Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-13T10:39:03.043Z Has data issue: false hasContentIssue false

Intervessel Pit Structure and Histochemistry of Two Mangrove Species as Revealed by Cellular UV Microspectrophotometry and Electron Microscopy: Intraspecific Variation and Functional Significance

Published online by Cambridge University Press:  16 September 2008

Nele Schmitz*
Affiliation:
Royal Museum for Central Africa (RMCA), Laboratory for Wood Biology and Xylarium, Leuvensesteenweg 13, 3080 Tervuren, Belgium Vrije Universiteit Brussel (VUB), Laboratory for Plant Biology and Nature Management (APNA), Pleinlaan 2, 1050 Brussels, Belgium
Gerald Koch
Affiliation:
Johann Heinrich von Thünen-Institut (vTI), Federal Research Institute for Rural Areas, Forestry and Fisheries, Institute for Wood Technology and Wood Biology, Leuschnerstrasse 91, 21031 Hamburg, Germany
Uwe Schmitt
Affiliation:
Johann Heinrich von Thünen-Institut (vTI), Federal Research Institute for Rural Areas, Forestry and Fisheries, Institute for Wood Technology and Wood Biology, Leuschnerstrasse 91, 21031 Hamburg, Germany
Hans Beeckman
Affiliation:
Royal Museum for Central Africa (RMCA), Laboratory for Wood Biology and Xylarium, Leuvensesteenweg 13, 3080 Tervuren, Belgium
Nico Koedam
Affiliation:
Vrije Universiteit Brussel (VUB), Laboratory for Plant Biology and Nature Management (APNA), Pleinlaan 2, 1050 Brussels, Belgium
*
Corresponding author. E-mail: nschmitz@vub.ac.be
Get access

Abstract

Intervessel pits play a key role in trees' water transport, lying at the base of drought-induced embolism, and in the regulation of hydraulic conductivity via hydrogels bordering pit canals. Recently, their microstructure has been the focus of numerous studies, but the considerable variation, even within species and the histochemistry of pit membranes, remains largely unexplained. In the present study, intervessel pits of the outermost wood were examined for Avicennia marina, of dry and rainy season wood separately for Rhizophora mucronata. The thickness of the pit membranes was measured on transmission electron micrographs while their topochemical nature was also analyzed via cellular UV microspectrophotometry. Pit membranes of R. mucronata were slightly thicker in dry season wood than in rainy season wood, but their spectra showed for both seasons a lignin and a yet unidentified higher wavelength absorbing component. It was suggested to be a derivative of the deposits, regularly filling pit canals. The vestures of A. marina chemically resembled pit membranes rather than cell walls.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alvarez, S., Marsh, E.L., Schroeder, S.G. & Schachtman, D.P. (2008). Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ 31(3), 325340.CrossRefGoogle ScholarPubMed
Bailey, I.W. (1957). Die Struktur der Tüpfelmembranen bei den Tracheiden der Koniferen. Holz Roh Werkst 15(5), 210213.CrossRefGoogle Scholar
Bamber, R.K. (1961). Staining reaction of the pit membrane of wood cells. Nature 191, 409410.CrossRefGoogle Scholar
Barnett, J.R. (1981). Pit formation. In Xylem Cell Development, Barnett, J.R. (Ed.), pp. 6776. Tunbridge Wells, Kent, UK: Castle House Publications Ltd.Google Scholar
Bauch, J. & Berndt, H. (1973). Variability in the chemical composition of pit membranes in bordered pits of gymnosperms. Wood Sci Technol 7, 619.CrossRefGoogle Scholar
Bonner, L.D. & Thomas, R.J. (1972). The ultrastructure of intercellular passageways in vessels of yellow poplar (Liriodendron tulipifera, L.) Part I: Vessel pitting. Wood Sci Technol 6, 196203.CrossRefGoogle Scholar
Boyce, C.K., Zwieniecki, M.A., Cody, G.D., Jacobsen, C., Wirick, S. & Knoll, A.H. (2004). Evolution of xylem lignification and hydrogel transport regulation. Proc Natl Acad Sci USA 101(50), 1755517558.CrossRefGoogle ScholarPubMed
Castro, M.A. (1991). Ultrastructure of vestures on the vesel wall in some species of Prosopis (Leguminosae-Mimosoideae). IAWA Bull 12(4), 425430.Google Scholar
Chafe, S.C. (1974). Cell wall formation and “protective layer” development in the xylem parenchyma of trembling aspen. Protoplasma 80, 335354.Google Scholar
Chaffey, N.J., Barnett, J.R. & Barlow, P.W. (1997). Cortical microtubule involvement in bordered pit formation in secondary xylem vessel elements of Aesculus hippocastanum L. (Hippocastanaceae): A correlative study using electron microscopy and indirect immunofluorescence microscopy. Protoplasma 197, 6475.CrossRefGoogle Scholar
Choat, B., Ball, M., Luly, J. & Holtum, J. (2003). Pit membrane porosity and water stress-induced cavitation in four co-existing dry rainforest tree species. Plant Physiol 131, 4148.CrossRefGoogle ScholarPubMed
Choat, B., Cobb, A.R. & Jansen, S. (2008). Structure and function of bordered pits: New discoveries and impacts on whole-plant hydraulic function xylem. New Phytol 177(3), 608625.CrossRefGoogle Scholar
Choat, B., Jansen, S., Zwiecniecki, M.A., Smets, E. & Holbrook, M. (2004). Changes in pit membrane porosity due to deflection and stretching: The role of vestured pits. J Exp Bot 55(402), 15691575.Google Scholar
Coleman, C.M., Prather, B.L., Valente, M.J., Dute, R.R. & Miller, M.E. (2004). Torus lignification in hardwoods. IAWA J 25(4), 435447.Google Scholar
Dahdouh-Guebas, F., De Bondt, R., Abeysinghe, P.D., Kairo, J.G., Cannicci, S., Triest, L. & Koedam, N. (2004). Comparative study of the disjunct zonation pattern of the grey mangrove Avicennia marina (Forsk.) Vierh. In Gazi Bay (Kenya). Bull Marine Sci 74(2), 237252.Google Scholar
Domec, J.C., Lachenbruch, B. & Meinzer, F.C. (2006). Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas-fir (Pseudotsuga menziesii; Pinaceae) trees. Am J Bot 93(11), 15881600.CrossRefGoogle ScholarPubMed
Donaldson, L.A. (2002). Abnormal lignin distribution in wood from severely drought stressed Pinus radiata trees. IAWA J 23(2), 161178.CrossRefGoogle Scholar
Donaldson, L.A. & Singh, A.P. (1990). Ultrastructure of Terminalia wood from an ancient Polynesian canoe. IAWA Bull 11(2), 195202.CrossRefGoogle Scholar
Ellmore, G.S., Zanne, A.E. & Orians, C.M. (2006). Comparative sectoriality in temperate hardwoods: Hydraulics and xylem anatomy. Bot J Linn Soc 150, 6171.CrossRefGoogle Scholar
Fengel, D. & Wolfsgruber, H. (1971). Untersuchung von imprägniertem Kiefern-Splintholz mit elektronenoptischen Methoden. Studies on impregnated pine sapwood by electron optical methods. Holz Roh Werkst 29, 6776.CrossRefGoogle Scholar
Frankenstein, C., Schmitt, U. & Koch, G. (2006). Topochemical studies on modified lignin distribution in the xylem of poplar (Populus spp.) after wounding. Ann Bot-London 97, 195204.CrossRefGoogle ScholarPubMed
Fromm, J., Rockel, B., Lautner, S., Windeisen, E. & Wanner, G. (2003). Lignin distribution in wood cell walls determined by TEM and backscattered SEM techniques. J Struct Biol 143, 7784.CrossRefGoogle ScholarPubMed
Gascó, A., Nardini, A., Gortan, E. & Salleo, S. (2006). Ion-mediated increase in the hydraulic conductivity of Laurel stems: Role of pits and consequences for the impact of cavitation on water transport. Plant Cell Environ 29, 19461955.CrossRefGoogle ScholarPubMed
Hacke, U.G., Sperry, J.S., Wheeler, J.K. & Castro, L. (2006). Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26, 689701.CrossRefGoogle ScholarPubMed
Hacke, U.G., Stiller, V., Sperry, J.S., Pittermann, J. & McCulloh, K.A. (2001). Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiol 125, 779786.CrossRefGoogle ScholarPubMed
Hammerschmidt, R. & Kuć, J. (1982). Lignification as a mechanism for induced systemic resistance in cucumber. Physiol Plant Pathol 20, 6171.CrossRefGoogle Scholar
Hoffmann, P. & Parameswaran, N. (1976). On the ultrastructural localization of hemicelluloses within delignified tracheids of spruce. Holzforschung 30, 6270.CrossRefGoogle Scholar
Holbrook, N.M. & Zwieniecki, M.A. (1999). Embolism repair and xylem tension: Do we need a miracle? Plant Physiol 120, 710.Google Scholar
Jansen, S., Baas, P., Gasson, P., Lens, F. & Smets, E. (2004). Variation in xylem structure from tropics to tundra: Evidence from vestured pits. Proc Natl Acad Sci 101(23), 88338837.CrossRefGoogle ScholarPubMed
Jansen, S., Baas, P., Gasson, P. & Smets, E. (2003). Vestured pits: Do they promote safer water transport? Int J Plant Sci 164(3), 405413.Google Scholar
Jansen, S., Smets, E. & Baas, P. (1998). Vestures in woody plants: A review. IAWA J 19(4), 347382.CrossRefGoogle Scholar
Kininmonth, J.A. (1972). Permeability and fine structure of certain hardwoods and effects on drying. Holzforschung 26, 3238.Google Scholar
Kitheka, J.U. (1997). Coastal tidally-driven circulation and the role of water exchange in the linkage between tropical coastal ecosystems. Estuar Coast Shelf S 45, 177187.CrossRefGoogle Scholar
Koch, G. & Grünwald, C. (2004). Application of UV microspectrophotometry for the topochemical detection of lignin and phenolic extractives in wood fibre cell walls. In Wood Fibre Cell Walls: Methods to Study Their Formation, Structure and Properties, Schmitt, U. (Ed.), pp. 119130. Uppsala, Sweden: Swedish University of Agricultural Sciences.Google Scholar
Koch, G. & Kleist, G. (2001). Application of scanning UV microspectrophotometry to localise lignins and phenolic extractives in plant cell walls. Holzforschung 55, 563567.Google Scholar
Koch, G., Richter, H.G. & Schmitt, U. (2006). Topochemical investigation on phenolic deposits in the vessels of afzelia (Afzelia spp.) and merbau (Intsia spp.) heartwood. Holzforschung 60, 583588.CrossRefGoogle Scholar
Lawn, A.M. (1960). The use of potassium permanganate as an electron-dense stain for sections of tissue embedded in epoxy resin. J Biophys Biochem Cytol 7, 197199.CrossRefGoogle ScholarPubMed
Melcher, P.J., Zwieniecki, M.A. & Holbrook, M. (2003). Vulnerability of xylem vessels to cavitation in sugar maple. Scaling from individual vessels to whole branches. Plant Physiol 131, 17751780.CrossRefGoogle ScholarPubMed
Meyra, A.G., Kuz, V.A. & Zarragoicoechea, G.J. (2007). Geometrical and physicochemical considerations of the pit membrane in relation to air seeding: The pit membrane as a capillary valve. Tree Physiol 27, 14011405.CrossRefGoogle ScholarPubMed
Morrow, A.C. & Dute, R.R. (1999). Electron microscopic investigation of the coating found on torus-bearing pit membranes of Botrychium dissectum, the common grape fern. IAWA J 20(4), 359373.CrossRefGoogle Scholar
Nemec, S. (1975). Vessel blockage by myelin forms in citrus with and without rough-lemon decline symptoms. Can J Bot 53, 102108.CrossRefGoogle Scholar
O'Brien, T.P. (1970). Further observations on hydrolysis of the cell wall in the xylem. Protoplasma 69, 114.CrossRefGoogle Scholar
Ohtani, J., Meylan, B.A. & Butterfield, B.G. (1984). Vestures or warts—Proposed terminology. IAWA Bull 5(1), 38.CrossRefGoogle Scholar
Orians, C.M., van Vuuren, M.M.I., Harris, N.L., Babst, B. & Ellmore, G.S. (2004). Differential sectoriality in long-distance transport in temperate tree species: Evidence from dye flow, 15N transport, and vessel element pitting. Trees 18, 501509.CrossRefGoogle Scholar
Panshin, A.J. (1932). An anatomical study of the woods of the Philippine mangrove swamps. Philipp J Sci 48(2), 143205.Google Scholar
Parameswaran, N. & Liese, W. (1977). Occurrence of warts in bamboo species. Wood Sci Technol 11, 313318.Google Scholar
Pesacreta, T.C., Groom, L.H. & Rials, T.G. (2005). Atomic force microscopy of the intervessel pit membrane in the stem of Sapium sebiferum (Euphorbiaceae). IAWA J 26(4), 397426.CrossRefGoogle Scholar
Ranjani, K. & Krishnamurthy, K.V. (1988). Nature of vestures in the vestured pits of some Caesalpiniaceae. IAWA Bull 9(1), 3133.CrossRefGoogle Scholar
Ridley, B.L., O'Neill, M.A. & Mohnen, D. (2001). Pectins: Structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57, 929967.CrossRefGoogle ScholarPubMed
Robb, J. & Busch, L.V. (1982). Ultrastructural changes in drought-induced wilt: A comparison with pathogen-induced flaccidity. Can J Plant Pathol 4, 97105.Google Scholar
Robb, J., Busch, L. & Rauser, W.E. (1980). Zinc toxicity and xylem vessel wall alterations in white beans. Ann Bot-London 46, 4350.CrossRefGoogle Scholar
Rudman, P. (1965). Fine structure of wood. Nature 208, 5556.CrossRefGoogle Scholar
Sano, Y. (2005). Inter- and intraspecific structural variations among intervascular pit membranes as revealed by field-emission scanning electron microscopy. Am J Bot 92(7), 10771084.CrossRefGoogle ScholarPubMed
Sano, Y. & Fukuzawa, K. (1994). Structural variations and secondary changes in pit membranes in Fraxinus mandschurica var. japonica. IAWA J 15(3), 283291.CrossRefGoogle Scholar
Sano, Y., Kawakami, Y. & Ohtani, J. (1999). Variation in the structure of intertracheary pit membranes in Abies sachalinensis, as observed by field-emission scanning electron microscopy. IAWA J 20(4), 375388.CrossRefGoogle Scholar
Sano, Y. & Nakada, R. (1998). Time course of the secondary deposition of incrusting materials on bordered pit membranes in Cryptomeria japonica. IAWA J 19(3), 285299.Google Scholar
Schmid, R. (1965). The fine structure of pits in hardwoods. In Cellular Ultrastructure of Woody Plants, Côté, W.A. (Ed.), pp. 291304. Syracuse, NY: Syracuse University Press.Google Scholar
Schmid, R. & Machado, R.D. (1968). Pit membranes in hardwoods—Fine structure and development. Protoplasma 66, 185204.CrossRefGoogle Scholar
Schmitz, N., Jansen, S., Verheyden, A., Kairo, J.G., Beeckman, H. & Koedam, N. (2007a). Comparative anatomy of intervessel pits in two mangrove species growing along a natural salinity gradient in Gazi Bay, Kenya. Ann Bot-London 100, 271281.CrossRefGoogle ScholarPubMed
Schmitz, N., Robert, E.M.R., Verheyden, A., Kairo, J.G., Beeckman, H. & Koedam, N. (2008). A patchy growth via successive and simultaneous cambia: Key to success of the most widespread mangrove species Avicennia marina? Ann Botany 101, 4958.Google Scholar
Schmitz, N., Verheyden, A., Beeckman, H., Kairo, J.G. & Koedam, N. (2006). Influence of a salinity gradient on the vessel characters of the mangrove species Rhizophora mucronata Lam. Ann Bot-London 98, 13211330.CrossRefGoogle Scholar
Schmitz, N., Verheyden, A., Kairo, J.G., Beeckman, H. & Koedam, N. (2007b). Successive cambia development in Avicennia marina (Forssk.) Vierh. is not climatically driven in the seasonal climate at Gazi Bay, Kenya. Dendrochronologia 25(2), 8796.CrossRefGoogle Scholar
Scurfield, G. (1967). The ultrastructure of reaction wood differentiation. Holzforschung 21, 613.CrossRefGoogle Scholar
Scurfield, G. (1970). The vestured pits of Eucalyptus regnans F. Muell.: A study using scanning electron microscopy. Bot J Linn Soc 63, 313320.CrossRefGoogle Scholar
Singh, A., Dawson, B., Franich, R., Cowan, F. & Warnes, J. (1999). The relationship between pit membrane ultrastructure and chemical impregnability of wood. Holzforschung 53, 341346.CrossRefGoogle Scholar
Singh, A.P., Kim, Y.S. & Wi, S.G. (2002). Inhomogeneity in the composition of vesture walls in an archaeological wood. IAWA J 23(1), 7782.CrossRefGoogle Scholar
Sperry, J.S. & Hacke, U.G. (2004). Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes. Am J Bot 91(3), 369385.CrossRefGoogle ScholarPubMed
Sperry, J.S., Hacke, U.G. & Pittermann, J. (2006). Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93(10), 14901500.CrossRefGoogle ScholarPubMed
Sperry, J.S., Perry, A.H. & Sullivan, J.E.M. (1991). Pit membrane degradation and air-embolism formation in ageing xylem vessels of Populus tremuloides Michx. J Exp Bot 42(244), 13991406.Google Scholar
Sperry, J.S. & Tyree, M.T. (1988). Mechanism of water stress-induced xylem embolism. Plant Physiol 88, 581587.Google Scholar
Street, P.F.S., Robb, J. & Ellis, B.E. (1986). Secretion of vascular coating components by xylem parenchyma cells of tomatoes infected with verticillium albo-atrum. Protoplasma 132, 111.Google Scholar
Streit, W. & Fengel, D. (1994). Heartwood formation in Quebracha colorado (Schinopsis balansae Engl.): Tannin distribution and penetration of extractives into the cell walls. Holzforschung 48, 361367.CrossRefGoogle Scholar
Thomas, R.J. (1976). Anatomical features affecting liquid penetrability in three hardwood species. Wood Fiber Sci 7(4), 256263.Google Scholar
Tibbits, C.W., MacDougall, A.J. & Ring, S.G. (1998). Calcium binding and swelling behaviour of a high methoxyl pectin gel. Carbohydr Res 310, 101107.CrossRefGoogle Scholar
Tomlinson, P.B. (1994). The Botany of Mangroves. Cambridge: Cambridge University Press.Google Scholar
van Ieperen, W. (2007). Ion-mediated changes of xylem hydraulic resistance in planta: Fact or fiction? Trends Plant Sci 12(4), 137142.CrossRefGoogle ScholarPubMed
Verheyden, A., Kairo, J.G., Beeckman, H. & Koedam, N. (2004). Growth rings, growth ring formation and age determination in the mangrove, Rhizophora mucronata. Ann Bot-London 94, 5966.CrossRefGoogle ScholarPubMed
Wardrop, A.B. (1957). The phase of lignification in the differentiation of wood fibers. Tappi 40(4), 225243.Google Scholar
Wardrop, A.B., Ingle, H.D. & Davies, G.W. (1963). Nature of vestured pits in angiosperms. Nature 197, 202203.CrossRefGoogle Scholar
Watanabe, Y., Sano, Y., Asada, T. & Funada, R. (2006). Histochemical study of the chemical composition of vestured pits in two species of eucalyptus. IAWA J 27(1), 3343.Google Scholar
Wheeler, E.A. (1981). Intervascular pitting in Fraxinus americana L. IAWA Bull 2(4), 169174.Google Scholar
Wheeler, E.A. (1982). Ultrastructural characteristics of red maple (Acer rubrum L.) wood. Wood and Fiber 14(1), 4353.Google Scholar
Wheeler, E.A. & Thomas, R.J. (1981). Ultrastructural characteristics of mature wood of southern red oak (Quercus falcata Michx.) and white oak (Quercus alba L.). Wood Fiber Sci 13(3), 169181.Google Scholar
Wheeler, J.K., Sperry, J.S., Hacke, U.G. & Hoang, N. (2005). Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: A basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ 28(6), 800812.CrossRefGoogle Scholar
Yang, K.-C. (1978). The fine structure of pits in yellow birch (Betula alleghaniensis britton). IAWA Bull 4, 7177.Google Scholar
Yang, K.-C. (1986). The ultrastructure of pits in Paulownia tomentosa. Wood Fiber Sci 18(1), 118126.Google Scholar
Zimmermann, U., Wagner, H.J., Heidecker, M., Mimietz, S., Schneider, H., Szimtenings, M., Haase, A., Mitlöhner, R., Kruck, W., Hoffmann, R. & König, W. (2002). Implications of mucilage on pressure bomb measurements and water lifting in trees rooting in high-salinity water. Trees 16, 100111.CrossRefGoogle Scholar
Zimmermann, U., Zhu, J.J., Meinzer, F.C., Goldstein, G., Schneider, H., Zimmermann, G., Benkert, R., Thürmer, F., Melcher, P., Webb, D. & Haase, A. (1994). High molecular weight organic compounds in the xylem sap of mangroves—Implications for long distance water transport. Bot Acta 107, 218229.CrossRefGoogle Scholar
Zweypfenning, R.C.V.J. (1978). A hypothesis on the function of vestured pits. IAWA Bull n.s. 1, 1315.Google Scholar
Zwieniecki, M.A. & Holbrook, N.M. (2000). Bordered pit structure and vessel wall surface properties. Implications for embolism repair. Plant Physiol 123, 10151020.CrossRefGoogle ScholarPubMed
Zwieniecki, M.A., Melcher, P.J. & Holbrook, N.M. (2001). Hydrogel control of xylem hydraulic resistance in plants. Science 291, 10591062.CrossRefGoogle ScholarPubMed