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Insights into evolution and speciation in the red alga Bostrychia: 15 years of research

  • Received : 2011.01.22
  • Accepted : 2011.02.14
  • Published : 2011.03.15

Abstract

Studies of the red algal genus Bostrychia over the last 15 years have made it a model system for many evolutionary processes within red algal species. The combination of newly developed, or first employed methods, in red algal species studies has made Bostrychia a pioneer genus in intraspecific studies. Bostrychia was the first genus in which a mitochondrial marker was used for intraspecific red algal phylogeny, and the first for which a 3-genome phylogeny was undertaken. The genus was the first red alga used to genetically show maternal plastid and mitochondria inheritance, and also to show correlation between cryptic species (genetically divergent intraspecific lineages) and reproductive incompatibility. The chemotaxonomic use, and physiological function of osmolytes, has also been extensively studied in Bostrychia. Our continuous studies of Bostrychia also highlight important aspects in algal species studies. Our worldwide sampling, and resampling in certain areas, show that intensive sampling is needed to accurately assess the genetic diversity and therefore phylogeographic history of algal species, with increased sampling altering evolutionary hypotheses. Our studies have also shown that long-term morphological character stability (stasis) and character convergence can only be correctly assessed with wide geographic sampling of morphological species. While reproductive incompatibility of divergent lineages supports the biological species nature of these lineages, reproductive incompatibility is also seen between isolates with little genetic divergence. It seems that reproductive incompatibility may evolve quickly in red algae and the unique early stages of fertilization (e.g., gametes covered by walls, active movement of spermatium nuclei to the distant egg nucleus), also well investigated in Bostrychia,. may be key to our understanding of this process.

Keywords

References

  1. Alvarez, I. & Wendel, J. F. 2003. Ribosomal ITS sequences and plant phylogenetic inference. Mol. Phylogenet. Evol. 29:417-434. https://doi.org/10.1016/S1055-7903(03)00208-2
  2. Bakker, F. T., Breman, F. & Merckx, V. 2006. DNA sequence evolution in fast evolving mitochondrial DNA nad1 exons in Geraniaceae and Plantaginaceae. Taxon 55:887-896. https://doi.org/10.2307/25065683
  3. Bown, P., Plumb, J., Sanchez-Baracaldo, P., Hayes, P. K. & Brodie, J. 2003. Sequence heterogeneity of green (Chlorophyta) endophytic algae associated with a population of Chondrus crispus (Gigartinaceae, Rhodophyta). Eur. J. Phycol. 38:153-163. https://doi.org/10.1080/0967026031000095525
  4. Brodie, J. & Zuccarello, G. C. 2007. Systematics of the species-rich algae: red algal classification, phylogeny and speciation. In Hodkinson, T. R. & Parnell, J. A. N. (Eds.) Reconstructing the Tree of Life: Taxonomy and Systematics of Species Rich Taxa. CRC Press, Boca Raton, pp. 323-336.
  5. Broom, J. E. S., Farr, T. J. & Nelson, W. A. 2004. Phylogeny of the Bangia flora of New Zealand suggests a southern origin for Porphyra and Bangia (Bangiales, Rhodophyta). Mol. Phylogenet. Evol. 31:1197-1207. https://doi.org/10.1016/j.ympev.2003.10.015
  6. Butterfield, N. J. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic / Neoproterozoic radiation of eukaryotes. Paleobiology 26:386-404. https://doi.org/10.1666/0094-8373(2000)026<0386:BPNGNS>2.0.CO;2
  7. Choi, S. -J., Park, E. -J., Endo, H., Kitade, Y. & Saga, N. 2008. Inheritance pattern of chloroplast and mitochondrial genomes in artificial hybrids of Porphyra yezoensis (Rhodophyta). Fish. Sci. 74:822-829. https://doi.org/10.1111/j.1444-2906.2008.01594.x
  8. Cock, J. M., Coelho, S. M., Brownlee, C. & Taylor, A. R. 2010. The Ectocarpus genome sequence: insights into brown algal biology and the evolutionary diversity of the eukaryotes. New Phytol. 188:1-4. https://doi.org/10.1111/j.1469-8137.2010.03454.x
  9. Coyne, J. A. & Orr, H. A. 2004. Speciation. Sinauer Associates, Sunderland, MA, 545 pp.
  10. Destombe, C. & Douglas, S. E. 1991. Rubisco spacer sequence divergence in the rhodophyte alga Gracilaria verrucosa and closely related species. Curr. Genet. 19:395-398. https://doi.org/10.1007/BF00309601
  11. Destombe, C. & Douglas, S. E. 1992. Erratum: rubisco spacer sequence divergence in the rhodophyte alga Gracilaria verrucosa and closely related species. Curr. Genet. 22:173. https://doi.org/10.1007/BF00351479
  12. Eggert, A. & Karsten, U. 2010. Low molecular weight carbohydrates in red algae: an ecophysiological and biochemical perspective. In Seckbach, J. & Chapman, D. J. (Eds.) Red Algae in the Genomic Age, Vol. 13. Springer Academic Press, Dordrecht, pp. 443-456.
  13. Eggert, A., Raimund, S., Van den Daele, K. & Karsten, U. 2006. Biochemical characterization of mannitol metabolism in the unicellular red alga Dixoniella grisea (Rhodellophyceae). Eur. J. Phycol. 41:405-413. https://doi.org/10.1080/09670260600919831
  14. Falkenberg, P. 1901. Die Rhodomelaceen des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna und Flora des Golfes von Neapel, Monographie 26. Friedlander, Berlin, 754 pp.
  15. Faugeron, S., Martinez, E. A., Correa, J. A., Cardenas, L., Destombe, C. & Valero, M. 2004. Reduced genetic diversity and increased population differentiation in peripheral and overharvested populations of Gigartina skottsbergii (Rhodophyta, Gigartinales) in southern Chile. J. Phycol. 40:454-462. https://doi.org/10.1111/j.1529-8817.2004.03114.x
  16. Faugeron, S., Valero, M., Destombe, C., Martínez, E. A. & Correa, J. A. 2001. Hierarchical spatial structure and discriminant analysis of genetic diversity in the red alga Mazzaella laminarioides (Gigartinales, Rhodophyta). J. Phycol. 37:705-716. https://doi.org/10.1046/j.1529-8817.2001.01072.x
  17. Freshwater, D. W., Fredericq, S., Butler, B. S., Hommersand, M. H. & Chase, M. W. 1994. A gene phylogeny of the red algae (Rhodophyta) based on plastid rbcL. Proc. Natl. Acad. Sci. U. S. A. 91:7281-7285. https://doi.org/10.1073/pnas.91.15.7281
  18. Goff, L. J. 1982. The biology of parasitic red algae. In Round, F. E. & Chapman, D. J. (Eds.) Progress in Phycological Research, Vol. 1. Elsevier Biomedical Press, New York, pp. 289-369.
  19. Goff, L. J. & Coleman, A. W. 1985. The role of secondary pit connections in red algal parasitism. J. Phycol. 21:483-508.
  20. Goff, L. J., Moon, D. A. & Coleman, A. W. 1994. Molecular delineation of species and species relationships in the red algal agarophytes Gracilariopsis and Gracilaria (Gracilariales). J. Phycol. 30:521-537. https://doi.org/10.1111/j.0022-3646.1994.00521.x
  21. Goff, L. J. & Zuccarello, G. 1994. The evolution of parasitism in red algae: cellular interactions of adelphoparasites and their hosts. J. Phycol. 30:695-720. https://doi.org/10.1111/j.0022-3646.1994.00695.x
  22. Haag, C. R. & Ebert, D. 2004. A new hypothesis to explain geographic parthenogenesis. Ann. Zool. Fenn. 41:539-544.
  23. Harper, J. T. & Saunders, G. W. 2001. The application of sequences of the ribosomal cistron to the systematics and classification of the florideophyte red algae (Florideophyceae, Rhodophyta). Cah. Biol. Mar. 42:25-38.
  24. Hommersand, M. H. & Fredericq, S. 1990. Sexual reproduction and cystocarp development. In Cole, K. M. & Sheath, R. G. (Eds.) Biology of the Red Algae. Cambridge University Press, Cambridge, pp. 305-345.
  25. Iomini, C., Till, J. E. & Dutcher, S. K. 2009. Genetic and phenotypic analysis of flagellar assembly mutants in Chlamydomonas reinhardtii. Methods Cell Biol. 93:121-143. https://doi.org/10.1016/S0091-679X(08)93007-7
  26. Karsten, U., Barrow, K. D., Nixdorf, O., West, J. A. & King, R. J. 1997. Characterization of mannitol metabolism in the mangrove red alga Caloglossa leprieurii (Montagne) J. Agardh. Planta 201:173-178.
  27. Karsten, U., Bock, C. & West, J. A. 1995a. $^{13}C$-NMR spectroscopy as a tool to study organic osmolytes in the mangrove red algal genera Bostrychia and Stictosiphonia (Ceramiales). Phycol. Res. 43:241-247. https://doi.org/10.1111/j.1440-1835.1995.tb00030.x
  28. Karsten, U., Bock, C. & West, J. A. 1995b. Low molecular weight carbohydrate patterns in geographically different isolates of the eulittoral red alga Bostrychia tenuissima from Australia. Bot. Acta. 108:321-326. https://doi.org/10.1111/j.1438-8677.1995.tb00501.x
  29. Karsten, U., Koch, S., West, J. A. & Kirst, G. O. 1994a. The intertidal red alga Bostrychia simpliciuscula Harvey ex J. Agardh from a mangrove swamp in Singapore: acclimation to light and salinity. Aquat. Bot. 48:313-323. https://doi.org/10.1016/0304-3770(94)90023-X
  30. Karsten, U., Koch, S., West, J. A. & Kirst, G. O. 1996. Physiological responses of the eulittoral macroalga Stictosiphonia hookeri (Rhodomelaceae, Rhodophyta) from Argentina and Chile: salinity, light and temperature acclimation. Eur. J. Phycol. 31:361-368. https://doi.org/10.1080/09670269600651591
  31. Karsten, U., West, J. A. & Ganesan, E. K. 1993. Comparative physiological ecology of Bostrychia moritziana (Ceramiales, Rhodophyta) from freshwater and marine habitats. Phycologia 32:401-409. https://doi.org/10.2216/i0031-8884-32-6-401.1
  32. Karsten, U., West, J. A. & Zuccarello, G. 1992. Polyol content of Bostrychia and Stictosiphonia (Rhodomelaceae, Rhodophyta) from field and culture. Bot. Mar. 35:11-19. https://doi.org/10.1515/botm.1992.35.1.11
  33. Karsten, U., West, J. A., Zuccarello, G. C., Engbrodt, R., Yokoyama, A., Hara, Y. & Brodie, J. 2003. Low molecular weight carbohydrates of the Bangiophycidae (Rhodophyta). J. Phycol. 39:584-589. https://doi.org/10.1046/j.1529-8817.2003.02192.x
  34. Karsten, U., West, J. A., Zuccarello, G. & Kirst, G. O. 1994b. Physiological ecotypes in the marine red alga Bostrychia radicans (Ceramiales, Rhodophyta) from the east coast of the USA. J. Phycol. 30:174-182. https://doi.org/10.1111/j.0022-3646.1994.00174.x
  35. Karsten, U., West, J. A., Zuccarello, G. C., Nixdorf, O., Barrow, K. D. & King, R. J. 1999. Low molecular weight carbohydrate patterns in the Bangiophyceae (Rhodophyta). J. Phycol. 35:967-976. https://doi.org/10.1046/j.1529-8817.1999.3550967.x
  36. Kim, G. H., Shim, J. B., Klochkova, T. A., West, J. A. & Zuccarello, G. C. 2008. The utility of proteomics in algal taxonomy: Bostrychia radicans / B. moritziana (Rhodomelaceae, Rhodophyta) as a model study. J. Phycol. 44:1519-1528. https://doi.org/10.1111/j.1529-8817.2008.00592.x
  37. King, R. J. & Puttock, C. F. 1989. Morphology and taxonomy of Bostrychia and Stictosiphonia (Rhodomelaceae / Rhodophyta). Aust. Syst. Bot. 2:1-73. https://doi.org/10.1071/SB9890001
  38. Knowlton, N. & Weigt, L. A. 1998. New dates and new rates for divergence across the Isthmus of Panama. Proc. R. Soc. Lond. Series B Biol. Sci. 265:2257-2263. https://doi.org/10.1098/rspb.1998.0568
  39. Kremer, B. P. 1976. Distribution of alditols in the genus Bostrychia. Biochem. Syst. Ecol. 4:139-141. https://doi.org/10.1016/0305-1978(76)90027-2
  40. Kugrens, P. & West, J. A. 1972. Ultrastructure of spermatial development in the parasitic red algae Levringiella gardneri and Erythrocystis saccata. J. Phycol. 8:331-343.
  41. Markmann, M. & Tautz, D. 2005. Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal RNA signature sequences. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:1917-1924. https://doi.org/10.1098/rstb.2005.1723
  42. Muller, D. G. & Eichenberger, W. 1995. Crossing experiments, lipid-composition, and the species concept in Ectocarpus siliculosus and E. fasciculatus (Phaeophyceae, Ectocarpales). J. Phycol. 31:173-176. https://doi.org/10.1111/j.0022-3646.1995.00173.x
  43. Muller, D. G., Sengco, M., Wolf, S., Brautigam, M., Schmid, C. E., Kapp, M. & Knippers, R. 1996. Comparison of two DNA viruses infecting the marine brown algae Ectocarpus siliculosus and E. fasciculatus. J. Gen. Virol. 77:2329-2333. https://doi.org/10.1099/0022-1317-77-9-2329
  44. Nishimura, Y. 2010. Uniparental inheritance of cpDNA and the genetic control of sexual differentiation in Chlamydomonas reinhardtii. J. Plant Res. 123:149-162. https://doi.org/10.1007/s10265-009-0292-y
  45. Palumbi, S. R., Cipriano, F. & Hare, M. P. 2001. Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55:859-868. https://doi.org/10.1554/0014-3820(2001)055[0859:PNGCFM]2.0.CO;2
  46. Pedroche, F. F., West, J. A., Zuccarello, G. C., Sentíes, A. & Karsten, U. 1995. Marine red algae of the mangroves in southern Pacific México and Pacific Guatemala. Bot. Mar. 38:111-119. https://doi.org/10.1515/botm.1995.38.1-6.111
  47. Pickett-Heaps, J. D. & West, J. 1998. Time-lapse video observations on sexual plasmogamy in the red alga Bostrychia. Eur. J. Phycol. 33:43-56. https://doi.org/10.1080/09670269810001736523
  48. Post, E. 1936. Systematische und pflanzengeographische Notizen zur Bostrychia-Caloglossa-Assoziation. Rev. Algol. 9:1-84.
  49. Ragan, M. A., Bird, C. J., Rice, E. L., Gutell, R. R., Murphy, C. A. & Singh, R. K. 1994. A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit rRNA gene. Proc. Natl. Acad. Sci. U. S. A. 91:7276-7280. https://doi.org/10.1073/pnas.91.15.7276
  50. Robba, L., Russell, S. J., Barker, G. L. & 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. https://doi.org/10.3732/ajb.93.8.1101
  51. Saunders, G. W. 2005. Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:1879-1888. https://doi.org/10.1098/rstb.2005.1719
  52. Sekimoto, S., Klochkova, T. A., West, J. A., Beakes, G. W. & Honda, D. 2009. Olpidiopsis bostrychiae sp. nov.: an endoparasitic oomycete that infects Bostrychia and other red algae (Rhodophyta). Phycologia 48:460-472. https://doi.org/10.2216/08-11.1
  53. Sunnucks, P., Wilson, A. C. C., Beheregaray, L. B., Zenger, K., French, J. & Taylor, A. C. 2000. SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Mol. Ecol. 9:1699-1710. https://doi.org/10.1046/j.1365-294x.2000.01084.x
  54. West, J. A., Klochkova, T. A., Kim, G. H. & Loiseaux-de Goër, S. 2006a. Olpidiopsis sp., an oomycete from Madagascar that infects Bostrychia and other red algae: host species susceptibility. Phycol. Res. 54:72-85. https://doi.org/10.1111/j.1440-1835.2006.00410.x
  55. West, J. A. & Zuccarello, G. C. 1999. Biogeography of sexual and asexual populations in Bostrychia moritziana (Rhodomelaceae, Rhodophyta). Phycol. Res. 47:115-123. https://doi.org/10.1111/j.1440-1835.1999.tb00292.x
  56. West, J. A., Zuccarello, G. & Calumpong, H. P. 1992a. Bostrychia bispora sp. nov. (Rhodomelaceae, Rhodophyta), an apomictic species from Darwin, Australia: reproduction and development in culture. Phycologia 31:37-52. https://doi.org/10.2216/i0031-8884-31-1-37.1
  57. West, J. A., Zuccarello, G. C., Hommersand, M., Karsten, U. & Görs, S. 2006b. Observations on Bostrychia radicosa comb. nov. (Rhodomelaceae, Rhodophyta). Phycol. Res. 54:1-14. https://doi.org/10.1111/j.1440-1835.2006.00403.x
  58. West, J. A., Zuccarello, G. C. & Kamiya, M. 2001. Reproductive patterns of Caloglossa species (Delesseriaceae, Rhodophyta) from Australia and New Zealand: multiple origins of asexuality in C. leprieurii. Literature review on apomixis, mixed-phase, bisexuality and sexual compatibility. Phycol. Res. 49:183-200. https://doi.org/10.1111/j.1440-1835.2001.tb00249.x
  59. West, J. A., Zuccarello, G. C. & Karsten, U. 1996. Reproductive biology of Stictosiphonia hookeri (Rhodomelaceae, Rhodophyta) from Argentina, Chile, South Africa and Australia in laboratory culture. Hydrobiologia 326/327:277-282.
  60. West, J. A., Zuccarello, G. C., Pedroche, F. F. & Karsten, U. 1992b. Marine red algae of the mangroves in Pacific México and their polyol content. Bot. Mar. 35:567-572. https://doi.org/10.1515/botm.1992.35.6.567
  61. White, T. J., Bruns, T., Lee, S. & Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. (Eds.) PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, pp. 315-322.
  62. Wilson, S. M., Pickett-Heaps, J. D. & West, J. A. 2002. Fertilization and the cytoskeleton in the red alga Bostrychia moritziana (Rhodomelaceae, Rhodophyta). Eur. J. Phycol. 37:509-522. https://doi.org/10.1017/S0967026202003931
  63. Wilson, S. M., West, J. A. & Pickett-Heaps, J. D. 2003. Time-lapse videomicroscopy of fertilization and the actin cytoskeleton in Murrayella periclados (Rhodomelaceae, Rhodophyta). Phycologia 42:638-645. https://doi.org/10.2216/i0031-8884-42-6-638.1
  64. Woese, C. R. 2000. Interpreting the universal phylogenetic tree. Proc. Natl. Acad. Sci. U. S. A. 97:8392-8396. https://doi.org/10.1073/pnas.97.15.8392
  65. Woese, C. R. & Fox, G. E. 1977. Phylogenetic structure of prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. U. S. A. 74:5088-5090. https://doi.org/10.1073/pnas.74.11.5088
  66. Zuccarello, G. C., Buchanan, J., West, J. A. & Pedroche, F. F. 2011. Genetic diversity of the mangrove-associated alga Bostrychia radicans / B. moritziana (Ceramiales, Rhodophyta) from southern Central America. Phycological Research (in press).
  67. Zuccarello, G. C., Burger, G., West, J. A. & King, R. J. 1999a. A mitochondrial marker for red algal intraspecific relationships. Mol. Ecol. 8:1443-1447. https://doi.org/10.1046/j.1365-294x.1999.00710.x
  68. Zuccarello, G. C. & West, J. A. 1994a. Comparative development of the red algal parasites Bostrychiocolax australis gen. et sp. nov. and Dawsoniocolax bostrychiae (Choreocolacaceae, Rhodophyta). J. Phycol. 30:137-146. https://doi.org/10.1111/j.0022-3646.1994.00137.x
  69. Zuccarello, G. C. & West, J. A. 1994b. Host-specificity in the red algal parasites Bostrychiocolax australis and Dawsoniocolax bostrychiae (Choreocolacaceae, Rhodophyta). J. Phycol. 30:462-473. https://doi.org/10.1111/j.0022-3646.1994.00462.x
  70. Zuccarello, G. C. & West, J. A. 1995. Hybridization studies in Bostrychia: 1. B. radicans (Rhodomelaceae, Rhodophyta) from Pacific and Atlantic North America. Phycol. Res. 43:233-240. https://doi.org/10.1111/j.1440-1835.1995.tb00029.x
  71. Zuccarello, G. C. & West, J. A. 1997. Hybridization studies in Bostrychia: 2. Correlation of crossing data and plastid DNA sequence data within B. radicans and B. moritziana (Ceramiales, Rhodophyta). Phycologia 36:293-304. https://doi.org/10.2216/i0031-8884-36-4-293.1
  72. Zuccarello, G. C. & West, J. A. 2002. Phylogeography of the Bostrychia calliptera-B. pinnata complex (Rhodomelaceae, Rhodophyta) and divergence rates based on nuclear, mitochondrial and plastid DNA markers. Phycologia 41:49-60. https://doi.org/10.2216/i0031-8884-41-1-49.1
  73. Zuccarello, G. C. & West, J. A. 2003. Multiple cryptic species: molecular diversity and reproductive isolation in the Bostrychia radicans / B. moritziana complex (Rhodomelaceae, Rhodophyta) with focus on North American isolates. J. Phycol. 39:948-959. https://doi.org/10.1046/j.1529-8817.2003.02171.x
  74. Zuccarello, G. C. & West, J. A. 2006. Molecular phylogeny of the subfamily Bostrychioideae (Ceramiales, Rhodophyta): subsuming Stictosiphonia and highlighting polyphyly in species of Bostrychia. Phycologia 45:24-36. https://doi.org/10.2216/05-07.1
  75. Zuccarello, G. C. & West, J. A. 2008. Bostrychia (Rhodomelaceae, Rhodophyta) species of New Zealand, and relationships in the Southern Hemisphere. N. Z. J. Mar. Freshw. Res. 42:315-324. https://doi.org/10.1080/00288330809509959
  76. Zuccarello, G. C., West, J. A. & Goer, S. L. D. 2006. Diversity of the Bostrychia radicans / Bostrychia moritziana species complex (Rhodomelaceae, Rhodophyta) in the mangroves of New Caledonia. Cryptogam. Algol. 27:245-254.
  77. Zuccarello, G. C., West, J. A., Kamiya, M. & King, R. J. 1999b. A rapid method to score plastid haplotypes in red seaweeds and its use in determining parental inheritance of plastids in the red alga Bostrychia (Ceramiales). Hydrobiologia 401:207-214. https://doi.org/10.1023/A:1003706931897
  78. Zuccarello, G. C., West, J. A., Karsten, U. & King, R. J. 1999c. Molecular relationships within Bostrychia tenuissima (Rhodomelaceae, Rhodophyta). Phycol. Res. 47:81-85. https://doi.org/10.1111/j.1440-1835.1999.tb00287.x
  79. Zuccarello, G. C., West, J. A. & King, R. J. 1999d. Evolutionary divergence in the Bostrychia moritziana / B. radicans complex (Rhodomelaceae, Rhodophyta): molecular and hybridization data. Phycologia 38:234-244. https://doi.org/10.2216/i0031-8884-38-3-234.1
  80. Zuccarello, G. C., Yeates, P. H., Wright, J. T. & Bartlett, J. 2001. Population structure and physiological differentiation of haplotypes of Caloglossa leprieurii (Rhodophyta) in a mangrove intertidal zone. J. Phycol. 37:235-244. https://doi.org/10.1046/j.1529-8817.2001.037002235.x

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  9. Molecular evidence confirms the parasite Congracilaria babae (Gracilariaceae, Rhodophyta) from Malaysia vol.26, pp.2, 2014, https://doi.org/10.1007/s10811-013-0166-5
  10. Keeping house: evaluation of housekeeping genes for real-time PCR in the red alga, Bostrychia moritziana (Florideophyceae) vol.31, pp.2, 2016, https://doi.org/10.4490/algae.2016.31.5.25
  11. (Ceramiales, Rhodophyta): Multiple species with very similar morphologies, a revised taxonomy of cryptic species vol.66, pp.2, 2017, https://doi.org/10.1111/pre.12207
  12. Plastid genome analysis of three Nemaliophycidae red algal species suggests environmental adaptation for iron limited habitats vol.13, pp.5, 2011, https://doi.org/10.1371/journal.pone.0196995
  13. Sex‐Specific Genes and their Expression in the Life History of the Red Alga Bostrychia moritziana (Ceramiales, Rhodomelaceae) vol.57, pp.2, 2021, https://doi.org/10.1111/jpy.13103
  14. Development of organelle single nucleotide polymorphism (SNP) markers and their application for the identification of cytoplasmic inheritance patterns in Pyropia yezoensis (Bangiales, Rhodophyta) vol.39, pp.4, 2021, https://doi.org/10.1007/s00343-020-0298-9