AOBPreview originally published online on January 21, 2008
Annals of Botany 2008 101(4):573-578; doi:10.1093/aob/mcm324
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Suppression of Host Photosynthesis by the Parasitic Plant Rhinanthus minor
1 School of Biological Science (Plant and Soil Science), University of Aberdeen, Cruickshank Building, St Machar Drive, Old Aberdeen AB24 3UU, UK
2 Ecole Nationale Supérieure Agronomique de Montpellier, 2 Place Pierre Viala, F-34060, Monpellier Cedex 1, France
* For correspondence. Present address: Department of Biological Science, Graduate School of Science, Osaka University, 1,1-Machikaneyama-cho, Toyonaka, Osaka 560 0043, Japan. E-mail ljirving{at}gmail.com
Received: 5 September 2007 Returned for revision: 15 October 2007 Accepted: 20 November 2007 Published electronically: 21 January 2008
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Background and Aims: Parasitism is well understood to have wide-ranging deleterious effects on host performance in species thus far characterized. Photosynthetic performance reductions have been noted in the Striga–Zea mays association; however, no such information exists for facultative hemiparasitic plants and their hosts, nor are the effects of host species understood.
Methods: Chlorophyll fluorimetry was used to study the effects of parasitism by the hemiparasite Rhinanthus minor on the grass Phleum bertolinii and the forb Plantago lanceolata, and the effects of host species on the photosynthetic apparatus of R. minor.
Key Results: Parasitism by Rhinanthus led to a significant decrease in the host, and total (host + parasite) biomass in Phleum; however, in Plantago, no significant repression of growth was noted. Maximum quantum yield (Fv/Fm) was reduced in parasitized Plantago, relative to control plants, but not in Phleum. Fv/Fm was significantly lower in R. minor parasitizing Phleum than Plantago, suggesting Phleum to be a superior host to Plantago for R. minor. Steady-state quantum yield (
PSII) was significantly depressed in parasitized Phleum, but only at low irradiances in Plantago. PSII was very low for R. minor grown on Plantago, but not Phleum.
Conclusions: Shown here is the first evidence of the suppression of host photosynthesis by a facultative hemiparasitic plant, which has significant effects on total biomass production. Host identity is a significant factor in parasite success, with the forb Plantago lanceolata exhibiting apparent chemical as well as previously identified physical defences to parasitism. It is proposed that the electron transport rate (as denoted by PSII) represents the limiting factor for biomass accumulation in this system, and that Plantago is able to suppress the growth of Rhinanthus by suppressing the electron transport rate.
Key words: Parasitic plant, Rhinanthus minor, photosynthesis, facultative hemiparasite, chlorophyll fluorescence, ABA, Rubisco
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Parasitic plants have significant, deleterious effects on their host in terms of photosynthetic rate and/or total canopy photosynthesis over the life of the plant (Watling and Press, 2001). Broadly, these effects can be classified in terms of direct effects of resources abstraction (source–sink interactions) and indirect, non-source–sink interactions (Watling and Press, 2001; Cameron et al., 2005). For example, tobacco (Nicotiana tabacum), in response to infection with the holoparasite Orobanche cernua, exhibits suppressed leaf senescence, with the net effect of increasing canopy photosynthesis over the life of the host by 20 %, although in the study it did not completely compensate for the carbon lost to the parasite (Hibberd et al., 1998). In contrast, in the Striga hermonthica–Zea mays association, only 20 % of the host biomass reduction effected by the parasite is attributable to the direct effects of resource abstraction with the remainder associated with parasite-induced suppression of host photosynthesis (Graves et al., 1989). The mechanisms through which S. hermonthica induces these deleterious effects on host photosynthesis are not fully elucidated (Gurney et al., 1995); however, host plants parasitized by S. hermonthica typically show elevated abscisic acid (ABA) levels (Taylor et al., 1996; Frost et al., 1998). Increased ABA concentrations result in a reduction in host stomatal conductance (Frost et al., 1998), increasing the effective sink strength of the parasite by reducing competition with the host for xylem sap (Taylor et al., 1996; Watling and Press, 2001). Xylem sap is drawn through the haustorium, the organ of attachment providing vascular continuity between Striga and its host, and into the parasite via cohesion due to elevated parasite transpiration (Press and Graves, 1995).
The negative effects of the obligate hemiparasitic weeds on host photosynthesis are well documented (Watling and Press, 2001); there are, however, virtually no such data for the effect of non-weedy, facultative hemiparasitic plants on host photosynthesis or, indeed, for the effect of the identity of the host on parasite photosynthesis. Cameron et al. (2005) reviewed the direct and indirect effects of the facultative hemiparasite Rhinanthus minor (Orobanchaceae) on its hosts providing some evidence that the parasite was able to lower the steady-state quantum yield of PSII (PSII) in host leaves. Moreover, the negative effects of R. minor on its hosts – in excess of 20 species (Gibson and Watkinson, 1989) – in terms of growth and reproduction, are highly variable. In general, graminoid and leguminous hosts are significantly damaged by attachment of the parasite whilst, in contrast, forbs remain undamaged (Cameron et al., 2005) due to their ability to express successful defence responses against the invading parasite haustorium (Cameron et al., 2006; Rümer et al., 2007). Similarly, graminoid and legume species represent the best hosts for R. minor in terms of growth and reproduction (Cameron et al., 2006) as the parasite is able to abstract significantly more of the host's resources from grasses than forbs (Cameron and Seel, 2007). This differential success in colonization of potential host species represents a potent tool to investigate the effects of facultative hemiparasites on host photochemistry and the reciprocal effect of host identity on parasite photochemistry.
Here, using chlorophyll fluorescence techniques, the effect of R. minor on the photosynthetic capacity of the host is investigated and the effect of host species on the photosynthetic capacity of the parasite is reciprocally investigated with two potential host species at opposing ends of the ‘quality’ spectrum.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Plant material
Twenty individual 6-week-old seedlings (hosts) of Phleum bertolonii (henceforth Phleum) and Plantago lanceolata (henceforth Plantago) were grown in 15-cm-diameter pots (one plant per pot) containing 50 : 50 sand:John Innes No. 3 compost. Rhinanthus minor seeds were germinated according to Keith et al. (2004). Briefly, seeds were surface-sterilized for 5 min in 3 % sodium hypochlorite solution, washed in distilled water and preconditioned on moist filter paper at 4 °C until germination (approx. 8 weeks). Four seedlings of Rhinanthus minor were transplanted into five of the pots containing the host species. The parasites were subsequently reduced to one per host when the first parasite showed morphological changes associated with attachment (Klaren and Janssen, 1978). Water was supplied to the soil daily and the pots were arranged in a randomized block design. The hosts together with the parasites were then grown for a further 14 weeks (after parasite attachment) in a glasshouse (temperature range 16–28 °C).
Chlorophyll fluorescence
One or two of the youngest fully expanded leaves were removed from three individuals of Rhinanthus growing on Phleum (a good host) and three Rhinanthus minor individuals growing on Plantago (a bad host) 14 weeks after parasite attachment. The fresh weight was recorded and, after fluorescence measurements had been conducted, the leaves were oven-dried (80 °C for 2 d) and the weight was recorded and added to the total parasite dry weight measured. The maximum and steady-state quantum yields (Fv/Fm and PSII, respectively) of the detached leaves were measured using a pulse-modulated fluorimeter (MFMS; Hansatech Ltd, King's Lynn, UK) as per the manufacturer's directions. Samples were dark-adapted for 15 min prior to measurements of Fv/Fm, and the intensity of the 0·7-s light pulse was varied to obtain Fv/Fm light-response curves. Leaves were adapted to an actinic beam of variable intensity for 15 min prior to measurement, or until Fo' stabilized, to obtain PSII light response curves. In the PSII measurements the pulse had an intensity of 3200 µmol photons m–2 s–1 for 0·7 s. Different irradiances were obtained by interrupting the light beam with a combination of neutral density filters. All fluorescence parameters were estimated as per the manufacturer's instructions.
Chlorophyll content
The second two youngest leaves were removed from all parasites and the fresh biomass recorded. Dry weights were estimated using the fresh weight/dry weight ratio of leaves harvested for chlorophyll fluorescence. Leaves were ground in a mortar and pestle with a small amount of acid-washed sand (as an abrasive) and 5 ml of 80 % ice-cold acetone. The mortar and pestle was washed out twice with a further 2 mL of acetone and transferred to a centrifuge tube. The samples were centrifuged at 8000 g for 5 min and the supernatant diluted to 10 mL total volume with 80 % ice-cold acetone. The optical density of the supernatant was measured at 645 nm and 663 nm using a Hitachi U-2001 spectrophotometer.
|
| (1) |
|
| (2) |
The chlorophyll concentration (mg L–1 of extract) was calculated according to Arnon (1949) using eqns (1) and (2) above and re-expressed as milligrams of chlorophyll per gram of tissue fresh weight (mg g–1).
Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) content
Following the protocol described by Irving and Robinson (2006), fresh leaf material was weighed, then ground in five times its mass of 50 mM sodium phosphate buffer (pH 7·5) containing 5 % glycerol, 0·8 % 2-mercaptoethanol and 3·5 % (w/v) iodoacetic acid. A 200-µL aliquot of the homogenate was diluted with a further 200 µL of extraction buffer. After adding 2 µL of 25 % Triton X-100, the solution was vortexed, followed by centrifugation for 5 min at 10 000 g. Then 8·6 µL of 25 % (w/v) lithium dodycyl sulfate and a further 5·3 µL of 2-mercaptoethanol were added. The sample was inverted twice before being boiled at 100 °C for 90 s, then pulse centrifuged. Samples were stored at –20 °C before being applied to an SDS–PAGE gel (5 % stacking gel, 12·5 % separating gel), along with a suitable wheat Rubisco standard, for protein separation. Gels were stained using Coomassie Brilliant Blue R250, the Rubisco containing band excised, and the protein concentration determined spectrophotometrically at 595 nm, after elution of the stain in formamide for 12 h.
Statistical analysis
Differences between treatment means were analysed by ANOVA and Fisher's multiple comparison test using Minitab 13 (Minitab Inc., Pennsylvania, USA).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Host biomass and total biomass (host + parasite) of infected Phleum bertolonii was significantly lower than the control plants (P > 0·05, two-way ANOVA, n = 3–5) by the end of the experimental period (Fig. 1). However, in Plantago lanceolata, no significant differences in host or total biomass were noted, while the parasite biomass was significantly lower than the biomass of Rhinanthus growing on Phleum (P < 0·05).
|
Maximum quantum yield (Fv/Fm) was measured for the two host species, either parasitized or un-parasitized, and for the parasite, Rhinanthus minor, attached to either host plant (Fig. 2). Fv/Fm was significantly lower for parasitized Plantago then non-parasitized plants, using pooled data from 310 µmol photons m–2 s–1 up (P < 0·001), whilst in Phleum the mean separation approached significance (P = 0·092). Fv/Fm was 18 ± 2 % higher in Rhinanthus plants parasitizing Phleum than Plantago (P < 0·001). Fv/Fm values for Rhinanthus parasitizing Plantago appeared to decrease with increasing flash irradiance; however, the decrease in mean values was coupled with an increase in the variance, and no significant change in the mean range was noted with increasing irradiance. However, this small decrease in mean Fv/Fm values may be the result of increased quenching at higher irradiances. The light-adapted quantum efficiency (
PSII) was determined for each host species, both parasitized and unparasitized, and for the parasite on each host (Fig. 3). In Phleum, PSII was significantly lower in infected than uninfected plants (P < 0·05) at each light intensity except 750 and 1170 µmol photons m–2 s–1, which approached significance (P =0·156 and 0·128, respectively). In Plantago, PSII was numerically lower in infected plants than uninfected plants at all light intensities, and significantly lower from 40 to 310 µmol photons m–2 s–1 (P < 0·005 at all points). At light intensities higher than 310 µmol photons m–2 s–1, PSII was not significantly different (P > 0·05) between treatments. Rhinanthus exhibited significantly lower values of PSII when grown on Plantago than Phleum at every light intensity from 40 to 500 µmol photons m–2 s–1, and zero values for Plantago cultured plants above 500 µmol photons m–2 s–1 (Fig. 3C).
|
|
In Phleum, whilst parasitism led to significant decreases in the total chlorophyll concentration (Fig. 4A), the chlorophyll a : b ratio did not alter significantly. A non-significant reduction in Rubisco concentration was also noted (Fig. 4B). Conversely, in Plantago, parasitism did not lead to a reduction in either chlorophyll content or in Rubisco concentration. Rhinanthus grown on Phleum had a higher Rubisco concentration in its leaves than Rhinanthus grown on Plantago, corresponding to differences in Rubisco concentrations in unparasitized host plants.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
Infection of Phleum by R. minor led to significant reductions in plant biomass, the quantum efficiency of PSII (
PSII), and chlorophyll concentration, and a non-significant reduction in Rubisco concentration. However, no such effects were noted in Plantago plants infected by R. minor, with the exception of significant decreases in PSII at low light intensities, below 310 µmol photons m–2 s–1, and in the maximum quantum yield (Fv/Fm) at high light intensities, above 310 µmol photons m–2 s–1. Although the decrease in Plantago Fv/Fm was not large, it may be indicative of mild light stress and the deactivation of some of the reaction centres at the growth irradiances used. Likewise, Fv/Fm values for R. minor parasitizing Plantago were significantly lower than the 0·83 multi-species average expected for healthy plants (Maxwell and Johnson, 2000), and significantly lower than the values from R. minor parasitizing Phleum, suggesting significant photoinhibition in these plants.
In infected Phleum plants, significant decreases in PSII were noted at all light intensities, except the very highest light levels to which the plants were exposed. Reductions in the electron transport rate (ETR), and thus PSII, may be a result of three processes; the sink strength of the Calvin cycle for photosynthetic reductants, ATP and NADPH (CO2 limitation); limitation by light interception and leaf area; or limitation by the thylakoids' electron transport capacity (Buckley and Farquhar, 2006). As PSII was measured under saturating irradiances light interception at the leaf surface can effectively be ruled out, and decreases in PSII must be the result of either decreased intracellular CO2 concentrations, potentially as a result of stomatal closure, or of diminished thylakoid capacity, characterized by the large decrease in chlorophyll concentration. Given the reduction in host leaf chlorophyll and Rubisco concentrations, and the fact that parasitism does not increase host ABA levels (Jiang, 2004), which prompt stomatal closure, the latter seems more likely. Potential differences in stomatal aperture should, however, be tested in future investigations. ETR (and hence PSII) is known to strongly correlate with photosynthetic rates, and may represent one factor explaining the growth repression suffered by Phleum.
Conversely, any reductions in PSII in parasitized Plantago relative to unparasitized controls occurred at low irradiances, between 40 and 310 µmol photons m–2 s–1, suggesting that reductions in ETR at these irradiances are due to reduced light harvesting by the PSII complex, which corresponds to the small but significant noted decrease in Fv/Fm. The specific reasons for these two phenomena are unknown, and require additional investigation, but may but may be attributable to a variety of possible causes. First, a decrease in chlorophyll concentration or a reduction in antenna size, would affect light capture at low irradiances, but not the ETR at higher irradiances. A decrease in antenna size would normally be accompanied by a change in the chlorophyll a : b ratio; however, neither this nor a decrease in chlorophyll concentration was noted. Second, recent evidence suggests that ATP is required in the synthesis of the D1 protein, which is required for PSII function (Murata et al., 2007); the noted decrease in PSII at low light levels may be attributable to low levels of active PSII molecules, if ATP were limiting for D1 biosynthesis. At higher light levels this stress would be relieved, and D1 synthesis would increase, leading to the progressive activation of PSII reaction centres. However, high light levels would still lead to photoinactivation of PSII, both directly and by an increase in active oxygen species that appear to target mRNAs involved in protein synthesis, especially the D1 protein. These hypotheses require further testing.
Rhinanthus minor plants grown on Phleum exhibited Fv/Fm values corresponding to a healthy plant; however, R. minor growing on Plantago exhibited decreased Fv/Fm, signifying deactivation of the PSII complex as a result of light stress. Incident radiation that cannot be utilized in the production of reductants, in this case due to a lack of oxidized substrates (ADP and NADP+), must be dissipated by non-photochemical means, either by non-photochemical quenching, the reduction of molecular oxygen by PSI and PSII, leading to the production of oxygen radicals (Edreva, 2005; Mullineaux et al., 2006) and premature leaf senescence (Nakano et al., 2006; Irving et al., 2007), or fluorescence. PSII was very low for R. minor plants grown on Plantago, suggesting that energy is not being dissipated photosynthetically, accounting for the very low parasite biomass attained. Since Rubisco and chlorophyll concentrations are not vastly different in R. minor grown on the two species, this suggests that either intracellular CO2 is very low in R. minor plants grown on Plantago, or the thylakoids are severely damaged under these conditions. However, it is known that reduced photosynthetic rates are not due to elevated ABA in host plants (Jiang, 2004), suggesting thylakoid damage, rather than stomatal closure. The reason for this poor thylakoid function is unknown, although it may be related to either a lack of a substrate that the parasite would ordinarily derive from its host, or from an inhibitory substance present in or secreted by Plantago, indeed P. lanceolata synthesizes significant amounts of bioactive compounds such as the antimicrobial phenolic glycoside ‘Acteoside’ (Tamura and Nishibe, 2002) which may be involved in the deleterious effects to R. minor of forming associations with P. lanceolata, although this hypothesis requires further investigation.
In Phleum, significant reductions in chlorophyll concentrations, and non-significant reductions in Rubisco concentration were noted compared with unparasitized plants, suggesting that the parasite is sequestering significant amounts of N from the host plant. These decreases were not mirrored in Plantago, presumably as a result of a lack of vascular connectivity between the host and the parasite (Cameron et al., 2006; Cameron and Seel, 2007).
The signalling mechanism between host and parasite facilitating such suppression of host photosynthesis is unclear, especially given the lack of vascular continuity between Rhinanthus and Plantago (Cameron et al., 2006). It is important, however, to note that vascular continuity is not essential for abstraction of host solutes by parasitic plants; it has been shown recently that there is no vascular continuity between the haustorium of Santalum album and its host Tithonia diversifolia, instead the host–parasite interface was characterized by the presence of significant amounts of interfacial parenchyma (Tennakoon and Cameron 2006). The occurrence of solute transfers between host and parasite in the absence of vascular continuity coupled with the observation of Cameron and Seel (2007) that the resistance mechanisms induced by Plantago significantly impede but do not absolutely prevent solute transfer, leaves a physiological mechanism for host–parasite signalling. The signal-transduction pathway, however, remains unclear but it appears, in contrast to other hemiparasites such as Striga, that this is not a function of ABA biosynthesis in either host or parasite (Jiang, 2004).
It has been long known that infection by parasitic Rhinanthus spp. can suppress the biomass of the associated host plant and, reciprocally, host identity strongly influences parasite success (Hwangbo, 2000). Differences in defence characteristics have recently been shown to underpin these differences in host quality and the associated parasite-induced host damage (Cameron et al., 2006; Cameron and Seel, 2007; Rümer et al., 2007). The degree of Rhinanthus-induced suppression of host biomass cannot, however, be explained in terms of source–sink relationships alone as the biomass achieved by the parasite is less than the biomass lost by the host as a result of infection. This ‘missing biomass’ may be a function of a number of factors, e.g. inefficient assimilation of host-derived solutes, or a result of solute ‘leakage’ from the haustoria. We show, however, for the first time in any facultative hemiparasitic plant, that at least a component of this ‘missing biomass’ is a result of host photosynthetic repression by R. minor.
|
ACKNOWLEDGEMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
We would like to thank Janet Woo and David Hadwen for expert technical support. This research was funded by the NERC (Award Number: NER/S/A/2001/05959) to D.D.C. and W.E.S. and the BBSRC (Award Number: 01/B1/P/07009) to L.J.I.
|
FOOTNOTES |
|---|
Present address: Department of Animal and Plant Sciences, University of Sheffield, Alfred Denny Building, Western Bank, Sheffield S10 2TN, UK. 
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
|---|
-
Arnon DI. Copper enzymes in isolated chloroplasts: polyphenoloxidase in. Beta vulgaris. Plant Physiology (1949) 24:1–15.
Buckley TN, Farquhar GD. A new analytical model for whole leaf potential electron transport rate. Plant, Cell and Environment (2006) 27:1447–1462.
Cameron DD, Seel WE. Functional anatomy of haustoria formed by Rhinanthus minor: linking evidence from histology and isotope tracing. New Phytologist (2007) 174:412–419.[CrossRef][Web of Science][Medline]
Cameron DD, Hwangbo J-K, Keith AM, Geniez J-M, Kraushaar D, Rowentree J, et al. Folia Geobotanica (2005) 40:217–229.
Cameron DD, Coats AM, Seel WE. Host and non-host resistance underlie variable success of the hemi-parasitic plant Rhinanthus minor. Annals of Botany (2006) 98:1289–1299.
Edreva A. Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agriculture Ecosystems and Environment (2005) 106:119–133.[CrossRef]
Frost DL, Gurney AL, Press MC, Scholes JD. Striga hermonthica reduces photosynthesis in Sorghum: the importance of stomatal limitation and a potential role for ABA? Plant, Cell and Environment (1998) 20:483–492.
Gibson CC, Watkinson AR. The host range and selectivity of a parasitic plant – Rhinanthus minor L. Oecologia (1989) 78:401–406.[CrossRef][Web of Science]
Graves JD, Press MC, Stewart GR. A carbon balance model of the Sorghum–Striga hermonthica host–parasite association. Plant, Cell and Environment (1989) 12:101–107.[CrossRef]
Gurney AL, Press MC, Ransom JK. The parasitic angiosperm Striga hermonthica can reduce photosynthesis of its sorghum and maize hosts in the field. Journal of Experimental Botany (1995) 46:1817–1823.
Hwangbo J. Interactions between a facultative annual root hemiparasite, Rhinanthus minor L. and its hosts. (2000) University of Aberdeen. PhD Thesis.
Hibberd JM, Quick WP, Press MC, Scholes JD. Can source sink–sink relations explain responses of tobacco to the root holoparasitic angiosperm Orobanche cernua? Plant, Cell and Environment (1998) 21:333–340.[Medline]
Irving LJ, Robinson D. A dynamic model of Rubisco turnover in cereal leaves. New Phytologist (2006) 169:493–504.[CrossRef][Web of Science][Medline]
Irving LJ, Sheng Y, Woolley D, Matthew C. Physiological effects of waterlogging on two lucerne varieties grown under glasshouse conditions. Journal of Agronomy and Crop Science (2007) 193:345–356.[CrossRef][Web of Science]
Jiang F. Water, mineral nutrient and hormone flows and exchanges in the hemiparasitic association between root hemiparasite Rhinanthus minor and the host Hordeum vulgare. (2004) University of Würzbürg. PhD Thesis.
Keith AM, Cameron DD, Seel WE. Spatial interactions between the hemiparasitic angiosperm Rhinanthus minor and its host are species-specific. Functional Ecology (2004) 18:435–442.[CrossRef]
Klaren CH, Janssen G. Physiological changes in hemiparasite Rhinanthus serotinus before and after attachment. Physiologia plantarum (1978) 42:151–155.[CrossRef]
Maxwell K, Johnson GN. Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany (2000) 51:659–668.
Mullineaux PM, Karpinski S, Baker NR. Spatial dependence for hydrogen peroxide-directed signalling in light stressed plants. Plant Physiology (2006) 141:346–350.
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI. Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta (2007) 1767:414–421.[Medline]
Nakano R, Ishida H, Makino A, Mae T. In vivo fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase by reactive oxygen species in an intact leaf of cucumber under chilling-light conditions. Plant and Cell Physiology (2006) 47:270–276.
Press MC, Graves JD. Parasitic plants (1995) London: Chapman and Hall.
Rümer S, Cameron DD, Wacker R, Hartung W, Jiang F. An anatomical study of the haustoria of Rhinanthus minor attached to roots of different hosts. Flora (2007) 202:194–200.
Tamura Y, Nishibe S. Changes in the concentrations of bioactive compounds in plantain leaves. Journal of Agricultural and Food Chemistry (2002) 50:2514–2518.[CrossRef][Web of Science][Medline]
Taylor A, Martin J, Seel WE. Physiology of the parasitic association between maize and witchweed (Striga hermonthica): is ABA involved? Journal of Experimental Botany (1996) 47:1057–1065.
Tennakoon KU, Cameron DD. The anatomy of Santalum album (sandalwood) haustoria. Canadian journal of Botany (2006) 84:1608–1616.
Watling JR, Press MC. Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biology (2001) 3:244–250.[CrossRef]
CiteULike 
Connotea 
Del.icio.us What's this?
Related articles in Ann Bot:
- ContentSnapshots
Ann Bot 2008 101: NP.[Extract] [Full Text] - John Bryant takes a closer look at some of this month's Original Articles
- J. A. Bryant
Ann Bot 2008 101: NP.[Extract] [Full Text]
This article has been cited by other articles:
|
|
 |
|
  J. Prider, J. Watling, and J. M. Facelli Impacts of a native parasitic plant on an introduced and a native host species: implications for the control of an invasive weed Ann. Bot., January 1, 2009; 103(1): 107 - 115. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||