Journal of Experimental Botany, Vol. 51, No. 352, pp. 1931-1938,
November 1, 2000
© 2000 Oxford University Press
Original Papers |
Atmospheric CO2 and mycorrhiza effects on biomass allocation and nutrient uptake of nodulated pea (Pisum sativum L.) plants
1 Plant Biology and Biogeochemistry Department, Risø National Laboratory, PO Box 49, DK-4000 Roskilde, Denmark
2 Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, Columbus, Ohio, USA
Received 7 February 2000; Accepted 21 June 2000
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The effect of ambient and elevated atmospheric CO2 on biomass partitioning and nutrient uptake of mycorrhizal and non-mycorrhizal pea plants grown in pots in a controlled environment was studied. The hypothesis tested was that mycorrhizae would increase C assimilation by increasing photosynthetic rates and reduce below-ground biomass allocation by improving nutrient uptake. This effect was expected to be more pronounced at elevated CO2 where plant C supply and nutrient demand would be increased. The results showed that mycorrhizae did not interact with atmospheric CO2 concentration in the variables measured. Mycorrhizae did not affect photosynthetic rates, had no effect on root weight or root length density and almost no effect on nutrient uptake, but still significantly increased shoot weight and reduced root/shoot ratio at harvest. Elevated CO2 increased photosynthetic rates with no evidence for down-regulation, increased shoot weight and nutrient uptake, had no effect on root weight, and actually reduced root/shoot ratio at harvest. Non-mycorrhizal plants growing at both CO2 concentrations had lower shoot weight than mycorrhizal plants with similar nutritional status and photosynthetic rates. It is suggested that the positive effect of mycorrhizal inoculation was caused by an enhanced C supply and C use in mycorrhizal plants than in non-mycorrhizal plants. The results indicate that plant growth was not limited by mineral nutrients, but partially source and sink limited for carbon. Mycorrhizal inoculation and elevated CO2 might have removed such limitations and their effects on above-ground biomass were independent, positive and additive.
Key words: Allocation, arbuscular mycorrhiza, elevated carbon dioxide, nitrogen, pea, phosphorus.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Atmospheric CO2 is rising and expected to double within the next hundred years (Watson et al., 1990
). Experimental increases in atmospheric CO2 concentration have often resulted in increased plant photosynthesis (Curtis and Wang, 1997; Stitt, 1991), growth and amount of C allocated below-ground (Rogers et al., 1994). However, limitation in nutrient availability, especially N (Berntson and Bazzaz, 1996) and/or in sink strength may restrict the capacity of plants to use increased photosynthates and down-regulation of photosynthesis can occur (Farrar and Williams, 1991; Wardlaw, 1990). Therefore, plant and ecosystem responses to increasing atmospheric CO2 are directly influenced by the size and activity of below-ground structures (Curtis et al., 1990).
Roots and their microbial symbionts are responsible for most of the nutrient uptake in legumes but they are also major sinks for plant photosynthates (Paul and Kucey, 1981; Harris and Paul, 1987; Jakobsen and Rosendahl, 1990). Mycorrhizal fungi are obligate biotrophs of plant roots of most plant species and they usually promote plant growth by improving plant uptake of P and other immobile nutrients (Smith and Read, 1997). Rhizobial bacteria form symbiotic associations with legume species and fix atmospheric N2. This process has high phosphate (ATP) and plant photosynthate requirements and has been stimulated by mycorrhizae and P fertilization in numerous studies (Barea and Azcón-Aguilar, 1983). Mycorrhizal and rhizobial functioning are therefore linked to each other in legumes. Furthermore, it has been hypothesized that the continuous removal of C compounds for mycorrhizal and rhizobial growth and activity increases sink strength (Pang and Paul, 1980) and prevents the accumulation of photosynthates in the leaves which could, in turn, lead to down-regulation of photosynthesis (Harris and Paul, 1987).
Increased sink activity may increase plant photosynthetic rates and the amount of C allocated below-ground independently of the symbiont's effect on plant growth and nutrition (Harris et al., 1985). The tripartite association would then have optimal performance at elevated CO2 with a combination of enhanced root and shoot activity. This has led to hypotheses and studies examining the possibility that below-ground sink activity in mycorrhizal plants is enhanced at elevated CO2 (Morgan et al., 1994). Symbiotic N2 fixation has increased at elevated CO2 and this amplified the plants growth response to the additional C availability (Hartwig, 1998). However, there is increasing evidence that elevated CO2 has little effect on mycorrhizae development (Staddon and Fitter, 1998) and functioning (Staddon et al., 1999a, b), although there may be some fungal interspecific differences to consider (Klironomos et al., 1998).
A study was carried out to test the following hypotheses:
- That mycorrhizae would increase C assimilation by increasing sink strength, and reduce below-ground biomass allocation by improving nutrient uptake. It was expected that the mycorrhizal effects to be more pronounced at elevated CO2 where increased plant C supply and nutrient demand were also expected.
- That elevated CO2 would increase photosynthetic rates and shoot growth by increasing C supply, and would increase root weight and root/shoot ratio by increasing nutrient demand in comparison with ambient CO2.
A growth-room experiment was conducted at the closest growing conditions to those prevailing in the field, testing two concentrations of atmospheric CO2 and the presence or absence of mycorrhiza on biomass allocation and nutrient uptake of nodulated pea plants.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Experimental design
A complete randomized block factorial experiment was set up allocating half of the pots to ambient atmospheric CO2 and the other half to elevated CO2. Half of the plants at each CO2 level were inoculated with a mycorrhizal fungus (M) and half were left uninoculated (NM). Each treatment combination had six replicates and is referred to as follows: 360M (ambient CO2, mycorrhizal), 360NM (ambient CO2, non-mycorrhizal), 700M (elevated CO2, mycorrhizal), and 700NM (elevated CO2, non-mycorrhizal).
Soil
The soil was collected from the arable layer of an organic cropping site in Denmark. This soil (49.9% sand, 31.8% silt, 16% clay, 1.36% OM) had 0.27 meq Mg l-1, 0.06 meq Na l-1, 10.98 meq Ca l-1, 0.27 meq K l-1, 11.58 meq CEC l-1, 0.14% total N, and 27 mg kg-1 NaHCO3-extractable P (Olsen et al., 1954). Soil was air-dried, sieved through an 8 mm mesh and mixed with quartz sand 1 : 1 w : w. This resulted in a reduction of plant available P to 18 mg kg-1. The soil was then irradiated to eliminate mycorrhizal propagules (10 kGy, 10 MeV electron beam), and mixed with the following nutrients as powder (mg kg-1): KCl (100), MgSO4.7H2O (100), MnSO4.H2O (10), CuSO4.5H2O (5), ZnSO4.7H2O (5), CoSO4.7H2O (1), Na MoO4.2H2O (0.5), and KH2PO4 (131.7). An initial application of 20 mg N kg-1 was also added as NH4NO3. PVC cylinders (20 cm diameter and 50 cm depth) sealed at the bottom were used as pots and filled with 14 kg of the soil:sand mixture with or without mycorrhizal inoculum.
Biological materials
Mycorrhizal inoculum consisting of soil with mycelium, spores and root pieces colonized with Glomus caledonium (Nicol. and Gerd.) Trappe and Gerdemann BEG 15 isolate was incorporated into the mycorrhizal treatments, 1 : 9 w : w, mixing thoroughly with the soil/sand mixture. One day after planting a filtrate was added to all pots obtained from the mycorrhizal inoculum, but from which the mycorrhizal propagules had been eliminated in an attempt to restore some of the other soil free-living microorganisms. The filtrate was obtained by passing an inoculum:water 1:9 v:v suspension through three overlapped layers of 25 µm nylon mesh. Pea seeds (cv. Solara) weighing between 0.27 and 0.32 g were germinated between wet tissue paper and planted 2 d later. Five ml of a yeast–mannitol broth culture of Rhizobium leguminosarum (Risø 18a isolate) were placed with each of the seven seeds planted to promote the formation of nodules. Plants were thinned to five plants per pot after seedling emergence.
Growing conditions
Watering was done by weight to measured field capacity for the first 2 weeks and then the water supply was increased by 1% of the gravimetric water content every subsequent week to ensure adequate moisture in the soil column as plants began to use more water. The pots were placed inside air-cooled chambers with 12 pots capacity where soil temperature in the pots could be controlled separately from room air temperature. The chambers were set to maintain approximately 15 °C soil temperature in the middle of the pots. Soil temperature selection is an average for the corresponding growth period in Denmark at 25 cm depth (Jakobsen and Nielsen, 1983; B Jensen, personal communication). Actual soil temperature in the pots was 14 °C constant at the bottom of the pots, 15–17 °C day fluctuation at 20 cm depth, and 15–20 °C towards the soil surface. Pots were not rotated within soil-cooling chamber but each chamber was divided in six blocks to account for differences due to position within each soil-cooling chamber. The soil-cooling chambers were placed in two growth rooms at Risø Experimental Risk Assessment Facility (RERAF, Risø National Laboratory, Denmark) running at ambient (set at 360 ppm, measured experiment mean 368 ppm) and elevated (set at 700 ppm, measured experiment mean 688 ppm) atmospheric CO2. To reduce position effects further, each growth room was set at either ambient or elevated atmospheric CO2 concentration for a 1 week period and then the CO2 concentration was switched every week. The soil-cooling chambers were moved to the appropriate room to maintain the CO2 treatments and rotated within the room to minimize differences due to position within a growth room.
Plants were grown for 9 weeks with gradual increases in air temperature typical of field conditions, 14/8 °C day/night for the first 3 weeks and 16/10 °C day/night during the last 6 weeks. Daylength was also increased from 14 h during the first 3 weeks to 16 h during the rest of the experiment. Photosynthetic photon flux density in the rooms increased gradually to, and decreased gradually from, a midday maximum of 750±50 µmol m-2 s-1, with a 6 h period at maximum light intensity during the first 3 weeks which was increased to 8 h during the rest of the experiment.
Sampling, measurements and harvest
Soil samples with roots were taken with a soil corer, 1.8 cm diameter and 20 cm depth, 5 weeks after planting. Roots were extracted with forceps from the soil and the root-free soil sample was inmediately frozen. Roots were washed, stained (Kormanik and McGraw, 1982) and mounted on slides to determine mycorrhizal colonization (McGonigle et al., 1990). Soil was thawed, thoroughly mixed and a subsample was taken for specific fatty acid signature analysis (Olsson et al., 1996). The phospholipid and neutral lipid fractions of the fatty acid 16:1
5 were used as indicators of arbuscular mycorrhizal external hyphae development in soil.
Photosynthetic rate measurements at the experimental CO2 concentration and at light saturation (PP systems, CIRAS-1 with automatic leaf cuvette) were taken 6 weeks after planting using a randomly selected second youngest fully developed leaf from each pot. A leaf disc of fixed area was taken from a neighbouring leaf, dried and weighed to determine specific leaf area. The leaves used for measuring photosynthetic rates were also dried and ground together with the leaf discs for nutrient analysis. Photosynthetic response measurements were taken 8 weeks after planting from five replicates in each treatment to study treatment effects on photosynthetic capacity. Light-saturated photosynthetic rates were measured from a randomly selected second youngest fully developed leaf from each pot after modifying the internal CO2 concentrations (Ci) of plants growing at ambient and elevated CO2 to 150 ppm and 500 ppm. These measurements made at two contrasting points of CO2 availability, one at very low availability and one at saturation, were used to explore down-regulation or acclimation of photosynthesis to growth at elevated CO2.
Plants were harvested 60 d after planting, 2 weeks after the onset of flowering. Shoots were cut, divided into stems with broad leaves, tendrils, flowers, and fruits, dried and weighed separately. Shoot components were then mixed, ground and analysed for P and N concentration. Soil cores of 3 cm diameter by 40 cm depth containing roots, were taken from the pot and frozen until processing. The rest of the roots in the pots were washed thoroughly, chopped, mixed in water and a subsample for root nutrient concentration was taken. Subsamples and the rest of the roots were blotted, weighed and dried, to estimate total root weight. Nutrient concentration was determined after grinding and digesting subsamples. Soil cores were thawed, roots were washed and root length was determined by the gridline intersect method (Tennant, 1975). Roots were stained, mycorrhizal colonization in roots was measured and fungal hyphae development in soil was determined as explained above.
Statistical analysis
Effects of atmospheric CO2 and mycorrhizal inoculation were tested by two-way ANOVA (SAS Institute Inc, release 6.12). A priori tests of preconceptualized hypotheses were carried out as linear contrasts regardless of significance level in ANOVA. Data sets not meeting assumptions for ANOVA were transformed as required but the results are presented in their original scale of measurement. It was considered that marginally significant differences were P<0.1 and significant differences at P<0.05.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Mycorrhiza development
Pea roots were extensively nodulated in all plants and colonized by Glomus caledonium 5 weeks after planting (w.a.p.) in mycorrhizal treatments (Table 1
). Elevated atmospheric CO2 had no effect on intraradical colonization, expressed as a percentage of total root length colonized (Table 1). Arbuscular colonization accounted for 85–90% of total colonization and vesicular colonization was virtually zero, even in samples taken at the end of the experiment. Closer examination of some of the samples gave no indication of differences in intraradical colonization intensity between plants growing at ambient and at elevated CO2. Some pots became contaminated with another arbuscular mycorrhizal fungus (‘fine endophyte’) towards the end of the experiment, but colonization in contaminated pots was very low and the only control pot where contamination exceeded 5% colonized root length was eliminated from the data analysis.
|
Extraradical mycorrhizal hyphae development measured with specific fatty-acid signatures was poor in these experiments in comparison with the extensive colonization measured in roots. There were no differences between ambient and elevated CO2 in any of the two fatty acid indicators at both sampling times (Table 1
). There were no significant differences among any of the treatments, including non-mycorrhizal controls (background), in the amount of the phospholipid fatty acid 16:15 along the experiment. The amount of the neutral lipid fatty acid 16:15 was significantly higher in the mycorrhizal than in the non-mycorrhizal treatments five w.a.p. and at harvest (Table 1). Hyphal length counts performed from some of the samples confirmed, in general, the results obtained with fatty-acid signature analysis.
Biomass allocation
No treatment interactions were significant for any of the biomass or biomass allocation variables. Dry weights of shoot and all shoot components were higher at elevated than at ambient CO2 and in mycorrhizal than in non-mycorrhizal plants (Fig. 1). Shoot weight mean for the 700M treatment was the highest, 360M and 700NM treatment means were intermediate and not different from each other, and 360NM treatment mean was the lowest (Fig. 1). Root weight at harvest was only marginally higher (P=0.092) at elevated than at ambient CO2 and not affected by inoculation with mycorrhizae. The differences in shoot weight resulted in (1) higher total plant weight at elevated than at ambient CO2 and in mycorrhizal than in non-mycorrhizal plants, and (2) lower root/shoot ratio of plants growing at elevated than at ambient CO2 and lower root/shoot ratio with mycorrhizae than without mycorrhizae (Fig. 1). Reproductive tissue was significantly higher at elevated CO2 as a consequence of differences in plant size, but neither allocation to flowers and fruits nor the number of stems were affected by CO2 or inoculation treatments (data not shown).
|
Interactions and mycorrhiza effects were not significant for specific leaf area (SLA) or C assimilation rate measurements. Elevated CO2 decreased SLA at both sampling times and increased also C assimilation rate (Table 2
). Measurements of C assimilation rate at two internal C concentrations (Ci) showed no significant differences between plants growing at ambient or at elevated CO2, indicating that the photosynthetic capacity of plants growing at elevated CO2 was not altered (no down-regulation or acclimation). Mycorrhizal inoculation increased water use but did not alter water use efficiency. In contrast, elevated CO2 had no effect on water use but increased significantly water use efficiency (Table 2).
|
Nutrient uptake
Treatment interactions were not significant for N or P concentration and N or P uptake or use efficiency variables. Atmospheric CO2 treatments had no effect on root-N and shoot-N concentration or root-N content, but the differences in shoot weight resulted in higher shoot-N and total-N content at elevated than at ambient CO2 (Fig. 2). N uptake g-1 and cm-1 root, and N use efficiency were not affected by atmospheric CO2 (data not shown). Root-N concentration was higher in non-mycorrhizal than in mycorrhizal plants, but their root-N content was the same. On the other hand, shoot-N concentration was the same in mycorrhizal as in non-mycorrhizal plants, but mycorrhizal plants had higher shoot-N and total-N content than non-mycorrhizal plants. N uptake g-1 and cm-1 of root was significantly higher in mycorrhizal (245±12 mg N g-1 root, 0.027±0.002 mg N cm-1 root) than in non-mycorrhizal (220±8 mg N g-1 root, 0.023±0.001 mg N cm-1 root) plants. There were no significant differences in N use efficiency of mycorrhizal and non-mycorrhizal plants.
|
Elevated CO2 marginally increased shoot-P and total-P content but otherwise had no effect on plant tissue P concentration, P uptake or P-use efficiency (Table 3
). Mycorrhizal inoculation reduced root-P concentration, shoot-P concentration and root-P content and increased P use efficiency at harvest time but had no effect on shoot-P and total-P content or P uptake g-1 and cm-1 of root.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Elevated CO2 and mycorrhiza had similar though independent effects on plant biomass and biomass allocation. Both resulted in increased shoot and total weight, and decreased root/shoot ratio. The effects of elevated CO2 and mycorrhiza on shoot and total plant weight were then stimulating and additive as predicted by our hypothesis, but the effect of mycorrhizal inoculation was not more pronounced at elevated than at ambient CO2. The lack of treatment effects in root weight and the reduced root/shoot ratio with elevated CO2 were also unexpected. However, these hypotheses were based on the existence of nutrient or C limitation.
One explanation for these results could be that increased nutrient uptake in mycorrhizal plants stimulated N2 fixation and enabled mycorrhizal plants to use more of the C assimilated at both CO2 concentrations for shoot growth. This considers that plant growth was mainly nutrient limited. Symbiotic activity in legumes may improve plant nutrient status and increase shoot biomass proportionally to C availability, thereby explaining the lack of response of below-ground biomass. Other studies have reported that below-ground biomass of the legume Trifolium repens was less responsive to elevated CO2 than that of Lolium perenne, while the opposite was true for above-ground biomass (Jongen et al., 1995; Hebeisen et al., 1997). N uptake was indeed increased by mycorrhiza in this experiment and mycorrhizal plants had higher N uptake g-1 and cm-1 of root than non-mycorrhizal plants at harvest. In experiments with Trifolium repens, symbiotic N2 fixation increased under elevated CO2 and was responsible for most of the additionally assimilated N (Zanetti et al., 1996; Zanetti and Hartwig, 1997) while an increase in N2 fixation with elevated CO2 has been reported, but only in plants with high P supply (Sa and Israel, 1998). Mycorrhizae, however, did not improve P uptake in the week 6–9 period and if it happened at all the improvement in P uptake must have been early and short-lasting. Six weeks after planting both mycorrhizal and non-mycorrhizal plants had higher shoot-P concentrations (data not shown) than those measured from field-grown peas in P-fertilized soils at equivalent growth stage (Jakobsen, 1986, 1987). Non-mycorrhizal plants had taken up the same or more P than mycorrhizal plants at two sampling times without developing more roots. This does not indicate nutrient limitation and can be explained if the amount of N and P added at the beginning of the experiment and the amount of N fixed were enough to meet plant demand in all treatments. The scarce development of the external mycorrhizal mycelium into the soil is in accordance with the lack of difference in P uptake by mycorrhizal and non-mycorrhizal plants. The absence of a nutritional benefit conflicts, however, with the difference observed in shoot biomass of mycorrhizal and non-mycorrhizal plants. The explanation of nutrient limitation seems then unlikely. Nevertheless, a transient, early improvement in P uptake cannot be completely ruled out since there are no measurements of early plant-P concentration. Early root development of some plants limits their P uptake capacity and makes them benefit from mycorrhizal colonization at early growth stages even in fertile soils, with long-lasting effects of improved early P nutrition in biomass allocation (Gavito and Miller, 1998).
If growth was limited only by C availability, biomass of non-mycorrhizal and mycorrhizal plants should have been the same at each CO2 concentration unless mycorrhizal inoculation altered either plant photosynthetic rates or leaf area. Elevated CO2 decreased SLA and increased C assimilation rates and water use efficiency, in accordance with the results of other studies (Drake et al., 1996; den Hertog et al., 1996; García et al., 1998; Ryle et al., 1992). The decrease in SLA at elevated CO2 is usually attributed to C accumulation in leaves resulting from insufficient sinks for the increased production of photosynthates. In these experiments, plants growing at ambient CO2 had higher SLA but lower shoot weight and C assimilation rate than those growing at elevated CO2 which indicates lower C assimilation on a whole plant basis at ambient CO2 than at elevated CO2. However, mycorrhizal plants had similar SLA and C assimilation rate but higher shoot weight than non-mycorrhizal plants indicating both higher leaf area and higher whole plant C assimilation with mycorrhiza than without mycorrhiza. Mycorrhizae increased leaf area expansion rate of nodulated soybean independently from plant nutritional effects (Fredeen and Terry, 1987). Accordingly, it seems likely that mycorrhizae increased leaf area and C assimilation on a whole plant basis in comparison with uninoculated plants and stimulated shoot growth proportionally to the availability of C. Results from a similar study conducted later with pea plants showed a significant CO2xinoculation interaction on C assimilation rates when measurements were taken at earlier growth stages (ME Gavito et al., unpublished results). Results from that study and the one conducted by Staddon et al. (Staddon et al., 1999b) indicated that photosynthetic rates of mycorrhizal and non-mycorrhizal plants were similar at ambient CO2 but the rates of mycorrhizal plants were higher with than those of non-mycorrhizal plants at elevated CO2. The effects of elevated CO2 and mycorrhizae would be positive and additive if plants were only C-source-limited and both factors partially removed such limitation.
It is possible that elevated CO2 increased C availability and that the increased sink strength in mycorrhizal plants (from growth and maintenance of one versus two symbionts) enhanced C use proportionally at both CO2 concentrations. This explanation assumes that plants were both source and sink limited and that elevated CO2 removed part of the source limitation whereas mycorrhiza removed part of the sink limitation. The main effects of elevated CO2 and mycorrhizal inoculation on shoot biomass of plants partially source- and sink-limited then would have been positive and their effects, when combined, would have been positive and additive. C assimilation rates were indeed higher at elevated than at ambient CO2 and showed no down-regulation at elevated CO2, as has been reported in other studies with adequate soil N fertility (Idso and Kimball, 1991) or with N2-fixing species even when growing in poor soils (Vogel and Curtis, 1995). There is then some evidence in this study that C supply increased at elevated CO2, but there is no conclusive evidence for higher sink strength in mycorrhizal than in non-mycorrhizal plants.
The lack of differences in root weight, root length density, intraradical colonization (as percentage, phenology or intensity) and extraradical hyphal development at both sampling times indicate that root and mycorrhizal development were not influenced by CO2 in this study. Extraradical mycorrhizal development was surprisingly low in comparison with intraradical colonization. One important remark is that this study was carried out at the soil temperatures plants experience in the field, which is much colder than those used in most indoor experiments, and at relatively high soil P level. High soil P seems to reduce both extraradical mycelium and intraradical colonization (Abbott et al., 1984), but there are interspecific differences in the extent to which the external and internal phases develop and no generalizations can be made. The effect of low temperature on intra- and extraradical colonization is even less well known, but is unlikely to affect the external and internal phases differently. Extraradical and intraradical mycorrhizal colonization was not affected by atmospheric CO2 in most studies conducted with other plant species (Staddon and Fitter, 1998; Staddon et al., 1999a). Total mycorrhizal root length increased with elevated CO2 in T. repens (Jongen et al., 1996) but this effect disappeared when differences in plant growth were considered (Staddon et al., 1998). The root length density and root weight measurements from this study gave no indication of differences in size of the root systems. Root/shoot ratio, however, decreased in mycorrhizal and elevated CO2 plants, indicating that the root systems of mycorrhizal and elevated CO2 plants were supporting larger plants. It is difficult to know if the differences in root/shoot ratio or in root and mycorrhiza development represent a smaller or larger C sink because they are not the only indicators of sink strength. C use for maintenance can account for a large proportion of the C allocated below-ground (Jakobsen and Rosendahl, 1990; Peng et al., 1993), and should be measured for a thorough estimation of sink strength.
It is concluded that, in the present work, the effects of atmospheric CO2 and mycorrhizae on biomass production and on allocation and uptake of nutrients were in general low. Atmospheric CO2 and mycorrhizal inoculation did not interact in this study, and this is in accordance with similar studies with the legume Trifolium repens (Jongen et al., 1996; Staddon et al., 1999a), and Plantago lanceolata (Rouhier and Read, 1998), but in contrast to a study carried out with Robinia pseudoacacia (Olesniewicz and Thomas, 1999). The conflicting results can be attributed to differences in growing conditions, in particular concerning rooting volume, soil nutrient level and control of soil and air temperature. Most of these results add to the evidence reviewed by Staddon et al. that the functioning and development of mycorrhizae and its effects on the plant are not affected by elevated CO2 (Staddon et al., 1999a).
These results indicate interesting trends to explore in relation to root and shoot activity. It has to be emphasized that these experiment was carried out with a legume growing under favourable conditions, with large rooting volume and at lower soil and air temperatures than is true for most growth chamber studies. Nutrient uptake (Cumbus and Nye, 1985; Clarkson et al., 1986), C assimilation, plant growth, and biomass allocation below-ground can be reduced at low temperatures (Ziska, 1998). Future studies should address unexplored potential increases in leaf area and whole plant C assimilation, sink strength, and the shoot growth-promoting effect in mycorrhizal plants, which occurs without any apparent plant nutritional benefit.
|
Acknowledgments |
|---|
This work was funded by grant no. 9501743 of the Danish Agricultural and Veterinary Research Council. We wish to thank Anne Olsen and Anette Olsen for skilful technical assistance, and John Larsen for the fatty acid signature analyses.
|
Notes |
|---|
3 To whom correspondence should be addressed: Fax: +45 46 77 4282. E-mail: mayra.gavito{at}risoe.dk
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Abbott LK, Robson AD, De Boer G.1984. The effect of phosphorus on the formation of hyphae in soil by the vesicular-arbuscular mycorrhizal fungus, Glomus fasciculatum. New Phytologist 97, 437–446.
Barea JM, Azcón-Aguilar C.1983. Mycorrhizas and their significance in nodulating nitrogen-fixing plants. Advances in Agronomy 36, 1–54.
Berntson GM, Bazzaz FA.1996. Below-ground positive and negative feedbacks on CO2 growth enhancement. Plant and Soil 187, 119–131.
Clarkson DT, Hopper MJ, Jones LHP.1986. The effect of root temperature on the uptake of nitrogen and the relative size of the root system in Lolium perenne. I. Solutions containing both NH+4 and NO-3. Plant, Cell and Environment 9, 535–545.
Cumbus IP, Nye PH.1985. Root zone temperature effects on growth and phosphate absorption in rape Brassica napus cv. Emerald. Journal of Experimental Botany 36, 219–227.
Curtis PS, Wang X.1998. A meta-analysis of elevated CO2 effects on woody plant mass, form and physiology. Oecologia 113, 299–313.[Web of Science]
Curtis PS, Balduman LM, Drake BG, Wingham DF.1990. Elevated atmospheric CO2 effects on below-ground processes in C3 and C4 estuarine marsh communities. Ecology 71, 2001–2006.
den Hertog J, Stulen I, Fonseca F, Delea P.1996. Modulation of carbon and nitrogen allocation in Urtica dioica and Plantago major by elevated CO2: impact of accumulation of nonstructural carbohydrates and ontogenetic drift. Physiologia Plantarum 98, 77–88.
Drake BG, González-Meler M, Long SP.1996. More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609–639.[Web of Science]
Farrar JF, Williams ML.1991. The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source–sink relations and respiration. Plant, Cell and Environment 14, 819–830.
Fredeen AL, Terry N.1987. Influence of vesicular-arbuscular mycorrhizal infection and soil phosphorus level on growth and carbon metabolism of soybean. Canadian Journal of Botany 66, 2311–2316.
García RL, Long SP, Wall GW, Osborne CP, Kimball BA, Nie GY, Pinter PJ, Lamorte RL, Wechsung F.1998. Photosynthesis and conductance of spring-wheat leaves: field response to continuous free-air atmospheric CO2 enrichment. Plant, Cell and Environment 21, 659–669.
Gavito ME, Miller MH.1998. Early phosphorus nutrition, mycorrhizae development, dry matter partitioning and yield of maize. Plant and Soil, 199, 177–186.
Harris D, Paul EA.1987. Carbon requirements of vesicular-arbuscular mycorrhizae. In: Safir GR, ed. Ecophysiology of VA mycorrhizal plants. Boca Raton, Florida: CRC Press, 93–105.
Harris D, Pacovsky RS, Paul EA.1985. Carbon economy of soybean–Rhizobium–Glomus associations. New Phytologist 101, 427–440.[Web of Science]
Hartwig UA.1998. The regulation of symbiotic N2 fixation: a conceptual model of N feedback from the ecosystem to the gene expression level. Perspectives in Plant Ecology, Evolution and Systematics 1, 107–135.
Hebeisen T, Luscher A, Zanetti S, Fischer BU, Hartwig UA, Frehner M, Hendrey GR, Blum H, Nösberger J.1997. Growth response of Trifolium repens L. and Lolium perenne L. as monocultures and bi-species mixture to free air CO2 enrichment and management. Global Change Biology 3, 149–160.
Idso SB, Kimball BA.1991. Downward regulation of photosynthesis and growth at high CO2 levels. Plant Physiology 96, 990–992.
Jakobsen I.1986. Vesicular-arbuscular mycorrhiza in field-grown crops. III. Mycorrhizal infection and rates of phosphorus inflow in pea plants. New Phytologist 104, 573–581.
Jakobsen I.1987. Effects of VA mycorrhiza on yield and harvest index of field-grown pea. Plant and Soil 98, 407–415.
Jakobsen I, Nielsen NE.1983. Vesicular-arbuscular mycorrhiza in field-grown crops. I. Mycorrhizal infection in cereals and peas at various times and soil depths. New Phytologist 93, 401–413.
Jakobsen I, Rosendahl L.1990. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytologist 115, 77–83.[Web of Science]
Jongen M, Fay P, Jones MB.1996. Effects of elevated carbon dioxide and arbuscular mycorrhizal infection on Trifolium repens. New Phytologist 132, 413–423.
Jongen M, Jones MB, Hebeisen T, Blum H, Hendrey GR.1995. The effects of elevated CO2 concentrations on the root growth of Lolium perenne and Trifolium repens grown in FACE system. Global Change Biology 1, 361–371.
Klironomos JN, Ursic M, Rillig M, Allen MF.1998. Interspecific differences in the response of arbuscular mycorrhizal fungi to Artemisia tridentata grown under elevated atmospheric CO2. New Phytologist 138, 599–605.[Web of Science]
Kormanik PP, McGraw AC.1982. Quantification of vesicular-arbuscular mycorrhiza in plant roots. In: Schenck NC, ed. Methods and principles of mycorrhizal research. St Paul: American Phytopathological Society, 37–45.
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA.1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115, 495–501.[Web of Science]
Morgan JA, Knight WG, Dudley LM, Hunt HW.1994. Enhanced root system C-sink activity, water relations and aspects of nutrient acquisition in mycotrophic Bouteloua gracilis subjected to CO2 enrichment. Plant and Soil 165, 139–146.
Olesniewicz KS, Thomas RB.1999. Effects of mycorrhizal colonization on biomass production and nitrogen fixation of black locust (Robinia pseudoacacia) seedlings grown under elevated atmospheric carbon dioxide. New Phytologist 142, 133–140.
Olsen SR, Cole CV, Watanabe FS, Dean LA.1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture Circular 939, 1–19.
Olsson PA, Bååth E, Jakobsen I, Söderström B.1996. The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycological Research 99, 623–629.
Pang PC, Paul EA.1980. Effects of vesicular-arbuscular mycorrhiza on 14C and 15N distribution in nodulated fababeans. Canadian Journal of Soil Science 60, 241–250.
Paul EA, Kucey RMN.1981. Carbon flow in plant microbial associations. Science 213, 473–474.
Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC.1993. Growth depression in mycorrhizal Citrus at high-phosphorus supply. Plant Physiology 101, 1063–1071.[Abstract]
Rogers HH, Runion GB, Krupa SV.1994. Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environmental Pollution 83, 155–189.[Medline]
Rouhier H, Read DJ.1998. The role of mycorrhiza in determining the response of Plantago lanceolata to CO2 enrichment. New Phytologist 139, 367–373.
Ryle GJA, Powell CE, Davidson IA.1992. Growth of white clover, dependent on N2 fixation, in elevated CO2 and temperature. Annals of Botany 70, 221–228.
Sa T, Israel DW.1998. Phosphorus-defficiency effects on response of symbiotic N2 fixation and carbohydrate status in soybean to atmospheric CO2 enrichment. Journal of Plant Nutrition 21, 2207–2218.
Smith SE, Read DJ.1997. Mycorrhizal symbiosis. London: Academic Press.
Staddon PL, Fitter AH.1998. Does elevated carbon dioxide affect arbuscular mycorrhizas? Trends in Ecology and Evolution 13, 455–458.
Staddon PL, Graves JD, Fitter AH.1998. Effect of enhanced atmospheric CO2 on mycorrhizal colonisation by Glomus mosseae in Plantago lanceolata and Trifolium repens. New Phytologist 139, 571–580.
Staddon PL, Fitter AH, Graves JD.1999a. Effect of elevated atmospheric CO2 on mycorrhizal colonization, external mycorrhizal hyphal production and phosphorus inflow in Plantago lanceolata and Trifolium repens in association with the arbuscular mycorrhizal fungus Glomus mosseae. Global Change Biology 5, 347–358.
Staddon PL, Fitter AH, Robinson D.1999b. Effect of mycorrhizal colonization and elevated atmospheric CO2 on carbon fixation and below-ground partitioning in Plantago lanceolata. Journal of Experimental Botany 50, 853–860.
Stitt M.1991. Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant, Cell and Environment 14, 741–762.
Tennant D.1975. A test of a modified line intersect method of estimating root length. Journal of Ecology 63, 995–1001.
Vogel CS, Curtis PS.1995. Leaf gas exchange and nitrogen dynamics of N2-fixing, field-grown Alnus glutinosa under elevated atmospheric CO2. Global Change Biology 1, 55–61.
Wardlaw IF.1990. The control of carbon partitioning in plants. New Phytologist 116, 341–381.[Web of Science]
Watson RT, Rodhe H, Oeschger H, Siegenthaler U.1990. Greenhouse gases and aerosols. In: Houghton JT, Jenkins GJ, Ephraums JJ, eds. Climate change: the IPCC scientific assessment. Cambridge: Cambridge University Press, 1–40.
Zanetti S, Hartwig UA.1997. Symbiotic N2 fixation increases under elevated atmospheric pCO2 in the field. Acta Oecologica 18, 285–290.
Zanetti S, Hartwig UA, Lüscher A, Hebeisen T, Frehner M, Fischer BU, Hendrey GR, Blum H, Nösberger J.1996. Stimulation of symbiotic N2 fixation in Trifolium repens L. under elevated atmospheric pCO2 in a grassland ecosystem. Plant Physiology 112, 575–583.[Abstract]
Ziska LH.1998. The influence of root zone temperature on photosynthetic acclimation to elevated carbon dioxide concentrations. Annals of Botany 81, 717–721.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  U.A. Hartwig, P. Wittmann, R. Braun, B. Hartwig-Raz, J. Jansa, A. Mozafar, A. Luscher, A. Leuchtmann, E. Frossard, and J. Nosberger Arbuscular mycorrhiza infection enhances the growth response of Lolium perenne to elevated atmospheric pCO2 J. Exp. Bot., May 1, 2002; 53(371): 1207 - 1213. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||