Summary
The haustorial structure of three African parasitic members of the family Scrophulariaceae (Buchnera hispida, Rhamphicarpa fistulosa, andStriga hermonthica) has been studied with regard to the interface between haustoria and the invaded host roots. Immunocytochemical observations at the light and electron microscopical level were carried out with monoclonal antibodies against pectin. JIM5, JIM7, and hydroxyproline-rich glycoprotein (HRGP), LM1. Lignins have been visualized by phloroglucinolhydrochloric acid staining. At the margin of the lateral interface (contact area of host root cortex and parasite cells), JIM5- and JIM7-labelled substances accumulate between parasite papillae and the host root surface indicating that pectins are implicated in sealing the parasite to the attacked host organ. The lateral interface is characterized by the presence of compressed, necrotic host cells, whereas the central interface (contact area between host stele and parasite cells) is generally devoid of host cell remnants. Phenolic substances and/or lignins can be found at the site of penetration of the haustorium into the host root. These observations and the fact that HRGPs accumulate at the host side of the interface support the view of, at least, a partial defense reaction in the invaded host root tissues. Within haustoria, HRGPs were restricted to differentiating xylem elements, implying a spatio-temporal regulation of HRGPs in developmental processes.
Similar content being viewed by others
Abbreviations
- BSA:
-
bovine serum albumin
- FITC:
-
fluorescein isothiocyanate
- HRGP:
-
hydroxyproline-rich glycoprotein
- LM:
-
light microscopy
- MAb:
-
monoclonal antibody
- TBSB:
-
Tris-buffered saline with bovine serum albumin
- TBSB-T:
-
Tris-buffered saline with bovine serum albumin and Tween 20
- TEM:
-
transmission electron microscopy
References
Adler E, Björquist KJ, Häggroth S (1948) Über die Ursache der Farbreaktionen des Holzes. Acta Chem Scand 2: 93–94
Arnaud MC, Thalouarn P, Fer A (1998) Caractérisation des mécanismes impliqués dans la résistance de plantes cultivées à deux phanérogames parasites (Cuscuta reflexa etStriga hermonthica). C R Soc Biol 192: 101–119
Benhamou N, Lafontaine PJ, Mazau D, Esquerré-Tugayé MT (1991) Differential accumulation of hydroxyproline-rich glycoproteins in bean root nodule cells infected with a wild type strain or a C4-dicarboxylic acid mutant ofRhizobium leguminosarum bv.phaseoli. Planta 184: 457–467
Bronner R (1975) Simultaneous demonstration of lipids and starch in plant tissues. Stain Technol 50: 1–4
Calder M, Bernhardt P (1983) The biology of mistletoes. Academic Press, Sydney
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3: 1–30
Coetzee J, Fineran BA (1987) The apoplastic continuum, nutrient absorption and plasmatubules in the dwarf mistletoeKorthalsella lindsayi (Viscaceae). Protoplasma 136: 145–153
Coppick S, Fowler WF (1939) The location of potential reducing substances in woody tissues. Paper Trade J 109: 81–86
Corbin DR, Sauer N, Lamb CJ (1987) Differential regulation of hydroxyproline-rich glycoprotein gene family in wounded and infected plants. Mol Cell Biol 7: 4337–4344
Dörr I, Staack A, Kollmann R (1994) Resistance of Helianthus to Orobanche: histological and cytological studies. In: Pieterse AH, Verkleij JAC, ter Borg SJ (eds) Biology and management of Orobanche: Proceedings of the 3rd International Workshop on Orobanche and related Striga research, Amsterdam, pp 276–289
Fineran BA (1987) A structural approach towards investigating transport systems between host and parasite, as exemplified by some mistletoes and root parasites. In: Weber HC, Forstreuter W (eds) Parasitic flowering plants: Proceedings of the 4th International Symposium on Parasitic Flowering Plants, Marburg, pp 201–220
— (1997) Cyto- and histochemical demonstration of lignins in plant cell walls: an evaluation of the chlorine water/ethanolamine-silver nitrate method of Coppick and Fowler. Protoplasma 198: 186–201
Fukuda H (1997) Tracheary element differentiation. Plant Cell 9: 1147–1156
Glauert AM, Glauert RH (1958) Araldite as an embedding medium for electron microscopy. J Biophys Biochem Cytol 4: 191–195
Hariri EB, Sallé G, Andary C (1991) Involvement of flavonoids in the resistance of two poplar cultivars to mistletoe (Viscum album L.). Protoplasma 162: 20–26
Heide-Jørgensen HS (1987) Changes in cuticle structure during development and attachment of the upper haustorium of Cuscuta L., Cassytha L., and Viscum L. In: Weber HC, Forstreuter W (eds) Parasitic flowering plants: Proceedings of the 4th International Symposium on Parasitic Flowering Plants, Marburg, pp 319–334
— (1989) Development and ultrastructure of the haustorium ofViscum minimum. I: the adhesive disk. Can J Bot 67: 1161–1173
— Kuijt J (1993) Epidermal derivates as xylem elements and transfer cells: a study of the host-parasite interface in two species ofTriphysaria (Scrophulariaceae). Protoplasma 174: 173–183
Hood ME, Condon JM, Timko MP, Riopel JL (1998) Primary haustorial development ofStriga asiatica on host and nonhost species. Phytopathology 88: 70–75
Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant Cell Environ 7: 153–164
— Forsyth W, Duncan HJ (1988) A survey of the pectic content of nonlignified monocot cell walls. Plant Physiol 88: 309–314
Joel DM, Losner-Goshen D (1994a) Early host-parasite interaction: models and observations of host root penetration by the haustorium of Orobanche. In: Pieterse AH, Verkleij JAC, ter Borg SJ (eds) Biology and management of Orobanche: Proceedings of the 3rd International Workshop on Orobanche and related Striga research, Amsterdam, pp 237–254
—— (1994b) The attachment organ of the parasitic angiospermsOrobanche cumana andO. aegyptiaca and its development. Can J Bot 72: 564–574
—, Portnoy VH (1998) The angiospermous root parasite Orobanche L. (Orobanchaceae) induces expression of a pathogenesis related (PR) gene in susceptible tobacco roots. Ann Bot 81: 779–781
- Losner-Goshen D, Hershenhorn J, Goldwasser Y, Assayag M (1996) The haustorium and its development in compatible and resistant hosts. In: Moreno MT, Cubero JI, Berner DK, Joel DM, Musselman LJ, Parker C (eds) Advances in parasitic plant research: Proceedings of the 6th International Parasitic Weed Symposium, Cordoba, pp 531–541
Joseleau JP, Ruel K (1997) Study of lignification by noninvasive techniques in growing maize internodes. Plant Physiol 114: 1123–1133
Knox JP (1995) Developmentally regulated proteoglycans and glycoproteins of the plant cell surface. FASEB J 9: 1004–1012
— (1997) The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int Rev Cytol 171: 79–120
—, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181: 512–521
Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley
— (1991) The haustorial interface: what does it tell us? In: Ransom JK, Musselman LJ, Worsham AD, Parker C (eds) Proceedings of the 5th International Symposium of Parasitic Weeds. Centro Internacional de Mejoramiento de Maiz y Trigo, Nairobi, pp 1–5
Kuo J, Pate JS, Davidson NJ (1989) Ultrastructure of the haustorial interface and apoplastic continuum between host and the root hemiparasiteOlax phyllanthi (Labbill.) R. Br. (Olacaceae). Protoplasma 150: 27–39
Lane JA, Bailey JA, Terry PJ (1991) An in vitro growth system for studying the parasitism of cowpea (Vigna unguiculata) byStriga gesnerioides. Weed Res 31: 211–217
Losner-Goshen D, Portnoy VH, Mayer AM, Joel DM (1998) Pectolytic activity by the haustorium of the parasitic plant Orobanche L. (Orobanchaceae) in host roots. Ann Bot 81: 319–326
Ludevid MD, Ruiz-Avila L, Vallès MP, Stiefel V, Torrent M, Torné JM, Puigdomènech P (1990) Expression of genes for cellwall proteins in dividing and wounded tissues ofZea mays L. Planta 180: 524–529
Maiti RK, Ramaiah KV, Bisen SS, Chidley VL (1984) A comparative study of the haustorial development ofStriga asiatica (L.) Kuntze on sorghum cultivars. Ann Bot 54: 447–457
Musselman LJ, Dickison WC (1975) The structure and development of the haustorium in parasitic Scrophulariaceae. Bot J Linn Soc 70: 183–212
Neumann U, Sallé G, Weber HC (1998) Development and structure of the haustorium of the parasiteRhamphicarpa fistulosa (Scrophulariaceae). Bot Acta 111: 354–365
O'Brien TP, Feder N, McCully ME (1964) Polychromatic stain of plant cell walls by toluidine blue O. Protoplasma 59: 367–373
Olivier A, Benhamou N, Leroux GD (1991) Cell surface interactions between sorghum roots and the parasitic weedStriga hermonthica: cytochemical aspects of cellulose distribution in resistant and susceptible host tissues. Can J Bot 69: 1679–1690
Parker C, Riches C (1993) Parasitic weeds of the world. CAB International, Wallingford
Pate JS, Kuo J, Davidson NJ (1990) Morphology and anatomy of the haustorium of the root hemiparasiteOlax phyllanthi (Olacaceae), with special reference to the haustorial interface. Ann Bot 65: 425–436
Piehl MA (1963) Mode of attachment, haustorium structure, and hosts ofPedicularis canadensis. Am J Bot 50: 978–985
Press M, Graves JD (1995) Parasitic plants. Chapman and Hall, London
Reiss GC, Bailey JA (1998)Striga gesnerioides parasitising cowpea: development of infection structures and mechanisms of penetration. Ann Bot 81: 431–440
Reynolds ES (1963) The use of lead citrate at high pH as an elctron opaque stain in electron microscopy. J Cell Biol 17: 208–212
Ruel K, Faix O, Joseleau JP (1994) New immunogold probes for studying the distribution of the different lignin types during plant cell wall biogenesis. J Trace Microprobe Tech 12: 267–276
Sallé G (1975) Étude cytologique, cytochimique et histoautoradiographique duViscum album L. (Loranthacées) I: la graine, sa germination et les modalités de la fixation sur l'hôte. Rev Cytol Biol Veg 38: 1–110
Schindler T, Bergfeld R, Schopfer P (1995) Arabinogalactan proteins in maize coleoptiles: developmental relationship to cell death during xylem differentiation but not to extension growth. Plant J 7: 25–36
Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5: 9–23
—, Bell JN, Cramer CL, Bailey JA, Varner JE, Lamb CJ (1985) Accumulation of hydroxyproline-rich glycoproteins mRNAs in response to fungal elicitor and infection. Proc Natl Acad Sci USA 82: 6551–6555
Smallwood M, Beven A, Donovan N, Neill SJ, Peart J, Roberts K, Knox JP (1994) Localization of cell wall proteins in relation to the developmental anatomy of the carrot root apex. Plant J 5: 237–246
—, Martin H, Knox JP (1995) An epitope of rice threonin- and hydroxyproline-rich glycoprotein is common to cell wall and hydrophobic plasma-membrane glycoproteins. Planta 196: 510–522
Sommer-Knudsen J, Bacic A, Clarke AE (1998) Hydroxy-proline rich plant glycoproteins. Phytochemistry 47: 483–497
Stacey NJ, Roberts K, Carpita NC, Wells B, McCann MC (1995) Dynamic changes in cell surface molecules are very early events in the differentiation of mesophyll cells fromZinnia elegans into tracheary elements. Plant J 8: 891–906
Stephens EL (1912) The structure and development of the haustorium ofStriga lutea. Ann Bot 26: 1067–1076
Tagu D, Walker N, Ruiz-Avila L, Burgess S, Martínez-Izquierdo JA, Leguay JJ, Netter P, Puigdomènech P (1992) Regulation of the maize HRGP gene expression by ethylene and wounding: mRNA accumulation and qualitative expression analysis of the promoter by microprojectile bombardement. Plant Mol Biol 20: 529–538
Thiéry JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6: 987–1018
Vance CP, Kirk TK, Sherwood RT (1980) Lignification as a mechanism of disease resistance. Annu Rev Phytopathol 180: 259–288
VandenBosch KA, Bradley DJ, Knox JP, Perotto S, Butcher GW, Brewin NJ (1989) Common components of the infection thread matrix and the intercellular space identified by immunocyto-chemical analysis of pea nodules and uninfected roots. EMBO J 8: 335–342
Visser JH, Dörr I, Kollmann R (1990) Compatibility ofAlectra vogelii with different leguminous host species. J Plant Physiol 135: 737–745
Weber HC (1993) Parasitismus von Blütenpflanzen. Wissenschaftliche Buchgesellschaft, Darmstadt
Westwood JH, Yu X, Foy CL, Cramer CL (1998) Expression of a defense-related 3-hydroxy-3-methylglutaryl CoA reductase gene in response to parasitization byOrobanche spp. Mol Plant Microbe Interact 11: 530–536
Whitmore FW (1978) Lignin-protein complex catalyzed by peroxidase. Plant Sci Lett 13: 241–245
Wiesner J (1878) Note über das Verhalten des Phloroglucins und einiger verwandter Körper zur verholzten Zellmembran. Sitzungsber Math Naturwiss Cl Akad Wiss Wien 77: 60–66
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Neumann, U., Vian, B., Weber, H.C. et al. Interface between haustoria of parasitic members of the Scrophulariaceae and their hosts: A histochemical and immunocytochemical approach. Protoplasma 207, 84–97 (1999). https://doi.org/10.1007/BF01294716
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01294716