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Germination of the seeds of parasitic angiosperms

Published online by Cambridge University Press:  19 September 2008

D. C. Logan  and
G. R. Stewart
D. C. Logan*
Affiliation:
Striga Research Group, Department of Biology (Darwin Bldg), University College London, Gower Street, London WC1E 6BT, UK
G. R. Stewart
Affiliation:
Striga Research Group, Department of Biology (Darwin Bldg), University College London, Gower Street, London WC1E 6BT, UK
*
* Correspondence and present address Department of Physiology, Horticulture Research International, East Malling, West Malling, Kent ME19 6BJ, UK
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Abstract

Totalling more than 3000 species, parasitic angiosperms are a most diverse group of organisms. Classified as either shoot or root parasites according to site of attachment, plant parasites are further classified, according to the degree of parasitism, into one of two divisions: holoparasitic or hemiparasitic. Within these divisions, angiosperm parasites are either obligate or facultative.

Obligate parasites cannot survive to maturity without attaching to a host plant, thus the need to germinate in close proximity to a host first characterizes the specialized germination and seed dispersal strategies of these plants. However, seeds of all species of the rootholoparasitic Orobanchaceae and four genera within the Scrophulariaceae have evolved very specialized germination strategies. Once the seeds have undergone an after-ripening period, they require a prolonged imbibition period at temperatures of approx. 30°C before they acquire the potential to germinate. Minute seeds with very little reserves, they must germinate within millimetres of the host root for successful host attachment and continued survival. To this end, germination only occurs in responseto specific chemical germination triggers released from the host root. In Striga hermonthica (Del.) Benth., the perception of the host-derived trigger results in stimulation of endogenous ethylene production and it is this ethylene that initiates germination. It is proposed that the chemical triggers released from the host be consideredas ‘elicitors’ which function primarily as allelochemicals and that the parasite seeds have become adapted in such a way as to have an absolute requirement for external germination triggers.

Keywords

StrigaOrobancheethyleneallelochemicals
Type
Invited Review
Information
Seed Science Research , Volume 2 , Issue 4 , December 1992 , pp. 179 - 190
Copyright
Copyright © Cambridge University Press 1992

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Footnotes

†

Present address Department of Botany, University of Queensland, St Lucia, Brisbane Qld, Australia 4067

References

Abeles, F.B. (1973)Ethylene in plant biology.New York, Academic Press.Google Scholar
Abeles, F.B. (1986) Role of ethylene in Lactuca sativa cv. Grand Rapids’ seed germination. Plant Physiology 81, 780–787.CrossRefGoogle Scholar
Abeles, F.B. and Lonski, J., (1969) Stimulation oflettuce seedgermination by ethylene. Plant Physiology 44, 277–280.CrossRefGoogle Scholar
Adams, D.O. and Yang, S.F., (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-l-carboxylic acid as an intermediate in the conversion of methionine to ethylene.Proceedings ofthe National Academy of Sciences of the USA 76, 170–174.CrossRefGoogle Scholar
Barton, L.V. (1965) Dormancy in seeds imposed by theseed coat. Handbook of Plant Physiology, 151, 727–745.Google Scholar
Bebawi, F.F. and Eplee, R.E., (1986) Efficacy of ethylene as agermination stimulant of Striga hermonthica. Weed Science 34, 694–698.CrossRefGoogle Scholar
Beck von Mannagetta, G., (1930) Orobanchaceae, pp. 1–348 in Engler, A., Das Pflanzenreich, 96, (IV 261).Google Scholar
Bewley, J.D. and Black, M., (1982) Physiology andbiochemistry of seeds in relation to germination. Springer-Verlag, Berlin.CrossRefGoogle Scholar
Botha, P.J., (1950) The germination of the seeds of angiospermous root-parasites. I. The nature of the changes occurring during pre-exposure of the seed of Alectra vogelii Benth. Journal of South African Botany 16, 23–28.Google Scholar
Bradow, J.M., Connick, W.J. and Pepperman, A.B., (1988) Comparison of the seed germination effects of synthetic analogues of strigol, gibberellic acid, cytokinins and other plant growth regulators. Journal of Plant Growth Regulation 7, 227–239.CrossRefGoogle Scholar
Bradow, J.M., Connick, W.J., Pepperman, A.B. and Wartelle, L.H. (1990) Germination stimulation in wild oats (Avena fatua L.) by synthetic strigolanalogues and gibberellic acid. Journal of Plant Growth Regulation 9, 35–41.CrossRefGoogle Scholar
Brooks, D.W., Bevinakatti, H.S. and Powell, D.R., (1985) The absolute structure of (+)-strigol. Journal of Organic Chemistry 50, 2779–2781.CrossRefGoogle Scholar
Brown, R. and Edwards, M., (1944) The germination of the seed of Striga lutea. I. Host influence and the progress of germination. Annals of Botany 8, 131–148.CrossRefGoogle Scholar
Brown, R. and Edwards, W.G.H., (1945) Effects of thiourea and allylthiourea on the germination of the seeds of Striga lutea. Nature 155, 455–456.CrossRefGoogle Scholar
Brown, R. and Edwards, M., (1946) The germination of the seed of Striga lutea. II. The effect of time of treatment and of concentration of the host stimulant. Annals of Botany 10, 133–142.CrossRefGoogle Scholar
Chang, M., Netzly, D.H., Butler, L.G. and Lynn, D.G., (1986) Chemical regulation of distance: characterization of the first natural host germinationstimulant for Striga asiatica. Journal of the American Chemical Society 108, 7858–7860.CrossRefGoogle ScholarPubMed
Chun, D., Wilhelm, S. and Sagen, J.E., (1979) Components of record germination in vitro of branched broomrape, Orobanche ramosa L. pp. 18 & 2 in Musselman, L.J., Worsham, A.D. and Eplee, R.E.(Eds), Supplement to the Proceedings of the Second International Symposium on Parasitic Weeds. Raleigh, North Carolina State University.Google Scholar
Cocucci, A.E., (1965) Estudios en el genero Prosopanche (Hydnoraceae). I. Revision taxonomica. Kurtziana 2, 53–73.Google Scholar
Cook, C.E., Whichard, L.P., Turner, B., Wall, M.E. and Egley, G.H., (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties ofa potent stimulant. Science 154, 1189–1190.CrossRefGoogle Scholar
Cook, C.E., Whichard, L.P., Wall, M.E., Egley, G.H., Coggan, P., Luhan, P.A. and McPhail, A.T. (1972) Germination stimulants. II. The structure of strigol—a potent seed germination stimulant for witchweed (Striga lutea Lour.). Journal of the American Chemical Society 94, 6198–6199.CrossRefGoogle Scholar
Curtis, R.W. (1968) Mediation of a plant response to malformin by ethylene. Plant Physiology 43, 76–80.CrossRefGoogle ScholarPubMed
Curtis, E.J.C. and Cantlon, J.E. (1963) Germination of Melampyrum lineare: interrelated effects of after-ripening and gibberellic acid. Science 140, 406–408.CrossRefGoogle Scholar
Curtis, E.J.C. and Cantlon, J.E., (1968) Seed dormancy and germination in Melampyrum lineare. American Journal of Botany 55, 26–32.CrossRefGoogle Scholar
Dawson, J.H., (1965) Prolonged emergence of field dodder. Weeds 13, 373–374.CrossRefGoogle Scholar
Doggett, H., (1965) Striga hermonthica on sorghum in East Africa. Journal of Agricultural Science 65, 83–94.Google Scholar
Edwards, W.G.H., (1972) Orobanche and other plant parasite factors. pp. 235–248 in Harborne, J.B. (Ed.) Phytochemical ecology New York, Academic Press.Google Scholar
Egley, G.H. (1972) Influence of the seed envelope and growth regulators upon seed dormancy in witchweed (Striga lutea Lour.). Annals of Botany 36, 755–770.CrossRefGoogle Scholar
Egley, G.H. and Dale, J.E., (1970) Ethylene, 2-chlorethylphosphonic acid and witchweed germination. Weed Science 18, 586–589.CrossRefGoogle Scholar
Eliasson, L., Bertell, G. and Bolander, E., (1989) Inhibitory action of auxin on root elongation not mediated by ethylene. Plant Physiology 91, 310–314.CrossRefGoogle Scholar
Fate, G.D., Chang, M. and Lynn, D.G., (1990) Control of germination in Striga asiatica: chemistry of spatial definition.Plant Physiology 93, 201–207.CrossRefGoogle ScholarPubMed
Ferguson, I.B. and Mitchell, R.E., (1985) Stimulation of ethylene production in bean leaf discs by the pseudomonad phytotoxin coronatine. Plant Physiology 77, 969–973.CrossRefGoogle ScholarPubMed
Fischer, N.H., Weidenhamer, J.D., Riopel, J.L., Quilano, L. and Menelaou, M.A., (1990) Stimulation of witchweed germination by sesquiterpene lactones: a structure activity study. Phytochemistry 29, 2479–2483.CrossRefGoogle Scholar
French, R.C. and Sherman, L.J., (1976) Factors affecting dormancy, germination and seedling development of Aeginetia indica. American Journal of Botany 63, 558–570.CrossRefGoogle Scholar
Gaertner, E.E., (1950) Studies of seed germination, seed identification and relationships in dodders, Cuscuta spp. Cornell University Agriculture Experimental Station Memoir 294.Google Scholar
Garman, H., (1903) The broomrapes. Bulletin of the Kentucky Agricultural Experimental Station 105,1–32.Google Scholar
Govier, R.N. and Harper, J.L., (1965) Angiospermous hemiparasites. Nature 205, 722–723.CrossRefGoogle Scholar
Hauck, C., Muller, S. and Schildknecht, H., (1992) A germination stimulant for parasitic flowering plants from Sorghum bicolor, a genuine host.Journal of Plant Physiology 139, 474–478.CrossRefGoogle Scholar
Heather, J.B., Mittal, R.S.D. and Sib, C.J., (1974) Total synthesis of dl-strigol. Journal of the American Chemical Society 96,1976–1977.CrossRefGoogle Scholar
Heather, J.B., Mittal, R.S.D. and Sih, C.J., (1976) Synthesisof the witchweed seed germination stimulant (+)-strigol. Journal of the American Chemical Society 98, 3661–3669.CrossRefGoogle Scholar
Heinricher, E., (1917) Zur Physiologie der schmarotzenden Rhinnantheen, besonders der Halbparasiten. Naturwissenschaften 5, 113–119.Google Scholar
Herb, R., Visser, J.H. and Schildknecht, H. (1987) Recovery, isolation and preliminary structural investigation of germination stimulants produced by Vigna unguiculata Walp. cv. Saunders Upright. pp. 351–356 in Weber, H.C. and Forstreuter, W. (Eds) Parasitic flowering plants. Proceedings of the 4th Inte rnational Symposium on Parasitic Flowering Plants. Marburg, Phillips Universitat.Google Scholar
Hsiao, A.I., Worsham, A.D. and Moreland, D.E. (1979) Factors affecting conditioning and germination of witchweed (Striga asiatica (L). Kuntze)seeds under laboratory conditions. pp. 193–201 in Musselman, L.J.,Worsham, A.D. and Eplee, R.E. (Eds) Proceedings of the 2nd Inte rnational Symposium on Parasitic Weeds. Raleigh, North Carolina State University.Google Scholar
Hsiao, A.I., Worsham, A.D. and Moreland, D.E., (1981) Effectsof sodium hypochlorite and certain growth regulators on germination of witchweed (Striga asiatica) seeds. Weed Science 29, 98–100.CrossRefGoogle Scholar
Hsiao, A.I., Worsham, A.D. and Moreland, D.E., (1987) Effectsof drying and dl-strigol on seed conditioning and germination of Striga asiatica (L.) Kuntze. Weed Research 27, 321–328.CrossRefGoogle Scholar
Igbinnosa, I. and Okonkwo, S.N.C. (1992) Stimulation of germination of seeds of cowpea witchweed (Striga gesnerioides) by sodium hypochlorite and some growth regulators. Weed Science 40, 25–28.CrossRefGoogle Scholar
Jackson, M.B. and Parker, C. (1991) Induction of germination bystrigol analogues requires ethylene action in Striga hermonthica but not in S. forbesii. Journal of Plant Physiology 138, 383–386.CrossRefGoogle Scholar
Johnson, A.W., Rosebury, G. and Parker, C. (1976) A novel approach to Striga and Orobanche control using synthetic germination stimulants. Weed Research 16, 223–227.CrossRefGoogle Scholar
Johnson, A.W., Gowda, G., Hassanali, A., Knox, J., Monaco, S., Razavi, Z. and Rosebury, G. (1981) The preparation of synthetic analogues of strigol. Journal of the Chemical Society, Perkin Transactions I (no volume nos.), 1734–1743.CrossRefGoogle Scholar
Kenyon, J. (1991) Investigation into the mechanism of action of coronatine—a phytotoxin. PhD thesis, University of East Anglia.Google Scholar
Ketring, D.L. and Morgan, P.W. (1969) Ethylene as a component of the emanations from germinating peanut seeds and its effect on dormant Virginia-typeseeds. Plant Physiology 44, 326–330.CrossRefGoogle Scholar
Ketring, D.L. and Morgan, P.W. (1971) Physiology of oil seeds. II. Dormancy release in Virginia-type peanut seeds by plant growth regulators. Plant Physiology 47, 488–492.CrossRefGoogle ScholarPubMed
Kuijt, J. (1969) The biology of parasitic flowering plants. Berkeley, University of California Press.Google Scholar
Kumar, U. and Rangaswamy, N.S. (1977) Regulation of seed germination and polarity in seedling development in Orobanche aegyptiaca by growth substances. Biologia Plantarum 19, 253–259.CrossRefGoogle Scholar
Kusano, S. (1908) Further studies on Aeginetia indica. [Not seen in original, as referred to in Kuijt, 1969].Google Scholar
Kust, C.A. (1966) A germination inhibitor in Striga seeds. Weeds 14, 327–329.CrossRefGoogle Scholar
Logan, D.C. and Stewart, G.R. (1991) Role of ethylene inthe germination of the hemiparasite Striga hermonthica. Plant Physiology, 97, 1435–1438.CrossRefGoogle Scholar
Lynn, D.G. and Chang, M. (1990) Phenolic signals in cohabitation: implications for plant development. Annual Review of Plant Physiology and Molecular Biology 41, 497–526.CrossRefGoogle Scholar
Malcolm, W.M. (1966) Root parasitism of Castilleja coccinea. Ecology 47, 179–186.CrossRefGoogle Scholar
Mayer, A.M. and Poljakoff-Mayber, A. (1989) The germination ofseeds, 4th edn. Oxford, Pergamon Press.Google Scholar
Mhehe, G.L. (1987), A novel chemical approach to the control ofwitchweed (Striga asiatica L. Kuntze) and other Striga spp. (Scrophulariacea). pp. 563–574 in Webber, H.C. and Forstreuter, W. (Eds) Parasitic flowering plants. Proceedings of the 4th Inte rnational Symposium on Parasitic Flowering Plants. Marburg, Phillips Universitat.Google Scholar
Musselman, L.J. (1969) Observations on the life history of Aureolaria grandiflora and Aureolaria pedicularia (Scrophulariaceae). American Midland Naturalist 82, 307–311.CrossRefGoogle Scholar
Netzly, D.H. and Butler, L.G. (1986) Roots of sorghum exude hydrophobic droplets containing biologically active components. Crop Science 26, 775–778.CrossRefGoogle Scholar
Netzly, D.H., Riopel, J.L., Ejeta, G. and Butler, L.G. (1988) Germination stimulants of witchweed (Striga asiatica) from hydrophobic root exudate of sorghum (Sorghum bicolor). Weed Science 36, 441–446.CrossRefGoogle Scholar
Okonkwo, S.N.C. and Nwoke, F.I.O. (1974) Seed germination of Buchnera hispida Buch. Annals of Botany 38, 409–417.CrossRefGoogle Scholar
Okonkwo, S.N.C. and Nwoke, F.I.O. (1975) Bleach-induced germination and breakage of dormancy of seeds of Alectra vogelii. PhysiologiaPlantarum 35, 175–180.Google Scholar
Pearson, H.H.W., (1911) On the rooibloem (isona or witchweed). South African Agricultural Journal 2, 651–655.Google Scholar
Pieterse, A.H. (1979) The broomrapes (Orobanchaceae) — a review. Abstracts on Tropical Agriculture 5, 9–35.Google Scholar
Pieterse, A.H., Ebbers, A.E.H. and Pesch, C.J. (1984) A studyon ‘wet dormancy’ in seeds of Striga hermonthica (Del.) Benth. invitro. pp. 99–107 in Parker, C., Musselman, L.J., Polhill, R.M. and Wilson, A.K. (Eds) Proceedings of the 3rd Inte rnational Symposium on Parasitic Weeds. Aleppo, ICARDA.Google Scholar
Press, M.C., Shah, N., Tuohy, J.M. and Stewart, G.R. (1987) Carbon isotope ratios demonstrate carbon flux from C4 host to C3 parasite. Plant Physiology 85, 1143–1145.CrossRefGoogle ScholarPubMed
Press, M.C., Graves, J.D. and Stewart, G.R. (1990) Physiologyof the interaction of angiosperm parasites and their higher plant hosts. Plant, Cell and Environment 13, 91–104.CrossRefGoogle Scholar
Ramasubramanian, T.S., Paliyath, G., Rajagopal, I., Maheshwari, R. and Mahadevan, S. (1988) Hormones and Cuscuta development: in vitro induction of haustoria by cytokinin and its inhibition by other hormones. Journal of Plant Growth Regulation 7, 133–144.CrossRefGoogle Scholar
Rangaswamy, N.S. and Rangan, T.S. (1966) Effects of seed germination stimulants on the witchweed Striga euphrasioides (Vahl.) Benth. Nature 210, 440–441.CrossRefGoogle Scholar
Reid, D.C. and Parker, C. (1979) Germination of Striga species. pp. 202–210 in Musselman, L.J., Worsham, A.D. and Eplee, R.E. (Eds) Proceedings of the 2nd Inte rnational Symposium on Parasitic Weeds.. Raleigh, North Carolina State University.Google Scholar
Roberts, D.W.A. (1951) Some effects of ethylene on germinating wheat. Canadian Journal of Botany 29, 10–25.CrossRefGoogle Scholar
Saghir, A.R. (1986) Dormancy and germination of Orobancheseeds in relation to control methods. pp. 25–34 in ter Borg, S.J. (Ed.) Biology and control of Orobanche. Wageningen, Netherlands, LH/VPO.Google Scholar
Sahai, A. and Shivanna, K.R. (1982) Seed germination and seedling morphogenesis in parasitic angiosperms of the families Scrophulariaceae and Orobanchaceae. Seed Science and Technology 10, 565–583.Google Scholar
Saunders, A.R. (1933) Studies on phanerogamic parasitism with particular reference to Striga lutea Lour. Department of Agriculture of South Africa Scientific Bulletin 128.Google Scholar
Shivanna, K.R. and Rangaswamy, N.S. (1976) Seedling germination and seedling morphogenesis of the root parasite Sopubia delphinifolia G. Don. Zeitschrift f¨r Pflanzenphysiologie 84, 391–398.Google Scholar
Stewart, G.R. and Press, M.C. (1990) The physiology and biochemistry of parasitic angiosperms. Annual Review of Plant Physiology and Molecular Biology 41, 127–151.CrossRefGoogle Scholar
Sunderland, N. (1960) The production of the Striga and Orobanche germination stimulants by maize roots. 1. The number and variety ofstimulants. Journal of Experimental Botany 11, 236–245.CrossRefGoogle Scholar
Suttle, J.C. (1984) Effect of the defoliant thidiazuron on ethylene evolution from mung bean hypocotyl segments. Plant Physiology 75, 902–907.CrossRefGoogle ScholarPubMed
Takeuchi, Y., Worsham, A.D. and Awad, A.E. (1991) Effects of brassinolide on conditioning and germination of witchweed (Striga asiatica) seeds. pp. 298–305 in Cutler, G.C., Yokota, T. and Adam, G. (Eds) Brassinosteroids Washington DC, ACS Symposium Series 474.CrossRefGoogle Scholar
Taylorson, R.B. (1979) Response of weed seeds to ethylene and related hydrocarbons. Weed Science 27, 7–10.CrossRefGoogle Scholar
Toole, V.K., Bailer, W.K. and Toole, E.H. (1964) Factors influencing dormancy of peanut seeds. Plant Physiology 39, 822–832.CrossRefGoogle ScholarPubMed
Vallance, K.B. (1950) Studies on the germination of the seeds of Striga hermonthica. I. The influence of moisture-treatment, stimulant-dilutionand after-ripening on germination. Annals of Botany 14, 347–363.CrossRefGoogle Scholar
Vallance, K.B. (1951) Studies on the germination of the seeds of Striga hermonthica. III. On the nature of pretreatment and after-ripening. Annals of Botany 15, 110–128.CrossRefGoogle Scholar
Vallance, K.B. (1952) The germination of Rhinanthus cristagalli. Annals of Botany 16, 409–420.CrossRefGoogle Scholar
Vaucher, J.P. (1823) Memoire sur la germination des orobanches. Memoires de Musee d'Histoire Naturelle de Paris 10, 261–273.Google Scholar
Visser, J.H. (1975) Germination stimulants of Alectra vogelii Benth. seed. Zeitschrift für Pflanzenphysiologie 74, 464–469.CrossRefGoogle Scholar
Visser, J.H. and Botha, P.J. (1974) Chromatographic investigation of the Striga seed germination stimulant. Zeitschrift für Pflanzenphysiologie 72, 352–358.CrossRefGoogle Scholar
Visser, J.H., Herb, R. and Schildknecht, H. (1987) Recovery and preliminary chromatographic investigation of germination stimulants produced by Vigna unguiculata Walp. cv. Saunders Upright. Journal of Plant Physiology 129, 375–381.CrossRefGoogle Scholar
Walzel, G. (1952) Colchicinierte Cuscuta Nikotinfrei. Phyton (Austria) 4, 137–143. (not seen in original; as cited by Kuijt, 1969).Google Scholar
Wild, H. (1954) Rhodesian witchweeds. Rhodesian Agricultural Journal 51, 330–342.Google Scholar
Williams, C.N. (1959) Action of inhibitor-B on the growth of Striga seedlings. Nature 184, 1577–1578.CrossRefGoogle Scholar
Williams, C.N. (1960) Growth movements of the radicle of Striga. Nature 188, 1043–1044.CrossRefGoogle Scholar
Williams, C.N. (1961a) Tropism and morphogenesis of Striga seedlings in the host rhizosphere. Annals of Botany 25 407–415.CrossRefGoogle Scholar
Williams, C.N. (1961b) Growth and morphogenesis of Striga seedlings. Nature 189, 378–381.CrossRefGoogle Scholar
Williams, C.N. (1962) Non-geotropic growth curvatures in the Striga radicle. Annals of Botany 26, 647–655.CrossRefGoogle Scholar
Witt, W.W. and Weber, J.B. (1975) Ethylene movement in soils and soil constituents. Weed Science 23, 302–307.CrossRefGoogle Scholar
Worsham, A.D. (1987) Germination of witchweed seeds.Google Scholar