Qiagen, Hilden, Germany), the type locality Jeju Island, during 2012–2016. When we following manufacturer instructions. Amplification for observed the cross-section of the cystocarp, we were con- the nuclear LSU, the plastid ribulose-1, 5-bisphosphate fused because the shape of their carposporophyte is very carboxylase large subunit gene (rbcL) and the mitochon- different from those of ordinary Delesseriacean species drial cytochrome c oxidase 1 barcode region (COI-5P) was including the type species, H. bonnemaisonii. To investi- conducted using primers T01N, G, X, 28F, T05, T15 (LSU; gate the taxonomic and phylogenetic significance of the Freshwater et al. 1999, Harper and Saunders 2001), F7, shape of the carposporophyte, we analyzed the morphol- R898, F762, R1442 (rbcL; Gavio and Fredericq 2002, Kim ogy as well as two gene sequences (rbcL and LSU) and et al. 2010), and GWSFn, COIR686 (COI; Le Gall and Saun- then compared the results with previous studies of closely ders 2010, Sherwood et al. 2010). related taxonomic groups. To certify the genetic homo- Amplification reactions were set up and run as geneity among the various populations of H. udoense, described in Saunders and Moore (2013). The PCR prod- we also compared the rbcL gene sequences from our ucts were purified with an AccuPrep PCR Purification Kit specimens including the holotype. In the present study, (Bioneer, Daejeon, Korea) and sequenced commercially we describe in detail the morphological characters from by Macrogen (Seoul, Korea). Electropherogram outputs of male and female reproductive structures to supplement each sample were edited using the Chromas Lite 2.01 soft- the previous study by Kim and Kang (2011), especially ware (Technelysium, Helensvale, Queensland, Australia) focussing on the developmental pattern of the carpospor- and PHYDIT version 3.1 software (Chun 2001). Sequences ophyte, and we establish the new genus Neoharaldiophyl- were assembled in BioEdit 7.0.5 (Hall 1999) and aligned lum based on H. udoense from Korea. with Clustal W (Sievers et al. 2011). The LSU alignment was adjusted by eye, and ambiguous regions and introns were removed prior to analyses. The alignments of rbcL and combined LSU + rbcL Materials and methods sequence data were constructed to explore the relation- ships of the Neoharaldiophyllum with related taxa. This Specimens were collected from the subtidal on the coasts alignment included 12 newly generated sequences (two of of South Korea by SCUBA diving and from the intertidal on LSU and 10 of rbcL). Phylogenetic analyses were performed the coasts of New Zealand and Australia (Table 1). Field- using RAxML (Stamatakis 2006) using the GTR + Γ + I collected samples were kept fresh in a cool box with an model.
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