Plant Biol (Stuttg) 2001; 3(3): 244-250
DOI: 10.1055/s-2001-15195
Review Article
Georg Thieme Verlag Stuttgart ·New York

Impacts of Infection by Parasitic Angiosperms on Host Photosynthesis

J. R. Watling 1 , M. C. Press 2
  • 1 Department of Environmental Biology, University of Adelaide, Adelaide, Australia
  • 2 Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK
Further Information

Publication History

February 1, 2001

April 6, 2001

Publication Date:
31 December 2001 (online)

Abstract

Parasitic angiosperms are a taxonomically diverse group of plants that invade host tissues and remove resources via a specialized structure known as the haustorium. Through the haustorium, carbon, water and mineral nutrients are withdrawn, often at the expense of host growth and vigour. In addition to the removal of resources from host plants, many parasitic angiosperms are also able to impact host growth via effects on host photosynthesis. In this paper we review what is known about how parasitic angiosperms affect host photosynthesis and the impact this has on host productivity. Holoparasites, that lack chlorophyll, act as extra sinks for host photosynthates and generally either enhance or have a neutral effect on host photosynthetic productivity. In contrast, hemiparasites, that are capable of some autotrophic carbon fixation, usually have a negative impact on host photosynthesis. Irrespective of the outcome of infection, the mechanisms involved in altering host photosynthesis are diverse and may act at either the leaf or whole-plant level. In some cases, parasites impact directly on host photosynthetic metabolism, while in others the effects are more indirect, for example through changing host architecture.

References

  • 01 Barker,  E. R.,, Press,  M. C.,, Scholes,  J. D.,, and Quick,  W. P.. (1996);  Interactions between the parasitic angiosperm Orobanche aegyptiaca and its tomato host: growth and biomass allocation.  New Phytologist. 133 637-642
  • 02 ter Borg,  S. J.. (1985) Effects of environmental factors on Orobanche-host relationships; a review and some recent results. Biology and Control of Orobanche . ter Borg, S. J., ed. Wageningen; The Netherlands pp. 57-69
  • 03 Callaway,  R. M., and Pennings,  S. C.. (1998);  Impact of a parasitic plant on the zonation of two salt marsh perennials.  Oecologia. 114 100-105
  • 04 von Caemmerer,  S., and Farquhar,  G. D.. (1981);  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.  Planta. 153 378-387
  • 05 von Caemmerer,  S., and Furbank,  R. T.. (1999) Modelling C4 photosynthesis. C4 Plant Biology. Sage, R. F. and Monson, R. K., ed. San Diego; Academic Press pp. 173-211
  • 06 Cechin,  I., and Press,  M. C.. (1993 a);  Nitrogen relations of the sorghum-Striga hermonthica host-parasite association: growth and photosynthesis.  Plant, Cell and Environment. 16 237-247
  • 07 Cechin,  I., and Press,  M. C.. (1993 b);  Influence of nitrogen on growth and photosynthesis of a C3 cereal, Oryza sativa, infected with the root hemiparasite Striga hermonthica. .  Journal of Experimental Botany. 45 925-930
  • 08 Dale,  H., and Press,  M. C.. (1998);  Elevated atmospheric CO2 influences the interaction between the parasitic angiosperm Orobanche minor and its host Trifolium repens. .  New Phytologist. 140 65-73
  • 09 Davies,  D. M., and Graves,  J. D.. (1998);  Interactions between arbuscular mycorrhizal fungi and the hemiparasitic angiosperm Rhinanthus minor during co-infection of a host.  New Phytologist. 139 555-563
  • 10 Demmig-Adams,  B., and Adams,  W. W. III. (1992);  Photoprotection and other responses of plants to light stress.  Annual Review of Plant Physiology and Plant Molecular Biology. 43 599-626
  • 11 Drennan,  D. S. H., and El Hiweris,  S. O.. (1979) Changes in growth regulating substances in Sorghum vulgare infected by Striga hermonthica. . Proceedings of the Second Symposium of Parasitic Weeds. Musselman, L. J., Worsham, A. D., and Eplee, R. E., eds. Raleigh, USA; North Carolina State University pp. 144-155
  • 12 Drake,  B. G.,, Gonzàlez-Meler,  M. A.,, and Long,  S. P.. (1997);  More efficient plants: a consequence of rising CO2?.  Annual Review of Plant Physiology and Plant Molecular Biology. 48 609-639
  • 13 Estabrook,  E. M., and Yoder,  J. I.. (1998);  Plant-plant communications: rhizosphere signalling between parasitic angiosperms and their hosts.  Plant Physiology. 116 1-7
  • 14 Farquhar,  G. D.. (1983);  On the nature of carbon isotope discrimination in C4 species.  Australian Journal of Plant Physiology. 10 205-226
  • 15 Fernandes,  G. W.,, de Mattos,  E. A.,, Franco,  A. C.,, Lüttge,  U.,, and Ziegler,  H.. (1998);  Influence of the parasite Pilostyles ingai (Rafflesiaceae) on some physiological parameters of the host plant, Mimosa naguirei (Mimosaceae).  Botanica Acta. 111 51-54
  • 16 Frost,  D. L.,, Gurney,  A. L.,, Press,  M. C.,, and Scholes,  J. D.. (1997);  Striga hermonthica reduces photosynthesis in sorghum: the importance of stomatal limitations and a potential role for ABA?.  Plant, Cell and Environment. 20 483-492
  • 17 Gehring,  C. A., and Whitham,  T. G.. (1992);  Reduced mycorrhizae on Juniperus monosperma with mistletoe: the influence of environmental stress and tree gender on plant parasite and plant-fungal mutualism.  Oecologia. 89 298-303
  • 18 Gómez,  J. M.. (1994);  Importance of direct and indirect effects in the interaction between a parasitic angiosperm (Cuscuta epithymum) and its host plant (Hormathophylla spinosa). .  Oikos. 71 97-106
  • 19 Graves,  J. D.,, Press,  M. C.,, and Stewart,  G. R.. (1989);  A carbon balance model of the sorghum-Striga hermonthica host-parasite association.  Plant, Cell and Environment. 12 101-107
  • 20 Graves,  J. D.. (1995) Host-plant responses to parasitism. Parasitic Plants. Press, M. C. and Graves, J. D., ed. London; Chapman and Hall pp. 206-225
  • 21 Gurney,  A. L.,, Press,  M. C.,, and Ransom,  J. K.. (1995);  The parasitic angiosperm Striga hermonthica can reduce photosynthesis of its sorghum and maize hosts in the field.  Journal of Experimental Botany. 46 1817-1823
  • 22 Hibberd,  J. M.,, Quick,  W. P.,, Press,  M. C.,, and Scholes,  J. D.. (1998);  Can source-sink relations explain responses of tobacco to infection by the root holoparasitic angiosperm Orobanche cernua? .  Plant, Cell and Environment. 21 333-340
  • 23 Hibberd,  J. M.,, Quick,  W. P.,, Press,  M. C.,, Scholes,  J. D.,, and Jeschke,  W. D.. (1999);  Solute fluxes from tobacco to the parasitic angiosperm Orobanche cernua and the influence of infection on host carbon and nitrogen relations.  Plant, Cell and Environment. 22 937-947
  • 24 Jeschke,  W. D.,, Baig,  A.,, and Hilpert,  A.. (1997);  Sink-stimulated photosynthesis, increased transpiration and increased demand-dependent stimulation of nitrate uptake: nitrogen and carbon relations in the parasitic association Cuscuta reflexa-Coleus blumei. .  Journal of Experimental Botany. 148 915-925
  • 25 Jeschke,  W. D.,, Bäumel,  P.,, Räth,  N.,, Czygan,  F-C.,, and Proksch,  P.. (1994);  Modelling the flow and partitioning of carbon and nitrogen in the holoparasite Cuscuta reflexa Roxb. & its host Lupinus albus L. II. Flows between host and parasite and within the parasitized host.  Journal of Experimental Botany. 45 801-812
  • 26 Jeschke,  W. D., and Hilpert,  A.. (1996) Does assimilate or nitrogen supply from the host limit growth of Cuscuta? Experiments with Ricinus communis and Cuscuta reflexa. . Advances in Parasitic Weed Research. Moreno, M. T., Cubero, J. I., Berner, D., Joel, D., Musselman, L. J., and Parker, C., eds. Sevilla, Spain; Junta de Andalucía pp. 373-383
  • 27 Jeschke,  W. D., and Hilpert,  A.. (1997);  Sink-stimulated photosynthesis and sink-dependent increase in nitrate uptake: nitrogen and carbon relations of the parasitic association Cuscuta reflexa-Ricinis communis. .  Journal of Experimental Botany. 20 47-56
  • 28 Kuijt,  J.. (1969) The Biology of Parasitic Flowering Plants. Berkeley; University of California Press
  • 29 Marvier,  M. A.. (1996);  Parasitic plant-host interaction: plant performance and indirect effects on parasite-feeding herbivores.  Ecology. 77 1398-1409
  • 30 Marvier,  M. A., and Smith,  D. L.. (1997);  Conservation implications of host use for rare parasitic plants.  Conservation Biology. 11 839-848
  • 31 Moore,  B. D.,, Cheng,  S.-H.,, Sims,  D.,, and Seemann,  J. R.. (1999);  The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2.  Plant, Cell and Environment. 22 567-582
  • 32 Parker,  C., and Riches,  C. R.. (1993) Parasitic Weeds of the World: Biology and Control. Wallingford, UK; CAB International
  • 33 Pate,  J. S.,, Pate,  S. R.,, Kuo,  J.,, and Davidson,  N. J.. (1990);  Growth, resource allocation and haustorial biology of the root hemiparasite Olax phyllanthi (Olacaceae).  Annals of Botany. 65 437-449
  • 34 Pennings,  S. C., and Callaway,  R. M.. (1996);  Impact of a parasitic plant on the structure and dynamics of salt marsh vegetation.  Ecology. 77 1410-1419
  • 35 Press,  M. C.. (1998);  Dracula or Robin Hood? A functional role for root hemiparasites in nutrient poor ecosystems.  Oikos. 82 609-611
  • 36 Press,  M. C.,, Scholes,  J. D.,, and Watling,  J. R.. (1999) Parasitic plants: physiological and ecological interactions with their hosts. Physiological Plant Ecology. Press, M. C., Scholes, J. D., and Barker, M. G., eds. Oxford; Blackwell Scientific Ltd. pp. 175-197
  • 37 Ramlan,  M. F., and Graves,  J. D.. (1996);  Estimation of the sensitivity to photoinhibition in Striga hermonthica-infected sorghum.  Journal of Experimental Botany. 47 71-78
  • 38 Sanders,  I. R.,, Koide,  R. T.,, and Shumway,  D. L.. (1993);  Mycorrhizal stimulation of plant parasitism.  Canadian Journal of Botany. 71 1143-1146
  • 39 Schans,  J.. (1991);  Reduction of leaf photosynthesis and transpiration rates of potato plants by second-stage juveniles of Globodera pallida. .  Plant, Cell and Environment. 14 707-712
  • 40 Seel,  W. E., and Press,  M. C.. (1996);  Effects of repeated parasitism by Rhinanthus minor on the growth and photosynthesis of the perennial grass, Poa alpina. .  New Phytologist. 134 495-502
  • 41 Smith,  L. H.,, Keys,  A. J.,, and Evans,  M. C. W.. (1995);  Striga hermonthica decreases photosynthesis in Zea mays through effects on leaf cell structure.  Journal of Experimental Botany. 46 759-765
  • 42 Taylor,  A.,, Martin,  J.,, and Seel,  W. E.. (1996);  Physiology of the parasitic association between maize and witchweed (Striga hermonthica): is ABA involved?.  Journal of Experimental Botany. 47 1057-1065
  • 43 Tennakoon,  K. U., and Pate,  J. S.. (1996);  Effects of parasitism by a mistletoe on the structure and functioning of branches of its host.  Plant, Cell and Environment. 19 517-528
  • 44 Trewavas,  A. J., and Jones,  H. G.. (1991) An assessment of the role of ABA in plant development. Abiscisic Acid: Physiology and Biochemistry. Davies, W. J. and Jones, H. G., eds. Oxford; Bios Scientific pp. 169-188
  • 45 Veenendaal,  E. M.,, Aberbrese,  I. K.,, Walsh,  M. F.,, and Swaine,  M. D.. (1996);  Root hemiparasitism in a West African rainforest tree Okoubaka aubrevillei (Santalaceae).  New Phytologist. 134 487-493
  • 46 Watling,  J. R., and Press,  M. C.. (1997);  How is the relationship between the C4 cereal Sorghum bicolor and the C3 root hemi-parasites Striga hermonthica and Striga asiatica affected by elevated CO2?.  Plant, Cell and Environment. 20 1292-1300
  • 47 Watling,  J. R., and Press,  M. C.. (1998);  How does the C4 grass Eragrostis pilosa respond to elevated CO2 and infection with the parasitic angiosperm Striga hermonthica? .  New Phytologist. 140 667-675
  • 48 Watling,  J. R., and Press,  M. C.. (2000);  Infection with the parasitic angiosperm Striga hermonthica influences the response of the C3 cereal Oryza sativa to elevated CO2.  Global Change Biology. 6 919-930

J. R. Watling

Department of Environmental Biology
University of Adelaide

Adelaide SA 5005
Australia

Email: j.r.watling@sheffield.ac.uk

Section Editor: U. Lüttge

    >