Single locus microsatellites in Gracilariales (Rhodophyta): High level of genetic variability within Gracilaria gracilis and conservation in related species

Journal of Phycology

Volumn 33, Issue 5, 1997, Pages 868-880

  Wattier, Rémi ^a   Dallas, John F ^a,c   Destombe, Christophe ^b   Saumitou Laprade, Pierre ^b   Valero, Myriam ^b  

^a CNRS   (France)

^b UNIV LILLE   (France)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Allelic diversity; Genetic markers; Gracilaria sp.; Gracilariopsis sp.; Haplo diploid life cycle; Microsatellite; Population; RDNA ITS

Indexed keywords

ALGAE; GRACILARIA GRACILIS; GRACILARIA SP.; GRACILARIACEAE; GRACILARIALES; GRACILARIOPSIS; GRACILARIOPSIS SP.; RHODOPHYTA;

EID: 0030846890     PISSN: 00223646     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0022-3646.1997.00868.x     Document Type: Article

References (80)

1. Akkaya, M. S., Bhagwat, A. A. & Cregan, P. B. 1992. Length polymorphisms of simple sequence repeat DNA in soybean. Genetics, 132:1131-9.
2. Angers, B. & Bernatchez, L. 1997. Complex evolution of a salmonid microsatellite locus and its consequences in inferring allelic divergence from size information. Mol. Biol. Evol. 14: 230-8.
3. Ashley, M. V. & Dow, B. D. 1994. The use of microsatellite analysis in population biology: background, methods and potential applications. In Schierwater, B., Streit, B., Wagner, G. P. & DeSalle, R. [Eds.] Molecular Ecology and Evolution: Approaches and Applications. Birkhäuser Verlag, Basel, pp. 185-201.
4. Becker, J. & Heun, M. 1995. Barley microsatellites: allele variation and mapping. Plant Mol. Biol. 27:835-45.
5. Beckmann, J. S. & Weber, J. L. 1992. Survey of human and rat microsatellites. Genomics 12:627-31.
6. Bird, C. J. 1995. A review of recent taxonomic concepts and developments in the Gracilariacea (Rhodophyta). J. Appl. Phycol. 7:255-67.
7. Bird, C. J., Nelson, W. A., Rice, E. L., Ryan, K. G. & Villemur, R. 1990. A critical comparison of Gracilaria chilensis and G. sordida (Rhodophyta, Gracilariales). J. Appl. Phycol. 2:375-82.
8. Bird, C. J., Ragan, M. A., Critchley, A. T., Rice, E. L. & Gutell, R. R. 1994. Molecular relationships among the Gracilariaceae (Rhodophyta): further observations on some undertermined species. Eur. J. Phycol. 29:195-202.
9. Bird, C. J. & Rice, E. L. 1990. Recent approaches to the taxonomy of the Gracilariaceae (Gracilariales, Rhodophyta) and the Gracilaria verrucosa problem. Hydrobiologia 204/205:111-8.
10. Bird, C. J., Rice, E. L., Murphy, C. A. & Ragan, M. A. 1992. Phylogenetic relationships in the Gracilariales (Rhodophyta) as determined by 18S rDNA sequences. Phycologia 31:510-22.
11. Breen, M., Downs, P., Irvin, Z. & Bell, K. 1994. Intrageneric amplification of horse microsatellite markers with emphasis on the Przewalski's horse (E. przewalskii). Anim. Genet. 25:401-5.
12. Broun, P. & Tanksley, S. D. 1996. Characterization and genetic mapping of simple repeat sequences in the tomato genome. Mol. Gen. Genet. 250:39-49.
13. Charlesworth, B., Snlegowski, P. & Stephan, W. 1994. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215-20.
14. Coltman, D. W., Don Bowen, W. & Wright, J. M. 1996. PCR primers for harbour seal (Phoca concolour) microsatellites amplify polymorphic loci in other pinniped species. Mol. Ecol. 5:161-3.
15. Coyer, A. C., Robertson, D. L. & Alberte, R. S. 1995. Genetic variability and parentage in Macrocystis pyrifera (Phaephyceae) using multi-locus DNA fingerprinting. J. Phycol. 31:819-23.
16. Dellaporta, S. L., Wood, V. P. & Hicks, J. B. 1983. A plant DNA mini-preparation: version II. Plant Mol. Biol. Rep. 1:19-21.
17. Destombe, C. & Douglas, S. E. 1991. Rubisco spacer sequence divergence in the rhodophyte alga Gracilaria verrucosa and closely related species. Curr. Genet. 19:395-8.
18. Engel, S. R., Linn, R. A., Taylor, J. E. & Davis, S. K. 1996. Conservation of microsatellite loci across species of artiodactyls: implications for population studies. J. Mammal. 77:504-18.
19. Estoup, A., Taillez, C., Solignac, M. & Cornuet, J. M. 1995. Size homoplasy and mutational processes of interrupted microsatellites in two bee species, Apis mellifera and Bombus terrestris (Apidae). Mol Biol. Evol. 12:1074-1084.
20. FitzSimmons, N. N., Craig, M. & Moore, S. S. 1995. Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Mol. Biol. Evol. 12:432-40.
21. Fredericq, S. & Hommersand, M. H. 1989a. Proposal of the gracilariales Ord, Nov. (Rhodophyta) based on analysis of the reproductive development of Gracilaria verrucosa. J. Phycol. 25: 213-27.
22. _ 1989b. Comparative morphology and taxonomic status of Gracilariopsis (Gracilariales, Rhodophyta). J. Phycol. 25:228-41.
23. Fredholm, M. & Wintero, A. K. 1995. Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm. Genome 6:11-8.
24. Freimer, N. B. & Slatkin, M. 1996. Microsatellites: Evolution and Mutational Processes. Variation in the Human Genome. John Wiley & Sons, New York.
25. Gacy, A. M., Goellner, G., Juranic, N., Macura, S. & McMurray, C. 1995. Trinucleotide repeats that expand in human diease form hairpin structures in vitro. Cell 81:533-40.
26. Godin, J., Destombe, C. & Maggs, C. A. 1993. Unusual chromosome number of Gracilaria verrucosa (Gracilariales, Rhodophyta) in the Cape Gris-Nez area, Northern France. Phycologia 32:291-4.
27. Goff, L. J. & Moon, D. A. 1993. PCR amplification of nuclear and plastid genes from algal herbarium specimens and algal spores. J. Phycol. 29:381-4.
28. Goff, L. J., Moon, D. A. & Coleman, A. W. 1994. Molecular delineation of species and species relationships in the red algal agarophytes Gracilariopsis Gracilaria (Gracilariales). J. Phycol. 30:521-37.
29. Goldstein, D. B., Linares, A. R., Cavalli-Sforza, L. L. & Feldman, M. W. 1995. An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463-71.
30. Guiry, M. D. 1992. Species concepts in marine red algae. In Round, F. E. & Chapman, D. J. [Eds.] Progress in Phycological Research. Biopress Ltd., Bristol, U.K. pp. 251-78.
31. Hadrys, H., Balick, M. & Sohierwater, B. 1992. Applications of random amplified polymorphic DNA (RAPD) in molecular ecology. Mol. Ecol. 1:55-63.
32. Innes, D. J. 1984. Genetic differentiation among populations of marine algae. Helgolander Meeresuntersuchungen 38:401-17.
33. Jarne, P. & Lagoda, P. J. L. 1996. Microsatellites, from molecules to populations and back. Trends Ecol. Evol. 11:424-8.
34. Jeffreys, A. J. & Pena, S. D. J. 1993. Brief introduction to human DNA fingerprinting. In Pena, S. D. J., Chakraborty, R., Epplen, J. T. & Jeffreys, A. J. [eds.] DNA Fingerprinting : State of the Science. Birkhäuser. Basel-Boston-Berlin, pp. 1-20.
35. Kapraun, D. F. 1993. Karyology and cytometric estimation of nuclear DNA content variation in Gracilaria, Gracilariopsis and Hydropuntia (Gracilariales, Rhodophyta). Eur. J. Phycol. 28: 253-60.
36. Kemp, S. J., Hishida, O., Wambugu, J., Rink, A., Longeri, M. L., Ma, R. Z., Da, Y., Lewin, H. A., Barendse, W. & Teale, A. J. 1995. A panel of polymorphic bovine, ovine and caprine microsatellite markers. Anim. Genet. 26:299-306.
37. Kijas, J. M. H., Fowler, J. C. S. & Thomas, M. R. 1995. An evaluation of sequence tagged microsatellite site markers for genetic analysis within Citrus and related species. Genome 38: 349-55.
38. Kimura, M. & Crow, J. F. 1964. The number of alleles that can be maintained in a finite population. Genetics 49:725-38.
39. Kresovich, S., Szewc-McFadden, A. K., Bliek, S. M. & McFerson, J. R. 1995. Abundance and characterization of simple-sequence repeats (SSRs) isolated from a size fractionated genomic library of Brassua napus L. (rapeseed). Theor. Appl. Genet. 91:206-11.
40. Levinson, G. & Gutman, G. A. 1987. High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K12. Nucl. Acids Res. 15:5323-38.
41. Litt, M. & Luty, J. A. 1989. A hypervariable microsatellite revealed by in vitro amplification of a di-nucleotide repeat within the cardiac muscle actin gene. Am. J. Hum. Genet. 44:397-401.
42. Lu, T. T. & Williams, S. L. 1994. Genetic diversity and genetic structure in the brown alga Halidrys dioica (Fucales: Cystoseiraceae) in southern California. Mar. Biol. 121:363-71.
43. Manhart, J. R. & McCourt, R. M. 1992. Molecular data and species concepts in the algae. J. Phycol. 28:730-7.
44. Menotti-Raymond, M. A. & O'Brien, S. J. 1995. Evolutionary conservation of ten microsatellite loci in four species of Felidae. J. Hered. 86:319-22.
45. Moore, S. S., Evans, D., Byrne, K., Barker, J. S. F., Tan, S. G., Vankan, D. & Hetze, D. J. S. 1995. A set of polymorphic DNA microsatellites useful in swamp and river buffalo (Bubalus bubalis). Anim. Genet. 26:355-9.
46. Moore, S. S., Sargeant, L. L., King, T. J., Mattick, J. S., Georges, M. & Hetzel, D. J. S. 1991. The conservation of di-nucleotide microsatellites among mammalian genomes allows the use of heterologous PCR primer pairs in closely related species. Genomics 10:654-60.
47. Morgante, M. & Olivieri, A. M. 1993. PCR-amplified microsatellites as markers in plant genetics. Plant J. 3:175-82.
48. Murray, V., Monchawin, C. & England, P. R. 1993. The determination of the sequences present in the shadow bands of a di-nucleotide repeat PCR. Nucl. Acids Res. 21:2395-8.
49. Ohta, T. & Kimura, M. 1973. A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet. Res. (Cambridge) 22:201-4.
50. Olsen, J. L. 1990. Nucleic acids in algal systematics. J. Phycol. 26: 209-14.
51. Pemberton, J. M., Slate, J., Bancroft, D. R. & Barrett, J. A. 1995. Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol. Ecol. 4:249-52.
52. Primmer, C. R., Ellegren, H., Saino, N. & Möller, A. P. 1996a. Directional evolution in germline microsatellite mutations. Nat. Genet. 13:391-2.
53. Primmer, C. R., Möller, A. P. & Ellegren, H. 1996b. A wide-range survey of cross-species microsatellite amplification in birds. Mol. Ecol. 5:365-78.
54. Primmer, C. R., Möller, A. P. & Ellegren, H. 1996c. New microsatellites from the pied flycatcher Ficedula hypoleuca and the swallow Hirundella rustica genomes. Hereditas 124:281-3.
55. Queller, D. C., Strassmann, J. E. & Hughes, C. R. 1993. Microsatellites and kinship. Trends Ecol. Evol. 8:285-8.
56. Rassmann, K., Schlötterer, C. & Tautz, D. 1991. Isolation of simple-sequence loci for use in polymerase chain reaction-based DNA fingerprinting. Electrophoresis 12:113-8.
57. Raymond, M. & Rousset, F. 1995. Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86:248-9.
58. Rice, E. L. & Bird, C. 1990. Relationships among geographically distant populations of Gracilaria verrucosa (Gracilariales, Rhodophyta) and related species. Phycologia 29:501-10.
59. Rico, C., Rico, I. & Hewitt, G. 1996. 470 million years of conservation of microsatellite loci among fish species. Proc. Royal Soc. London B 263:549-57.
60. Sambrook, J., Fritsch, E. F. & Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
61. Schlötteren C., Amos, B. & Tautz, D. 1991. Conservation of polymorphic simple sequence loci in cetacean species. Nature 354:63-5.
62. Schlötterer, C. & Pemberton, J. 1994. The use of microsatellites for genetic analysis of natural populations. In Schierwater, B., Streit, B., Wagner, G. P. & DeSalle, R. [Eds.] Molecular Ecology and Evolution: Approaches and Applications. Birkhäuser Verlag, Basel, pp. 203-14.
63. Scholfield, C. I., Gacesa, P., Price, J. H., Russell, S. J. & Bhoday, R. 1991. Restriction fragment length polymorphisms of enzymically-amplified small-subunit rRNA-coding regions from Gracilaria and Gracilariopsis (Rhodophyta) - a rapid method for assessing 'species' limits. J. Appl. Phycol. 3:329-34.
64. Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457-62.
65. Sosa, P. A., Cabrera-Pérez, M. A. & Garcia-Reina, G. 1996. Genetic variation of Gracilaria cervicornis (Rhodophyta) gametophytes from the Canary Islands. Eur. J. Phycol. 31:143-7.
66. Sosa, P. A. & Garcia-Reina, G. 1991. Electrophoresis in seaweeds. In Garcia-Reina, G. & Pedersen, M. [Eds.] Seaweed Cellular Biotechnology, Physiology and Intensive Cultivation. Las Palmas, Canary Island, Spain COST 48, pp. 257-64.
67. Sosa, P. A. & Oliveira, M. C. 1992. DNA extraction from macroalgae. Appl. Phycol. Forum 9:7-9.
68. Steentoft, M., Irvine, L. M. & Farnham, W. F. 1995. Two terete species of Gracilaria and Gracilariopsis (Gracilariales, Rhodophyta) in Britain. Phycologia 34:113-27.
69. Tautz, D. 1989. Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucl. Acids Res. 17: 6463-71.
70. Tautz, D. & Renz, M. 1984. Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nurl. Acids Res. 12:4127-38.
71. Valdes, A. M., Slatkin, M. & Freimer, N. B. 1993. Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133:737-49.
72. van Oppen, M. J. H., Klerk, H., de Graaf, M., Stam, W. T. & Olsen, J. L. 1996a. Assessing the limits of random amplified polymorphic DNAs (RAPDs) in seaweed biogeography. J. Phycol. 32:433-44.
73. van Oppen, M. J. H., Klerk, H., Olsen, J. L. & Stam, W. T. 1996b. Hidden diversity in the marine algae: some examples of genetic variation below the species level. J. Mar. Biol. Assoc. U.K. 76:239-42.
74. Wang, Z., Weber, J. L., Zhong, G. & Tanksley, S. D. 1994. Survey of plant short tandem DNA repeats. Theor. Appl. Genet. 88:1-6.
75. Weber, J. L. 1990. Informativeness of human (dC-dA)n.(dG-dT)n polymorphisms. Genomics 7:524-30.
76. Weber, J. L. & May, P. E. 1989. Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. Am. J. Hum. Genet. 44:388-96.
77. Weissenbach, J., Gyapay, G., Dib, C., Vignal, A., Morissette, J., Millasseau, P., Vaysseix, G. & Lathrop, M. 1992. A second-generation linkage map of the human genome. Nature 359: 794-801.
78. Williams, S. L. & di Fiori, R. E. 1996. Genetic diversity and structure in Pelvetia fastigiata. (Phaephyta: Fucales): does a small effective neighborhood size explain fine-scale genetic structure. Mar. Biol. 126:371-82.
79. Wu, K.-S. & Tanksley, S. D. 1993. Abundance, polymorphism and genetic mapping of microsatellites in rice. Mol. Gen. Genet. 241:225-35.
80. Yang, G. P., Saghai Maroof, M. A., Xu, C. G., Zhang, Q. & Biyashev, R. M. 1994. Comparative analysis of microsatellite DNA polymorphism in landraces and cultivars of rice. Mol. Gen. Genet. 245:187-94.