Solute flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite nutrient relationsFan Jiang A , W. Dieter Jeschke A and Wolfram Hartung A B
A Julius von Sachs Institut für Biowissenschaften der Universität, Lehrstuhl Botanik I, Julius von Sachs Platz 2, D 97082 Würzburg, Germany.
B Corresponding author; email: email@example.com
Functional Plant Biology 31(6) 633-643 https://doi.org/10.1071/FP03225
Submitted: 26 November 2003 Accepted: 2 March 2004 Published: 23 June 2004
Using the facultative root hemiparasite Rhinanthus minor and Hordeum vulgare L. as a host, the flows and partitioning of mineral nutrients within the host, the parasite and between host and parasite have been studied during the study period 41–54 d after planting, i.e approximately 30–43 d after successful attachment of the parasite to the host. In parasitising Rhinanthus shoot growth was 12-fold, but root growth only 2-fold increased compared to non-parasitising plants. Conversely, in the Hordeum host, shoot dry matter growth was clearly reduced, by 33% in leaf laminae and by 52% in leaf sheaths, whereas root growth was only slightly reduced as a consequence of parasitism. Growth-dependent increments of total nitrogen (N) and phosphorus (P) and of potassium (K), calcium (Ca) and magnesium (Mg) in parasitising Rhinanthus shoot were strongly increased, particularly increments of total N and P, which were 18 and 42 times, respectively, higher than in solitary Rhinanthus. However, increments of the above mineral nutrients in leaf sheaths of parasitised Hordeum vulgare were more strongly decreased than in leaf laminae in response to parasitic attack. Estimation of the flows of nutrients revealed that Rhinanthus withdrew from the host xylem sap about the same percentage of each nutrients: 18% of total N, 22% of P and 20% of K. Within the host almost all net flows of nutrient ions were decreased due to parasitism, but retranslocation from shoot to root was somewhat increased for all nutrients. Quantitative information is provided to show that the substantially increased growth in the shoot of attached Rhinanthus and the observed decrease in Hordeum shoot growth after infection were related to strongly elevated supply of nitrogen and phosphorus in the parasite and to incipient deficiency of these nutrients in the parasitised host. The flows of nutrients between host and parasite are discussed in terms of low selectivity of nutrient abstraction from the host xylem by the hemiparasite Rhinanthus minor.
Keywords: mineral nutrients, modelling, nitrogen, parasite angiosperm, phosphorus, Rhinanthus minor, solute flows.
We thank Dr Wendy Seel and Duncan Cameron (University of Aberdeen, UK) for stimulating discussion and for helpful advice, and an anonymous referee for constructive critical comments and to Dr Hermann Heilmeier for help the statistical analysis. We also thank Mrs. Bianca Röger, Eva Wirth and Elfriede Reisberg for expert technical help and Deutsche Forschungsgemeinschaft for generous financial support (SFB 567, TPA6).
Cooper HD, Clarkson DT (1989) Cycling of amino nitrogen and other nutrients between shoots and roots in cereals — a possible mechanism integrating shoot and root in the regulation if nutrient uptake. Journal of Experimental Botany 40, 753–762.
Dobbins DR, Kuijt J (1973) Studies on the haustorium of Castilleja (Scrophlariaceae). Canadian Journal of Botany 51, 917–931.
Fredeen AL, Rao IM, Terry N (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiology 89, 225–230.
Hecht-Buchholz C (1967) Über die Dunkelfärbung des Blattgrüns bei Phosphormangel Zeitschrift für Pflanzenernährung and Bodenkunde 118, 12–22.
Hibberd JM, Quick WP, Press MC, Scholes JD, Jeschke WD (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.
| CrossRef |
Jeschke WD, Pate JS, Atkins CA (1987) Partitioning of K+, Na+ and Mg2+ and Ca2+ through xylem and phloem to component organs of nodulated white lupin under mild salinity. Journal of Plant Physiology 128, 77–93.
Jeschke WD, Pate JS (1991a) Modelling of the uptake, flow and utilisation of C, N and H2O within whole plants of Ricinus communis L. based on empirical data. Journal of Plant Physiology 137, 488–498.
Jeschke WD, Pate JS (1991b) Modelling of the partitioning, assimilation and storage of nitrate within root and shoot organs of castor bean (Ricinus communis L.). Journal of Experimental Botany 42, 1091–1103.
Jeschke WD, Räth N, Bäumel P, Czygan FC, Proksch P (1994a) Modelling the flow and partitioning of carbon and nitrogen in the holoparasite Cuscuta reflexa Roxb. and its host Lupinus albus L. I. Methods for estimating net flows. Journal of Experimental Botany 45, 791–800.
Jeschke WD, Bäumel P, Räth N, Czygan FC, Proksch P (1994b) Modelling of the flows and partitioning of carbon and nitrogen in the holoparasite Cuscuta reflesa Roxb. and its host Lupinus albus L. II. Flows between host and parasite and within the parasitised host. Journal of Experimental Botany 45, 801–802.
Jeschke WD, Bäumel P, Räth N (1995) Partitioning of nutrients in the Cuscuta reflexs–Lupinus albus association. Physiological response of plants to pathogen. Aspects of Applied Biology 42, 71–79.
Jeschke WD, Kirkby EA, Peuke A, Pate JS, Hartung W (1997) Effects of P deficiency on assimilation and transport of nitrate and phosphate in intact plants of castor bean (Ricinus communis L.). Journal of Experimental Botany 48, 1737–1747.
| CrossRef |
Jiang F, Li CJ, Jeschke WD, Zhang FS (2001) Effect of top excision and replacement by 1-naphylacetic acid on partition and flow of potassium in tobacco plants. Journal of Experimental Botany 52, 341–349.
| CrossRef | PubMed |
Jiang F, Jeschke WD, Hartung W (2003) Water flows in the parasitic association Rhinanthus minor / Hordeum vulgare. Journal of Experimental Botany 54, 1985–1993.
| CrossRef | PubMed |
Klaren CH, Janssen G (1978) Physiological changes in the hemiparasite Rhinanthus serotinus before and after attachment. Physiologia Plantarum 42, 151–155.
Marschner, H (1995).
Marschner H, Kirkby EA, Cakmak I (1996) Effect of mineral nutritional status on shoot-root partitioning of photoassimilates and cycling of mineral nutrients. Journal of Experimental Botany 47, 1255–1263.
Marshall JD, Ehleringer JR, Schulze ED, Farquhar GD (1994) Carbon isotope composition, gas exchange and heterotrophy in Australian mistletoes. Functional Ecology 8, 237–241.
Okonkwo SNC (1966) Studies on Striga senegalensis Benth. I. Mode of host – parasite union and haustorial structure. Phytomorphology 16, 453–463.
Parker, C , and Riches, CR (1993).
Pate JS, Layzell DB, McNeil DL (1979) Modeling the transport and utilisation of carbon and nitrogen in a nodulated legume. Plant Physiology 63, 730–737.
Pate JS, Layzell DB (1981) Carbon and nitrogen partitioning in the whole plant — a thesis based on empirical modelling. ‘Nitrogen and carbon metabolism’. (Ed. JD Bewley) pp. 94–134. (Dr W Junk: The Hague, The Netherlands)
Pate JS, Pate SR, Kuo J, Davidson NJ (1990a) Growth, resource allocation and haustorial biology of the root hemiparasite Olax phyllanthi (Olacaceae). Annals of Botany 65, 437–449.
Pate JS, Kuo J, Davidson NJ (1990b) Morphology and anatomy of the haustorium of the root hemiparasite Olax phyllanthi (Olacaceae), with special reference to the haustorial interface. Annals of Botany 65, 425–436.
Press MC, Shah N, Tuohy JM, Stewart GR (1987) Carbon isotope ratios demonstrate carbon flux from C4 host to C3 parasite. Plant Physiology 85, 1143–1145.
Rao IM, Terry N (1989) Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. I. Changes in growth, gas exchange and Calvin cycle enzymes. Plant Physiology 90, 814–819.
Seel WE, Press MC (1993) Influence of the host on three sub-Arctic annual facultative root hemiparasites. I. Growth, mineral accumulation and above-ground dry-matter partitioning. New Phytologist 125, 131–138.
Seel WE, Cooper RE, Press MC (1993a) Growth, gas exchange and water use efficiency of the facultative hemiparasite Rhinanthus minor associated with hosts differing in foliar nitrogen concentration. Physiologia Plantarum 89, 64–70.
| CrossRef |
Seel WE, Parsons AN, Press MC (1993b) Do inorganic solutes limit growth of the facultative hemiparasite Rhinanthus minor L. in the absence of a host? New Phytologist 124, 283–289.
Seel WE, Press MC (1996) Effects of repeated parasitism by Rhinanthus minor on the growth and photosynthesis of a perennial grass, Poa alpine. New Phytologist 134, 495–502.
Seel WE, Jeschke WD (1999) Simultaneous collection of xylem sap from Rhinanthus minor and hosts Hordeum and Trifolium: hydraulic properties, xylem sap composition and effects of attachment. New Phytologist 143, 281–298.
| CrossRef |
Stewart GR, Press MC (1990) The physiology and biochemistry of parasitic angiosperms. Annual Review of Plant Physiology and Plant Molecular Biology 41, 127–151.
| CrossRef |
Tennakoon KU, Pate JS, Fineran BA (1997) Growth and partitioning of C and fixed N in the shrub legume Acacia littrea in the presence or absence of the root hemiparasite Olax phyllanthi. Journal of Experimental Botany 48, 1047–1060.
Weber HC (1976) Host plants and parasitism in some middle-European Rhinanthoideae (Scrophulariaceae). Plant Systematics and Evolution 125, 97–107.
Wolf O, Munns R, Tonnet ML, Jeschke WD (1990) Concentrations and transport of solutes in xylem and phloem along the leaf axis of NaCl-treated Hordeum vulgare. Journal of Experimental Botany 41, 1133–1141.