Abstract
Seagrasses, which form an integral part of the worldwide coastal habitat, are considered highly relevant from an ecological point of view. Due to the scarcity of anatomical information, the present study analyzed the morphoanatomy, histochemistry, and ultrastructure of Halophila decipiens, Halodule wrightii, and Ruppia maritima leaves, discussing their adaptations to the marine environments observed throughout the southwestern tropical and subtropical Atlantic coast. The leaves of these three species feature a uniseriate epidermis with the presence of chloroplasts in large quantities and absence of stomata. The vascular system consists of a central vascular bundle with sieve tube elements of the phloem and protoxylem lacunae, as well as small vascular bundles near the leaf margins. The leaves of H. decipiens possess trichomes, but no mesophyll in the leaf margins. The mesophyll of H. wrightii and R. maritima is homogeneous with chlorenchyma cells and air lacunae scattered throughout the leaf. The histochemistry analysis revealed the absence of amyloplasts and the presence of proteins in the outer periclinal walls of ordinary epidermal cells of the three species. It was also possible to detect the presence of idioblasts containing phenolic compounds in H. decipiens and R. maritima. The ultrastructural analysis of the three species revealed many elliptical chloroplasts, with organized thylakoids, expansion of the epidermal cell wall into the cytoplasm, and a thin cuticle. Hydropoten were also observed in the three specimens. The results show that the species analyzed have important adaptations which enable their survival in the marine environment.
Similar content being viewed by others
References
Alquini Y, Bona C, Boeger MRT, Costa CG, Barros CF (2006) Epiderme. In: Appezzato-da-Gloria B, Carmello-Guerreiro SM (eds) Anatomia vegetal, 2nd edn. UFV, Viçosa, pp 87–97
Bosabalidis AM (2010) Wall protuberance formation and function in secreting salt glands of Tamarix aphylla L. Acta Bot Bras 69:229–235
Brouillard R, Dangles O (1994) Flavonoids and flower colour. In: Harborne JB (ed) The flavonoids: advances in research since 1986. Chapman and Hall, London, pp 565–588
Carletti P, Masi A, Wonisch A, Grill D, Tausz M, Ferretti M (2003) Changes in antioxidant and pigment pool dimensions in UV-B irradiated maize seedlings. Environ Exp Bot 50:149–157
Castro MM, Machado SR (2006) Células e tecidos secretores. In: Appezzato-da-Gloria B, Carmello-Guerreiro SM (eds) Anatomia Vegetal, 2nd edn. UFV, Viçosa, pp 179–203
Copertino MS (2011) Add coastal vegetation to the climate critical list. Nature 473:255
Creed JC, Paixão AM, Aoki AL, Barbosa MBS, Moreira D, Patrício ED, Casares FA, Almeida M (2004) Monitoramento de fanerógamas marinhas no arquipélago dos Abrolhos-BA. In: Programa SeagrassNet: Relatório de Atividades entre abril 2003 a agosto 2004. Ministério do Meio Ambiente, Brasília, Brasil
CETESB Companhia de Tecnologia de Saneamento Ambiental (2011) Qualidade das águas Superficiais no Estado de São Paulo 2010. Recurso eletrônico CETESB. http://www.cetesb.sp.gov.br/agua/aguas-superficiais/35-publicacoes-/-relatorios. Accessed 15 July 2012
den Hartog C (1970) The sea-grasses of the world. North-Holland Publishing Company, Amsterdam
den Hartog C, Kuo J (2006) Taxonomy and biogeography of seagrasses. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, pp 1–29
Dickison WC (2000) Integrative plant anatomy. Harcourt/Academic Press, Massachusetts
Doohan ME, Newcomb EH (1976) Leaf ultrastructure and δ13C values of three seagrasses from the great barrier reef. Aust J Plant Physiol 3:9–23
Duarte CM (2002) The future of seagrass meadows. Environ Conserv 29:192–206
Esteves BS, Suzuki MS (2008) Efeito da salinidade sobre as plantas. Oecol Bras 12:662–679
Fahn A (1979) Secretory tissues in plants. Academic, New York
Fonseca MS, Fisher JS (1986) A comparison of canopy friction and sediment movement between 4 species of seagrass with reference to their ecology and restoration. Mar Ecol-Prog Ser 29:15–22
Gahan PB (1984) Plant histochemistry and cytochemistry: an introduction. Academic, London
Garcia AB, Engler JA, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169
Gordon EM, McCandless EL (1973) Ultrastructure and histochemistry of Chondrus crispus Stack. P N S I Sci 27:111–133
Gullström M, de la Torre Castro M, Bandeira S, Björk M, Dahlberg M, Kautsky N, Rönnbäck P, Öhman MC (2002) Seagrass ecosystems in the Western Indian ocean. AMBIO J Human Environ 31:588–596
Hemminga M, Duarte CM (2000) Seagrass ecology. Cambridge University Press, Cambridge
Hogarth PJ (2007) The biology of mangroves and seagrasses. Oxford University Press, New York
Jagel RH (1973) Studies of a marine grass Thalassia testudinum. I. Ultrastructure of osmoregulatory leafcefts. Am J Bot 60:1003–1009
Johansen DA (1940) Plant microtechnique. McGraw Hill Book Company, New York
Kuo J (1978) Morphology, anatomy and histochemistry of the Australian seagrasses of the genus Posidonia könig (posidoniaceae). I. Leaf blade and leaf sheath of Posidonia australis hook F. Aquat Bot 5:171–190
Kuo J, den Hartog C (2006) Seagrass morphology, anatomy, and ultrastructure. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, pp 51–87
Larkum WD, Orth RJ, Duarte CM (2006) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, 691p
Les DH, Tippery NP (2013) In time and with water…the systematics of alismatid monocotyledons. In: Wilkin P (ed) Early events in monocot evolution. Cambridge University Press, Cambridge, pp 118–164
Les DH, Cleland MA, Waycott M (1997) Phylogenetic studies in the monocot subclass Alismatidae II: evolution of marine angiosperms (“seagrasses”) and hydrophily. Syst Bot 22:443–463
Lyshede OB (1980) Structure of the outer epidermal wall in xerophytes. In: Cutler DF, Alvin KF, Price CE (eds) The plant cuticle. Academic, London, pp 87–98
Marcondes J, Garcia AB (2009) Aspectos citomorfologicos do estresse salino em plântulas de arroz (Oryza sativa L.). Arq Inst Biol 76:187–194
Mauseth JD (2009) Botany: an introduction to plant biology, 4th edn. Jones and Bartlett Publishers, Boston
McCoy ED, Heck KL (1976) Biogeography of corals, seagrasses and mangroves: an alternative to the centre of origin concept. Syst Zool 25:201–210
Mendes BSS (2009) Efeitos fisiológicos e bioquímicos do estresse salino em Ananas porteanus Hort Veitch ex C. Koch. Dissertation, Federal Rural University of Pernambuco
Menezes NL, Silva DC, Pinna GFM (2006) Folha. In: Appezzato-da-Gloria B, Carmello-Guerreiro SM (eds) Anatomia vegetal, 2nd edn. UFV, Viçosa, pp 87–97
Metcalfe CR, Chalk L (1979) Anatomy of the dicotyledons, vol 1, 2nd edn. Claredon Press, Oxford
Oliveira Filho EC, Pirani JR, Giulietti AM (1983) The Brazilian seagrass. Aquat Bot 16:251–267
Oliveira EC, Horta PA, Amâncio CE, Sant’anna CL (1999) Algas e angiospermas marinhas bênticas do litoral brasileiro: diversidade, exploração e conservação. In: Workshop sobre avaliação e ações prioritárias para conservação da biodiversidade das zonas costeira e marinha. Relatório Técnico. Ministério do Meio Ambiente, Brasília, Brasil, 2002. 1 CD-ROM
Orth RJ, Carruthers TJB, Short FT, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bio Sci 56:987–996
Pang CA, Wang B (2008) Oxidative stress and salt tolerance in plants. Prog Bot 69:231–246
Sand-Jensen K, Pedersen O, Binzer T, Borum J (2005) Contrasting oxygen dynamics in the freshwater isoetid Lobelia dortmanna and the marine seagrass Zostera marina. Ann Bot 96:613–623
Shoemaker G, Wyllie-Echeverria S (2013) Occurrence of rhizomal endophytes in three temperate northeast pacific seagrasses. Aquat Bot 111:71–73
Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169–196
Short FT, Koch EW, Creed JC, Magalhães KM, Fernandez E, Gaeckle JL (2006) SeagrassNet monitoring across the Americas: case studies of seagrass decline. Mar Ecol 27:277–289
Souza VL, Silva DC, Santana KB, Mielke MS, Almeida AF, Mangabeira PA, Rocha EA (2009) Efeito do cádmio na anatomia e na fotossíntese de duas macrófitas aquáticas. Acta Bot Bras 23:343–354
Taiz L, Zeiger E (2009) Fisiologia vegetal, 4th edn. Artmed, Porto Alegre
Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323
Waycott M (2000) Mating systems and population genetics of marine angiosperms (seagrasses). In: Wilson KL, Morrison D (eds) Monocots: systematics and evolution, vol 1. CSIRO Publishing, Sydney, pp 277–285
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Acknowledgments
We are grateful for the staff of the Laboratory of Plant Anatomy (LAVEG/UFSC), Laboratory of Marine Algae (LAMAR/UFSC), Laboratory Studies in Biology Multiuser II (LAMEB II/UFSC), and for the Central Laboratory of Electron Microscopy (LCME/UFSC) for all the help provided and for making space and equipment available in these laboratories and to Conselho Nacional de Pesquisa (CNPq) for granting the fellowship for the second author. This study is part of the master’s degree of the first author.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Néstor Carrillo
Rights and permissions
About this article
Cite this article
Ferreira, C., Horta, P.A., Almeida, G.M. et al. Anatomical and ultrastructural adaptations of seagrass leaves: an evaluation of the southern Atlantic groups. Protoplasma 252, 3–20 (2015). https://doi.org/10.1007/s00709-014-0661-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-014-0661-9