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Dichogamy in Salicornieae species: establishment of floral sex phases and evaluation of their frequency and efficacy in four species

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Abstract

Dichogamy in Salicornieae species is not clearly described in literature, and its efficiency remains untested. In this work we aim to establish the pathway for flower development, the degree of interaction between the two sexes, and the efficiency in overcoming selfing. Flower development was studied in six populations of four Salicornieae species at the Odiel Marsh Natural Park (Huelva, SW Spain) by calculating the percentage of different floral phases established in accordance with the position of their stamens and stigmas. To study the sexual functionality of each phase, the lengths of the perianth, stigma, and ovule were measured, and the number of germinated pollen grains on the stigmas was counted. In the Arthrocnemum macrostachyum and Salicornia ramosissima populations, the stigma protrudes from the perianth when the anthers have shed their pollen. In the Sarcocornia fruticosa and Sarcocornia perennis populations, anthesis starts with the extrusion of one anther, but in the most common pattern the stigma protrudes from the perianth while the anthers are shedding their pollen. All species studied were morphologically protandrous, but only in one population of Arthrocnemum macrostachyum was the number of germinated pollen grains on the stigma significantly greater when the stigma was exserted than in the previous phases.

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References

  • Ball PW (1964) A taxonomic review of Salicornia in Europe. Feddes Repert 69:1–8

    Google Scholar 

  • Ball PW, Tutin TG (1959) Notes on annual species of Salicornia in Britain. Watsonia 4:193–205

    Google Scholar 

  • Bertin RI (1993) Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms. Am J Bot 80:557–583

    Article  Google Scholar 

  • Bertin RI, Newman CM (1993) Dichogamy in angiosperms. Bot Rev 59(2):112–152

    Article  Google Scholar 

  • Bhardwaj M, Eckert CG (2001) Functional analysis of synchronous dichogamy in flowering rush Butomus umbellatus (Butomaceae). Am J Bot 88(12):2204–2213

    Article  PubMed  CAS  Google Scholar 

  • Castroviejo S, Coello P (1980) Datos cariológicos y taxonómicos sobre las Salicorniinae A J Scott ibéricas. Anal Jard Bot Madrid 37(l):41–73

    Google Scholar 

  • Castroviejo S et al (1990) Chenopodiaceae. In: Castroviejo S (ed) Flora Ibérica, vol II. Real Jardín Botánico CSIC, Madrid, pp 476–553

  • Connor HE (1984) Gynodioecism in Sarcocornia quinqueflora (Salicornieae) in New Zealand. NZ J Bot 22:433–439

    Google Scholar 

  • Cooke FW (1912) Observations on Salicornia australis. Trans NZ Inst 44:349–362

    Google Scholar 

  • Cuguen J, Wattier R, Saumitou-Laprade P, Forcioli D, Mörchen M, Van Dijk H, Vernet P (1994) Gynodioecy and mitochondrial DNA polymorphism in natural populations of Beta vulgaris ssp. maritima. Genet Sel Evol 26:87–101

    Article  Google Scholar 

  • Dalby DH (1962) Chromosome number morphology and breeding behaviour in the British Salicorniae. Watsonia 5(3):150–162

    Google Scholar 

  • Davy AJ, Bishop GF, Costa CSB (2001) Salicornia L. (Salicornia pusilla J. Woods, S. ramosissima J. Woods, S. europaea L., S. obscura P.W. Ball and Tutin, S. nitens P.W. Ball and Tutin, S. fragilis P.W. Ball and Tutin and S. dolichostachya Moss). J Ecol 89:681–707

    Article  Google Scholar 

  • Ferguson IK (1964) Notes on the stigma morphology and flowering behaviour in British Salicorniae. Watsonia 6(1):25–27

    Google Scholar 

  • Fernández-Illescas F, Cabrera J, Nieva FJJ, Márquez-García B, Sánchez-Gullón E, Muñoz-Rodríguez AF (2010a) Production of aborted pollen in marsh species of Chenopodiaceae: evidence of partial male sterility in Suadeae and Salsoleae species. Plant Syst Evol 288(3–4):167–176

    Article  Google Scholar 

  • Fernández-Illescas F, Nieva FJJ, Muñoz AF (2010b) Pollen production in halophytic species of the Chenopodiaceae family in a Mediterranean marsh. Grana 49:300–307

    Article  Google Scholar 

  • Fernández-Illescas F, Nieva FJJ, Silva I, Tormo R, Muñoz AF (2010c) Pollen production of Chenopodiaceae species at habitat and landscape scale in Mediterranean salt marshes: an ecological and phenological study. Rev Palaeobot Palynol 161:127–136

    Article  Google Scholar 

  • Haines A (2000) Clarifying the taxonomy of Salicornia sensu lato of the northern United States. Bot Notes 2(Topsham USA):1–4. http://www.woodlotalt.com/publications/BotNotesv1n2.PDF. Accessed on 13 October 2007

  • Harder LD, Barrett SCH, Cole WW (2000) The mating consequences of sexual segregation within inflorescences of flowering plants. Proc R Soc Lond B 267:315–320

    Article  CAS  Google Scholar 

  • Jefferies RL, Gottlieb LD (1982) Genetic differentiation of the microspecies Salicornia europaea L. (sensu stricto) and S. ramosissima J. Woods. New Phytol 92:123–129

    Article  Google Scholar 

  • Jefferies RL, Davy AJ, Rudmik T (1981) Population biology of the salt marsh annual Salicornia europaea agg. J Ecol 69(1):17–31

    Article  Google Scholar 

  • Kadereit G, Mucina L, Freitag H (2006) Phylogeny of Salicornioideae (Chenopodiaceae): diversification biogeography and evolutionary trends in leaf and flower morphology. Taxon 55:617–642

    Article  Google Scholar 

  • Kadereit G, Ball P, Beer S, Mucina L, Sokoloff D, Teege P, Yaprak AE, Freitag H (2007) A taxonomic nightmare comes true: phylogeny and biogeography of glassworts (Salicornia L. Chenopodiaceae). Taxon 56:1143–1170

    Article  Google Scholar 

  • Kadereit G, Mavrodiev EV, Zacharias EH, Sukhorukov HP (2010) Molecular phylogeny of Atripliceae (Chenopodioideae, Chenopodiaceae): implications for systematics, biogeography, flower and fruit evolution, and the origin of C4 photosynthesis. Am J Bot 97:1664–1687

    Article  PubMed  Google Scholar 

  • Knuth P (1909) Handbook of flower pollination, vol 3. Clarendon Press, Oxford

  • Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy. NZ J Bot 24:135–162

    Google Scholar 

  • Lloyd DG, Yates JMA (1982) Intrasexual selection and the segregation of pollen and stigmas in hermaphrodite plants exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36:903–913

    Article  Google Scholar 

  • Lundqvist A, Osterbye U, Larsen K, Linde-Laursen I (1973) Complex self-incompatibility systems in Ranunculus acris L. and Beta vulgaris L. Hereditas 74:161–168

    Article  Google Scholar 

  • Luque T, Ruiz C, Avalos J, Calderón IL, Figueroa ME (1995) Detection and analysis of genetic variation in Salicornieae (Chenopodiaceae) using random amplified polymorphic DNA (RAPD) markers. Taxon 44:53–63

    Article  Google Scholar 

  • Moss CE (1954) The species of Arthrocnemum and Salicornia in Southern Africa. J S Afr Bot 20:1–22

    Google Scholar 

  • Mulugeta D, Maxwell BD, Fay PK, Dyer WE (1994) Kochia (Kochia scoparia) pollen dispersion, viability and germination. Weed Sci 42:548–552

    CAS  Google Scholar 

  • Navarro L (1997) Is the dichogamy of Salvia verbenaca (Lamiaceae) an effective barrier to self-fertilization? Plant Syst Evol 207:111–117

    Article  Google Scholar 

  • Noble SM, Davy AJ, Oliver RM (1992) Ribosomal DNA variation and population differentiation in Salicornia L. New Phytol 122:553–565

    Article  CAS  Google Scholar 

  • Packham JR, Willis AJ (1997) Ecology of dunes, saltmarsh and shingle. Chapman and Hall, London

  • Pandey KK (1960) Evolution of gametophytic and sporophytic systems of self-incompatibility in angiosperms. Evolution 14:98–115

    Article  Google Scholar 

  • Preston RE (1991) The intrafloral phenology of Streptanthus tortuosus (Brassicaceae). Am J Bot 78:1044–1053

    Article  Google Scholar 

  • Scott AJ (1978) Reinstatement and revision of Salicorniaceae J. Agardh (Caryophyllales). Bot J Linn Soc 75:357–374

    Article  Google Scholar 

  • Shamsutdinov ZS, Khamidov AA (1984) Flowering biology and the phenomenon of male sterility in Kochia prostrata (L.) Schrad. Probl Desert Dev 4:20–28

    Google Scholar 

  • Soriano A (1947) Las quenopodiáceas de la tribu “Salicornieae” en la Republica Argentina. Rev Argentina Agronom 14:148–172

    Google Scholar 

  • Stace CA (1997) New flora of the British Isles, 2nd edn. Cambridge University Press, Cambridge

  • Tölken HR (1967) The species of Arthrocnemum and Salicornia (Chenopodiaceae) in southern Africa. Bothalia 9:255–307

    Google Scholar 

  • Valdés B (1987) Salicornia. In: Valdés B, Talavera S, Fernández-Galiano E (eds) Flora vascular de Andalucía occidental, vol I. Ketres, Barcelona, pp 184–185

  • Valdés B, Castroviejo S (1990) Salicornia. In: Castroviejo S (ed) Flora Ibérica, vol II. Real Jardín Botánico CSIC, Madrid, pp 531–534

  • Vanderpoorten A, Hardy OJ, Lambinon J, Raspé O (2010) Two reproductively isolated cytotypes and a swarm of highly inbred, disconnected populations: a glimpse into Salicornia’s evolutionary history and challenging taxonomy. J Evol Biol 24:630–644

    Article  PubMed  Google Scholar 

  • Wilson PG (1980) A revision of the Australian species of Salicornieae (Chenopodiaceae). Nuytsia 3:3–154

    Google Scholar 

  • Wolff SL, Jefferies RL (1987) Morphological and isozyme variation in Salicornia europaea (sl) (Chenopodiaceae) in northeastern North America. Can J Bot 65:1410–1419

    Article  Google Scholar 

  • Wyatt R (1983) Pollinator–plant interactions and the evolution of breeding systems. In: Real L (ed) Pollination biology. Academic Press, Orlando, pp 51–95

  • Zare G, Keshavarzi M (2007) Morphological study of Salicornieae (Chenopodiaceae) native to Iran. Pakistan J Biol Sci 10(6):852–860

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the institution and staff of the Marismas del Odiel Natural Park, with special thanks to Enrique Sánchez-Gullón for his help and collaboration.

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Correspondence to Adolfo F. Muñoz-Rodríguez.

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Fernández-Illescas, F., Nieva, F.J.J., de las Heras, M.Á. et al. Dichogamy in Salicornieae species: establishment of floral sex phases and evaluation of their frequency and efficacy in four species. Plant Syst Evol 296, 255–264 (2011). https://doi.org/10.1007/s00606-011-0492-5

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