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不同氨基酸浓度下,土壤和植物的竞争吸收氨基酸


Soil Biology & Biochemistry 37 (2005) 179–181 www.elsevier.com/locate/soilbio

Short communication

Plant capture of free amino acids is maximized under high soil amin

o acid concentrations
David L. Jonesa,*, David Shannonb, Thippaya Junvee-Fortunea, John F. Farrarc
b a School of Agricultural and Forest Sciences, University of Wales, Bangor, Gwynedd LL57 2UW, Wales, UK School of Biological Sciences, Discipline of Plant and Soil Science, University of Aberdeen, AB24 3UU, Scotland, UK c School of Biological Sciences, University of Wales, Bangor, Gwynedd LL57 2UW, Wales, UK

Received 23 January 2004; received in revised form 28 May 2004; accepted 21 July 2004

Abstract Free amino acids (AA’s) represent a signi?cant source of available N for some plants and soil microorganisms. It can be expected, however, that signi?cant competition will exist between plants and microorganisms for this organic N resource. Our study indicated that microbial capture and utilization of glycine was very rapid at a range of soil solution concentrations (0.1 mM to 10 mM) indicating that signi?cant competition will exist between roots and soil microorganisms. Plant capture of free AA’s was maximal at high soil solution concentrations where microbial utilization was slowest. Our results suggest that plant capture of soil dissolved organic N may primarily occur in organic rich patches in soil where concentrations of free AA’s are high. q 2004 Elsevier Ltd. All rights reserved.
Keywords: Amino acids; Dissolved organic nitrogen; Glycine; Mineralization; Nitrogen uptake; Rhizosphere; Soil solution

Dissolved organic nitrogen (DON) has been shown to represent a signi?cant pool of soluble N in both soils and freshwaters (Siemens and Kaupenjohann, 2002; Yu, 2002). In particular, the direct root uptake of free amino acids (AA’s) from soil may be a mechanism of capturing N released from SOM, effectively short circuiting the reliance ¨ of the microbial community to create inorganic N (Nasholm et al., 2000). Competition experiments have suggested that at low added concentrations, however, microorganisms effectively outcompete roots for AA’s in soil (Owen and Jones, 2001; Bardgett et al., 2003). However, it is well documented that N is heterogeneously distributed in soil (Hodge, 2001). Whilst the concentration of individual free AA’s in the bulk soil solution is in the region of 0.01–10 mM, the concentration of AA’s in plant and animal cells is in the region of 1–10 mM (Jones and Darrah, 1994). Therefore, upon cell death it can be expected that very
* Corresponding author. Tel.: C44-1248-382579; fax: C44-1248354997. E-mail address: d.jones@bangor.ac.uk (D.L. Jones). 0038-0717/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2004.07.021

high concentrations of organic N will exist at least transiently in soil. Our aim was therefore to determine whether the competitive ability of plant roots to capture free AA’s from soil was regulated by external concentration. Soil (Eutric Cambisol) was collected from the Ah horizon (0–15 cm) of a fertilised freely draining grassland (Lolium perenne L. and Trifolium repens L.) which is grazed by sheep and located in Abergwyngregyn, Gwynedd, North Wales (53814 0 N, 4801 0 W). The soil had a pH of 5.7G0.1, total C content of 35G2 g kgK1, total N content of 2.6G0.2 g kg-1 and basal soil respiration of 252G6 mmol CO2 kgK1 h-1 at 18 8C. Further details of the site and soil characteristics are described in Jones et al. (2004). Within 12 h of soil collection, the soil solution was obtained by the centrifugal drainage technique of Giesler ¨ and Lundstrom (1993). Individual free AA’s were determined by reverse-phase Varian Analytical ProStar HPLC by the method of Jones (1986). Total dissolved N (TDN) in soil solution was determined with a Shimadzu TOCV-TNM1 analyzer (Shimadzu Corp., Kyoto, Japan). NHC, NO- and 4 3 DON were determined colorimetrically as described in

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D.L. Jones et al. / Soil Biology & Biochemistry 37 (2005) 179–181

Table 1 Mean concentrations (mM) of free amino acids in soil solutions collected from a Eutric Cambisol from February to July 2002 Month of year February Glutamic acid Asparagine Serine Histadine Glycine Threonine Arginine Alanine Tyrosine Methionine Valine Phenylalanine Isoleucine Leucine Lysine Total 7.31G3.34 1.30G1.04 3.81G1.49 0.75G0.30 3.14G0.83 3.17G1.31 0.88G1.03 5.39G2.11 1.27G0.56 0.16G0.01 2.84G1.16 1.66G0.77 2.09G1.10 3.41G1.61 0.36G0.17 37.5G16.0 March 6.31G1.34 1.03G0.41 4.00G0.38 0.77G0.18 2.98G0.76 2.78G0.53 0.68G0.24 5.34G0.79 1.11G0.24 0.03G0.00 2.26G0.36 1.40G0.31 1.92G0.39 2.96G0.48 0.69G0.07 34.2G5.8 April 4.29G1.10 0.46G0.12 2.69G0.57 0.47G0.08 1.74G0.24 1.82G0.43 0.27G0.14 3.56G0.88 0.73G0.17 0.22G0.03 2.84G1.16 1.13G0.37 1.55G0.47 2.24G0.76 0.11G0 05 23.5G5.8 May 6.02G0.60 0.70G0.19 3.85G0.68 0.58G0.12 2.88G0.60 2.46G0.42 0.43G0.16 4.28G0.48 0.83G0.17 0.40G0.07 2.37G0.29 1.10G0.20 1.36G0.22 1.98G0.35 0.27G0.09 29.5G4.4 June 8.87G4.10 1.24G0.74 3.93G1.48 0.66G0.23 3.01G1.14 3.38G1.39 0.84G0.42 7.50G3.09 1.09G0.47 0.44G0.13 4.47G1.91 1.59G0.61 2.68G1.14 4.30G1.85 0.48G0.24 44.5G18.4 July 9.13G4.66 1.71G1.01 4.99G3.34 1.19G0.68 4.11G2.97 4.63G3.34 0.88G0.86 9.78G7.34 1.25G0.97 0.28G0.12 6.51G5.04 2.25G1.83 4.04G3.28 7.17G6.25 0.13G0.00 58.1G41.5

Values represent meansGSEM (nZ3). The limit of detection of the HPLC technique was 130G10 nM (meanGSEM; nZ15).

Jones et al. (2004). Soil solutions were obtained monthly from March to July with three independent replicates taken randomly each month from an area 6!2 m in size. Seeds of maize (Zea mays L. cv ‘Merit’) were soaked for 24 h in deionised water and allowed to germinate on moistened ?lter paper for 48 h at 20 8C. After 3 d, each plant had one main root axis 1.5 cm in length. The plant–soil microcosms were constructed from nylon tube as described in Owen and Jones (2001). Brie?y, the microcosms were composed of a 21 cm long, 0.8 cm dia. main ‘rhizotube’ section expanding over a 0.5 cm span to a 4 cm long, 1.8 cm dia. section which was used to hold the seed. The microcosms were ?lled with soil to a bulk density of 1.16 g cmK3. After seedling addition, the microcosms were placed in a growth room with day/night rhythm of 18/22 8C, 16 h photoperiod and light intensity of 300 mmol m-2s-1. When the main root axis was approximately 20 cm long (7 d after transplantation; shoots 8 cm long), 500 ml of a uniformly 14C-labelled glycine solution (37 kBq mlK1; 3–9 GBq mmol-1; ICN Pharmaceuticals Inc., Irvine, CA) was injected through a hole into the soil, approximately 10 cm behind the root tip and within the root hair zone. Root hairs ?lled the microcosm. After 24 h, the shoots were removed and oven-dried (80 8C, 24 h). The 14C content of the shoots was determined using a OX400 Biological Oxidiser (Harvey Instruments Corp., Hillsdale, NJ) and liquid scintillation counting (Wallac 1409; EGandG Ltd, Milton Keynes, UK). Glycine was added to soil at concentrations of 0.1, 1.0, 10, 1000 and 10000 mM with ?ve replicates for each treatment. To determine the rate of AA turnover in soil, a uniformly labelled 14C-labelled glycine solution (0.36 kBq mlK1; 0.1, 1.0, 10, 1000 and 10000 mM) was added to soil (0.1 ml g-1) collected from 7 d old microcosms and from which roots had been removed. The subsequent removal of glycine from

the soil together with their evolution of 14CO2 was measured in triplicate over a 48 h period as described in Jones et al. (2004). Statistical analyses (t-tests, linear regression, two way ANOVA) were performed using Sigmaplot 8.0 (SPSS Inc., Chicago, ILL) and Minitab 13 (Minitab Inc., State College, PA). The total concentration of free AA’s was similar at all sampling dates ranging from 20 to 60 mM with the mean concentration over a 6 month period being 38G5 mM (Table 1). In contrast, the relative proportion of individual AA’s within the total free AA pool remained similar for each sampling date. No one AA dominated the free AA pool. For comparison, the mean (GSEM) concentration of other soil solution N pools over the same period was 478G 36 mM for DON, 1085G628 mM for NO- , and 50G7 mM 3 for NHC. 4

Fig. 1. Concentration-dependent uptake of 14C-glycine from the rhizosphere by maize plants (solid bars) and the half-life of glycine in the soil (symbols and line). Values for plant uptake represent meansGSEM (nZ5) and values for soil half-lives represent meansGSEM (nZ3).

D.L. Jones et al. / Soil Biology & Biochemistry 37 (2005) 179–181

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becomes saturated at high exogenous concentrations (O1 mM; Vinolas et al., 2001; Jones and Hodge, 2001). We hypothesize therefore that typically the uptake of AA’s by roots will contribute little to the overall N supply of a plant particularly when the soil possesses either high rates of mineralisation or large inputs of anthropogenic N. However, in ecosystems where nutrient reserves are low and highly spatially heterogeneous, plants may compete better with soil microorganisms at least in resource rich patches where roots are known to proliferate (Hodge, 2001).

Acknowledgements
Fig. 2. Time-dependent mineralization of Values represent meansGSEM (nZ3).
14

C-labelled glycine in soil.

This work was funded by the UK Natural Environment Research Council.

Generally, the amount of 14C-glycine recovered in the shoots was similar at low soil solution concentrations (0.1–10 mM; PO0.05; Fig. 1). In contrast, 14C-glycine uptake in the plant was signi?cantly greater at concentrations exceeding 1 mM (P!0.05). Based upon the partitioning of glycine-C within the plant presented in Owen and Jones (2001) we estimate that the total glycine uptake by the plant ranged from 1 to 15% indicating that most glycine was captured by the soil microbial community. The mineralisation of AA’s to 14CO2 was rapid at each of the added glycine concentrations although the rate of mineralisation decreased with increasing concentration (Fig. 2). After 24 h, the rate of 14CO2 production was very low and almost no 14C-remained in solution at this time (!0.5% of the total added). After 48 h, approximately 25% of the added glycine was recovered as 14CO2 with the remaining 75% assumed to be present in the microbial biomass (Jones and Hodge, 2001). The depletion of glycine in the soil was inversely correlated with the appearance of 14 CO2 in accordance with the results of Jones (1999) and Jones et al. (2004). The half-lives of glycine in soil ranged from 0.75 to 3.5 h depending upon glycine concentration and were linearly correlated with the amount of glycine acid uptake by the plants (r2Z0.989; Fig. 1). Our results suggest that free AA’s are present in low concentrations in bulk soil solution in comparison to inorganic NO- and NHC. Based upon the results presented 3 4 here and elsewhere the low observed concentration of free AA’s is probably due to their rapid mineralisation by the soil microbial community rather than their low rate of production (Jones et al., 2004). Our results show that at low soil AA concentrations plants are poor competitors for free AA’s in comparison to the soil microbial community. However, the results presented here also suggests that at high soil solution concentrations plants become more competitive for free AA’s in soil. Our ?ndings support the hypothesis that the capacity of the soil microbial community to take up AA’s

References
Bardgett, R.D., Streeter, T.C., Bol, R., 2003. Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84, 1277–1287. ¨ Giesler, R., Lundstrom, U.S., 1993. Soil solution chemistry—the effects of bulking soil samples and spatial variation. Soil Science Society of America Journal 57, 1283–1288. Hodge, A., 2001. Arbuscular mycorrhizal fungi in?uence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytologist 151, 725–734. Jones, B.N., 1986. Amino acid analysis by o-phthaldialdehyde pre-column derivitization and reverse-phase HPLC, in: Shively, J.E. (Ed.), In Methods of Protein Microcharacterization: A Practical Handbook. Humana Press, Totowa, NJ, pp. 121–151. Jones, D.L., 1999. Amino acid biodegradation and its potential effects on organic nitrogen capture by plants. Soil Biology & Biochemistry 31, 613–622. Jones, D.L., Darrah, P.R., 1994. Amino acid in?ux at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant and Soil 163, 1–12. Jones, D.L., Hodge, A., 1999. Biodegradation kinetics and sorption reactions of three differently charged amino acids in soil and their effects on plant organic nitrogen availability. Soil Biology & Biochemistry 31, 1331–1342. Jones, D.L., Shannon, D., Murphy, D., Farrar, J.F., 2004. Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biology & Biochemistry 36, 749–756. ¨ Nasholm, T., Huss-Danell, K., Hogberg, P., 2000. Uptake of organic nitrogen in the ?eld by four agriculturally important plant species. Ecology 81, 1155–1161. Owen, A.G., Jones, D.L., 2001. Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biology & Biochemistry 33, 651–657. Siemens, J., Kaupenjohann, M., 2002. Contribution of dissolved organic nitrogen to N leaching from four German agricultural soils. Journal of Plant Nutrition and Soil Science 165, 675–681. Vinolas, L.C., Healey, J.R., Jones, D.L., 2001. Kinetics of soil microbial uptake of free amino acids. Biology and Fertility of Soils 33, 67–74. Yu, Z., Zhang, Q., Kraus, T.E.C., Dahlgren, R.A., Anastasio, C., Zasoski, R.J., 2002. Contribution of amino compounds to dissolved organic nitrogen in forest soils. Biogeochemistry 61, 173–198.


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