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Molecular evidence confirms the parasite Congracilaria babae (Gracilariaceae, Rhodophyta) from Malaysia

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Abstract

A phylogenetic study of two parasites found on the common host species Gracilaria salicornia from Japan and Malaysia based on nuclear, plastid, and mitochondrial molecular markers was conducted. The Japanese and Malaysian parasites were placed in the same cluster in the nuclear phylogenies inferred from the LSU rRNA gene and ITS region, supporting the monophyly of these parasites despite the slight anatomical variations observed. In addition to the molecular analyses, shared morphological and reproductive features including the lack of rhizoids, similar coloration to hosts, and the presence of deep spermatangial conceptacles supported the inclusion of both the Japanese and Malaysian parasites in Congracilaria babae. Phylogenetic analyses based on ITS sequences indicated that C. babae most likely evolved directly from its current host species, G. salicornia. C. babae was shown to be a member of Gracilaria sensu stricto along with its host. C. babae growing on G. salicornia is characterized by having plastid rbcL and mitochondrial cox1 gene sequences identical to those of its host, whereas the nuclear LSU rRNA gene and ITS region sequences are different from those of its host.

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References

  • Ashen JB, Goff LJ (2000) Molecular and ecological evidence for species specificity and coevolution in a group of marine algal-bacterial symbioses. Appl Environ Microbiol 6:3024–3030

    Article  Google Scholar 

  • Bellorin AM, Oliveira MC, Oliveira EC (2002) Phylogeny and systematic of the marine algal family Gracilariaceae (Gracilariales, Rhodophyta) based on small subunit rDNA and ITS sequences of Atlantic and Pacific species. J Phycol 38:551–563

    Article  CAS  Google Scholar 

  • Farr ER, Leussink JA, Stafleu FA (1979) Index nominum genericorum (Plantarum). 3 vols. Bohn, Scheltema and Holkema, Utrecht (Regnum Vegetabile vol. 100–102), pp 1896

  • Feldmann J, Feldmann G (1958) Recherches sur quelques floridées parasites. Rev Gén Bot 65:49–128

    Google Scholar 

  • Fredericq S, Hommersand MH (1990a) Diagnoses and key to the genera of the Gracilariaceae (Gracilariales, Rhodophyta). Hydrobiologia 204/205:173–178

    Article  Google Scholar 

  • Fredericq S, Hommersand MH (1990b) Morphology and systematics of Holmsella pachyderma (Pterocladiophilaceae, Gracilariales). Brit Phycol J 25:39–51

    Article  Google Scholar 

  • Fredericq S, Hommersand MH, Norris JN (1989) Morphological observations on the adelphoparasite Gracilariophila oryzoides (Gracilariales, Rhodophyta). Jpn J Phycol 37:167–179

    Google Scholar 

  • Freshwater DW, Rueness J (1994) Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33:187–194

    Article  Google Scholar 

  • Gavio B, Fredericq S (2002) Grateloupia turuturu (Halymeniaceae, Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora. Eur J Phycol 37:349–359

    Article  Google Scholar 

  • Geraldino PJL, Yang EC, Boo SM (2006) Morphology and molecular phylogeny of Hypnea flexicaulis (Gigartinales, Rhodophyta) from Korea. Algae 21:417–423

    Article  Google Scholar 

  • Gerung SG, Yamamoto H (2002) The taxonomy of parasitic genera growing on Gracilaria (Rhodophyta, Gracilariaceae). In: Abbott IA, Mcdermid KJ (eds) Taxonomy of Economic Seaweeds with reference to some Pacific species vol. VIII. California Sea Grant College Program, La Jolla, pp 209–213

  • Gerung GS, Terada R, Yamamoto H, Ohno M (1999) An adelphoparasite growing on Gracilaria edulis (Gracilariaceae, Rhodophyta) from Manado, Indonesia. In: Abbott IA (ed) Taxonomy of Economic seaweeds with reference to some Pacific species vol. VII. California Sea Grant College Program, La Jolla, pp 131–136

  • Goff LJ, Coleman AW (1987) Nuclear transfer from parasite to host: a new regulatory mechanism of parasitism. Ann NY Acad Sci 503:402–423

    Article  Google Scholar 

  • Goff LJ, Coleman AW (1995) The fate of parasite and host organelle DNA during cellular transformation of red algae by their parasites. Plant Cell 7:1899–1911

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Goff LJ, Moon DA, Coleman AW (1994) Molecular delineation of species and species relationships in the red algal agarophytes Gracilariopsis and Gracilaria (Gracilariales). J Phycol 30:521–537

    Article  CAS  Google Scholar 

  • Goff LJ, Moon DA, Nyvall P, Stache B, Mangin K, Zuccarello G (1996) The evolution of parasitism in the red algae: molecular comparisons of adelphoparasites and their hosts. J Phycol 32:297–312

    Article  CAS  Google Scholar 

  • Goff LJ, Ashen J, Moon D (1997) The evolution of parasites from their hosts: a case study in the parasitic red algae. Evolution 51:1068–1078

    Article  Google Scholar 

  • Guiry MD (1978) The importance of sporangia in the classification of the Florideophyceae. In: Irvine DEG, Price JH (eds) Modern approaches to the taxonomy of red and brown algae. Academic Press, London, pp 111–114

    Google Scholar 

  • Gurgel CFD, Fredericq S (2004) Systematics of the Gracilariaceae (Gracilariales, Rhodophyta): a critical assessment based on rbcL sequence analyses. J Phycol 40:138–159

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41:95–98

    CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York, p 523

    Google Scholar 

  • Kongkittayapun N, Chirapart A (2011) Morphometric and molecular analysis of Gracilaria salicornia and its adelphoparasite in Thailand. ScienceAsia 37:6–16

    Article  CAS  Google Scholar 

  • Kurihara A, Abe T, Tani M, Sherwood AR (2010) Molecular phylogeny and evolution of red algal parasites: a case study of Benzaitenia, Janczewskia and Ululania (Ceramiales). J Phycol 46:580–590

    Article  CAS  Google Scholar 

  • Le Gall L, Dalen JL, Saunders GW (2008) Phylogenetic analyses of the red algal order Rhodymeniales supports recognition of the Hymenocladiaceae fam. nov. Fryeellaceae fam. nov., and Neogastroclonium gen. nov. J Phycol 44:1556–1571

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer v1.5, Available free from http://beast.bio.ed.ac.uk/Tracer

  • Robba L, Russell SJ, Barker GL, Brodie J (2006) Assessing the use of the mitochondrial cox1 marker for use in DNA barcoding of red algae (Rhodophyta). Am J Bot 93:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos T R Soc B 360:1879–1888

    Article  CAS  Google Scholar 

  • Schneider CW, Wynne MJ (2007) A synoptic review of the classification of red algal genera a half century after Kylin’s ‘Die Gattungen der Rhodophyceen”. Bot Mar 50:197–249

    Google Scholar 

  • Sherwood AR, Kurihara A, Conklin KY, Sauvage T, Presting GG (2010) The Hawaiian Rhodophyta Biodiversity Survey (2006–2010): a summary of principal findings. BMC Plant Biol 10:258–287

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sturch HH (1926) Choreocolax polysiphoniae Reinsch. Ann Bot 40:585–605

    Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Sinauer Associates, Sunderland

    Google Scholar 

  • Tanabe AS (2007) KAKUSAN: a computer program to automate the selection of a nucleotide substitution model and the configuration of a mixed model on multilocus data. Mol Ecol Notes 7:962–964

    Article  CAS  Google Scholar 

  • Terada R, Yamamoto H, Maraoka D (1999) Observations on an adelphoparasite growing on Gracilaria salicornia from Thailand. In: Abbott IA (ed) Taxonomy of Economic seaweeds with reference to some Pacific species vol. VII. California Sea Grant College Program, La Jolla, pp 121–130

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Weber-van Bosse A (1928) Liste des algues du Siboga. IV. Rhodophyceae, troisieme partie: Gigartinales et Rhodymeniales. Siboga-Expeditie Monographie, E. J. Brill, Leiden, pp 393–533

  • Wilson HL (1910) Gracilariophila, a new parasite on Gracilaria confervoides. Univ Calif Publ Bot 4:75–84

    Google Scholar 

  • Yamamoto H (1986) Congracilaria babae gen. et sp. nov. (Gracilariaceae), an adelphoparasite growing on Gracilaria salicornia of Japan. Bull Fac Fish Hokkaido Univ 37:281–290

    Google Scholar 

  • Yamamoto H (1991) Observation on the adelphoparasite Congracilaria babae Yamamoto (Gracilariaceae, Rhodophyta) of the Philippines. Jpn J Phycol 39:381–384

    Google Scholar 

  • Yamamoto H, Phang SM (1997) An adelphoparasitic alga growing on Gracilaria salicornia from Malaysia. In: Abbott IA (ed) Taxonomy of Economic Seaweeds with reference to some Pacific and Caribbean species vol. VI. California Sea Grant College Program, La Jolla, pp 91–96

  • Yang EC, Kim MS, Geraldino PJL, Sahoo D, Shin JA, Boo SM (2008) Mitochondrial cox1 and plastid rbcL genes of Gracilaria vermiculophylla (Gracilariaceae, Rhodophyta). J Appl Phycol 20:161–168

    Article  CAS  Google Scholar 

  • Yow YY, Lim PE, Phang SM (2011) Genetic diversity of Gracilaria changii (Gracilariaceae, Rhodophyta) from west coast, Peninsular Malaysia based on mitochondrial cox1 gene analysis. J Appl Phycol 23:219–226

    Article  Google Scholar 

  • Zuccarello GC, West JA (2006) Molecular phylogeny of the subfamily Bostrychioideae (Ceramiales, Rhodophyta): subsuming Stictosiphonia and highlighting polyphyly in species of Bostrychia. Phycologia 45:24–36

    Article  Google Scholar 

  • Zuccarello GC, West JA (2011) Insights into evolution and speciation in the red alga Bostrychia: 15 years of research. Algae 26:21–32

    Article  Google Scholar 

  • Zuccarello GC, Moon D, Goff LJ (2004) A phylogenetic study of parasitic genera placed in the family Choreocolacaceae (Rhodophyta). J Phycol 40:937–945

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Madam Patricia Loh for the technical assistance in preparing sections of tissue using paraffin method. This study was funded in part by the Postgraduate Research Fund from University of Malaya (PS275/2009C and PV082/2011B), Fundamental Research Grant Scheme (FP033-2012A) and MoHE-HIR grant (H-50001-00-A000025) from the Ministry of Higher Education (MOHE), Malaysia and a grant awarded by the Malaysia Toray Science Foundation (MTSF1052-2010).

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Authors and Affiliations

  1. Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Poh-Kheng Ng, Phaik-Eem Lim & Siew-Moi Phang

  2. Institute of Ocean and Earth Sciences, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Poh-Kheng Ng, Phaik-Eem Lim & Siew-Moi Phang

  3. Takehara Fisheries Research Station, Center for Education and Research of Field Science, Hiroshima University, Minato-machi 5-8-1, Takehara, Hiroshima, 725-0024, Japan

    Aki Kato

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  1. Poh-Kheng Ng
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Correspondence to Phaik-Eem Lim.

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Ng, PK., Lim, PE., Kato, A. et al. Molecular evidence confirms the parasite Congracilaria babae (Gracilariaceae, Rhodophyta) from Malaysia. J Appl Phycol 26, 1287–1300 (2014). https://doi.org/10.1007/s10811-013-0166-5

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