Growth and development of the facultative root hemiparasite Rhinanthus minor after removal of its host
Fan Jiang A B , Leila Timergalina C , Guzel Kudoyarova C , W. Dieter Jeschke B and Wolfram Hartung B DA College of Life Sciences, Beijing Normal University, Xin Jie Kou Wai Da Jie 19, 100875 Beijing, China.
B Lehrstuhl Botanik I der Universität Würzburg, Julius von Sachs Platz 2, D 97082 Würzburg, Germany.
C Institute of Biology of Russian Academy of Sciences, Ufa Research Center, pr. Octyabrya, 69, Ufa 450054, Russia.
D Corresponding author. Email: hartung@botanik.uni-wuerzburg.de
Functional Plant Biology 34(3) 237-245 https://doi.org/10.1071/FP06262
Submitted: 18 October 2006 Accepted: 22 February 2007 Published: 22 March 2007
Abstract
Facultative plant hemiparasites exhibit optimal growth only when attached to a suitable host. After attachment, stomata of the parasite remain continuously open, thus, optimising the extraction of host xylem sap. When the host shoot was removed from the hemiparasitic Rhinanthus/barley association ~14 days after attachment, the resulting host-free attached Rhinanthus continued to grow and develop similarly well as the attached parasites. These plants, however, showed altered stomatal behaviour: their stomata were open at daytime and closed at night, whereas parasitising Rhinanthus has continuously open stomata all day and night and unattached single Rhinanthus has practically closed stomata throughout day and night. After removal of the host the root growth was strongly increased, thereby increasing the root-to-shoot ratio. Abscisic acid and cytokinin relationships became more ‘normal’ with the Rhinanthus roots becoming able to synthesise zeatin nucleotides and zeatin ribosides, thus, behaving much as non-parasitic plants in general. It is suggested that the degrading root system of the host plant produces signals that trigger this conversion. Two explanations for these changes are discussed, the supply of dissolved organic nitrogen by the degrading host root system and a possible strong growth of growth promoting soil microorganisms using the degrading host root system as a substrate.
Additional keywords: abscisic acid, cytokinins, stomatal behaviour, zeatin.
Acknowledgments
We are grateful to Mrs Bianca Röger for expert technical help, to Professor E. W. Weiler (Ruhr-University Bochum, Germany) for generous supply of immunochemicals and to Deutsche Forschungsgemeinschaft for generous financial support (SFB 567, TP A6).
Arkhipova TN,
Veselov SU,
Melentiev AI,
Martynenko EV, Kugoyarova GR
(2005) Ability of bacterium Bacillis subtilis to produce cytokinins and to influence the growth and endogenous homone content of lettuce plants. Plant and Soil 272, 201–209.
| Crossref | GoogleScholarGoogle Scholar |
Cameron DD,
Coats AM, Seel WE
(2006) Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor. Annals of Botany 98, 1289–1299.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chiwocha SDS,
Cutler AJ,
Abrams SR,
Ambrose SJ,
Yang J,
Ross ARS, Kermode AR
(2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintainance of seed dormancy, moist-chilling and germination. The Plant Journal 42, 35–48.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hansen H, Grossmann K
(2000) Auxin induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiology 124, 1437–1448.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hartung W, Ratcliffe RG
(2002) The utilization of glycine and serine as nitrogen sources in roots of Zea mays and Chamaegigas intrepidus. Journal of Experimental Botany 53, 2305–2314.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 & Environment 22, 937–947.
| Crossref | GoogleScholarGoogle Scholar |
Jeschke WD, Pate JS
(1991) Modelling of the uptake, flow and utilization of C, N and H2O within whole plants of Ricinus communis L. based on empirical data. Journal of Plant Physiology 137, 488–498.
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 | GoogleScholarGoogle Scholar | PubMed |
Jiang F,
Jeschke WD, Hartung W
(2004a) Solute flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite nutrient relations. Functional Plant Biology 31, 633–643.
| Crossref | GoogleScholarGoogle Scholar |
Jiang F,
Jeschke WD, Hartung W
(2004b) Abscisic acid (ABA) flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite abscisic acid relations. Journal of Experimental Botany 55, 2323–2329.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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, 2143–2150.
| Crossref |
PubMed |
Jiang F,
Veselova S,
Veselov D,
Kudoyarova G,
Jeschke WD, Hartung W
(2005) Cytokinins flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite cytokinins relations. Functional Plant Biology 32, 619–629.
| Crossref | GoogleScholarGoogle Scholar |
Lipson D, Näsholm T
(2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128, 305–316.
| Crossref | GoogleScholarGoogle Scholar |
Lucy M,
Reed E, Glick BR
(2004) Application of free living plant growth promoting bacteria. Antonie van Leeuwenhoek 86, 1–25.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Matthies D
(1995a) Parasitic and competitive interactions between the hemiparasites Rhinanthus serotinus and Odontites rubra and their host Medicago sativa. Journal of Ecology 83, 245–251.
| Crossref | GoogleScholarGoogle Scholar |
Matthies D
(1995b) Host parasite relations in the root hemiparasite Melampyrum arvense. Flora 190, 383–394.
Mertens RJ,
Deus-Neumann B, Weiler EW
(1983) Monoclonal antibodies for the detection and quantitation of the endogenous plant growth regulator, abscisic acid. FEBS Letters 160, 269–272.
| Crossref | GoogleScholarGoogle Scholar |
Pate JS,
Layzell DB, McNeil DL
(1979) Modeling the transport and utilization of carbon and nitrogen in a nodulated legume. Plant Physiology 63, 730–737.
| PubMed |
Peuke AD,
Jeschke WD, Hartung W
(1994) The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. III. Long-distance transport of abscisic acid depending on nitrogen nutrition and salt stress. Journal of Experimental Botany 45, 741–747.
| Crossref | GoogleScholarGoogle Scholar |
Rümer S,
Cameron DD,
Wacker R,
Hartung W, Jiang F
(2007) A microscopical study of the haustoria of Rhinanthus minor attached to roots of different hosts. Flora in press ,
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 | GoogleScholarGoogle Scholar |
Seel WE,
Parsons AN, Press MC
(1993) Do inorganic solutes limit growth of the facultative hemiparasite Rhinanthus minor L. in the absence of a host? New Phytologist 124, 283–289.
| Crossref | GoogleScholarGoogle Scholar |
Seel WE, Press MC
(1993) Influence of the host on three subarctic annual facultative root hemiparasites. I. Growth mineral accumulation and above ground dry matter partitioning. New Phytologist 125, 131–138.
| Crossref | GoogleScholarGoogle Scholar |
Veselov SU,
Valcke R,
Van Onckelen H, Kudoyarova
(1999) Cytokinin content and location in the leaves of the wild-type and transgenic tobacco plants. Russian Journal of Plant Physiology 46, 26–33.
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.
| Crossref | GoogleScholarGoogle Scholar |
