The Pneumathodes of Laguncularia racemosa: Little Known Rootlets of Surprising Structure, and Notes on a New Fluorescent Dye for Lipophilic Substances

Abstract

Two types of negatively geotropic aerial roots may be observed on the root system of Laguncularia racemosa: pneumatophores with secondary growth, and short-lived pneumathodes which remain in the primary anatomical state. The pneumathodes distinguish themselves by the absence of an epidermis; instead, the outer cortex takes the place of the outermost tissue. This tissue forms a three-dimensional network of rod-like cells and gas spaces. The cell walls contain a lipophilic substance which ensures that the intercellular spaces remain gas-filled during submergence. An uniseriate cellular layer separates the outer and inner cortex. This uniseriate cellular layer, which we term a “pore layer”, is characterized by cells with suberized and lignified cell walls and occasional pores among the cells. The pores permit the diffusion of oxygen-rich air from the surface of the pneumathode to the aerenchyma of the inner cortex and the escape of carbon dioxide from the interior of the root. The structure of the differentiated pneumathode originates from frequent cell divisions in the part of the apical meristem where the outer cortex emerges. Because of the pressure thereby exerted on the epidermis and hypodermis, these two cell layers tear and become separated from the outer cortex. Their remnants remain visible at the base of the pneumathode and as an appendage of the calyptra. The function and significance of the pneumathodes for L. racemosa are discussed. An extract of Xanthoria parietina was employed as a new fluorescent dye to stain suberine in cell walls. The staining technique is presented in this paper.

Key words

Mangrove - Laguncularia racemosa - pneumatophore - pneumathode - aerenchyma - fluorescent dye

References

• 01 Allaway,  W. G.,, Curran,  M.,, Hollington,  L. M.,, Ricketts,  M. C.,, and Skelton,  N. J.. (2001);  Gas space and oxygen exchange in roots of Avicennia marina (Forssk.) Vierh. var. australica (Walp.) Moldenke ex N.C. Duke, the grey mangrove.  Wetl. Ecol. Manag.. 9 211-218
• 02 Armstrong,  J., and Armstrong,  W.. (2001);  An overview of the effects of phytotoxins on Phragmites australis in relation to die-back.  Aquatic Bot.. 69 251-268
• 03 Armstrong,  W.,, Brändle,  R.,, and Jackson,  M. B.. (1994);  Mechanisms of flood tolerance in plants.  Acta Bot. Neerl.. 43 307-358
• 04 Becker,  E.. (1983) Fluoreszenzmikroskopie. Wetzlar; Leitz
• 05 Chapman,  V. J.. (1944);  1939 Cambridge University Expedition to Jamaica. III. The morphology of Avicennia nitida Jacq. and the function of its pneumatophores.  J. Lin. Soc. Bot. (London). 52 487-533
• 06 Chapman,  V. J.. (1976) Mangrove vegetation. Vaduz; J. Cramer
• 07 Curran,  M.. (1985);  Gas movements in the roots of Avicennia marina (Forsk.) Vierh.  Austral. J. Plant Physiol.. 12 97-108
• 08 Fahn,  A.. (1967) Plant anatomy. Oxford, London, Edinburgh, New York, Toronto, Sidney, Paris, Braunschweig; Pergamon Press
• 09 Flegler,  S. L.,, Heckmann,  J. W.,, and Klomparens,  K. L.. (1995) Elektronenmikroskopie. Heidelberg; Spektrum Akademischer Verlag
• 10 Gaynard,  T. J., and Armstrong,  W.. (1987) Some aspects of internal plant aeration in amphibious habitats. Plant life in aquatic and amphibious habitats. British Ecological Society Special Publication No. 5. Crawford, R. M. M., ed. Oxford; Blackwell pp. 303-320
• 11 Gerlach,  D.. (1984) Botanische Mikrotechnik. Eine Einführung, 3rd. edn. Stuttgart; Georg Thieme Verlag
• 12 Gill,  A. M., and Tomlinson,  P. B.. (1975) Aerial roots: An array of forms and functions. The development and function of roots. Torrey, J. and Clarkson, D., eds. London; Academic Press pp. 237-260
• 13 Granville,  J. J. de. (1974);  Aperçu sur la structure des pneumatophores de deux espèces des sols hydromorphes en Guyane.  Cah. ORSTOM, Sér. Biol.. 23 3-22
• 14 Gutenberg,  H. von. (1968) Der primäre Bau der Angiospermenwurzel. Handbuch der Pflanzenanatomie Bd. 8 (5). Berlin, Stuttgart; Gebrüder Borntraeger
• 15 Hovenden,  M. J.,, Curran,  M.,, Cole,  M. A.,, Goulter,  P. F. E.,, Skelton,  N. J.,, and Allaway,  W. G.. (1995);  Ventilation and respiration in roots of one-year-old seedlings of grey mangrove Avicennia marina (Forsk.) Vierh.  Hydrobiologia. 295 23-29
• 16 Huneck,  S., and Yoshimura,  I.. (1996) Identification of lichen substances. Berlin, Heidelberg; Springer Verlag
• 17 Jackson,  M. B., and Armstrong,  W.. (1999);  Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence.  Plant Biol.. 1 274-287
• 18 Jenik,  J.. (1970);  Root systems of tropical trees. 5. The peg-root and the pneumathodes of Laguncularia racemosa Gaertn.  Preslia. 42 105-113
• 19 Jensen,  W. A.. (1962) Botanical histochemistry. San Francisco; W. H. Freeman and Company
• 20 Jost,  L.. (1887);  Ein Beitrag zur Kenntnis der Athmungsorgane der Pflanzen.  Bot. Zeitung. 45 601-606 618-628 633-642
• 21 Kahn,  F.. (1977);  Analyse structurale des système racinaire des plantes ligneuse de la forêt tropicale dense humide.  Candollea. 32 321-358
• 22 Lambers,  H.,, Atkin,  O. K.,, and Scheurwater,  I.. (1996) Respiratory pattern in roots in relation to their functioning. Plant roots. The hidden half. 2nd edn. Waisel, Y., Eshel, A., and Kafkafi, U., eds. New York, Basel, Hong Kong; Marcel Dekker, Inc. pp. 323-362
• 23 McKee,  K. L.. (1995);  Interspecific variation in growth, biomass partitioning, and defensive characteristics of neotropical mangrove seedlings: response to light and nutrient availability.  Am. J. Bot.. 82 299-307
• 24 McKee,  K. L.. (1996);  Growth and physiological responses of neotropical mangrove seedlings to root zone hypoxia.  Tree Physiol.. 16 883-889
• 25 Merck Company,. (undated) Data sheet No. 12957 a. Darmstadt
• 26 Peirson,  D. R., and Dumbroff,  E. B.. (1969);  Demonstration of a complete Casparian strip in Avena and Ipomoea by a fluorescent staining technique.  Can. J. Bot.. 47 1869-1871
• 27 Perdomo,  L.. (2001) Evaluación de procesos de regeneración natural del manglar después de la reapertura de caños de agua dulce (Ciénaga Grande de Santa Marta, Colombia). Santa Marta; Tesis de posgrado, Universidad Nacional de Colombia - INVEMAR
• 28 Perdomo,  L.,, Ensminger,  I.,, Espinosa,  L. F.,, Elster,  C.,, Wallner-Kersanach,  M.,, and Schnetter,  M. L.. (1998);  The mangrove ecosystem of the Ciénaga Grande de Santa Marta (Colombia): Observations on regeneration and trace metals in sediment.  Mar. Poll. Bull.. 37 393-403
• 29 Raven,  J. A.. (1996);  Into the voids: The distribution, function, development and maintenance of gas spaces in plants.  Ann. Bot.. 78 137-142
• 30 Rost,  F. W. D.. (1995) Fluorescence microscopy. Vol. II. Cambridge; Cambridge University Press
• 31 Schenk,  H.. (1889);  Über die Luftwurzeln von Avicennia tomentosa und Laguncularia racemosa. .  Flora. 47 83-88
• 32 Schnetter,  M. L.. (2002);  El sistema radical del mangle blanco (Avicennia germinans), un ejemplo de adaptaciones morfológicas y anatómicas en espermatófitos a condiciones ecológicas adversas.  Rev. Acad. Col. Cienc. Exact., Fis., Nat.. 26 (98) 111-126
• 33 Scholander,  P. F.,, van Dam,  L.,, and Scholander,  S. J.. (1955);  Gas exchange in the roots of mangroves.  Am. J. Bot.. 42 92-98
• 34 Skelton,  N. J., and Allaway,  W. G.. (1996);  Oxygen and pressure changes measured in situ during flooding in roots of the grey mangrove Avicennia marina (Forssk.) Vierh.  Aquatic Bot.. 54 165-175
• 35 Tomlinson,  P. B.. (1961) Anatomy of the Monocotyledons. II. Palmae. Oxford; Clarendon Press
• 36 Tomlinson,  P. B.. (1986) The botany of mangroves. Cambridge, London, New York, New Rochelle, Melbourne, Sydney; Cambridge University Press
• 37 Troll,  W.. (1967) Vergleichende Morphologie der höheren Pflanzen. 1. Band. 3. Teil: Wurzel und Wurzelsysteme. Koenigstein/Taunus; Verlag Otto Koeltz
• 38 Troll,  W., and Dragendorff,  O.. (1931);  Über die Luftwurzeln von Sonneratia Linn. f. und ihre biologische Bedeutung. Mit einem rechnerischen Anhang von Hans Fromherz.  Planta. 13 311-473
• 39 Windholm,  J. M.. (1972);  The use of fluorescein diacetate and phenosafranine for determining viability of cultured plant cells.  Stain Techn.. 47 189-194
• 40 Wilson,  B. F.. (1975) Distribution of secondary thickening in tree root systems. The development and function of roots. Torrey, J. and Clarkson, D., eds. London; Academic Press pp. 197-219
• 41 Yampolsky,  C.. (1924);  The pneumathodes on the roots of the oil palm Elaeis guineenis Jacq.  Amer. J. Bot.. 11 502-515

Section Editor: M. Ball