植物吸收土壤有机氮的研究进展

doi:10.11849/zrzyxb.2011.04.017

摘要/Abstract

摘要： 传统的氮循环模式认为,土壤有机氮只有经过微生物分解转化为无机氮(NH₄⁺+NO₃^-)后才能为植物吸收利用。然而,近年来许多研究证实多种陆地植物具有从土壤中获取小分子有机物质(如自由态氨基酸)的能力,对传统的氮循环模式形成巨大的挑战。论文从土壤中氮素的形态、植物吸收有机氮的证据、有机氮吸收的机制、以有机氮为重要氮源的生态系统类型以及根系吸收与分泌有机氮之间的平衡等5个方面进行了综述,分析了当前研究方法的优缺点,针对本领域内核心科学问题,提出了未来植物吸收有机氮的改进方法及研究方向,为进行植物利用有机氮的研究提供方法基础。

关键词: 土壤有机氮, 无机氮, 氨基酸, 氨基酸转运载体, 同位素技术, 氮循环

Abstract: Traditional concept of nitrogen cycling in terrestrial ecosystems has assumed that organic nitrogen can be used by terrestrial plants only after it is decomposed by soil microorganisms into inorganic nitrogen (NH₄⁺+NO₃^-). Recent studies have confirmed that a variety of plant species have the capacity to take up soil organic nitrogen in the form of low molecular weight substances, e.g. free amino acids, challenging the core of the traditional concept of nitrogen cycling. We here reviewed major advances made in the studies of organic nitrogen uptake by plants from five aspects: nitrogen forms in soil, evidence of organic nitrogen uptake by plants, mechanisms responsible for organic nitrogen uptake by plants, main plants and ecosystems with importance of organic nitrogen uptake and the balance between exudates and uptake of organic nitrogen by roots. We also assessed advantages and limits of research approaches. According to the central question within this research field, we suggested several directions we should focus on in future studies. We call for new research for a better understanding of organic nitrogen uptake by plants.

Key words: organic nitrogen, inorganic nitrogen, amino acid, transporter of amino acid, stable isotope technique, nitrogen cycle

中图分类号:

S154.4

徐兴良, 白洁冰, 欧阳华. 植物吸收土壤有机氮的研究进展[J]. 自然资源学报, 2011, 26(4): 715-724.

XU Xing-liang, BAI Jie-bing, OUYANG Hua. Advances in Studies on Organic Nitrogen Uptake by Terrestrial Plants[J]. JOURNAL OF NATURAL RESOURCES, 2011, 26(4): 715-724.

参考文献

[1] Schimel J P, Bennett J. Nitrogen mineralization: Challenges of a changing paradigm[J]. Ecology, 2004, 85(3): 591-602. [2] 吴良欢, 陶勤南. 植物有机营养研究进展[M]//冯锋, 张福锁, 杨新泉. 植物营养研究——进展与展望. 北京: 中国农业大学出版社, 2000: 58-71. [3] Nsholm T, Persson J. Plant acquisition of organic N in boreal forests[J]. Physiology Plantarum, 2001, 111: 419-426. [4] 莫良玉, 吴良欢, 陶勤南. 高等植物对有机氮吸收与利用研究进展[J]. 生态学报, 2002, 22(1): 118-124. [5] Jones D L, Healey J R, Willett V B, et al. Dissolved organic nitrogen uptake by plants—An important N uptake pathway? [J] Soil Biology and Biochemistry, 2005, 37: 413-423. [6] Nasholm T, Kielland K, Ganeteg U. Uptake of organic nitrogen by plants[J]. New Phytologist, 2009, 182: 31-48. [7] 王文颖, 刘俊英. 植物吸收利用有机氮营养研究进展[J]. 应用生态学报, 2009, 20(5): 1223-1228. [8] Bronson K F. Forms of inorganic nitrogen in soil[M]//Schepers J S, Raun W R. Nitrogen in Agricultural Systems. 3rd Edition. Agronomy Monograph, 2008, 49: 31-56. [9] Schulten H-R, Schnitzer M. The chemistry of soil organic nitrogen: A review[J]. Biology and Fertility of Soils, 1998, 26: 1-15. [10] Chen C R, Xu Z H. Analysis and behavior of soluble organic nitrogen in forest soils[J]. Journal of Soils and Sediments, 2008, 8: 363-378. [11] Olk D C. Forms of inorganic nitrogen in soil[M]//Schepers J S, Raun W R. Nitrogen in Agricultural Systems. 3rd Edition. Agronomy Monograph, 2008, 49: 57-100. [12] Bremner J M. Organic nitrogen in soils[M]//Batholomew W V, Clark F E. Soil Nitrogen. American Society of Agronomy, Madison, Wis., 1965: 93-149. [13] Stevenson F J. Nitrogen in Agricultural Soils[M]. ASA, CSSA, SSSA, Madison, Wis., 1982. [14] Warman P R, Isnor R A. Amino acid composition of peptides present in organic matter fractions of sandy loam soil[J]. Soil Science, 1991, 152: 7-13. [15] Senwo Z N, Tabatabai M A. Amino acid composition of soil organic matter[J]. Biology and Fertility of Soils, 1998, 26: 1-15. [16] Friedel J K, Scheller E. Composition of hydrolysable amino acids in soil organic matter and soil microbial biomass[J]. Soil Biology and Biochemistry, 2002, 34: 315-325. [17] Martens D A, Loeffelmann K L. Soil amino acid composition quantified by acid hydrolysis and anion chromatography-pulsed amperometry[J]. Journal of Agricultural and Food Chemistry, 2003, 51: 6521-6529. [18] Fischer H, Meyer A, Fischer K, et al. Carbohydrate and amino acid composition of dissolved organic matter leached from soil[J]. Soil Biology and Biochemistry, 2007, 39: 2926-2935. [19] Werdin-Pfisterer, Kielland K, Boone R D. Soil amino acid composition across a boreal forest successional sequence[J]. Soil Biology and Biochemistry, 2009, 41: 1210-1220. [20] Galloway J N, Schlesinger W, Levy II H, et al. Nitrogen fixation: Anthropogenic enhancement-environmental response[J]. Global Biogeochemical Cycles, 1995, 9: 235-252. [21] Talbot J M, Treseder K K. Controls over mycorrhizal uptake of organic nitrogen[J]. Pedobiologia, 2010, 53: 169-179. [22] Hutchinson H B, Miller N H J. The direct assimilation of inorganic and organic forms of nitrogen by higher plants[J]. Centbl Bakt II, 1911, 30: 513-547. [23] Brigham R O. Assimilation of organic nitrogen by Zea mays and the influence of Bacillus subtilis on such assimilation[J]. Soil Science, 1917, 3: 155-195. [24] Wright D E. Amino acid uptake by plant roots[J]. Archives of Biochemistry and Biophysics, 1962, 97: 174-180. [25] Bright S W J, Kueh J S H, Rognes S E. Lysine transport in two barley mutants with altered uptake of basic amino acids in the root[J]. Plant Physiology, 1983, 72: 821-824. [26] Schobert C, Komor E. Amino acids uptake by Ricinus communis roots: Characterization and physiological significance[J]. Plant, Cell and Environment, 1987, 10: 494-500. [27] Jones D L, Darrah P R. Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere[J]. Plant and Soil, 1994, 163: 1-12. [28] Kielland K. Amino acids absorption by arctic plants: Implications for plant nutrition and nitrogen cycling[J]. Ecology, 1994, 75: 2373-2383. [29] Raab T K, Lipson D A, Monson R M. Non-mycorrhizal uptake of amino acids by roots of the alpine Kobresia myosuroides: Implications for the alpine N cycle[J]. Oecologia, 1996, 108: 488-494. [30] Heremans B, Borstlap AC, Jacobs M. The rlt11 and raec1 mutants of Arabidopsis haliana lack the activity of a basic-amino-acid transporter[J]. Planta, 1997, 201: 219-226. [31] Raab T K, Lipson D A, Monson R M. Soil amino acid utilization among species of the Cyperaceae: Plant and soil processes[J]. Ecology, 1999, 80: 2408-2419. [32] Falkengren-Grerup U, Mnsson K F, Olsson M O. Uptake capacity of amino acids by ten grasses and forbs in relation to soil acidity and N availability[J]. Environmental and Experimental Botany, 2000, 44: 207-219. [33] Persson J, Nsholm T. Amino acid uptake: A widespread ability among boreal forest plants[J]. Ecology Letters, 2001, 4: 434-438. [34] Persson J, Gardestrm P, Nsholm T. Uptake, metabolism and distribution of organic and inorganic nitrogen sources by Pinus sylvestris[J]. Journal of Experimental Botany, 2006, 57: 2651-2659. [35] Forsum O, Svennerstam H, Ganeteg U, et al. Capacities and constraints of amino acid utilization in Arabidopsis[J]. New Phytologist, 2008, 179(4): 1058-1069. [36] Jmtgrd S, Nsholm T, Huss-Danell K. Characteristics of amino acid uptake in barley[J]. Plant and Soil, 2008, 302: 221-231. [37] Kahmen A, Livesley S J, Arndt S K. High potential, but low actual, glycine uptake of dominant plant species in three Australian land-use types with intermediate N availability[J]. Plant and Soil, 2009, 325: 109-121. [38] Lipson D, Nsholm T. The unexpected versatility of plants: Organic nitrogen use and availability in terrestrial ecosystems[J]. Oecologia, 2001, 128: 305-316. [39] Xu X L, Kuzyakov Y, Stange F, et al. Light affected the competition for inorganic and organic nitrogen between maize and soil microorganisms[J]. Plant and Soil, 2008, 304: 59-72. [40] Nsholm T, Huss-Danell K, Hgberg P. Uptake of glycine by field grown wheat[J]. New Phytologist, 2001, 150: 59-63. [41] Yamagata M, Ae N. Direct acquisition of organic N by crops[J]. JARQ, 1999, 33: 13-21. [42] Nsholm T, Huss-Danell K, Hgberg P. Uptake of organic nitrogen in the field by four agriculturally important plant species[J]. Ecology, 2000, 81: 1155-1161. [43] Thornton B. Uptake of glycine by non-mycorrhizal Lolium perenne[J]. Journal of Experimental Botany, 2001, 52: 1-8. [44] Stribley D P, Read D J. The biology of mycorrhiza in the Ericacea. VII. The relationship between mycorrhizal infection and the capacity to utilize simple and complex organic N sources[J]. New Phytologist, 1980, 86: 365-371. [45] Alexander I J. The significance of ectomycorrhizas in the nitrogen cycle[M]//Lee J A, McNeoll S, Rorison L H. Nitrogen as Ecological Factor. Oxford: Blackwell Scientific Publications, 1983: 69-94. [46] Read D J, Bajwa R. Some nutritional aspects of biology of ericaceous mycorrhizas[J]. Proceedings of Royal Society of Edinburg, 1985, 85B: 317-332. [47] Read D J. Mycorrhizas in ecosystems[J]. Experientia, 1991, 47: 376-391. [48] Turnbull M H, Goodall R, Stewart D R. The impact of mycorrhizal colonization upon nitrogen source utilization and metabolism in seedlings of Eucalyptus grandis Hill ex Maiden and Eucalptus maculata Hook[J]. Plant, Cell and Environment, 1995, 18: 1386-1394. [49] Lipson D A, Raab T K, Schmidt S K, et al. Variation in competitive abilities of plants and microbes for specific amino acids[J]. Oecologia, 1999, 29: 257-261. [50] Hawkins H-J, Johansen A, George E. Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi[J]. Plant and Soil, 2000, 226: 275-285. [51] Melin E, Nisson H. Transfer of labeled nitrogen from glutamin acid to pine seedlings through the mycelium of Boletus variegatus (Sw.)[J]. Nature, 1953, 171: 134. [52] Went F W, Stark N. Mycorrhiza[J]. BioScience, 1968, 18: 1035-1039. [53] Chapin III F S, Moilainen L, Kielland K. Preferential use of organic acid N by a non-mycorrhizal arctic sedge[J]. Nature, 1993, 361: 150-153. [54] Bush D R. Proton-coupled sugar and amino acid transporters in plants[J]. Annual Review of Plant Physiology and Molecular Biology, 1993, 44: 513-542. [55] Tanner W, Caspari T. Membrane transport carriers[J]. Annual Review of Plant Physiology and Molecular Biology, 1996, 47: 595-626. [56] Fischer W-F, André B, Rentsch D, et al. Amino acid transport in plant[J]. Trends in Plant Science, 1998, 3: 188-195. [57] Kinraide T B. Interamino acid inhibition of transport in higher plants. Evidence for two transport channels with ascertainable affinities for amino acids[J]. Plant Physiology, 1981, 68: 1327-1333. [58] Datko A H, Mudd S H. Uptake of amino acids and other organic compounds by Lemna paucicostata Hegelm[J]. Plant Physiology, 1985, 77: 770-778. [59] Fischer W-F, Kwart M, Hummel S, et al. Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis[J]. Joural of Biological Chemistry, 1995, 270: 16315-16320. [60] Rentsch D, Hirner B, Schmeltzer E, et al. Salt stress-induced praline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant[J]. Plant Cell, 1996, 8: 1437-1446. [61] Chen L, Bush D R. LHT1, a lysine- and histidine-specific amino acid transporter in Arabidopsis[J]. Plant Physiology, 1997, 115: 1127-1134. [62] Bick J A, Neelam A, Hall J L, et al. Amino acid carriers of Ricinus communis expressed during seedling development: molecular cloning and expression analysis of two putative amino acid transporters, RcAAP1 and RcAAP2[J]. Plant Molecular Biology, 1998, 36: 377-385. [63] Rentsch D, Schmidt S, Tegeder M. Transporters for uptake and allocation of organic nitrogen compounds in plants[J]. FEBS Letters, 2007, 581: 2281-2289. [64] Hirner A, Ladwig F, Stransky H, et al. Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll[J]. Plant Cell, 2006, 18: 1931-1946. [65] Svennerstam H, Ganeteg U, Bellini C, et al. Comprehensive screening of Arabidopsis mutants suggests the lysine histidine transporter 1 to be involved in plant uptake of amino acids[J]. Plant Physiology, 2007, 143(4): 1853-1860. [66] Liu X, Bush D. Expression and transcriptional regulation of amino acid transporters in plants[J]. Amino Acids, 2006, 30: 113-120. [67] Grov A. Amino acids in soils[J]. Acta Chemica Scandinavica, 1963, 17: 2316-2318. [68] Ivarson K C, Sowden F J. Free amino acid composition of the plant root environment under field conditions[J]. Canadian Journal of Soil Society, 1969, 49: 121-127. [69] Ktsoyev B K. Free amino acids in the soils of the northern Caucasus[J]. Soviet Soil Science, 1978, 9: 312-315. [70] Nsholm T, Ekblad A, Nordin A, et al. Boreal forest plants take up organic nitrogen[J]. Nature, 1998, 392: 914-916. [71] Finzi A C, Berthrong S T. The uptake of amino acids by microbes and trees in three cold-temperature forests[J]. Ecology, 2005, 86: 3345-3353. [72] LeDuc S D, Rothstein D E. Plant-available organic and mineral nitrogen shift in dominance with forest stand age[J]. Ecology, 2010, 91(3): 708-720. [73] Abuzinadha R A, Read D J. Amino acids as nitrogen sources for ecomycorrhizal fungi: Utilization of individual amino acids[J]. Transactions of British Mycological Society, 1988, 91: 473-479. [74] Kielland K. Landscape patterns of free amino acids in arctic tundra soils[J]. Biogeochemistry, 1995, 31: 85-98. [75] Schimel J P, Chapin F S. Tundra plant uptake of amino acid and NH₄⁺-N in situ: Plants compete well for amino acid N[J]. Ecology, 1996, 77: 2142-2147. [76] Nordin A, Schmidt I K, Shaver G R. Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply[J]. Ecology, 2004, 85(4): 955-962. [77] Lipson D A, Raab T K, Schmidt S K, et al. An empirical model of amino acid transformations in an alpine soil[J]. Soil Biology and Biochemistry, 2001, 33: 189-198. [78] Miller A E, Bowman W D. Alpine plants show species-level differences in the uptake of organic and inorganic nitrogen[J]. Plant and Soil, 2003, 250: 283-292. [79] Xu X L, Ouyang H, Cao G M, et al. Uptake of organic nitrogen by eight dominant plant species in Kobresia meadows[J]. Nutrient Cycling in Agroecosystems, 2004, 69: 5-10. [80] Miller A E, Bowman W D, Suding K N. Plant uptake of inorganic and organic nitrogen: Neighbor identity matters[J]. Ecology, 2007, 88: 1832-1840. [81] Harrison K A, Bol R, Bardgett R D. Preferences for different nitrogen forms by coexisting plant species and soil microbes[J]. Ecology, 2007, 88(4): 989-999. [82] Bardgett R D, Steeter TC, Bol R. Soil microorganisms compete effectively with plants for organic-nitrogen inputs to temperate grasslands[J]. Ecology, 2003, 84: 1277-1387. [83] Xu X L, Ouyang H, Kuzyakov Y, et al. Significance of organic nitrogen acquisition for dominant species in an alpine meadow on the Tibet Plateau, China[J]. Plant and Soil, 2006, 285: 221-231. [84] Brophy L S, Heichel G H. Nitrogen release from roots of alfalfa and soybean grown in sand culture[J]. Plant and Soil, 1989, 116: 77-84. [85] Ta T C, MacDowall D H, Faris M A. Excretion of nitrogen assimilated from N₂ fixed by nodulated roots of alfalfa (Medicago sativa)[J]. Canadian Journal of Botany, 1986, 64: 2063-2067. [86] Shepherd T, Davies H V. Pattern of short-term amino acid accumulation and loss in the root zone of liquid-cultured forage rape[J]. Plant and Soil, 1994, 158: 99-109. [87] Jones D L, Darrah P R. Influx and efflux of amino acids from Zea mays L. roots and their implications for N nutrition and the rhizosphere[J]. Plant and Soil, 1993, 155-156: 87-90. [88] Klein D A, Frederik B A, Biondini M, et al. Rhizosphere micro-organism effects on soluble amino acids, sugars and organic acids in the root of zone of Agropyron cristatum, A. smithii and Bouteloua gracilis[J]. Plant and Soil, 1988, 110: 19-25. [89] Paynel F, Murray P J, Cliquet J B. Root exudates: A pathway for short-term N transfer from clover and ryegrass[J]. Plant and Soil, 2001, 229: 235-243. [90] Phillips D A, Fox T C, King M D, et al. Microbial products trigger amino acid exudation from plant roots[J]. Plant Physiology, 2004, 136: 2887-2894. [91] Phillips D A, Fox T C, Six J. Root exudation (net efflux of amino acids) may increase rhizodeposition under elevated CO₂[J]. Global Change Biology, 2006, 12: 561-567. [92] Jones D L. Amino acid degradation and its potential effects on organic nitrogen capture by plants[J]. Soil Biology and Biochemistry, 1999, 31: 613-622. [93] Jones D L, Kielland K. Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils[J]. Soil Biology and Biochemistry, 2002, 34: 209-219. [94] Kuzyakov Y, Jones D L. Glucose uptake by maize roots and its transformation in the rhizosphere[J]. Soil Biology and Biochemistry, 2006, 38: 851-860. [95] Biernath C, Fischer H, Kuzyakov Y. Root uptake of N-containing and N-free low molecular weight organic substances by maize-a¹⁴C/¹⁵N tracer study[J]. Soil Biology and Biochemistry, 2008, 9(40): 2237-2245. [96] Rasmussen J, Sauheitl L, Eriksen J, et al. Plant organic N uptake is biased by inorganic C: Results of triple labeling study[J]. Soil Biology and Biochemistry, 2010, 42: 524-527. [97] 邓若磊, 徐海荣, 曹云飞, 等. 植物吸收铵态氮的分子生物学基础[J]. 植物营养与肥料学报, 2007, 13(3): 512-519. [98] McKane R B, Johnson L C, Shaver G R, et al. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra[J]. Nature, 2002, 415: 68-71.