Temperature-Respiration Relationships Differ in Mycorrhizal and Non-Mycorrhizal Root Systems of Picea abies (L.) Karst.
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1 Short Research Paper 545 Temperature-Respiration Relationships Differ in Mycorrhizal and Non-Mycorrhizal Root Systems of Picea abies (L.) Karst. N. Koch 1, C. P. Andersen 2, S. Raidl 3, R. Agerer 3, R. Matyssek 1, and T. E. E. Grams 1 1 Department of Ecology, Ecophysiology of Plants, Technische Universität München, Am Hochanger 13, Freising, Germany 2 US Environmental Protection Agency, Western Ecology Division, National Health and Environmental Effects Research Laboratory, Office of Research and Development, 200 SW 35th Street, Corvallis, Oregon 97333, USA 3 Department Biology I and GeoBio-Center LMU, Biodiverstity Research, Systematic Mycology, Ludwig-Maximilians-Universität München, Menzinger Straße 67, München, Germany Received: September 12, 2006; Accepted: October 30, 2006 Abstract: Root respiration has been shown to increase with temperature, but less is known about how this relationship is affected by the fungal partner in mycorrhizal root systems. In order to test respiratory temperature dependence, in particular Q 10 of mycorrhizal and non-mycorrhizal root systems, seedlings of Picea abies (L.) Karst. (Norway spruce) were inoculated with the ectomycorrhizal fungus Piloderma croceum (Eriksson and Hjortstam, SR430; synonym: Piloderma fallax: [Libert] Stalpers) and planted in soil respiration cuvettes (mycocosms). Temperature dependence of hyphal respiration in sterile cultures was determined and compared with respiration of mycorrhizal roots. Respiration rates of mycorrhizal and non-mycorrhizal root systems as well as sterile cultures were sensitive to temperature. Q 10 of mycorrhizal root systems of 3.0 ± 0.1 was significantly higher than that of non-mycorrhizal systems (2.5 ± 0.2). Q 10 of P. croceum in sterile cultures (older than 2 months) was similar to that of mycorrhizal root systems, suggesting that mycorrhizae may have a large influence on the temperature sensitivity of roots in spite of their small biomass. Our results stress the importance of considering mycorrhization when modeling the temperature sensitivity of spruce roots. Key words: Picea abies (L.) Karst. (Norway spruce), Piloderma croceum, root respiration, mycorrhizal respiration, temperature dependence, Q 10. Introduction Carbon efflux from soil has been estimated to comprise as much as 75% of ecosystem respiration (Law et al., 1999; Hanson et al., 2000), which represents the largest global source of carbon and is perhaps the least understood component of climate change models (Jones et al., 2003). The relative contribution of roots and soil heterotrophs to overall soil CO 2 efflux varies among ecosystems, but root respiration often comprises as much as 40 50% of total soil CO 2 efflux (Hanson et al., 2000; Epron et al., 2001; Högberg et al., 2001). In order to estimate shifts in carbon flux to the atmosphere in response to climate Plant Biol. 9 (2007): Georg Thieme Verlag KG Stuttgart New York DOI /s Published online February 15, 2007 ISSN warming, accurate models of temperature-respiration relationships (Lloyd and Taylor, 1994; Kirschbaum, 1995, 2000) and Q 10 are needed. Predicting respiratory belowground responses is particularly difficult due to the restricted accessibility of roots and soil organisms, their high diversity, and the complex interactions that occur in the mycorrhizosphere. Nevertheless, because most plant species worldwide have obligate mycorrhizal associations, the temperature dependence of respiration of mycorrhizal roots systems is of high ecological relevance. Although root respiration is often reported to have a Q 10 between 2 and 3 (Burton et al., 2002; Lipp and Andersen, 2003; Reichenstein et al., 2005), many recent long-term studies have shown total soil respiration to have a Q 10 above 4 (Kirschbaum, 2000; Janssens and Pilegaard, 2003; Wieser, 2004). In a longerterm study, Boone et al. (1998) found that root plus mycorrhizosphere respiration is more sensitive to temperature than bulk soil respiration, with a Q 10 of 4.6. They suggested that, in particular, mycorrhizae may account for the high Q 10. Janssens and Pilegaard (2003) and Wieser (2004) found a similarly high Q 10 of total soil respiration in forests of beech and cembran pine, respectively. Apart from methodological differences, unique temperature dependencies of the individual components of soil respiration in ecosystems may be responsible for the range in sensitivity. Field approaches may have methodological shortcomings since they often make use of natural temperature gradients over time, and thus temperature sensitivity may be confounded with that of other seasonally changing factors like growth, nutrient uptake, and soil moisture (Boone et al., 1998; Yuste et al., 2004). Scant information is available regarding the temperature sensitivity of mycorrhizae and it is therefore uncertain how they will respond to elevated temperature in a changing climate (Staddon et al., 2002; Pietikainen et al., 2005; Heinemeyer et al., 2006). In an arbuscular mycorrhizal rhizocosm system using sunflower, temperature sensitivity of mycorrhizal and nonmycorrhizal plants was found to be similar (Langley et al., 2005). Heinemeyer et al. (2006) found that respiration of external arbuscular mycelium acclimates to temperature. Bååth and Wallander (2003) used a model system to analyze temperature sensitivity of ectomycorrhizal Pinus muricata seedlings, and found no difference between total soil respiration (root plus mycorrhizae plus bulk soil microbes), respiration of bulk soil minus roots, and mycelial respiration.
2 546 Plant Biology 9 (2007) N. Koch et al. We hypothesized that ectomycorrhizal and non-ectomycorrhizal roots have different Q 10, given their differences in carbon turnover (Andersen and Rygiewicz, 1995; Smith and Read, 1997). The hypothesis was tested using a model system that allowed separate and detailed control of shoot and root temperature of Picea abies (L.) Karst. seedlings (Norway spruce). This approach prevented effects of changing shoot temperature and, thus, carbon supply for root respiration (Lipp and Andersen, 2003). A short-term approach for calculations of temperature sensitivity and Q 10 was chosen to avoid confounding effects such as seasonally varying carbon allocation to roots or changes in root growth dynamics. The degree to which mycorrhizal temperature sensitivity may be influenced by the fungus is estimated by assessments of hyphal respiration in sterile culture. Materials and Methods Plant and fungal material In autumn 2001 sterilized seeds from the German provenance (Staatliche Samenklenge Laufen, Germany) of Picea abies (L.) Karst. (Norway spruce) were germinated and grown for 4 6 weeks in a substrate mixture (1 : 1) of peat (specification H 3 -H 5, ph in CaCl 2 : ; Kölle, Munich, Germany) and agriperl perlite (Dämmstoff GmbH, Darmstadt, Germany). Seedlings were then transplanted into Petri dish rhizotrons containing peat. In this system, roots were inoculated with nylon sheets carrying fungal plugs of Piloderma croceum (Eriksson and Hjortstam, SR430; synonym: Piloderma fallax: [Libert] Stalpers) (Agerer and Raidl, 2004; Herrmann et al., 2004) as described below. After the establishment of mycorrhizal associations, seedlings were transplanted into the root chamber ( cm) of modified mycocosms (Rygiewicz et al., 1988; Andersen and Rygiewicz, 1991) using peat as substrate. Non-mycorrhizal spruce seedlings (germinated in June 2002) were transplanted into mycocosms using the same procedures. Plants were grown in climate chambers under standardized conditions (15/20 8C day/night temperatures, relative humidity of 65 80%, photosynthetic photon flux density, PPFD, up to a maximum of ± 4.5 μmol m 2 s 1 ) and were kept well watered using distilled water. Sterile fungal cultures and inoculation material Sterile cultures of P. croceum were maintained from a stock culture by transferring agar plugs onto round Petri dishes (5 and 9 cm diameter; VWR International, Darmstadt, Germany) with 0.5 modified Melin-Norkrans (MMN) agar medium (Marx, 1969), supplemented with 1% (w/v) tetracycline to prevent potential bacterial infection. The cultures were kept at room temperature and regularly tested for hyphal vitality by staining small samples of selected plates with the vital staining agents acridine orange and bisbenzimide (Serva, Heidelberg, Germany). For the inoculation of the seedlings, the fungal material was transferred onto bigger, square Petri dishes ( cm; VWR International, Darmstadt, Germany) covered with a sterile nylon grid (mesh width 80 μm; Draht Center, Stuttgart, Germany) as described in Schubert et al. (2003). Assessments of respiration and biomass Mycorrhizal and non-mycorrhizal plants were used to assess the temperature dependence (4.9 8C, C, C, C). To measure respiration in the root compartment, mycocosms were sealed gas-tight with silicon grease (Siliconfett, Wacker- Chemie, Stuttgart, Germany) and terostat (Teroson Henkel, Heidelberg, Germany) and connected to a differential infrared CO 2 /H 2 O gas analyzer of a gas exchange system (CQP130, Walz, Effeltrich, Germany; Schulze et al., 1982). Empty mycocosm (root compartment) readings were taken as zero controls. Mycocosms were wrapped in plastic bags and transferred into a water bath to control the temperature of the root compartment. Temperature of aboveground plant parts remained unchanged at 25.6 ± 0.1 8C (climate chamber conditions). Mycocosms were held for at least 3 h prior to measurement at each temperature level to achieve stable root temperature. To test for hysteresis, respiration was measured in descending and ascending order for two of the four temperatures (108C and 15 8C). No significant differences in respiration rate were found between readings at the same temperature but at different times (p = , no hysteresis was found). In order to measure microbial respiration in soil without roots, respiration of soil from non-mycorrhizal plants was measured repeatedly at 21.4 ± 0.08C one to five days after harvesting the plant material. The amount of microbial respiration per unit soil mass was negligible (0.11 ± 0.00 to 0.12 ± 0.00 nmol CO 2 g 1 s 1 measured one to five days after removal of the plant material, respectively). Respiration of sterile cultures of P. croceum was assessed using a minicuvette gas exchange system (Walz, Effeltrich, Germany) equipped with a differential infrared CO 2 /H 2 O gas analyzer. Petri dishes of cultures were placed inside the thermoelectrically controlled cuvette, where relative humidity was maintained at 90 95%. Temperature dependence of fungal respiration was measured at three different temperatures (5.0 8C, C, C). Prior to measurement, cultures had been exposed to each temperature for at least 4 h. Studied cultures were 40, 65, and 92 days old. Since 65- and 92-day-old cultures did not differ significantly in respiration (p = 0.102), data were pooled and are denoted, in the following, as older than 65 days. At harvest, the surrounding peat substrate, including the ectomycorrhizal mycelium, was separated from the plant roots by carefully stripping off the emanating mycelium from the mycorrhizal mantle using fine forceps and a binocular microscope. Then, the total plant was removed from the rhizotron and separated into needles, stem, coarse roots (> 1 mm), fine roots ( 1 mm), and mycorrhizal root tips (the latter being recognizable as the characteristically yellow mantle of P. croceum; Brand, 1991). Dry mass of separated plant fractions was assessed after drying for 3 days (60 8C) to constant weight. Substrate dry mass was assessed in aliquots. Mycelial biomass in the substrate fraction was measured with the anatomical agar film technique according to Bååth and Söderström (1979) and Kunzweiler and Kottke (1986), with the modifications mentioned by Schubert et al. (2003). Mycelial length of P. croceum was converted into mycelial dry mass according to Schubert et al. (2003). The mycelial biomass in the sterile cultures was determined in the same way.
3 Temperature-Respiration Relationships Plant Biology 9 (2007) 547 Calculation of Q 10 In a first step, respiration values at exactly 10.08C and C were calculated from the following exponential regression: y=β 0 e β1t, where y is the respiration rate, β 0 and β 1 are fitted constants and T represents soil temperature (Buchmann, 2000; Boone et al., 1998). Q 10 was then calculated in a second step as the quotient of respiration rate at T + 108C and respiration rate at T (Atkin et al., 2000). Statistical analyses Statistical analyses were conducted with SPSS 12.0 (SPSS Inc., Chicago, USA). Significant differences in biomass partitioning of mycorrhizal and non-mycorrhizal seedlings, fungal hyphae biomass in cultures, photosynthesis, and Q 10 were tested by t-tests. Table 1 Biomass partitioning of non-mycorrhizal and mycorrhizal spruce seedlings. Data are means ± SE, n = 4. No significant difference for any biomass fraction was found (see p values) Non-mycorrhizal seedling Mycorrhizal seedling p value Total biomass (mg) ± ± Needle (mg) ± ± Stem (mg) 87.7 ± ± Coarse root (mg) 47.1 ± ± Fine root (mg) ± ± Mycorrhizal root 19.3 ± 4.0 tips (mg) Extraradical mycelium (mg) 1.0 ± 0.2 Results Biomass partitioning and fungal hyphae biomass in sterile cultures Total biomass of non-mycorrhizal and mycorrhizal spruce seedlings was not significantly different at the end of the experiment (p = 0.658; Table 1). Likewise, the biomass partitioning among stems, needles, coarse, and fine roots was not significantly affected by mycorrhization. Non-mycorrhizal seedlings tended to have more woody material than mycorrhizal seedlings (p = for stems and p = for coarse roots), whereas the latter seedlings had higher fine root biomass (p = 0.104; Table 1). Biomass of mycorrhizal root tips (19.3 ± 4.0 mg) was about 10% of that of fine roots (210.5 ± 24.2 mg) and extraradical mycelium had a biomass of 1.0 ± 0.2 mg. Biomass of 40-day-old and more than 65-day-old fungal hyphae grown in sterile cultures was not significantly different (p = 0.389). Hyphal biomass of the young cultures (40 days old) was 38.6 ± 1.3 mg and of the cultures older than 65 days, 41.7 ± 2.2 mg per Petri dish. Respiration rates and Q 10 Respiration rates of both non-mycorrhizal and mycorrhizal root systems were found to be temperature sensitive: Respiration rates were in the range of 2.5 to 12.3 nmol CO 2 g 1 s 1 at 5 to 208C, respectively. Q 10 was significantly increased (p = 0.038) in mycorrhizal compared with non-mycorrhizal root systems (3.0 ± 0.1 and 2.5 ± 0.2, respectively; Fig.1a). Respiration rates of young fungal cultures (40 days old) increased with temperature from 4.2 to 22.1 nmol CO 2 g 1 s 1 (mean values at 5 to 25 8C, respectively), whereas rates of fungal hyphae in older cultures ranged from 1.8 to 8.1 nmol CO 2 g 1 s 1 at 5 to 25 8C, respectively. Q 10 of hyphal respiration in the culture experiment was 1.9 ± 0.1 in the 40-day-old and 2.9 ± 0.5 in older cultures, respectively, although the difference was not significant (p = 0.135; Fig. 1b). Fig.1 Q 10 of root (a) and hyphal (b) respiration. Data are means ± SE (n = 4 10). The significant effect by mycorrhization (p < 0.05) is indicated by ( ). Discussion and Conclusion Uncertainties in modelling temperature dependence of rootassociated respiration (Jones et al., 2003), especially that of mycorrhizae, led us to study this relationship in non-mycorrhizal and mycorrhizal roots, as well as hyphal respiration in sterile cultures. The hypothesis was supported in that non-mycorrhizal and mycorrhizal roots differ in their Q 10, perhaps due to differences in carbon turnover. Our values for respiration of spruce mycorrhizae were similar to those reported by Rygiewicz and Andersen (1994) for Pinus ponderosa seedlings which were colonized with the ectomycorrhizal fungus Hebeloma crustuliniforme. In the present study, relationships between temperature and respiration existed both in non-mycorrhizal and mycorrhizal root systems of Norway spruce as well as in fungal cultures of P. croceum. Q 10 differed significantly between non-mycorrhizal (2.5 ± 0.2) and mycorrhizal roots (3.0 ± 0.1; Fig.1a). This was in the range described by Burton et al. (2002), with a Q 10 of ectomycorrhizal species of about 2.7. In contrast, Boone et al. (1998) reported a Q 10 of 4.6 for mycorrhizal roots, but root and mycorrhizal respiration were not separated from decomposition of detritus
4 548 Plant Biology 9 (2007) N. Koch et al. and root excudates. Field estimates of Q 10, such as those reported in the longer-term study by Boone et al. (1998), are not directly comparable to Q 10 as derived from controlled laboratory conditions because of seasonal variation in respiratory temperature functions and different carbon allocation over the time. In the short-term approach applied in this study, such confounding influences were not present. In addition, root growth changes seasonally in the field (and so does growth respiration) along with mycorrhizal development so that temperature effects on root metabolism can be biased. Our results differ from those reported for ectomycorrhizal seedlings of Pinus muricata in a similar system but using a different technique (Bååth and Wallander, 2003). Bååth and Wallander (2003) found no differences in Q 10 of mycorrhizal root, hyphal and soil compartments when measured separately. They found aq 10 ranging from 2.2 to 2.4, slightly lower than our results with spruce. One reason for the differing results besides interspecies variation might be that Bååth and Wallander (2003) lowered the shoot temperature along with root temperature, while we lowered root temperature while maintaining a constant shoot temperature. It is possible that lowering shoot and root temperature together may have affected carbon gain of photosynthesis, and thus carbon allocation to roots, during measurements (cf. Lipp and Andersen, 2003). In conclusion, our results confirm the hypothesis that mycorrhizal and non-mycorrhizal roots of spruce have different temperature sensitivities, and stress the importance of characterizing Q 10 of mycorrhizal roots for understanding and modelling soil carbon dynamics. Thus, mycorrhizal root systems will respond more strongly than non-mycorrhizal root systems to global warming and therefore incorporation of the higher Q 10 for mycorrhizal roots will increase the responsiveness of soil respiration rates to projected soil temperature increases. The fact that mycorrhizal roots demonstrated respiratory temperature responses similar to those of fungal cultures of comparable age suggests that the fungus may exert a rather large influence on root metabolism even though it comprises only a small fraction of total mycorrhizal-root biomass. Based on our results, the respiratory temperature dependence of sterile cultures appears to be an appropriate estimator of the relationship in mycorrhizal roots of spruce. Acknowledgements The authors express their thanks to Andreas Egl, Markus Hoffmann, and Petra Kowalick for their assistance in the laboratory. Dr. Jana Barbro Winkler (GSF National Research Center for Environment and Health) is acknowledged for providing the minicuvette system. We thank Dr. Peter Högberg for providing valuable comments to a previous version of the manuscript. The investigation was funded through SFB 607 Growth and Parasite Defence Competition for Resources in Economic Plants from Agronomy and Forestry, Projects B5 and B7 of the Deutsche Forschungsgemeinschaft (DFG). Dr. Nina Koch was funded in part through SFB 607 and the HWP: Programm Chancengleichheit für Frauen in Forschung und Lehre (Technische Universität München). The information in this document has been subjected to the U.S. Environmental Protection Agency s peer and administrative review. Mention of trade names or commercial products does not constitute endorsement or recommendation for use. References Agerer, R. and Raidl, S. 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