Organic N compounds in plant nutrition: have methodologies based on stable isotopes provided unequivocal evidence of direct N uptake?

References

• Chalk P, Smith C. On inorganic N uptake by vascular plants: Can 15N tracer techniques resolve the NH4+ versus NO3− “preference” conundrum? Eur J Soil Sci. 2020. doi:10.1111/ejss.13069.
   Google Scholar
• Paungfoo-Lonhienne C, Visser J, Lonhienne TGA, et al. Past, present and future of organic nutrients. Plant Soil. 2012;359:1–18.
   Web of Science ®Google Scholar
• Näsholm T, Kielland K, Ganeteg U. Uptake of organic nitrogen by plants. New Phytol. 2009;182:31–48.
   PubMed Web of Science ®Google Scholar
• Jones DL, Owen AG, Farrar JF. Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol Biochem. 2002;34:1893–1902.
   Web of Science ®Google Scholar
• Rasmussen J, Sauheitl L, Eriksen J, et al. Plant uptake of dual-labeled organic N biased by inorganic C uptake: results of a triple labelling study. Soil Biol Biochem. 2010;42:524–527.
   Web of Science ®Google Scholar
• Hill PW, Jones DL. Plant–microbe competition: does injection of isotopes of C and N into the rhizosphere effectively characterise plant use of soil N? New Phytol. 2019;221:796–806.
   PubMed Web of Science ®Google Scholar
• Yang L, Yu C, Zhang L, et al. Substrate availability affects the partitioning of C and N in glycine between plants and soil microorganisms. Arch Agron Soil Sci. 2021;67:109–121.
   Web of Science ®Google Scholar
• Finzi AC, Berthrong ST. The uptake of amino acids by microbes and trees in three cold-temperate forests. Ecology. 2005;86:3345–3353.
   Web of Science ®Google Scholar
• Jones DL, Kielland K, Sinclair FL, et al. Soil organic nitrogen mineralization across a global latitudinal gradient. Glob Biogeochem Cycl. 2009;23:GB1016.
   Web of Science ®Google Scholar
• Moe LA. Amino acids in the rhizosphere: from plants to microbes. Am J Bot. 2013;100:1692–1705.
   PubMed Web of Science ®Google Scholar
• Yang L, Zhang L, Yu C, et al. Nitrogen fertilizer and straw applications affect uptake of 13C, 15N-glycine by soil microorganisms in wheat growth stages. PloS One. 2017;12:e0169016.
   PubMed Web of Science ®Google Scholar
• Hu Y, Zheng Q, Zhang S, et al. Significant release and microbial utilization of amino sugars and d-amino acid enantiomers from microbial cell wall decomposition in soils. Soil Biol Biochem. 2018;123:115–125.
   PubMed Web of Science ®Google Scholar
• Jones DL, Healey JR, Willett VB, et al. Dissolved organic nitrogen uptake by plants – an important N uptake pathway? Soil Biol Biochem. 2005;37:413–423.
   Web of Science ®Google Scholar
• Dunn RM, Mikola J, Bol R, et al. Influence of microbial activity on plant–microbial competition for organic and inorganic nitrogen. Plant Soil. 2006;289:321–334.
   Web of Science ®Google Scholar
• Henry HAL, Jefferies RL. Plant amino acid uptake, soluble N turnover and microbial N capture in soils of a grazed Arctic salt marsh. J Ecol. 2003;91:627–636.
   Web of Science ®Google Scholar
• Schimel JP, Chapin FS. Tundra plant uptake of amino acid and NH4+ nitrogen in situ: plants complete well for amino acid N. Ecology. 1996;77:2142–2147.
   Web of Science ®Google Scholar
• Jones DL, Shannon D, Murphy DV, et al. Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biol Biochem. 2004;36:749–756.
   Web of Science ®Google Scholar
• Ma S, Zhu X, Zhang J, et al. Warming decreased and grazing increased plant uptake of amino acids in an alpine meadow. Ecol Evol. 2015;5:3995–4005.
   PubMed Web of Science ®Google Scholar
• Vinolas LC, Healey JR, Jones DL. Kinetics of soil microbial uptake of free amino acids. Biol Fertil Soils. 2001;33:67–74.
   Web of Science ®Google Scholar
• Hodge A, Robinson D, Fitter A. Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci. 2000;5:304–308.
   PubMed Web of Science ®Google Scholar
• Schimel JP, Bennett J. Nitrogen mineralization: challenges of a changing paradigm. Ecology. 2004;85:591–602.
   Web of Science ®Google Scholar
• van Hees PAW, Jones DL, Finlay R, et al. The carbon we do not see—the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem. 2005;37:1–13.
   Web of Science ®Google Scholar
• Andersen KM, Mayor JR, Turner BL. Plasticity in nitrogen uptake among plant species with contrasting nutrient acquisition strategies in a tropical forest. Ecology. 2017;98:1388–1398.
   PubMed Web of Science ®Google Scholar
• Bardgett RD, Streeter TC, Bol R. Soil microbes compete effectively with plants for organic nitrogen inputs to temperate grasslands. Ecology. 2003;84:1277–1287.
   Web of Science ®Google Scholar
• Hofmockel KS, Schlesinger WH, Jackson RB. Effects of elevated atmospheric carbon dioxide on amino acid and NH4+-N cycling in a temperate pine ecosystem. Glob Change Biol. 2007;13:1950–1959.
   Web of Science ®Google Scholar
• Lipson DA, Monson RK. Plant-microbe competition for soil amino acids in the alpine tundra: effects of freeze-thaw and dry-rewet events. Oecologia. 1998;113:406–414.
   PubMed Web of Science ®Google Scholar
• Lipson DA, Raab TK, Schmidt SK, et al. Variation in competitive abilities of plants and microbes for specific amino acids. Biol Fertil Soils. 1999;29:257–261.
   Web of Science ®Google Scholar
• McFarland JW, Ruess RW, Kielland K, et al. Cycling dynamics of NH4+ and amino acid nitrogen in soils of a deciduous boreal forest ecosystem. Ecosystems. 2002;5:775–788.
   Web of Science ®Google Scholar
• McFarland JW, Ruess RW, Kielland K, et al. Cross-ecosystem comparisons of in situ plant uptake of amino acid-N and NH4+. Ecosystems. 2010;13:177–193.
   Web of Science ®Google Scholar
• Sorensen PL, Clemmensen KE, Michelsen A, et al. Plant and microbial uptake and allocation of organic and inorganic nitrogen related to plant growth forms and soil conditions at two subarctic tundra sites in Sweden. Arct Antarct Alp Res. 2008;40:171–180.
   Web of Science ®Google Scholar
• Cliquet JB, Murray PJ, Boucaud J. Effect of the arbuscular mycorrhizal fungus Glomus fasciculatum on the uptake of amino nitrogen by Lolium perenne. New Phytol. 1997;137:345–349.
   PubMed Web of Science ®Google Scholar
• Thornton B. Uptake of glycine by non-mycorrhizal Lolium perenne. J Exp Bot. 2001;52:1315–1322.
   PubMed Web of Science ®Google Scholar
• Xu X, Ouyang H, Cao G, et al. Uptake of organic nitrogen by eight dominant plant species in Kobresia meadows. Nutr Cycl Agroecosys. 2004;69:5–10.
   Web of Science ®Google Scholar
• Thornton B, Robinson D. Uptake and assimilation of nitrogen from solutions containing multiple N sources. Plant Cell Environ. 2005;28:813–821.
   Web of Science ®Google Scholar
• Aanderud ZT, Bledsoe CS. Preferences for 15N-ammonium, 15N-nitrate, and 15N-glycine differ among dominant exotic and subordinate native grasses from a California oak woodland. Environ Exp Bot. 2009;65:205–209.
   Web of Science ®Google Scholar
• Hong J, Ma X, Yan Y, et al. Which root traits determine nitrogen uptake by alpine plant species on the Tibetan Plateau? Plant Soil. 2018;424:63–72.
   Web of Science ®Google Scholar
• Zhu F, Dai L, Hobbie EA, et al. Uptake patterns of glycine, ammonium, and nitrate differ among four common tree species of northeast China. Front Plant Sci. 2019;10:799.
   PubMed Web of Science ®Google Scholar
• Tian Y, Yu M, Xu F, et al. Uptake of amino acids and inorganic nitrogen by two dominant temperate grasses. Rhizosphere. 2020;14:100199.
   Web of Science ®Google Scholar
• Jones DL, Darrah PR. Influx and efflux of amino-acids from Zea mays L roots and their implications for N-nutrition and the rhizosphere. Plant Soil. 1993;156:87–90.
   Google Scholar
• Warren CR. Wheat roots efflux a diverse array of organic N compounds and are highly proficient at their recapture. Plant Soil. 2015;397:147–162.
   Web of Science ®Google Scholar
• Pate JS. Transport and partitioning of nitrogenous solutes. Annu Rev Plant Physiol Plant Mol Biol. 1980;31:313–340.
   Web of Science ®Google Scholar
• Yang G, Wei Q, Huang H, et al. Amino acid transporters in plant cells: A brief review. Plants. 2020;9:967.
   Google Scholar
• Pratelli R, Pilot G. Regulation of amino acid metabolic enzymes and transporters in plants. J Exp Bot. 2014;65:5535–5556.
   PubMed Web of Science ®Google Scholar
• Sauheitl L, Glaser B, Weigelt A. Advantages of compound-specific stable isotope measurements over bulk measurements in studies on plant uptake of intact amino acids. Rapid Commun Mass Spectrom. 2009;23:3333–3342.
   PubMed Web of Science ®Google Scholar
• Persson J, Näsholm T. A GC-MS method for determination of amino acid uptake by plants. Physiol Plant. 2001;113:352–358.
   PubMed Web of Science ®Google Scholar
• Nordin A, Schmidt IK, Shaver GR. Nitrogen uptake by Arctic soil microbes and plants in relation to soil nitrogen supply. Ecology. 2004;85:955–962.
   Web of Science ®Google Scholar
• Hildebrandt TM, Nesi AN, Araújo WL, et al. Amino acid catabolism in plants. Mol Plant. 2015;8:1563–1579.
   PubMed Web of Science ®Google Scholar
• Phillips DL, Gregg JW. Source partitioning using stable isotopes: coping with too many sources. Oecologia. 2003;136:261–269.
   PubMed Web of Science ®Google Scholar
• Phillips DL, Newsome SD, Gregg JW. Combining sources in stable isotope mixing models: alternative methods. Oecologia. 2005;144:520–527.
   PubMed Web of Science ®Google Scholar
• Houlton BZ, Sigman DM, Schuur EAG, et al. A climate driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci USA. 2007;104:8902–8906.
   PubMed Web of Science ®Google Scholar
• Takebayashi Y, Koba K, Sasaki Y, et al. The natural abundance of 15N in plant and soil-available N indicates a shift of main plant N resources to NO3– from NH4+ along the N leaching gradient. Rapid Commun Mass Spectrom. 2010;24:1001–1008.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Li N, Xiao J, et al. Changes in plant nitrogen acquisition strategies during the restoration of spruce plantations on the eastern Tibetan Plateau, China. Soil Biol Biochem. 2018;119:50–58.
   Web of Science ®Google Scholar
• Vallano DM, Sparks JP. Foliar δ15N is affected by foliar nitrogen uptake, soil nitrogen, and mycorrhizae along a nitrogen deposition gradient. Oecologia. 2013;172:47–58.
   PubMed Web of Science ®Google Scholar
• Craine JM, Brookshire ENJ, Cramer MD, et al. Ecological interpretations of nitrogen isotope ratios of terrestrial plant and soils. Plant Soil. 2015;396:1–26.
   Web of Science ®Google Scholar
• Chalk PM, Balieiro FC, Chen D. Quantitative estimation of carbon dynamics in terrestrial ecosystems using natural variations in the δ13C abundance of soils and biota: A review. Adv Agron. 2021;167:63–104.
   Google Scholar
• Raab TK, Lipson DA, Monson RK. Non-mycorrhizal uptake of amino acids by roots of the alpine sedge Kobresia myosuroides: implications for the alpine nitrogen cycle. Oecologia. 1996;108:488–494.
   PubMed Web of Science ®Google Scholar
• Rasmussen J, Kuzyakov Y. Carbon isotopes as proof for plant uptake of organic nitrogen: Relevance of inorganic carbon uptake. Soil Biol Biochem. 2009;41:1586–1587.
   Web of Science ®Google Scholar
• Näsholm T, Högberg MN, Högberg P, et al. Carbon isotopes as proof for plant uptake of organic nitrogen: Relevance of inorganic carbon uptake: reply to Rasmussen and Kuzyakov. Soil Biol Biochem. 2009;41:1588–1589.
   Web of Science ®Google Scholar
• Näsholm T, Ekblad A, Nordin A, et al. Boreal forest plants take up organic nitrogen. Nature. 1998;392:914–916.
   Web of Science ®Google Scholar
• Näsholm T, Huss-Danell K, Högberg P. Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology. 2000;81:1155–1161.
   Web of Science ®Google Scholar
• Nordin A, Högberg P, Näsholm T. Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia. 2001;129:125–132.
   PubMed Web of Science ®Google Scholar
• Öhlund J, Näsholm T. Regulation of organic and inorganic nitrogen uptake in Scots pine (Pinus sylvestris) seedlings. Tree Physiol. 2004;24:1397–1402.
   PubMed Web of Science ®Google Scholar
• Warren CR, Adams PR. Uptake of nitrate, ammonium and glycine by plants of Tasmanian wet eucalypt forests. Tree Physiol. 2007;27:413–419.
   PubMed Web of Science ®Google Scholar
• Clemmensen KE, Sorensen PL, Michelsen A, et al. Site-dependent N uptake from N-form mixtures by Arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia. 2008;155:771–783.
   PubMed Web of Science ®Google Scholar
• Ge T, Song S, Roberts P, et al. Amino acids as a nitrogen source for tomato seedlings: The use of dual-labeled (13C, 15N) glycine to test for direct uptake by tomato seedlings. Environ Exp Bot. 2009;66:357–361.
   Web of Science ®Google Scholar
• Warren CR. Does nitrogen concentration affect relative uptake rates of nitrate, ammonium, and glycine? J Plant Nutr Soil Sci. 2009;172:224–229.
   Web of Science ®Google Scholar
• Gioseffi E, Neergaard AD, Schjørring JK. Interactions between uptake of amino acids and inorganic nitrogen in wheat plants. Biogeosciences. 2012;9:1509–1518.
   Web of Science ®Google Scholar
• Wilkinson A, Hill PW, Vaieretti MV, et al. Challenging the paradigm of nitrogen cycling: no evidence of in situ resource partitioning by coexisting plant species in grasslands of contrasting fertility. Ecol Evol. 2015;5:275–287.
   PubMed Web of Science ®Google Scholar
• Gao L, Cui X, Hill PW, et al. Uptake of various nitrogen forms by co-existing plant species in temperate and cold-temperate forests in northeast China. Appl Soil Ecol. 2020;147:103398.
   Web of Science ®Google Scholar
• Dion PP, Jämtgård S, Bertrand A, et al. Organic nitrogen uptake and assimilation in Cucumis sativus using position-specific labeling and compound-specific isotope analysis. Front Plant Sci. 2018;9:1596.
   PubMed Web of Science ®Google Scholar
• Weigelt A, King R, Bol R, et al. Inter-specific variability in organic nitrogen uptake of three temperate grassland species. J Plant Nutr Soil Sci. 2003;166:606–611.
   Web of Science ®Google Scholar
• Oliver DJ. The glycine decarboxylase complex from plant mitochondria. Annu Rev Plant Physiol Plant Mol Biol. 1994;45:323–337.
   Web of Science ®Google Scholar
• Knowles TDJ, Chadwick DR, Bol R, et al. Tracing the rate and extent of N and C flow from 13C, 15N-glycine and glutamate into individual de novo synthesised soil amino acids. Org Geochem. 2010;41:1259–1268.
   Web of Science ®Google Scholar
• Warren CR. Post-uptake metabolism affects quantification of amino acid uptake. New Phytol. 2012;193:522–531.
   PubMed Web of Science ®Google Scholar
• Warren CR. High diversity of small organic N observed in soil water. Soil Biol Biochem. 2013;57:444–450.
   Web of Science ®Google Scholar
• Warren CR. Quaternary ammonium compounds can be abundant in some soils and are taken up as intact molecules by plants. New Phytol. 2013;198:476–485.
   PubMed Web of Science ®Google Scholar
• Ma Q, Cao X, Ma J, et al. Hexavalent chromium stress enhances the uptake of nitrate but reduces the uptake of ammonium and glycine in pak choi (Brassica chinensis L.). Ecotox Environ Saf. 2017;139:384–393.
   PubMed Web of Science ®Google Scholar
• Ma Q, Cao X, Tan X, et al. Effects of cadmium stress on pakchoi (Brassica chinensis L.) growth and uptake of inorganic and organic nitrogenous compounds. Environ Exp Bot. 2017;137:49–57.
   Web of Science ®Google Scholar
• Ma Q, Cao X, Xie Y, et al. Effect of pH on the uptake and metabolism of glycine in pak choi (Brassica chinensis L.). Environ Exp Bot. 2017;133:139–150.
   Web of Science ®Google Scholar
• Streeter TC, Bol R, Bardgett RD. Amino acids as a nitrogen source in temperate upland grasslands: the use of dual labelled (13C, 15N) glycine to test for direct uptake by dominant grasses. Rapid Commun Mass Spectrom. 2000;14:1351–1355.
   PubMed Web of Science ®Google Scholar
• Näsholm T, Persson J. Plant acquisition of organic nitrogen in boreal forests. Physiol Plant. 2001;111:419–426.
   PubMed Web of Science ®Google Scholar
• Jämtgård S, Näsholm T, Huss-Danell K. Characteristics of amino acid uptake in barley. Plant Soil. 2008;302:221–231.
   Web of Science ®Google Scholar
• Ma S, He F, Tian D, et al. Variations and determinants of carbon content in plants: a global synthesis. Biogeosciences. 2018;15:693–702.
   Web of Science ®Google Scholar
• Gordon WS, Jackson RB. Nutrient concentrations in fine roots. Ecology. 2000;81:275–280.
   Web of Science ®Google Scholar
• Gallet-Budynek A, Brzostek E, Rodgers VL, et al. Intact amino acid uptake by northern hardwood and conifer trees. Oecologia. 2009;160:129–138.
   PubMed Web of Science ®Google Scholar
• Coplen TB. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom. 2011;25:2538–2560.
   PubMed Web of Science ®Google Scholar
• Chalk PM, Inácio CT, Craswell ET, et al. On the usage of absolute (x) and relative (δ) values of 15N abundance. Soil Biol Biochem. 2015;85:51–53.
   Web of Science ®Google Scholar
• Sauheitl L, Glaser B, Weigelt A. Uptake of intact amino acids by plants depends on soil amino acid concentrations. Environ Exp Bot. 2009;66:145–152.
   Web of Science ®Google Scholar
• Henry HAL, Jefferies RL. Interactions in the uptake of amino acids, ammonium and nitrate ions in the Arctic salt-marsh grass, Puccinella phryganodes. Plant Cell Environ. 2003;26:419–428.
   Web of Science ®Google Scholar