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Gelidiales, Rhodophyta) Using Cox1 and Rbcl Sequences

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Gelidiales, Rhodophyta) Using Cox1 and Rbcl Sequences Research Article Algae 2012, 27(2): 83-94 http://dx.doi.org/10.4490/algae.2012.27.2.083 Open Access Phylogenetic relationships and distribution of Gelidium crinale and G. pusillum (Gelidiales, Rhodophyta) using cox1 and rbcL sequences Kyeong Mi Kim1 and Sung Min Boo1,* 1Department of Biology, Chungnam National University, Daejeon 305-764, Korea The taxonomic distinctiveness and cosmopolitan distributions of the red algae Gelidium crinale and G. pusillum re- main unclear. Both species were first described in Devon in southwestern England; namely in Ilfracome forG. crinale and Sidmouth for G. pusillum. We analyzed mitochondrial cox1 and plastid rbcL sequences from specimens collected in East Asia, Australia, Europe and North America. In all phylogenetic analyses of cox1 and rbcL sequences, G. crinale was distinct from congeners of the genus. The analyses also revealed a sister relationship with the G. coulteri and G. capense clade. Nineteen cox1 haplotypes were identified forG. crinale, and they were likely geographically structured. Despite the distinctiveness in both cox1 and rbcL datasets, the sister relationship of G. pusillum in the genus was not resolved. Our cox1 and rbcL datasets indicate that G. crinale is a cosmopolitan species, found in East Asia, Australia, Europe and North America, while the distribution of G. pusillum is restricted to Europe and Atlantic North America. Our results suggest that infraspecific classification of G. pusillum may be abandoned. Key Words: cox1; distribution; Gelidium crinale; Gelidium pusillum; phylogeny; rbcL INTRODUCTION Gelidium Lamour. is composed of approximately 127 lum (Stackhouse) Le Jolis, which are small and morpho- described species distributed globally along tropical, sub- logically diverse, are among the most difficult species to tropical, and artic shorelines (Freshwater and Rueness identify in red algae, and their distributions are unclear. 1994, Shimada et al. 2000, Millar and Freshwater 2005, These species are traditionally recognized as two distinct Kim et al. 2011, in press, Guiry and Guiry 2012). Members species (Feldmann and Hamel 1936, Silva et al. 1996), and of the genus can be the most abundant organisms within Womersley and Guiry (1994) found a difference between intertidal algal assemblages. Gelidium is economically the types of G. crinale and G. pusillum. On the contrary, G. important as food, and one of the most promising agar crinale and G. pusillum were merged by Dixon and Irvine sources in rhodophytes. It has recently been used for in- (1977a, 1977b). Seven to nine varieties or formas have dustrial paper pulp production in Korea (Seo et al. 2010). been described in each of G. crinale and G. pusillum (Silva However, identification of individualGelidium speci- et al. 1996, Guiry and Guiry 2012). The name G. pusillum mens is notoriously difficult because of the high degree of is commonly used for any small tuft-forming Gelidium morphological variation, particularly in the smaller and (Silva et al. 1996). Although G. crinale and G. pusillum are medium-sized species (Dixon and Irvine 1977a). considered as the most widely distributed species in the Gelidium crinale (Hare ex Turner) Gallion and G. pusil- genus AlgaeBase (Guiry and Guiry 2012), the occurrence This is an Open Access article distributed under the terms of the Received February 27, 2012, Accepted May 28, 2012 Creative Commons Attribution Non-Commercial License (http://cre- Corresponding Author ativecommons.org/licenses/by-nc/3.0/) which permits unrestricted * non-commercial use, distribution, and reproduction in any medium, E-mail: [email protected] provided the original work is properly cited. Tel: +82-42-821-6555, Fax: +82-42-822-9690 Copyright © The Korean Society of Phycology 83 http://e-algae.kr pISSN: 1226-2617 eISSN: 2093-0860 Algae 2012, 27(2): 83-94 of both species in many countries should be reassessed. and Fredericq 2002); and for cox1, cox143F-cox11549R In this study we characterized two species, namely G. (Geraldino et al. 2006) and C622F-C880R (Yang et al. crinale and G. pusillum, using two molecular markers. 2008). To evaluate the relationship and distribution of G. crinale Ninety-three rbcL sequences including 13 new se- and G. pusillum, we analyzed plastid rbcL, and mitochon- quences and 65 cox1 sequences including 24 new Gelid- drial cox1 including type locality materials. Plastid rbcL is ium sequences were collated using the Se-Al version commonly used for Gelidium phylogeny (Freshwater and 2.0a11 software (Rambaut 1996) and aligned visually. Rueness 1994, Freshwater et al. 1995, Shimada et al. 2000, Outgroup taxa used were representatives from Gelidiella Millar and Freshwater 2005, Nelson et al. 2006, Kim et al. Feldmann et G. Hamel, Pterocladia J. Agardh, Pterocla- 2011). Recent studies have revealed that mitochondrial diella Santelices et Hommersand, and Ptilophora (Suhr) cox1 is useful for both DNA bar-coding of gelidioid red Kützing (Freshwater et al. 1995, Kim et al. 2011). algae and to examine their distribution patterns (Fresh- Maximum likelihood (ML) phylogenetic analysis of water et al. 2010, Wiriyadamrikul et al. 2010, Kim et al. rbcL was performed using the GTR + Γ + I model imple- 2012). In this study, we included published rbcL sequenc- mented in RAxML software (Stamatakis 2006). We used es analyzed from G. crinale type material (Freshwater et 200 independent tree inferences with the “number of al. 2010) and samples collected in the G. pusillum type run” option, with default optimized subtree pruning and locality. regrafting (SPR) rearrangement and 25 distinct rate cate- gories to identify the best tree. Statistical support for each branch was obtained from 1,000 bootstrap replications MATERIALS AND METHODS using the same substitution model and RAxML program settings. Taxon sampling and morphological observation Bayesian analyses (BA) were performed for combined and individual datasets with MrBayes v.3.1.1 (Ronquist A total of 18 specimens of G. crinale were obtained for and Huelsenbeck 2003) using the Metropolis-coupled this study: 17 collected from 10 locations including Chi- Markov chain Monte Carlo (MC3) with the GTR + Γ + I na, Hong Kong, Korea, Spain and the UK, and one strain model. For each matrix, one million generations of two from the culture collection of the University of Texas, independent runs were performed with four chains and UTEX (Appendix A). Ten G. pusillum field collections sampling trees every 100 generations. The burn-in peri- were made at five locations in France, Spain and the UK. od was identified graphically by tracking the likelihoods Materials for morphological observations were mounted at each generation to determine whether they reached on herbarium sheets, while clean apical parts of the spec- a plateau. The 15,001 trees for rbcL and 22,501 trees for imens were desiccated in silica gel for DNA extraction. cox1 sampled at the stationary state were used to infer the Tissues were sectioned using a freezing microtome (FX- Bayesian posterior probability. 802A; Coper Electronics Co., Ltd., Kanagawa, Japan), and A statistical parsimony network of cox1 haplotypes was sectioned preparations were stained with 1% aqueous created using TCS version 1.21 software (Clement et al. aniline blue. Photographs were taken with an FX-35DX 2000). Haplotype and nucleotide diversity measurements camera (Nikon, Tokyo, Japan) attached to a Vanox AHBT3 were performed using DnaSP software (Rozas and Rozas microscope (Olympus, Tokyo, Japan). Voucher specimens 1999). were deposited at the herbarium of Chungnam National University (CNUK), Daejeon, Korea. RESULTS DNA extraction, sequencing and phylogenetic analyses Molecular analyses Twenty-eight specimens were available for DNA extrac- A total of 93 sequences from Gelidium and outgroups tion (Appendix A). DNA extraction, PCR amplification, were aligned using a 1,266-nucleotide (nt) portion of and sequencing are described in Geraldino et al. (2010). rbcL. Variable sites were found at 492 portions (38.9%), Primer pairs for amplification and sequencing of each and 393 portions (31%) were parsimoniously informa- gene were as follows: for rbcL, F7-R753 and F645-RrbcS tive. All GenBank accessions of G. crinale from nine coun- start (Freshwater and Rueness 1994, Lin et al. 2001, Gavio tries formed a single monophyletic group with maximum http://dx.doi.org/10.4490/algae.2012.27.2.083 84 Kim & Boo Gelidium crinale and G. pusillum Fig. 1. Maximum likelihood tree of Gelidium using 93 rbcL sequences calculated using the GTR + Γ + I evolution model (-lnL = 10511.506124; substitution rate matrix RAC = 0.951940, RAG = 5.742494, RAT = 1.371355, RCG = 1.258690, RCT = 10.348932, RGT = 1; shape parameter [α] = 1.575834). Maximum likelihood bootstrap values and Bayesian posterior probabilities are shown for each clade. Only bootstrap values ≥50% and ≥0.95 Bayesian posterior probabilities are shown. 85 http://e-algae.kr Algae 2012, 27(2): 83-94 Fig. 2. Maximum likelihood tree of Gelidium using 65 cox1 sequences calculated using the GTR + Γ + I evolution model (-lnL = 9341.027999; substitution rate matrix RAC = 1.153854, RAG = 10.881554, RAT = 1.077417, RCG = 0.000017, RCT = 20.342285, RGT = 1; shape parameter [α] = 1.101521). Maximum likelihood bootstrap values and Bayesian posterior probabilities are shown for each clade. Only bootstrap values ≥50% and ≥0.95 Bayesian posterior probabilities are shown. http://dx.doi.org/10.4490/algae.2012.27.2.083 86 Kim & Boo Gelidium crinale and G. pusillum support (Fig. 1). The G. crinale clade consisted of three terete to flattened distally (up to 550 µm wide). Spanish subgroup; Asian, Australian, and European / American specimen appears to have cylindrical branches (Fig. 4D). group. Piarwise divergence of G. crinale was up to 2.74%. Large dome-shaped apical cells are evident at the apices G. crinale was sister to the clade of G. coulteri Harvey and and project over the cortical margin (Fig. 4E). Axes and G. capense (S. G. Gmelin) P. C. Silva (93% for ML and 1.0 branches consist of cortex and medulla (Fig.
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