Journal of Experimental Botany

JXB Advance Access originally published online on July 1, 2003

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Journal of Experimental Botany, Vol. 54, No. 389, pp. 1951-1955, August 1, 2003
© 2003 Oxford University Press

Short-term exposure to elevated atmospheric CO₂ benefits the growth of a facultative annual root hemiparasite, Rhinanthus minor (L.), more than that of its host, Poa pratensis (L.)

Received 10 April 2003; Accepted 16 April 2003

Jun-Kwon Hwangbo^*,, Wendy E. Seel^, and Sarah J. Woodin

School of Biological Sciences, Department of Plant and Soil Science, University of Aberdeen, Aberdeen AB24 3UU, UK

* Present address: Radiation Application Research Team, Korea Atomic Energy Research Institute, Taejeon, Korea.
To whom correspondence should be addressed. Fax: +44 (0)1224 272703. E-mail: w.e.seel{at}abdn.ac.uk

	Abstract

Top Abstract Introduction Materials and methods Results Discussion References

 
The effects of elevated CO₂ (650 ppm) on interactions between a chlorophyllous parasitic angiosperm, Rhinanthus minor (L.) and a host, Poa pratensis (L.) were investigated. R. minor benefited from elevated CO₂, with both photosynthesis and biomass increasing, and transpiration and tissue N concentration remaining unaffected. However, this did not alleviate the negative effect of the parasite on the host; R. minor reduced host photosynthesis, transpiration, leaf area and biomass, irrespective of CO₂ concentration. Elevated CO₂ resulted in increased host photosynthesis, but there was no concomitant increase in biomass and foliar N decreased. It appears that the parasite may reduce host growth more by competition for nitrogen than for carbon. Contrary to expectation, R. minor did not reduce the productivity of the host–parasite association, and it actually contributed to the stimulation of productivity of the association by elevated CO₂.

Key words: Elevated CO₂, nitrogen, parasitic angiosperm, photosynthesis, Poa pratensis, Rhinanthus minor.

	Introduction

Top Abstract Introduction Materials and methods Results Discussion References

 
Parasitic plants frequently inhibit biomass accumulation in their hosts. This can have serious consequences for agriculture, particularly in the mediterranean and in the semi-arid tropics where millions of hectares are infested with parasitic plants (Parker and Riches, 1993). Parasites also have effects on community composition within natural/semi-natural communities (Davies et al., 1997; Gibson and Watkinson, 1992; Pennings and Callaway, 1996; Callaway and Pennings, 1998), the consequences of which are currently unknown. Amongst the possible causes of the detrimental effects of parasites on hosts the diversion of resources, including carbon, from hosts to parasites is a key issue (Stewart and Press, 1990). The question of what happens to the host–parasite association if the availability of resources increases is pertinent in the context of current increases in global atmospheric CO₂ concentrations. This question is especially relevant to those parasites which possess chlorophyll (the hemiparasites) and are capable of some degree of photoautotrophy.

Rhinanthus minor is a facultative hemiparasite found in natural and semi-natural grasslands throughout the UK and Europe (Gibson and Watkinson, 1989, 1992; Davies et al., 1997). It has a C₃ photosynthetic pathway (Seel et al., 1993) and, at least in the short-term may thus be expected to respond positively to increased atmospheric CO₂. In experiments under elevated atmospheric CO₂, a closely related, obligate hemiparasite, Striga hermonthica (Del.) Benth. showed increased photosynthetic rate per unit leaf area. However, this was not reflected in increased biomass accumulation, nor was the detrimental effect of the parasite on the host alleviated (Watling and Press, 1997, 1998). The effect of increased atmospheric CO₂ on the photosynthetic capacity of the facultative parasite R. minor is unknown. On a unit leaf area basis R. minor has higher photosynthetic rates than Striga (Press et al., 1987; Seel and Press, 1994), and it may have a greater capacity to increase photoautotrophy than obligate parasites such as Striga. If this is the case then increased atmospheric CO₂ could boost autotrophic carbon gain to the extent that the detrimental effect of R. minor on its host is moderated.

The relationship between host and parasite is not a simple one, and just as the parasite affects the host, so the host affects the parasite. Xylem-feeding parasites, such as Rhinanthus, derive a proportion of their nitrogen, as well as carbon and water, from the host, and are clearly influenced by the volume and composition of N in the host transport stream (Seel et al., 1993; Seel and Jeschke, 1999). Elevated atmospheric CO₂ has been shown to alter the carbon/nitrogen composition of plants, and to have knock-on effects on insect herbivores. Such effects could also affect the growth of parasitic plants.

This study addresses the question of whether or not elevated atmospheric CO₂ affects the interactions between the parasite Rhinanthus minor and a common host, Poa pratensis. The aims of this study were to determine whether or not elevated atmospheric CO₂ (1) enhances photosynthesis and biomass accumulation of R. minor, (2) reduces negative effects of R. minor on P. pratensis through positive effects on parasite growth, and (3) alters the total productivity of the parasite–host association.

	Materials and methods

Top Abstract Introduction Materials and methods Results Discussion References

 
Carbon dioxide fumigation system
Four open-top CO₂ chambers were used, constructed to a design specified and parameterized by Ashenden et al. (1992) and located in the Cruickshank Botanic Garden, Aberdeen, UK. Chambers were arranged in pairs, each pair being served by a single air pump via a split ducting pipe. The experiment used a block design, each block comprising a pair of chambers, one receiving ambient atmospheric CO₂ and the other elevated CO₂. The target elevated CO₂ concentration was 650 ppm; actual concentrations fluctuated within the range 630–680 ppm.

Plants
Seeds of Poa pratensis were sown on trays of washed sand, and the seedlings were transferred to individual pots (10x10x10 cm) and supplied with 50 ml of Long Ashton solution (50% strength, with 3 mM NO₃) three times a week throughout the experiment. Once established (when the Poa pratensis was 4-weeks-old), half of these hosts were infected with pregerminated R. minor. One month later (early June), five parasitized and five non-parasitized hosts were transferred to each CO₂ chamber, and watered as required to prevent drought due to the air circulation. Plants were harvested 8 weeks later.

Measurements
Light-saturated photosynthesis (A_max) and transpiration rate (E) were measured by infrared gas analysis (ADC LCA-3) at growth CO₂ concentrations (650 ppm and 350 ppm). This was done when the parasites were fully grown and forming flower buds. On each R minor plant the youngest pair of fully expanded leaves were used for gas exchange measurement. These were detatched from the plant and allowed to equilibrate in the leaf chamber until the CO₂ differential stabilized (typically 2–3 min). Measurements on P. pratensis were made by placing a few of the youngest fully expanded leaves in parallel across the leaf chamber. Measurements were made between 10.00 h and 16.00 h, and to ensure saturating irradiance (>1500 µmol m^–2 s^–1) additional lighting was supplied by a 12 V, 20 W tungsten halide lamp. Temperature within the leaf chamber was maintained between 20–23 °C. A_max and E were determined on a leaf area basis (von Caemmerer and Farquhar, 1981), leaf area being determined using a scanner (Win-Rhizo, Regent Instrument Inc., Canada) and an area measurement system (Delta-T Devices Ltd, Cambridge, UK).

Plant materials were oven-dried at 80 °C prior to weighing and tissue-nutrient analysis. Tissue nitrogen and carbon concentrations were determined by an NCS autoanalyser (NA1500, Fisons, UK).

Statistical analysis
All data were analysed by two-way ANOVA (General Linear Model, GLM) and Tukey’s HSD test (Minitab). In order to avoid any problems of pseudoreplication, the main effects of CO₂ on R. minor and hosts were tested for significance against an error term which described overall between-chamber variation, and which was obtained by pooling the block and blockxCO₂ interaction terms (df=2) (Hurlbert, 1984). The significance of effects of the presence of R. minor was tested against residual between-plant variation (df=25) since R. minor treatment was nested within chambers, as was the interaction between R. minor and CO₂.

	Results

Top Abstract Introduction Materials and methods Results Discussion References

 
Responses of R. minor to elevated atmospheric CO₂
Elevated CO₂ increased photosynthetic rate per unit leaf area and biomass accumulation of R. minor (Table 1). By contrast, transpiration rate per unit leaf area and tissue N concentration and content were unaffected by CO₂ enrichment (Table 1).

View this table: [in this window] [in a new window]   Table 1. Growth and physiological parameters of attached R. minor grown at ambient (n=7) and elevated CO2 (n=8) Data are means ±1 SE, F ratio and P value from ANOVA.

 
Responses of hosts to elevated CO₂ and R. minor infection
Elevated CO₂ increased photosynthetic rate per unit leaf area in P. pratensis, had no effect on transpiration or on whole plant biomass accumulation, and resulted in decreased tissue N concentration (Table 2). R. minor decreased the photosynthetic and transpiration rates and biomass of its host, but had no effect on host tissue N concentration (Table 2). There were no significant interactions between the effects of CO₂ and R. minor on the host parameters investigated.

View this table: [in this window] [in a new window]   Table 2. Growth and physiological parameters of hosts with (+) and without (–) R. minor grown under ambient and elevated CO2 Values with different letters within each row are significantly different from each other at the level of 0.05 (Tukey test). Values represent means ±1 SE. n indicates number of samples measured. Analysis of two-way ANOVA are shown by symbols (: increase, : decrease, ***: P <0.001, **: P <0.01, *: P <0.05 and n.s.: not significant). CO2, infection and interaction represent effects of elevated CO2, R. minor infection and interaction between those factors, respectively.

 
Response of the host–parasite association to elevated CO₂ and R. minor infection
Total productivity of the host–parasite association (the sum of R. minor and P. pratensis dry weight) increased in elevated CO₂ (Table 2). The presence of R. minor did not alter total productivity of the association, irrespective of CO₂ treatment.

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
Does elevated atmospheric CO₂ benefit attached R. minor?
Elevated CO₂ increased the photosynthetic rate per unit leaf area of R. minor. Moreover, R. minor did not show the decreased transpiration rates (common to many non-parasitic plants in high CO₂) which could compromise its ability to capture host-derived, xylem-borne resources. It was also able to maintain its tissue nitrogen concentration despite a decline in that of its host, showing either strong competitive ability or increased ability to take N directly from the soil via its own roots (see below). The fact that photosynthesis is stimulated by relatively short-term (weeks) exposure to elevated CO₂ suggests that, like most C₃ plants in today’s atmosphere, R. minor is CO₂ limited and not operating at physiological capacity.

Reflecting the increase in photosynthesis, growth of R. minor was significantly increased in elevated CO₂. This is in marked contrast to the response of Striga hermonthica (Watling and Press, 1998), a discrepancy which might be at least partly explained by the fact that R. minor has relatively high photosynthetic rates (Gibson and Watkinson, 1992; Seel and Press, 1994), and low night-time respiration rates compared to Striga (Press et al., 1987). The difference may also be related to the fact that R. minor is a facultative parasite, whilst Striga cannot survive without a host and may be unable to manufacture in sufficient quantitiy compounds, other than photosynthates, which are necessary to support extra growth.

Thus both photosynthesis and growth of R. minor respond positively to elevated CO₂, and the plant does not suffer any significant dilution of tissue N as biomass increases. Is this improvement in performance due to increased autotrophy, or to increased exploitation of the host? A full answer to this requires further experimentation, but the question can be addressed in part by consideration of the effects of CO₂ on the parasite–host interaction.

Does elevated atmospheric CO₂ alleviate negative effects of the parasite on its host?
Despite the positive effect of elevated atmospheric CO₂ on the performance of R. minor, it did not significantly alter the magnitude of effect of R. minor on its host. The presence of R. minor reduced biomass of P. pratensis by 25–30%, and leaf area by 36% (compared to uninfected controls) under both ambient and elevated CO₂. This is consistent with results of other studies on hemi-parasitic plant associations under elevated CO₂ (Watling and Press, 1997, 1998; Matthies and Egli, 1999), and suggests that carbon abstraction alone does not explain the reduction in the growth of parasitized hosts. In further support of this, calculation of the data shows the parasite-induced carbon deficit of parasitized, compared to non-parasitized, host plant to be very similar in both ambient and elevated CO₂ (4.75 and 4.20 mg C plant^–1, respectively). Thus carbon extraction from the host by the parasite is not alleviated by elevated CO_2, and so host growth reduction must be attributable in part to some other factor. As for the parasite, it appears that the host provides less than 20% of its total carbon gain.

Nitrogen may be more influential. As noted above, R. minor appears to compete strongly for xylem-borne host N, and may also access some N from the soil. If N is of key importance, then the effect of the parasite on the host should be larger where N is limiting. This is indeed the case for Striga-infected Sorghum (Cechin, 1994), but our study’s experimental design did not enable this comparison. However, suggestion of the effect of elevated CO₂ on parasite acquisition of N can be gained from an inspection of the data. As with carbon, the parasitized hosts in ambient and elevated CO₂ suffered equal reductions, of 32%, in total N content (11.07 and 11.17 mg N plant^–1, respectively). These amounts are slightly less than the total N gain of the parasite (12.3 and 15.4 mg plant^–1 in ambient and elevated CO₂, respectively), suggesting that R minor may exhibit some autotrophy for N. Although not significant, the trend toward higher parasite total N content in elevated CO₂ does suggest that if CO₂ exposure were prolonged (for the full growth period), parasite autotrophy for N might increase, as well as maintenance of the level of theft from the host plant.

Although the photosynthetic rate of P. pratensis increased under elevated CO₂, its growth was not significantly improved during the experimental period. As in other elevated CO₂ studies (Aben et al., 1999) the concentration of N in P. pratensis tissues declined. Reduction in foliar N can inhibit leaf growth (MacDonald, 1990). However, this does not appear to be the mechanism operating in this case as host leaf area was reduced by parasite infection, but was not affected by elevated CO₂. Parasites can reduce host leaf area directly by inducing an alteration in host growth regulators, as seen in Striga-infected maize (Drennan and El Hiweris, 1979; Taylor et al., 1996).

These findings indicate that the observed lack of growth response of P. pratensis to CO₂ is not due either to foiliar N-induced reduction in leaf growth or to an increase in resource theft by the parasite. Rather, explanation should be sought in respiratory and root C efflux mechanisms, and possibly in leaf and root turnover rates.

How is productivity of the host–parasite association affected?
Parasites have inherently lower resource use efficiency than their host so that the total productivity of the host–parasite association is expected to be lower than that of the uninfected host (Matthies, 1995). This was not the case for the R. minor–P. pratensis association. Despite the negative effects of R. minor on its host, the total biomass of the association was no less than that of the uninfected host, suggesting that R. minor is using host-derived resources very efficiently and/or contributing resources to the association. Stable isotope tracer experiments would be needed to identify exact mechanisms, but the observations do suggest that R. minor was largely autotrophic for carbon, and possibly somewhat so for N. Indeed, the increase in biomass of R. minor in elevated CO₂ makes a significant contribution to the overall increase in biomass of the association.

Prediction of the longer term effects of elevated atmospheric CO₂ on parasitized communities would require further experimentation. Speculation by Pate (1993) suggests that the relative responsiveness of the host and parasite species concerned will be crucial. Data of Matthies and Egli (1999) suggest that the differential between host and parasite responsiveness may be a complex function of both biotic and abiotic factors, and thus not easy to predict. With respect to the Rhinanthus minor–Poa pratensis association however, it can be concluded that short-term elevation of atmospheric CO₂ enhances photosynthesis and biomass accumulation of R. minor, does not reduce negative effects of R. minor on P. pratensis, but does increase the total productivity of the parasite–host association.

	References

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This Article Abstract FREE Full Text (PDF) All Versions of this Article: 54/389/1951    most recent erg194v1 E-letters: Submit a response Alert me when this article is cited Alert me when E-letters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (1) Request Permissions Disclaimer Google Scholar Articles by Hwangbo, J.-K. Articles by Woodin, S. J. Search for Related Content PubMed PubMed Citation Articles by Hwangbo, J.-K. Articles by Woodin, S. J. Agricola Articles by Hwangbo, J.-K. Articles by Woodin, S. J. Social Bookmarking          What's this?

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