Skip to main content
SpringerLink
Log in

Epidermal derivatives as xylem elements and transfer cells: a study of the host-parasite interface in two species of Triphysaria (Scrophulariaceae)

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Haustoria ofTriphysaria pusilla andT. versicolor subsp.faucibarbata from a natural habitat were analysed by light and electron microscopy. The keel-shaped edge of the secondary haustorium generally splits the epidermis and cortex of the host root parallel to the root axis, and penetrates to the host vascular tissue. Anticlinally elongated epidermal cells of the haustorium constitute most of the host/parasite interface. Some of these epidermal cells are divided by oblique cell walls. Some of their oblique daughter cells as well as some undivided epidermal cells differentiate into xylem elements. Single epidermal cells occasionally intrude into the vascular tissue of the host and individual host cells can be invaded. The surface area of the plasmalemma in parasitic parenchymatous interface cells is increased by the differentiation of wall labyrinths characteristic of transfer cells and by the development of membrane-lined cytoplasmic tubules or flattened sacs which become embedded in the partly lignified interface cell-wall. Mycorrhizal fungal hyphae enter the xylem bridge in some haustoria. Implications of these observations for the function of the haustorium are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alexander T, Weber HC (1985) Zur parasitischen Lebensweise vonParentucellia latifolia (L.) Caruel (Scrophulariaceae). Beitr Biol Pflanzen 60: 23–34

    Google Scholar 

  • Alosi MC, Calvin CL (1985) The ultrastructure of dwarf mistletoe (Arceuthobium spp.) sinker cells in the region of the host secondary vasculature. Can J Bot 63: 889–898

    Google Scholar 

  • Atsatt PR, Hansen IM (1978) Correlations between haustoria formation and parasitic development inOrthocarpus purpurascens (Scrophulariaceae). Ann Bot 42: 1271–1276

    Google Scholar 

  • Baird WV, Riopel JL (1984) Experimental studies of haustorium initiation and early development inAgalinis purpurea (L.) Raf. (Scrophulariaceae). Amer J Bot 71: 803–814

    Google Scholar 

  • — — (1985) Surface characteristics of root and haustorial hairs of parasitic Scrophulariaceae. Bot Gaz 146: 63–69

    Google Scholar 

  • Cantlon JE, Curtis EJC, Malcolm WM (1963) Studies ofMelampyrum lineare. Ecology 44: 466–474

    Google Scholar 

  • Chuang TI, Heckard LR (1991) Generic realignment and synopsis of subtribe Castillejinae (Scrophulariaceae — tribe Pediculareae). Syst Bot 16: 644–666

    Google Scholar 

  • Coetzee J, Fineran BA (1987) The apoplastic continuum, nutrient absorption and plasmatubules in the dwarf mistletoeKorthalsella lindsayi (Viscaceae). Protoplasma 136: 145–153

    Google Scholar 

  • Dobbins DR, Kuijt J (1973) Studies on the haustorium of Castilleja (Scrophulariaceae). II. The endophyte. Can J Bot 51: 923–931+6 plates

    Google Scholar 

  • Dörr I (1969) Feinstruktur intrazellular wachsender Cuscuta-Hyphen. Protoplasma 67: 123–137

    Google Scholar 

  • — (1972) Der Anschluß der Cuscuta-Hyphen an die Siebröhren ihrer Wirtspflanzen. Protoplasma 75: 167–184

    Google Scholar 

  • —, Kollmann R (1974) Strukturelle Grundlage des Parasitismus bei Orobanche. I. Wachstum der Haustorialzellen im Wirtsgewebe. Protoplasma 80: 245–259

    Google Scholar 

  • — — (1976) Strukturelle Grundlagen des Parasitismus bei Orobanche. III. Die Differenzierung des Xylemanschlusses beiO. crenata. Protoplasma 89: 235–249

    Google Scholar 

  • Eschrich W, Currier HB (1964) Identification of callose by its diachrome and fluorochrome reactions. Stain Technol 39: 303–307

    Google Scholar 

  • Fahn A (1982) Plant anatomy, 3rd edn. Pergamon Press, Oxford

    Google Scholar 

  • Feder N, O'Brien TP (1968) Plant microtechnique: some principles and new methods. Amer J Bot 55: 123–142

    Google Scholar 

  • 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

  • Gedalovich-Shedletzky E, Kuijt J (1990) An ultrastructural study of the tuber of Balanophora (Balanophoraceae). Can J Bot 68: 1271–1279

    Google Scholar 

  • Gunning BES, Pate JS (1969) “Transfer cells”. Plant cells with wall ingrowths, specialized in relation to short distance transport of solutes — their occurrence, structure and development. Protoplasma 68: 107–133

    Google Scholar 

  • — — (1974) Transfer cells. In: Robards AW (ed) Dynamic aspects of plant ultrastructure. McGraw-Hill, London, pp 441–480

    Google Scholar 

  • Guttenberg H von (1968) Der primäre Bau der Angiospermenwurzel. Handbuch der Pflanzenanatomie vol VIII, 5. Gebrüder Borntraeger, Berlin

    Google Scholar 

  • Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic Press, London

    Google Scholar 

  • Harris N, Oparka KJ, Walker-Smith DJ (1982) Plasmatubules: an alternative to transfer cells? Planta 156: 461–465

    Google Scholar 

  • Heide-JØrgensen HS (1989) Development and ultrastructure of the haustorium ofViscum minimum Harvey. I. The adhesive disk. Can J Bot 67: 1161–1173

    Google Scholar 

  • — (1991) Anatomy and ultrastructure of the haustorium ofCassytha pubescens R. Br. I. The adhesive disk. Bot Gaz 152: 321–334

    Google Scholar 

  • Hofmann M, Voigt H (1987)Pedicularis groenlandica Retz. andPedicularis rosea Wulf. two hemiparasitic members of the Scrophulariaceae. In: Weber HC, Forstreuter W (eds) Parasitic flowering plants. Proceedings of the 4th International Symposium on Parasitic Flowering Plants, Marburg, pp 391–402

  • Jensen WA (1962) Botanical histochemistry. Principles and practice. Freeman, San Francisco

    Google Scholar 

  • Joel DM, Heide-JØrgensen HS (1985) Ultrastructure and development of the pitcher epithelium ofSarracenia. Israel J Bot 34: 331–349

    Google Scholar 

  • Krause D (1989) Striga — Biologie, Schaden, Kontrolle. Mikrokosmos 78: 289–294

    Google Scholar 

  • Kubat R, Weber HC (1988) Zur Biologie vonRhynchocorys elephas (L.) Griseb. (Scrophulariaceae). Beitr Biol Pflanzen 62: 239–250

    Google Scholar 

  • Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley

    Google Scholar 

  • — (1977) Haustoria of phanerogamic parasites. Annu Rev Phytopathol 17: 91–118

    Google Scholar 

  • — (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. CIM-MYT, Nairobi, pp 1–5

    Google Scholar 

  • —, Toth R (1976) Ultrastructure of angiosperm haustoria — a review. Ann Bot 40: 1121–1130

    Google Scholar 

  • Kuo J, Pate JS, Davidson NJ (1989) Ultrastructure of the haustorial interface and apoplastic continuum between host and the root hemiparasiteOlax phyllanthi (Labill.) R. Br. (Olacaceae). Protoplasma 150: 27–39

    Google Scholar 

  • Letvenuk LJ, Peterson RL (1976) Occurrence of transfer cells in vascular parenchyma ofHieracium florentinum roots. Can J Bot 54: 1458–1471

    Google Scholar 

  • Moore R (1982) Further evidence for cell wall deposition during graft formation. Ann Bot 50: 599–604

    Google Scholar 

  • Musselman LJ, Dickison WC (1975) The structure and development of the haustorium in parasitic Scrophulariaceae. Bot J Linn Soc 70: 183–212

    Google Scholar 

  • Nwoke FIO (1982) The initiation of the secondary haustorium inAlectra vogelii Benth. Ann Bot 49: 669–676

    Google Scholar 

  • Okonkwo SNC, Nwoke FIO (1978) Initiation, development and structure of the primary haustorium inStriga gesneroides (Scrophulariaceae). Ann Bot 42: 455–463

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Peterson RL, Yeung EC (1975) Ontogeny of phloem transfer cells inHieracium floribundum. Can J Bot 53: 2745–2758

    Google Scholar 

  • Piehl MA (1962) The parasitic behavior ofMelampyrum lineare and a note on its seed color. Rhodora 64: 15–23

    Google Scholar 

  • Ransom JK, Musselman LJ, Worsham AD, Parker C (eds) (1991) Proceedings of the 5th International Symposium of Parasitic Weeds. CIMMYT, Nairobi

    Google Scholar 

  • Richardson KC, Jarett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35: 313–323

    PubMed  Google Scholar 

  • Riopel JL, Musselman LJ (1979) Experimental initiation of haustoria inAgalinis purpurea (Scrophulariaceae). Amer J Bot 66: 570–575

    Google Scholar 

  • Rogers WE, Nelson RR (1962) Penetration and nutrition ofStriga asiatica. Phytopathology 52: 1064–1070

    Google Scholar 

  • Sablon ML du (1887) Recherches sur les organes d'absorption des plantes parasites (Rhinanthées et Santalacées). Ann Sci Nat Ser 7 [Bot] 6: 90–117+3 plates

    Google Scholar 

  • Sallé G (1975) Etude 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

    Google Scholar 

  • Snetselaar KM, Whitney KD (1990) Fungal calcium oxalate in mycorrhiza ofMonotropa uniflora. Can J Bot 68: 533–543

    Google Scholar 

  • Strullu DG (1985) Les mycorhizes. Handbuch der Pflanzenanatomie vol XIII, 2. Gebrüder Borntraeger, Berlin

    Google Scholar 

  • Thomson J (1925) Studies in irregular nutrition. No. I. The parasitism ofCuscuta reflexa (Roxb.). Trans R Soc Edin 54: 343–356

    Google Scholar 

  • Thurman LD (1966) Genecological studies in Orthocarpus subgenus Triphysaria (Scrophulariaceae). Doctoral dissertation, University of California, Berkeley

    Google Scholar 

  • Tiedemann R (1989) Graft union development and symplastic phloem contact in the heterograftCucumis sativus onCucurbita ficifolia. J Plant Physiol 134: 427–440

    Google Scholar 

  • Toth R, Kuijt R (1977) Anatomy and ultrastructure of the haustorium in Comandra (Santalaceae). Can J Bot 55: 455–469

    Google Scholar 

  • Weber HC (1976) Anatomische Studien an den Haustorien einiger parasitischer Scrophulariaceen Mitteleuropas. Ber Dtsch Bot Ges 89: 57–84

    Google Scholar 

  • - (1987) Untersuchungen an parasitischen Scrophulariaceen (Rhinanthoideen) in Kultur. II. Interaktionen zwischen Parasit und Wirt. Flora: 35–44

  • - Forstreuter W (eds) (1987) Parasitic flowering plants. Proceedings of the 4th International Symposium on Parasitic Flowering Plants, Marburg

  • —, Sunaryo (1990) Kolbenträgerschmarotzer (Balanophoraceae): extreme Blütenpflanzen mit pilzlichem Charakter. Biol Rundsch 28: 83–86

    Google Scholar 

  • Yeung EC, Peterson RL (1975) Fine structure during ontogeny of xylem transfer cells in the rhizome ofHieracium floribundum. Can J Bot 53: 432–438

    Google Scholar 

Download references

Author information

Author notes

  1. H. S. Heide-JØrgensen

    Present address: Botanical Institute, Department of Plant Ecology, University of Copenhagen, Øster Farimagsgade 2D, DK-1353, Copenhagen K, Denmark

Authors and Affiliations

  1. Department of Biology, University of Victoria, Victoria, British Columbia

    H. S. Heide-JØrgensen & J. Kuijt

Authors
  1. H. S. Heide-JØrgensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Kuijt
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heide-JØrgensen, H.S., Kuijt, J. Epidermal derivatives as xylem elements and transfer cells: a study of the host-parasite interface in two species of Triphysaria (Scrophulariaceae). Protoplasma 174, 173–183 (1993). https://doi.org/10.1007/BF01379049

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01379049

Keywords

Search

Navigation