Fottea 2017, 17(2):222-239 | DOI: 10.5507/fot.2017.004
Taxonomical analysis of closely related species of Chara L. section Hartmania (Streptophyta: Charales) based on morphological and molecular data
- 1Department of Botany and Plant Ecology, Wroc³aw University of Environmental and Life Sciences, pl. Grunwaldzki 24a , 50-363 Wroc³aw, Poland; Corresponding author e-mail: jacek.urbaniak@upwr.edu.pl
- 2 Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe 657-8501, Japan
In this study, five charophyte species belonging to the genus Chara L. section Hartmania, collected in Poland, were examined to determine their taxonomic status. Oospore dimensions of all investigated species differed significantly in their length, width and number of striae. However, no clear differences were found in the case of the oospore wall ornamentation that could be used for clear differentiation of the studied species. Detailed SEM images showed that the ornamentation on the oospore wall is not species specific, and also does not allow for differentiation of the species. Moreover, molecular phylogenetic analyses based on the matK and atpB DNA sequences reveal that the five studied species of section Hartmania are closely related and exhibit low genetic variation. Both types of analyses, based on oospore morphology and DNA barcoding, suggest a close phylogenetic relationship among the investigated species. The low levels of variability between species suggest that they had a relatively recent common ancestor, and probably exhibit a still incomplete, speciation process.
Keywords: : atpB, Chara, Characeae, Charophyta, Europe, matK, molecular phylogeny, morphology, oospore, taxonomy
Received: October 26, 2016; Accepted: January 31, 2017; Prepublished online: August 23, 2017; Published: September 20, 2017 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Abascal, F.; Zardoya, R. & Telford, M.J. (2010): TranslatorX, multiple alignment of nucleotide sequences guided by amino acid translations. - Nucleic Acids Research 38: 7-13.
Go to original source... - Blume, M.; Blindow, I.; Dahlke, S. & Vedder, F. (2009): Oospore variation in closely related Chara taxa. - Journal of Phycology 45: 995-1002.
Go to original source... - Bluemel, C. (2003): Chara baltica Wahlst. 1862. In: Schubert H, Blindow I. (eds): Charophytes of the Baltic Sea. - pp. 53 - 63, Gantner, Ruggell.
- Boegle, M.G.; Schneider, S.; Mannschreck, B. & Melzer, A. (2007): Differentiation of Chara intermedia and C. baltica compared to C. hispida based on morphology and amplified fragment length polymorphism. - Hydrobiologia 586: 155-166.
Go to original source... - Boegle, M.G.; Schneider, S.C.; Schubert, H. & Melzer, A. (2010): Chara baltica Bruzelius 1824 and Chara intermedia A. Braun 1859 - distinct species or habitat specific modifications? - Aquatic Botany 93: 195-201.
Go to original source... - Braun, A. & Nordsteadt, C.F.O. (1882): Fragmente einer Monographie der Characeen. Nach den hinterlassenden Manuscripten A. Braun's. - Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin, Physikalisch-Mathematische Klasse 1882: 1-221.
- Casanova, M.T. (1997): Oospore variation in three species of Chara (Charales, Chlorophyta). - Phycologia 36: 274-80.
Go to original source... - Casanova, M.T. (2015): Chromosome numbers in Australian charophytes (Characeae, Charophyceae). - Phycologia 54: 149-160.
Go to original source... - Cimino, M.T. & Delwiche, C.F. (2002): Molecular and morphological data idetify a cryptic species complex in endophytic members of the genus Coleochaete Bréb. (Charophyta: Coleochaetaceae). - Journal of Phycology 38: 1213-1221.
Go to original source... - Edgar, R.C. (2004a): MUSCLE, a multiple sequence alignment method with reduced time and space complexity. - BMC Bioinformatics 5: 113.
Go to original source... - Edgar, R.C. (2004b): MUSCLE, multiple sequence alignment with high accuracy and high throughput. - Nucleic Acids Research 32: 1792-1797.
Go to original source... - Erdtman, G. (1960): The acetolysis method. - Svensk Botanisk Tidskrift 54: 561-564.
- Felsenstein, J. (1985): Confidence limits on phylogenies, an approach using bootstrap. - Evolution 38: 16-24.
Go to original source... - Guindon, S. & Gascuel, O. (2003): A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. - Systematic biology 52: 696-704.
Go to original source... - Haas, J.N. (1994): First identification key for charophyte oospores from central Europe. - European Journal of Phycology 29: 227-235.
Go to original source... - Horn af Rantizen, H. (1956): Morphological terminology relating to female charophyte gametangia and fructifications. - Botaniska Notiser 109: 212-259.
- John, D.M. & Moore, J.A. (1987): An SEM study of some oospore Nitella species (Charales, Chlorophyta) with descriptions of wall ornamentation and an assessment of its taxonomic importance. - Phycologia 26: 334-355.
Go to original source... - John, D.M.; Moore, J.A. & Green, D.R. (1990): Preliminary Observations on the Structure and Ornamentation of the Oosporangial Wall in Chara (Charales, Chlorophyta). - British Phycological Journal 25: 1-24.
Go to original source... - Jukes, T.H. & Cantor, C.R. (1969): Mammalian Protein Metabolism. - In: Munro M.N. (ed.): Evolution of protein molecules. - pp. 21 - 132, Academic Press, New York.
Go to original source... - Kamiya, N. & Kuroda, K. (1956): Artificial modification of the osmotic pressure of the plant cell. - Protoplasma 46: 423-436.
Go to original source... - Karol, K.G.; McCourt, R.M.; Cimino, M.T & Delwiche, C.F. (2001): The closest living relatives of land plants. - Science 294: 2351-2353.
Go to original source... - Krause, W. (1997): Charales (Charophceae).- In: Ettl, H.; Gaertner, G.; Heyning, H. & Mollenhauer, D. (eds): Süßwasserflora von Mitteleuropa, Band 18. - 202 pp., Gustav Fischer Verlag, Stuttgart - Jena, Germany.
- Laurin-Lemay, S.; Brinkmann, H. & Philippe, H. (2012): Origin of land plants revisited in the light of sequence contamination and missing data. - Current biology 22: 593-594.
Go to original source... - Leitch, A.R. (1989): Formation and ultrastructure of a complex, multilayered wall around the oospore of Chara and Lamprothamnium (Characeae). - British Phycological Journal 24: 229-236.
Go to original source... - Leitch, A.R.; John, D.M. & Moore, J.A. (1990): The oosporangium of the Characeae (Chlorphyta, Charales). - Progress in Phycological Research 7: 213-268.
- Mandal, D. K.; Bla¾enèiæ, J. & Ray, S. (2002): SEM study of compound oospore wall ornamentation of some members of Charales from Yugoslavia, Croatia and Slovenia. - Archives of Biological Sciences, Belgrade 54: 29-34.
Go to original source... - Mannchreck, B.; Fink, T. & Melzer, A. (2002): Biosystematics of selected Chara species (Charophyta) using amplified fragment length polymorphism. - Phycologia 41: 657 - 666.
Go to original source... - Mattox, K.R. & Stewart, K.D. (1984): Classification of the green algae, a concept based on comparative cytology. - In: Irvine, D.E.G. & John D.M. (eds): Systematics of the Green Algae. - pp. 29-72, Academic Press, London and Orlando.
- Meiers, S.T.; Proctor, W.V. & Chapman, R.L. (1999): Phylogeny and biogeography of Chara (Charophyta) inferred from 18S rDNA sequences. - Australian Journal of Botany 47: 347-360.
Go to original source... - McCourt, R.M.; Casanova, M.T.; Karol, K.G. & Feist, M. (1999): Monophyly of genera and species of Characeae based on rbcL sequences, with special reference to Australian and European Lychnothamnus barbatus (Characeae, Charophyceae). - Australian Journal of Botany 47: 361-369.
Go to original source... - McCourt, R.M.; Karol, K.G.; Guerlesquin, M. & Feist, M. (1996): Phylogeny of extant genera in the family Characeae (Charales, Charophyceae) based on rbcL sequences and morphology. - American Journal of Botany 83: 125-131.
Go to original source... - Nowak, P.; Schubert, H.; Schaible, R. (2016): Molecular evaluation of the validity of the morphological charactersof three Swedish Chara sections: Chara, Grovesia, and Desvauxia(Charales, Charophyceae). - Aquatic Botany 134: 113-119.
Go to original source... - Nylander, J.A.A.; Ronquist, F.; Huelsenbeck, J.P. & Nieves-Aldrey, J.L. (2004): Bayesian phylogenetic analysis of combined data. - Systematic biology 53: 47-67.
Go to original source... - Olsen, S. (1944): Danish Charophyta. Chorological, ecological and biological investigations. - Kongelige Danske Videnskabernes Selskabs. Biologiske Skrifter 3: 1-240.
- Perez, W.; Hall, J.; McCourt, R. & Karol, K.G. (2014): Phylogeny of North America Tolypella (Charophyceae: charophyta) based on plastid DNA Sequences with adescription of Tolypella ramosissima sp. nov. - Journal of Phycology 50: 776-789.
Go to original source... - Ray, S.; Pekkari, S. & Snoeijs, P. (2001): Oospore dimensions and wall ornamentation patterns in Swedish charophytes. - Nordic Journal of Botany 21: 207-224.
Go to original source... - Romanov, R.E.; Gontcharov, A.A. & Barinova, S.S. (2015). Chara globata Mig. (Streptophyta: Charales): rare species revised. - Fottea 15: 39-50.
Go to original source... - Ronquist, F. & Huelsenbeck, J.P. (2003): MrBayes 3: Bayesian phylogenetic inference under mixed models. - Bioinformatics 19: 1572-1574.
Go to original source... - Saito, N. & Nei, M. (1987): The neighbor-joining method, a new method for reconstruction phylogenetic trees. - Molecular Biology and Evolution 4: 406-425.
- Sakayama, H. (2008): Taxonomy of Nitella (Charales, Charophyceae) based on comparative morphology of oospores and multiple DNA marker phylogeny using cultured material. - Phycological Research 56: 202-215.
Go to original source... - Sakayama, H.; Hara, Y. & Nozaki, H. (2004): Taxonomic re-examination of six species of Nitella (Charales, Charophyceae) from Asia, and phylogentical relationships within the genus based on rbcL and atpB gene sequences. - Phycologia 43: 91-104.
Go to original source... - Sakayama, H.; Kai, A.; Nishiyama, M.; Watanabe, M.M.; Kato, S.; Ito, M.; Nozaki, H. & Kawai, H. (2015): Taxonomy, morphology, and genetic variation of Nitella flexilis var. bifurcata (Charales, Characeae) from Japan. - Phycological Research 63: 159-166.
Go to original source... - Sakayama, H.; Kasai, F.; Nozaki, H.; Watanabe, M.M.; Kawachi, M.; Shigyo, M.; Nishihiro, J.; Washitani, I.; Krienitz, L. & Ito A.M. (2009): Taxonomic reexamination of Chara globularis (Charales, Charophyceae) from Japan based on oospore morphology and rbcL gene sequences, and the description of C. leptospora sp. nov. - Journal of Phycology 45: 917-927.
Go to original source... - Sakayama, H.; Miyaji, K.; Nagumo, T.; Kato, M.; Hara, Y. & Nozaki, H. (2005): Taxonomic reexamination of 17 species of Nitella subgenus Tieffallenia (Charales, Charophyceae) based on internal morphology of the oospore wall and multiple DNA marker sequences. - Journal of Phycology 41: 195-211.
Go to original source... - Sakayama, H.; Nozaki, H.; Kasaki, H. & Hara, Y. (2002): Taxonomic re-examination of Nitella (Charales, Charophyceae) from Japan, based on microscopical studies of oospore wall ornamentation and rbcL gene sequences. - Phycologia 41: 397-408.
Go to original source... - Sanders, E.R.; Karol, K.G. & McCourt, R.M. (2003): Occurrence of matK in a trnK group II intron in charophyte green algae and phylogeny of the Characeae. - American Journal of Botany 90: 628-633.
Go to original source... - Schneider, S.C.; Nowak, P.; Ammon, U. & Ballot, A. (2016): Species differentiation in the genus Chara (Charophyceae): considerable phenotypic plasticity occurs within homogenous genetic groups. - European Journal of Phycology 51: 282-293.
Go to original source... - Schneider, S.C.; Rodrigues, A.; Moe, T.F. & Ballot, A. (2015): DNA barcoding the genus Chara , molecular evidence recovers fewer taxa than the classical morphological approach. - Journal of Phycology 51: 367-380.
Go to original source... - Schneider, S.C.; Ziegler, C. & Melzer, A. (2006): Growth towards light as an adaptation to high light conditions in Chara branches. - New Phytologist 172: 83-91.
Go to original source... - StatSoft, Inc. (2010): STATISTICA (data analysis software system). Version 9.1. Tulsa, USA.
- Swofford, D.L. (2002): PAUP* - Phylogenetic Analysis Using Parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland, USA.
- Tanabe, A.S. (2011): Kakusan 4 and Aminosan, two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. - Molecular Ecology Resources 11: 914-921.
Go to original source... - Thompson, J.D.; Higgins, D.G. & Gibson, T.J. (1994): CLUSTAL W, Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. - Nucleic Acids Research 22: 4673-4680.
Go to original source... - Turmel, M.; Otis, C. & Lemieux, C. (2006): The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. - Molecular Biology and Evolution 23: 1324-1338.
Go to original source... - Urbaniak, J. (2009): Oospore variation in Nitella gracilis and Nitella mucronata (Charales, Charophyceae) from Poland. - Biologia 64: 252-260.
Go to original source... - Urbaniak, J. (2010): Analysis of morphological characters of Chara baltica, C. hispida, C. horrida and C. rudis from Europe. - Plant Systematics and Evolution 286: 209-221.
Go to original source... - Urbaniak, J. (2011a): An SEM and light microscopy study of the oospore wall ornamentation in Polish charophytes (Charales, Charophyceae) - genus Chara. - Nova Hedvigia 93: 1-28.
Go to original source... - Urbaniak, J. (2011b): An SEM study of the oospore wall ornamentation in Polish charophytes (Charales, Charophyceae) - genus Lychnothamnus, Nitella and Nitellopsis. - Nova Hedvigia 93: 537-549.
Go to original source... - Urbaniak, J. & Bla¾enèiæ, J. (2012): SEM study of oospore characteristics in endemic and endangered Balkan Charophytes. - Cryptogamie, Algologie 33: 277-288.
Go to original source... - Urbaniak, J. & Combik, M. (2013): Genetic and morphological data fail to differentiate Chara intermedia from C. baltica, or C. polyacantha and C. rudis from C. hispida. - European Journal of Phycology 48: 253-259.
Go to original source... - Urbaniak, J. & Combik, M. (2017): Taxonomic status of Chara tenuspina A. Br. (Streptophyta: Charales) based on LM morphology, matK, atpB and rbcL of cpDNA sequences. - Fottea 17: 20-33.
Go to original source... - Urbaniak, J. & G±bka, M. (2014): Polish Charophytes. An illustrated guide to identification. - 120 pp., Wydawnictwo Uniwersytetu Przyrodniczego we Wroc³awiu, Wroc³aw.
- Urbaniak, J.; Langangen, A. & Raam, J. (2012): Oospore Wall Ornamentation in the Genus Tolypella (Charales, Charophyceae). - Journal of Phycology 48: 1538-1545.
Go to original source... - Winter, U.; Soulie-Märsche, I. & Kirst, G.O. (1996): Effects of salinity on turgor pressure and fertility in Tolypella (Characeae). - Plant, Cell and Environment 19: 869-879.
Go to original source... - Vedder, F. (2004): Morphologie und Taxonomie rezenter und subfossiler Characeen-Oosporen aus der Ostsee. - Rostocker Meeresbiologishe Beitrage 13: 43-54.
- Wodniok, S.; Brinkmann, H.; Glöckner, G.; Heidel, A.J.; Philippe, H.; Melkonian, M. & Becker, B. (2011): Origin of land plants, do conjugating green algae hold the key? - BMC Evolutionary Biology 11: 104.
Go to original source... - Wood, R.D. (1962): New combinations and taxa in the revision of Characeae. - Taxon 11: 7-25.
Go to original source... - Wood, R.D. & Imahori, K.A. (1965): A revision of the Characeae. First part, Monograph of the Characeae. - 904 pp., J. Cramer Verlag, Weinheim.



