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Reproductive strategies of Lessonia berteroana (Laminariales, Phaeophyceae) gametophytes from Chile: Apogamy, parthenogenesis and cross-fertility with L. spicata

  • Dieter G. Müller
  • Pedro Murúa
  • Renato Westermeier
Article

Abstract

Lessonia berteroana is one of the most exploited seaweeds in the Southeastern Pacific and its populations are recurrently facing overexploitation in northern Chile. Since germplasms are not available, we decided to start gametophyte biobanking to support conservation measures for this important resource in the future. Spores of L. berteroana from nine localities at the Atacama coast were used to establish clonal male and female gametophyte cultures. Unexpectedly, after isolation and under low light conditions, juvenile sporophytes originated from somatic cells via apogamy in most female gametophyte strains. In addition, eggs from solitary female gametophytes from Caleta Cisnes and Torres del Inca had a strong tendency to generate sporophytes by parthenogenesis, some of them even under low light regimes. Contrarily, female gametophytes of the sister species Lessonia spicata from southern Chile showed no evidence for apomixis. When one of these L. berteroana strains is cross-fertilized with L. spicata, true hybrids emerged based on the presence of eggs and subsequent sperm attraction. These observations contrast with (i) kelp recruitment assumed to be majorly by sexual reproduction and (ii) the strict reproductive separation of the two taxa reported for natural populations within their contact zone at 30°S and highlight their consideration for future repopulation and breeding programs of Lessonia.

Keywords

Phaeophyta Lessonia berteroana L. spicata Apogamy Apomixis Interspecific hybridization Kelp Life history Parthenogenesis 

Notes

Acknowledgements

Sincere thanks are due to C. Atero for collection of field samples, U. Hueppeler and I. Maier for support with art-work and to the three anonymous reviewers for their contributions that helped to improve the earlier version of this MS. This work was done in the framework of the projects FIC 2013 33-91-243, FIC 2015 33-01-244 and FIC 2016 40486116 (GORE Atacama), FONDEF D04I1288 and VW Foundation, granted to the Universidad Austral de Chile (RW).

Supplementary material

10811_2018_1625_MOESM1_ESM.docx (20 kb)
Table S1 (DOCX 19 kb)

References

  1. Barcaccia G, Albertini E (2013) Apomixis in plant reproduction: a novel perspective on an old dilemma. Plant Reprod 26:159–179CrossRefGoogle Scholar
  2. Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16:S228–S245CrossRefGoogle Scholar
  3. Coleman M, Wernberg T (2018) Genetic and morphological diversity in sympatric kelps with contrasting reproductive strategies. Aquat Biol 27:65–73CrossRefGoogle Scholar
  4. Cosendai A-C, Hörandl E (2010) Cytotype stability, facultative apomixis and geographical parthenogenesis in Ranunculus kuepferi (Ranunculaceae). Ann Bot 105:457–470CrossRefGoogle Scholar
  5. Demes KW, Graham MH (2011) Abiotic regulation of investment in sexual versus vegetative reproduction in the clonal kelp Laminaria sinclairii (Laminariales, Phaeophyceae). J Phycol 47:463–470CrossRefGoogle Scholar
  6. González A, Beltrán J, Hiriart-Bertrand L, Flores V, de Reviers B, Correa JA, Santelices B (2012) Identification of cryptic species in the Lessonia nigrescens complex (Phaeophyceae, Laminariales). J Phycol 48:1153–1165CrossRefGoogle Scholar
  7. Hoffmann AJ, Santelices B (1982) Effects of light intensity and nutrients on gametophytes and gametogenesis of Lessonia nigrescens Bory (Phaeophyta). J Exp Mar Biol Ecol 60:77–89CrossRefGoogle Scholar
  8. Krueger-Hadfield SA, Kollars NM, Byers JE, Greig TW, Hammann M, Murray DC, Murren CJ, Strand AE, Terada R, Weinberg F, Sotka EE (2016) Invasion of novel habitats uncouples haplo-diplontic life cycles. Mol Ecol 25:3801–3816CrossRefGoogle Scholar
  9. Le Gall Y, Asensi A, Marie D, Kloareg B (1996) Parthenogenesis and apospory in the Laminariales: a flow cytometry analysis. Eur J Phycol 31:369–380CrossRefGoogle Scholar
  10. Lüning K, Dring MJ (1975) Reproduction, growth and photosynthesis of gametophytes of Laminaria saccharina grown in blue and red light. Mar Biol 29:195–200CrossRefGoogle Scholar
  11. Lüning K, Neushul M (1978) Light and temperature demands for growth and reproduction of laminarian gametophytes in southern and Central California. Mar Biol 45:297–309CrossRefGoogle Scholar
  12. Macaya EC, Zuccarello GC (2010) DNA barcoding and genetic divergence in the giant kelp Macrocystis (laminariales). J Phycol 46:736–742CrossRefGoogle Scholar
  13. Müller DG, Gachon CMM, Küpper FC (2008) Axenic clonal cultures of filamentous brown algae: initiation and maintenance. Cah Biol Mar 49:59–65Google Scholar
  14. Müller DG, Maier I, Marie D, Westermeier R (2016) Nuclear DNA level and life cycle of kelps: evidence for sex-specific polyteny in Macrocystis (Laminariales, Phaeophyceae). J Phycol 52:157–160CrossRefGoogle Scholar
  15. Murúa P, Westermeier R, Patiño DJ, Müller DG (2013) Culture studies on early development of Lessonia trabeculata (Phaeophyceae, Laminariales): seasonality and acclimation to light and temperature. Phycol Res 61:145–153CrossRefGoogle Scholar
  16. Murúa P, Müller DG, Patiño DJ, Westermeier R (2017) Giant kelp vegetative propagation: adventitious holdfast elements rejuvenate senescent individuals of the Macrocystis pyriferaintegrifolia” ecomorph. J Phycol 53:230–234CrossRefGoogle Scholar
  17. Nakahara H, Nakamura Y (1973) Parthenogenesis, apogamy and apospory in Alaria crassifolia (Laminariales). Mar Biol 18:327–332Google Scholar
  18. Oppliger LV, Correa JA, Peters AF (2007) Parthenogenesis in the brown alga Lessonia nigrescens (Laminariales, Phaeophyceae) from Central Chile. J Phycol 43:1295–1301CrossRefGoogle Scholar
  19. Oppliger LV, von Dassow P, Bouchemousse S, Robuchon M, Valero M, Correa JA, Mauger S, Destombre C (2014) Alteration of sexual reproduction and genetic diversity in the kelp species Laminaria digitata at the southern limit of its range. PLoS One 9:e102518CrossRefGoogle Scholar
  20. Percival EE, Venegas Jara MF, Weigel H (1983) Carbohydrates of the brown seaweed Lessonia nigrescens. Phytochemistry 22:1429–1432CrossRefGoogle Scholar
  21. Peteiro C (2018) Alginate production from marine macroalgae, with emphasis on kelp farming. In: Rehm B, Moradali M (eds) Alginates and their biomedical applications. Springer, Singapore, pp 27–66CrossRefGoogle Scholar
  22. Richards AJ (2003) Apomixis in flowering plants: an overview. Philos Trans R Soc B 358:1085–1093CrossRefGoogle Scholar
  23. Shan TF, Pang SJ, Gao SQ (2013) Novel means for variety breeding and sporeling production in the brown seaweed Undaria pinnatifida (Phaeophyceae): crossing female gametophytes from parthenosporophytes with male gametophyte clones. Phycol Res 61:154–161CrossRefGoogle Scholar
  24. Starr RC, Zeikus JA (1993) UTEX-the culture collection of algae at the University of Texas at Austin 1993. List of cultures. J Phycol 29:1–106CrossRefGoogle Scholar
  25. Tatarenkov A, Bergström L, Jönsson RB, Serrao EA, Kautsky L, Johannesson K (2005) Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus. Mol Ecol 14:647–651CrossRefGoogle Scholar
  26. Tellier F, Tapia J, Faugeron S, Destombe C, Valero M (2011) The Lessonia nigrescens species complex (Laminariales, Phaeophyceae) shows strict parapatry and complete reproductive isolation in a secondary contact zone. J Phycol 47:894–903CrossRefGoogle Scholar
  27. Voigt PW (1971) Discovery of sexuality in Eragrostis curvula (Schrad.) Nees. Crop Sci 11:424CrossRefGoogle Scholar
  28. Voigt PW, Bashaw EC (1976) Facultative apomixis in Eragrostis curvula. Crop Sci 16:803CrossRefGoogle Scholar
  29. Walther G-R, Roques A, Hulme PE, Sykes MT, Pysek P, Kühn I, Zobel M, Bacher S, Botta-Dukát Z, Bugmann H, Czúcz B, Dauber J, Hickler T, Jarosík V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov VE, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vilà M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24:686–693CrossRefGoogle Scholar
  30. Westermeier R, Patino D, Piel MI, Maier I, Müller DG (2006) A new approach to kelp mariculture in Chile: production of free-floating sporophyte seedlings from gametophyte cultures of Lessonia trabeculata and Macrocystis pyrifera. Aquac Res 37:164–171CrossRefGoogle Scholar
  31. Westermeier R, Patiño D, Müller DG (2007) Sexual compatibility and hybrid formation between the giant kelp species Macrocystis pyrifera and M. integrifolia (Laminariales, Phaeophyceae) in Chile. J Appl Phycol 19:215–221CrossRefGoogle Scholar
  32. Westermeier R, Patiño DJ, Murúa P, Müller DG (2011) Macrocystis mariculture in Chile: growth performance of heterosis genotype constructs under field conditions. J Appl Phycol 23:819–825CrossRefGoogle Scholar
  33. Westermeier R, Murúa P, Patiño DJ, Muñoz L, Müller DG (2016) Holdfast fragmentation of Macrocystis pyrifera (integrifolia morph) and Lessonia berteroana in Atacama (Chile): a novel approach for kelp bed restoration. J Appl Phycol 28:2969–2977CrossRefGoogle Scholar
  34. Westermeier R, Murúa P, Patiño DJ, Manoli G, Müller DG (2018) Evaluation of kelp harvest strategies: recovery of Lessonia berteroana (Phaeophyceae, Laminariales) in Pan de Azucar, Atacama, Chile. J Appl Phycol.  https://doi.org/10.1007/s10811-018-1500-8
  35. Zappacosta DC, Ochogavía AC, Rodrigo JM, Romero JR, Meier MS, Garbus I, Pessino SC, Echenique VC (2015) Increased apomixis expression concurrent with genetic and epigenetic variation in a newly synthesized Eragrostis curvula polyploid. Sci Rep 4:4423CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Fachbereich Biologie der Universität KonstanzKonstanzGermany
  2. 2.The Scottish Association for Marine Science, Scottish Marine Institute, Culture Collection for Algae and ProtozoaObanUnited Kingdom
  3. 3.Instituto de AcuiculturaUniversidad Austral de ChilePuerto MonttChile

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