Two-Phase Conceptual Framework of Phosphatase Activity and Phosphorus Bioavailability
Tóm tắt
The activity of extracellular phosphatases is a dynamic process controlled by both plant roots and microorganisms, which is responsible for the mineralization of soil phosphorus (P). Plants regulate the availability of soil P through the release of root mucilage and the exudation of low-molecular weight organic acids (LMWOAs). Mucilage increases soil hydraulic conductivity as well as pore connectivity, both of which are associated with increased phosphatase activity. The LMWOAs, in turn, stimulate the mineralization of soil P through their synergistic effects of acidification, chelation, and exchange reactions. This article reviews the catalytic properties of extracellular phosphatases and their interactions with the rhizosphere interfaces. We observed a biphasic effect of root metabolic products on extracellular phosphatases, which notably altered their catalytic mechanism. In accordance with the proposed conceptual framework, soil P is acquired by both plants and microorganisms in a coupled manner that is characterized by the exudation of their metabolic products. Due to inactive or reduced root exudation, plants recycle P through adsorption on the soil matrix, thereby reducing the rhizosphere phosphatase activity. The two-phase conceptual framework might assist in understanding P-acquisition (substrate turnover) and P-restoration (phosphatase adsorption by soil) in various terrestrial ecosystems.
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Adeleke, 2012, Culturable microorganisms associated with Sishen iron ore and their potential roles in biobeneficiation, World J. Microbiol. Biotechnol, 28, 1057, 10.1007/s11274-011-0904-2
Ahmed, 2018, Soil microorganisms exhibit enzymatic and priming response to root mucilage under drought, Soil Biol. Biochem, 116, 410, 10.1016/j.soilbio.2017.10.041
Ahn, 2006, Transformation of catechol in the presence of a laccase and birnessite, Soil Biol. Biochem, 38, 1015, 10.1016/j.soilbio.2005.08.016
Ajmera, 2019, An integrative systems perspective on plant phosphate research, Genes (Basel)., 13, 139, 10.3390/genes10020139
Ali, 2015, Modelling in situ activities of enzymes as a tool to explain seasonal variation of soil respiration from agro–ecosystems, Soil Biol. Biochem, 81, 291, 10.1016/j.soilbio.2014.12.001
Allison, 2007, Soil enzymes: linking proteomics and ecological processes, Man. Environ. Microbiol, 704e711, 10.1128/9781555815882.ch58
Allison, 2011, Evolutionary–economic principles as regulators of soil enzyme production and ecosystem function, Soil Enzymology. Soil Biology, 229
Allison, 2007, Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand, Soil Biol. Biochem, 39, 1770e1781, 10.1016/j.soilbio.2007.02.006
Andrade, 2013, Organic acid adsorption and mineralization in oxisols with different textures, Rev. Bras. Cienc. Solo, 37, 976, 10.1590/S0100-06832013000400015
Araujo, 2012, Microbiological process in agroforestry systems. A review, Agron. Sustainable Dev, 32, 215, 10.1007/s13593-011-0026-0
Aziz, 2011, Variation in phosphorus efficiency among brassica cultivars II: Changes in root morphology and carboxylate exudation, J. Plant Nutr, 34, 2127, 10.1080/01904167.2011.618573
Badri, 2009, Regulation and function of root exudates, Plant Cell Environ, 32, 666, 10.1111/j.1365-3040.2009.01926.x
Bais, 2008, Root exudates modulate plant–microbe interactions in the rhizosphere, Secondary Metabolites in Soil Ecology. Soil Biol, 10.1007/978-3-540-74543-3_11
Benard, , Microhydrological niches in soils: how mucilage and EPS alter the biophysical properties of the rhizosphere and other biological hotspots, Vadose Zone. J, 18, 1, 10.2136/vzj2018.12.0211
Benard, , Physics and hydraulics of the rhizosphere network, J. Plant Nutr. Soil Sci, 182, 5, 10.1002/jpln.201800042
Bhadoria, 1991, Phosphate diffusion coefficients in soil as affected by bulk density and water content, Zeitschrift für Pflanzenernährung und Bodenkunde, 154, 53, 10.1002/jpln.19911540111
Bhattacharyya, 2008, Arsenic fractions and enzyme activities in arsenic-contaminated soils by groundwater irrigation in West Bengal, Ecotoxicol. Environ. Saf, 71, 149, 10.1016/j.ecoenv.2007.08.015
Bhatti, 1998, Influence of soil organic matter removal and pH on oxalate sorption onto a spodic horizon, Soil Sci. Soc. Am. J., 62, 152, 10.2136/sssaj1998.03615995006200010020x
Bilyera, 2022, Co–localised phosphorus mobilization processes in the rhizosphere of field-grown maize jointly contribute to plant nutrition, Soil Biol. Biochem, 165, 108497, 10.1016/j.soilbio.2021.108497
Brax, 2020, Influence of the physico-chemical properties of root mucilage and model substances on the microstructural stability of sand, Biogeochemistry, 147, 35, 10.1007/s10533-019-00626-w
Brucker, 2020, Release of phosphorus and silicon from minerals by soil microorganisms depends on the availability of organic carbon, Soil Biol. Biochem, 143, 107737, 10.1016/j.soilbio.2020.107737
Burns, 1982, Enzyme activity in soil: location and a possible role in microbial ecology, Soil Biol. Biochem, 14, 423, 10.1016/0038-0717(82)90099-2
Burns, 2013, Soil enzymes in a changing environment: current knowledge and future directions, Soil Biol. Biochem, 58, 216, 10.1016/j.soilbio.2012.11.009
Canarini, 2019, Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli, Front. Plant Sci, 10, 157, 10.3389/fpls.2019.00157
Čapek, 2021, Biochemical inhibition of acid phosphatase activity in two mountain spruce forest soils, Biol Fertil Soils, 57, 991, 10.1007/s00374-021-01587-9
Carminati, 2017, Liquid bridges at the root–soil interface, Plant Soil., 417, 1, 10.1007/s11104-017-3227-8
Carminati, 2010, Dynamics of soil water content in the rhizosphere, Plant Soil, 332, 163, 10.1007/s11104-010-0283-8
Carminati, 2016, Biophysical rhizosphere processes affecting root water uptake, Ann. Bot. (Oxford, U. K.)., 118, 561, 10.1093/aob/mcw113
Chen, 2002, Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus Radiata D. Don.), Soil Biol. Biochem, 34, 487, 10.1016/S0038-0717(01)00207-3
Clarholm, 2015, Organic acid induced release of nutrients from metal–stabilized soil organic matter–The unbutton model, Soil Biol. Biochem, 84, 168, 10.1016/j.soilbio.2015.02.019
Cornish–Bowden, 2015, One hundred years of michaelis-menten kinetics, Perspectives in Sci, 4, 3, 10.1016/j.pisc.2014.12.002.
Crawford, 2005, Towards an evolutionary ecology of life in soil, Trends Ecol Evol, 20, 81, 10.1016/j.tree.2004.11.014
Dalling, 2016, Nutrient availability in tropical rain forests: the paradigm of phosphorus limitation, Tropical Tree Physiology, 261, 10.1007/978-3-319-27422-5_12
Datta, 2017, How enzymes are adsorbed on soil solid phase and factors limiting its activity: A review, Int. Agrophys, 31, 287, 10.1515/intag-2016-0049
De Schepper, 2013, Phloem transport: a review of mechanisms and controls, J. Exp. Bot, 64, 4839, 10.1093/jxb/ert302
Delhaize, 2012, Aluminium tolerance of root hairs underlies genotypic differences in rhizosheath size of wheat (Triticum aestivum) grown on acid soil, New Phytol, 195, 609, 10.1111/j.1469-8137.2012.04183.x
Demanèche, 2009, Dissimilar pH-dependent adsorption features of bovine serum albumin and α-chymotrypsin on mica probed by AFM, Colloids Surf. B., 70, 226, 10.1016/j.colsurfb.2008.12.036
Deng, 1995, Cellulase activity of soils: effect of trace elements, Soil Biol. Biochem, 27, 977, 10.1016/0038-0717(95)00005-Y
Denton, 2007, Banksia species (Proteaceae) from severely phosphorus impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus, Plant, Cell Environ, 30, 1557, 10.1111/j.1365-3040.2007.01733.x
Dick, 1987, Kinetics and activities of phosphatase–clay complexes1, Soil Sci, 5, 10.1097/00010694-198701000-00002
Doan, 2017, A low–cost imaging method for the temporal and spatial colorimetric detection of free amines on maize root surfaces, Front. Plant Sci, 8, 1513, 10.3389/fpls.2017.01513
Eberwein, 2017, Michaelis–Menten kinetics of soil respiration feedbacks to nitrogen deposition and climate change in subtropical forests, Sci. Rep, 7, 1752, 10.1038/s41598-017-01941-8
Gang, 2012, The role of root-released organic acids and anions in phosphorus transformations in a sandy loam soil from Yantai, China, Afr. J. Microbiol. Res, 6, 674, 10.5897/AJMR11.1296
Geelhoed, 1998, Competition interaction between phosphate and citrate on goethite, Environ. Sci. Technol, 32, 2119, 10.1021/es970908y
George, 2014, Understanding the genetic control and physiological traits associated with rhizosheath production by barley (Hordeum vulgare), New Phytol, 203, 195, 10.1111/nph.12786
George, 2002, Phosphatase activity and organic acids in the rhizosphere of potential agroforestry species and maize, Soil Biol. Biochem, 34, 1487, 10.1016/S0038-0717(02)00093-7
Gianfreda, 2015, Enzymes of importance to rhizosphere processes, J. Soil Sci. Plant Nutr, 15, 283, 10.4067/S0718-95162015005000022
Gianfreda, 2006, Enzyme activities in soil, Nucleic acids and proteins in soil. Series Soil Biology, 257, 10.1007/3-540-29449-X_12
Gilliham, 2016, Linking metabolism to membrane signaling: the GABA-Malate connection, Trends Plant Sci, 21, 295, 10.1016/j.tplants.2015.11.011
Grafe, 2018, Bacterial potentials for uptake, solubilization and mineralization of extracellular phosphorus in agricultural soils are highly stable under different fertilization regimes, Environ. Microbiol. Rep, 10, 320, 10.1111/1758-2229.12651
Guber, 2022, Are enzymes transported in soils by water fluxes?, Soil Biol. Biochem, 168, 108633, 10.1016/j.soilbio.2022.108633
Haque, 2005, Ecology of phosphate solubilizers in semi-arid agricultural soils, Indian J. Microbiol, 45, 27
Hengge, 2005, Mechanistic studies on enzyme–catalyzed phosphoryl transfer, Adv. Phys. Org. Chem, 40, 49, 10.1016/S0065-3160(05)40002-7
Hill, 2015, Living roots magnify the response of soil organic carbon decomposition to temperature in temperate grassland, GCB Bioenergy., 21, 1368, 10.1111/gcb.12784
Hinsinger, 2008, Soil–root–microbe interactions in the rhizosphere – a key to understanding and predicting nutrient bioavailability to plants, J. Soil Sci. Plant Nutr, 8, 39, 10.4067/S0718-27912008000400008
Holz, 2019, Increased water retention in the rhizosphere allows for high phosphatase activity in drying soil, Plant Soil., 443, 259, 10.1007/s11104-019-04234-3
Hu, 2018, Antioxidant metabolism, photosystem II, and fatty acid composition of two tall fescue genotypes with different heat tolerance under high temperature stress, Front. Plant Sci, 9, 1242, 10.3389/fpls.2018.01242
Huang, 2005, Adsorption, desorption and activities of acid phosphatase on various colloidal particles from an Ultisol, Colloids Surf., B., 45, 209, 10.1016/j.colsurfb.2005.08.011
Huang, 2003, Effects of several low-molecular weight organic acids and phosphate on the adsorption of acid phosphatase by soil colloids and minerals, Chemosphere., 52, 571, 10.1016/S0045-6535(03)00238-8
Hummel, 2021, Co–occurring increased phosphatase activity and labile P depletion in the rhizosphere of Lupinus angustifolius assessed with a novel, combined 2D–imaging approach, Soil Biol. Biochem, 153, 107963, 10.1016/j.soilbio.2020.107963
Hunter, 2014, Root traits and microbial community interactions in relation to phosphorus availability and acquisition, with particular reference to Brassica, Front. Plant Sci, 5, 1, 10.3389/fpls.2014.00027
Hussain, 2012, Use of two–surface Langmuir-type equations for assessment of phosphorus requirements of lentil on differently textured alluvial soils, Comm. Soil Sci. Plant Anal, 43, 2575, 10.1080/00103624.2012.716121
Ikeda, 2011, Why does the silica-binding protein “Si-tag” bind strongly to silica surfaces? Implications of conformational adaptation of the intrinsically disordered polypeptide to solid surfaces, Colloids Surf., B., 86, 359, 10.1016/j.colsurfb.2011.04.020
Jarosch, 2019, Is the enzymatic hydrolysis of soil organic phosphorus compounds limited by enzyme or substrate availability?, Soil Biol. Biochem., 139, 107628, 10.1016/j.soilbio.2019.107628
Joner, 2000, Phosphatase activity of external hyphae of two arbuscular mycorrhizal fungi, Mycol. Res, 104, 81, 10.1017/S0953756299001240
Jones, 2009, Carbon flow in the rhizosphere: carbon trading at the soil–root interface, Plant Soil, 321, 5, 10.1007/s11104-009-9925-0
Kafkafi, 1988, Phosphorus adsorption by kaolinite and montmorillonite: II. organic anion competition, Soil Sci. Soc. Am. J, 52, 1585, 10.2136/sssaj1988.03615995005200060012x
Kedi, 2013, Diversity of adsorption affinity and catalytic activity of fungal phosphatases adsorbed on some tropical soils, Soil Biol. Biochem. Vol., 56, 13, 10.1016/j.soilbio.2012.02.006
Kelleher, 2004, Acid phosphatase interactions with organo-mineral complexes: influence on catalytic activity, Biogeochemistry., 71, 285, 10.1023/B:BIOG.0000049348.53070.6f
Khademi, 2009, Organic acid mediated nutrient extraction efficiency in three calcareous soils, Aust. J. Soil Res, 47, 213, 10.1071/SR07179
Kirk, 1999, Phosphate solubilization by organic anion excretion from rice growing in aerobic soil: rates of excretion and decomposition, effects on rhizosphere pH and effects on phosphate solubility and uptake, New Phytol, 142, 185, 10.1046/j.1469-8137.1999.00400.x
Koester, 2021, From rock eating to vegetarian ecosystems — disentangling processes of phosphorus acquisition across biomes, Geoderma., 388, 114827, 10.1016/j.geoderma.2020.114827
Korenblum, 2020, Rhizosphere microbiome mediates systemic root metabolite exudation by root-to-root signaling, PNAS., 117, 3874, 10.1073/pnas.1912130117
Kroener, 2014, Nonequilibrium water dynamics in the rhizosphere: How mucilage affects water flow in soils, Water Resour. Res, 50, 6479, 10.1002/2013WR014756
Kruse, 2015, Innovative methods in soil phosphorus research: a review, J. Plant Nutr. Soil Sci, 178, 43, 10.1002/jpln.201400327
Lambers, 2015, Leaf manganese accumulation and phosphorus-acquisition efficiency, Tren. Plant Sci, 20, 83, 10.1016/j.tplants.2014.10.007
Lang, 2017, Soil phosphorus supply controls P nutrition strategies of beech forest ecosystems in Central Europe, Biogeochemistry., 136, 5, 10.1007/s10533-017-0375-0
Lassila, 2011, Biological phosphoryl-transfer reactions: understanding mechanism and catalysis, Annu Rev Biochem, 80, 669, 10.1146/annurev-biochem-060409-092741
Leake, 1996, Phosphodiesters as mycorrhizal P sources I. phosphodiesterase production and the utilization of DNA as a phosphorus source by the ericoid mycorrhizal fungus Hymenoscyphus ericae, New Phytol, 132, 435, 10.1111/j.1469-8137.1996.tb01863.x
Leprince, 1996, Extracellular enzyme activity in soil: effect of pH and ionic strength on the interaction with montmorillonite of two acid phosphatases secreted by the ectomycorrhizal fungus Hebeloma cylindrosporum, Eur. J. Soil Sci, 47, 511, 10.1111/j.1365-2389.1996.tb01851.x
Loeppmann, , Substrate quality affects kinetics and catalytic efficiency of exo–enzymes in rhizosphere and detritusphere, Soil Biol. Biochem. Vol, 92, 111, 10.1016/j.soilbio.2015.09.020
Loeppmann, 2020, Organic nutrients induced coupled C– and P–cycling enzyme activities during microbial growth in forest soils, Front. For. Glob. Change, 3, 100, 10.3389/ffgc.2020.00100
Loeppmann, , Substrate quality affects microbial– and enzyme activities in rooted soil, J. Plant Nut. Soil Sci, 179, 39, 10.1002/jpln.201400518
Loeppmann, 2018, Shift from dormancy to microbial growth revealed by RNA:DNA ratio, Ecol. Indic, 85, 603, 10.1016/j.ecolind.2017.11.020
Lu, 2020, Long–term application of fertilizer and manures affect P fractions in Mollisol, Sci. Rep, 10, 10.1038/s41598-020-71448-2
Manzoni, 2021, Intracellular storage reduces stoichiometric imbalances in soil microbial biomass – a theoretical exploration, Front. Ecol. Evol, 663, 10.3389/fevo.2021.714134
Manzoni, 2014, A theoretical analysis of microbial eco–physiological and diffusion limitations to carbon cycling in drying soils, Soil Biol. Biochem, 73, 69, 10.1016/j.soilbio.2014.02.008
Margalef, 2017, Global patterns of phosphatase activity in natural soils, Sci. Rep, 7, 1337, 10.1038/s41598-017-01418-8
Marklein, 2012, Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems, New Phytol, 193, 696, 10.1111/j.1469-8137.2011.03967.x
Maseko, 2013, Rhizosphere acid and alkaline phosphatase activity as a marker of Pb nutrition in nodulated Cyclopia and Aspalathus species in the Cape fynbos of South Africa, South African J. Bot, 89, 289, 10.1016/j.sajb.2013.06.023
McConnell, 2020, Reviews and syntheses: Ironing out wrinkles in the soil phosphorus cycling paradigm, Biogeosciences., 5309, 10.5194/bg-17-5309-2020
McCully, 1997, The expansion of maize root-cap mucilage during hydration. 3. Changes in water potential and water content, Physiol. Plant, 99, 169, 10.1111/j.1399-3054.1997.tb03445.x
Menezes–Blackburn, 2013, Phytases and phytase-labile organic phosphorus in manures and soils, Crit. Rev. Environ. Sci. Technol, 43, 916, 10.1080/10643389.2011.627019
Merlin, 2016, Non-labile phosphorus acquisition by Brachiaria, J. Plant Nutr, 39, 1319, 10.1080/01904167.2015.1109117
Mora–Macías, 2017, Malate–dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate, Proc. Natl. Acad. Sci, 114, E3563, 10.1073/pnas.1701952114
Moscatelli, 2005, Seasonality of soil biological properties in a poplar plantation growing under elevated atmospheric CO2, Appl. Soil Ecol, 30, 162, 10.1016/j.apsoil.2005.02.008
Nannipieri, 1988, Characterization of humus–phosphatase complexes extracted from soil, Soil Biol. Biochem, 20, 683, 10.1016/0038-0717(88)90153-8
Nannipieri, 2011, Role of phosphatase enzymes in soil, Phosphorus in Action, 215, 10.1007/978-3-642-15271-9_9
Noll, 2019, Wide–spread limitation of soil organic nitrogen transformations by substrate availability and not by extracellular enzyme content, Soil Biol. Biochem, 133, 37, 10.1016/j.soilbio.2019.02.016
Nuruzzaman, 2006, Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes, Plant Soil, 281, 109, 10.1007/s11104-005-3936-2
Nwoke, 2008, Organic acids in the rhizosphere and root characteristics of soybean (Glycine max) and cowpea (Vigna unguiculata) in relation to phosphorus uptake in poor savannah soils, Afr. J. Biotechnol, 7, 3620
Oburger, 2018, Sampling root exudates – mission impossible?, Rhizosphere, 6, 116, 10.1016/j.rhisph.2018.06.004
Oburger, 2011, Adsorption and desorption dynamics of citric acid anions in soil, Eur. J. Soil Sci, 62, 733, 10.1111/j.1365-2389.2011.01384.x
Oehl, 2001, Kinetics of microbial phosphorus uptake in cultivated soils, Biol. Fertil. Soils, 34, 31, 10.1007/s003740100362
Ohno, 1996, Green and animal manure–derived dissolved organic matter effects on phosphorus sorption, J. Environ. Qual, 25, 1137, 10.2134/jeq1996.00472425002500050029x
Pascual, 2002, Persistence of immobilized and total urease and phosphatase activities in a soil amended with organic wastes, Biores. Tech, 82, 73, 10.1016/S0960-8524(01)00127-4
Paul, 1989, Soil Microbiology and Biochemistry, 272
Pausch, 2016, Rhizosphere priming of barley with and without root hairs, Soil Biol. Biochem, 100, 74, 10.1016/j.soilbio.2016.05.009
Pearse, 2007, Carboxylate composition of root exudates does not relate consistently to a crop species' ability to use phosphorus from aluminium, iron or calcium phosphate sources, New Phytol, 173, 181, 10.1111/j.1469-8137.2006.01897.x
Pereira, 2019, Trait convergence in photosynthetic nutrient-use efficiency along a 2–million year dune chronosequence in a global biodiversity hotspot, J. Ecol, 107, 2006, 10.1111/1365-2745.13158
Peth, 2008, Three–dimensional quantification of intra-aggregate pore-space features using synchrotron–radiation–based microtomography, Soil Sci. Soc. Am. J, 72, 897, 10.2136/sssaj2007.0130
Pettridge, 2017, Using stable isotopes to explore root–microbe–mineral interactions in soil, Rhizosphere., 1, 10.1016/j.rhisph.2017.04.016
Pistocchi, 2020, In or out of equilibrium? How microbial activity controls the oxygen isotopic composition of phosphate in forest organic horizons with low and high phosphorus availability, Front. Environ. Sci, 8, 1, 10.3389/fenvs.2020.564778
Pizzeghello, 2011, Phosphorus forms and P-sorption properties in three alkaline soils after long-term mineral and manure applications in north-eastern Italy, Agric. Ecosyst. Environ, 141, 58, 10.1016/j.agee.2011.02.011
Quiquampoix, 2005, Enzymatic hydrolysis of organic phosphorus, Organic Phosphorus in the Environment, 89, 10.1079/9780851998220.0089
Quiquampoix, 2002, Enzyme adsorption on soil mineral surfaces and consequences for the catalytic activity, Enzymes in the Environment: Activity, Ecology, and Application, 285, 10.1201/9780203904039.ch11
Ramesh, 2015, GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters, Nat. Commun, 6, 7879, 10.1038/ncomms8879
Reddy, 1980, Phosphorus adsorption-desorption characteristics of two soils utilized for disposal of animal wastes, J. Environ. Qual, 9, 86, 10.2134/jeq1980.00472425000900010020x
Reed, 2015, Incorporating phosphorus cycling into global modeling efforts: a worthwhile, tractable endeavor, New Phytol, 208, 324, 10.1111/nph.13521
Rejsek, 2012, Acid phosphomonoesterase (E.C. 3.1.3.2) location in soil, J Plant Nutr. Soil Sci, 175, 196, 10.1002/jpln.201000139
Renella, 2007, Microbial and hydrolase activity after release of low molecular weight organic compounds by a model root surface in a clayey and a sandy soil, Appl. Soil Ecol, 36, 124, 10.1016/j.apsoil.2007.01.001
Richardson, 2009, Plant mechanisms to optimise access to soil phosphorus, Crop Pasture Sci, 60, 124, 10.1071/CP07125
Rombola, 2014, Identification and enzymatic characterization of acid phosphatase from Burkholderia gladioli, BMC Res. Notes., 7, 221, 10.1186/1756-0500-7-221
Ross–Elliott, 2017, Phloem unloading in Arabidopsis roots is convective and regulated by the phloem–pole pericycle, eLife., 6, e24125, 10.7554/eLife.24125.022
Sasse, 2019, Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass, New Phytol, 222, 1149, 10.1111/nph.15662
Schachtman, 1998, Phosphorus uptake by plants: from soil to cell, J. Plant Physiol, 116, 447, 10.1104/pp.116.2.447
Schimel, 2007, Microbial stress-response physiology and its implications for ecosystem function, Ecol., 88, 1386, 10.1890/06-0219
Schimel, 2003, The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model, Soil Biol. Biochem, 35, 549, 10.1016/S0038-0717(03)00015-4
Shindo, 2002, Adsorption, activity, and kinetics of acid phosphatase as influenced by selected oxides and clay minerals, Soil Sci. Plant Nutr, 48, 763, 10.1080/00380768.2002.10409268
Sinsabaugh, 1994, Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition, Soil Biol. Biochem, 26, 1305, 10.1016/0038-0717(94)90211-9
Song, 2012, Response to water stress of soil enzymes and root exudates from drought and non-drought tolerant corn hybrids at different growth stages, Can. J. Soil Sci, 92, 501, 10.4141/cjss2010-057
Spohn, 2013, Phosphorus mineralization can be driven by microbial need for carbon, Soil Biol. Biochem, 61, 69, 10.1016/j.soilbio.2013.02.013
Steinweg, 2013, Microbial responses to multi-factor climate change: effects on soil enzymes, Front. Microbiol, 4, 146, 10.3389/fmicb.2013.00146
Strobel, 2001, Influence of vegetation on low-molecular-weight carboxylic acids in soil solution—a review, Geoderma, 99, 169, 10.1016/S0016-7061(00)00102-6
Tang, 2021, On the modeling paradigm of plant root nutrient acquisition, Plant Soil, 459, 441, 10.1007/s11104-020-04798-5
Tian, 2018, Arsenate inhibition on kinetic characteristics of alkaline phosphatase as influenced by pH, Ecol. Indic, 85, 1101, 10.1016/j.ecolind.2017.11.041
Tietjen, 2003, Extracellular enzyme–clay mineral complexes: Enzyme adsorption, alteration of enzyme activity, and protection from photodegradation, Aquat. Ecol, 37, 331, 10.1023/B:AECO.0000007044.52801.6b
Treseder, 2001, Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian Rain Forests, Spec. Publ. - Ecol. Soc. Am, 82, 946e954, 10.1890/0012-9658(2001)082[0946:EOSNAO]2.0.CO;2
Turner, 2008, Resource partitioning for soil phosphorus: a hypothesis, J. Ecol, 96, 698, 10.1111/j.1365-2745.2008.01384.x
Turner, 2005, Phosphatase activity in temperate pasture soils: Potential regulation of labile organic phosphorus turnover by phosphodiesterase activity, Sci Total Environ, 344, 27, 10.1016/j.scitotenv.2005.02.003
Vidal, 2018, Linking 3D soil structure and plant-microbe-soil carbon transfer in the rhizosphere, Front. Environ. Sci, 6, 9, 10.3389/fenvs.2018.00009
Wallenstein, 2011, Ecology of extracellular enzyme activities and organic matter degradation in soil: a complex community-driven process, Methods of Soil Enzymology, Vol. 9, 10.2136/sssabookser9.c2
Wang, 2017, Impact of phosphorus on rhizosphere organic anions of wheat at different growth stages under field conditions, AoB Plants., 9, plx008, 10.1093/aobpla/plx008
Wang, 2021, Characterization of sedimentary phosphorus in lake erie and on-site quantification of internal phosphorus loading, Water Res., 188, 116525, 10.1016/j.watres.2020.116525
Wang, 2018, Catalytic efficiency is a better predictor of arsenic toxicity to soil alkaline phosphatase, Ecotoxicol. Environ. Saf, 148, 721, 10.1016/j.ecoenv.2017.11.040
Wang, 2017, Effect of arsenate contamination on free, immobilized and soil alkaline phosphatases: activity, kinetics and thermodynamics, Eur J Soil Sci, 68, 126, 10.1111/ejss.12397
Weintraub, 2005, The seasonal dynamics of amino acids and other nutrients in Alaskan Arctic tundra soils, Biogeochemistry, 73, 359e, 10.1007/s10533-004-0363-z
Weisskopf, 2006, White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition, Plant, Cell Environ, 29, 919, 10.1111/j.1365-3040.2005.01473.x
Williams, 2019, Plant root exudation under drought: implications for ecosystem functioning, New Phytol, 5, 1899, 10.1111/nph.16223
Williams, 2007, Seven years of enhanced water availability influences the physiological, structural, and functional attributes of a soil microbial community, Appl. Soil Ecol., 35, 535, 10.1016/j.apsoil.2006.09.014
Zarebanadkouki, 2019, Root water uptake and its pathways across the root: quantification at the cellular scale, Sci. Rep, 9, 12979, 10.1038/s41598-019-49528-9
Zhang, 2018, Closing the Loop on Phosphorus Loss from Intensive Agricultural Soil: A Microbial Immobilization Solution?, Front. Microbiol, 104, 10.3389/fmicb.2018.00104
Zhao, 2012, Effects of Addition Sequence and pH of Oxalate on the Adsorption and Activity of Acid Phosphatase on Soil Colloids and Minerals, Commun. Soil Sci. Plant Anal, 43, 1436, 10.1080/00103624.2012.670343
Zhu, 2016, Interaction of alkaline phosphatase with minerals and sediments: Activities, kinetics and hydrolysis of organic phosphorus, Colloid Surf. Physicochem. Eng. Asp, 495, 46, 10.1016/j.colsurfa.2016.01.056
Zhuravlev, 2000, The surface chemistry of Amorphous silica. Zhuravlev model, Colloid Surf. Physicochem. Eng. Asp, 173, 1, 10.1016/S0927-7757(00)00556-2
Zickenrott, 2016, An efficient method for the collection of root mucilage from different plant species-a case study on the effect of mucilage on soil water repellency, J. Plant Nutr. Soil Sci, 179, 294, 10.1002/jpln.201500511