Does the combination of citrate and phytase exudation in Nicotiana tabacum promote the acquisition of endogenous soil organic phosphorus?

Background and Aims: Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study investigated the interaction of citrate and phytase exudation in controlling the accumulation of P and depletion of soil organic P by transgenic...

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Published inPlant and soil Vol. 412; no. 1/2; pp. 43 - 59
Main Authors Giles, Courtney D., George, Timothy S., Brown, Lawrie K., Mezeli, Malika M., Richardson, Alan E., Shand, Charles A., Wendler, Renate, Darch, Tegan, Menezes-Blackburn, Daniel, Cooper, Patricia, Stutter, Marc I., Lumsdon, David G., Blackwell, Martin S. A., Wearing, Catherine, Zhang, Hao, Haygarth, Philip M.
Format Journal Article
LanguageEnglish
Published Cham Springer 01.03.2017
Springer International Publishing
Springer Nature B.V
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Abstract Background and Aims: Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study investigated the interaction of citrate and phytase exudation in controlling the accumulation of P and depletion of soil organic P by transgenic Nicotiana tabacum plants. Methods: N. tabacum plant lines including wild-type, vector controls, transgenic plants with single-trait expression of a citrate transporter (A. thaliana frd3) or fungal phytases (phyA: A. niger, P. lycii) and crossed plant lines expressing both traits, were characterized for citrate efflux and phytase exudation. Monocultures and intercropped combinations of single-trait plants were grown in a low available P soil (12 weeks). Plant biomass, shoot P accumulation, rhizosphere soil pH and citrate-extractable-P fractions were determined. Land Equivalent Ratio and complementarity effect was determined in intercropped treatments and multiple-linearregression was used to predict shoot P accumulation based on plant exudation and soil P depletion. Results: Crossed plant lines with co-expression of citrate and phytase accumulated more shoot P than single-trait and intercropped plant treatments. Shoot P accumulation was predicted based on phytase-labile soil P, citrate efflux, and phytase activity (Rsq=0.58, P < .0001). Positive complementarity occurred between intercropped citrate-and phytase-exuding plants, with the greatest gains in shoot P occurring in plant treatments with A. niger phyA expression. Conclusions: We show for the first time that trait synergism associated with the exudation of citrate and phytase by tobacco can be linked to the improved acquisition of P and the depletion of soil organic P.
AbstractList Background and Aims Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study investigated the interaction of citrate and phytase exudation in controlling the accumulation of P and depletion of soil organic P by transgenic Nicotiana tabacum plants. Methods N. tabacum plant lines including wild-type, vector controls, transgenic plants with single-trait expression of a citrate transporter (A. thaliana frd3) or fungal phytases (phyA: A. niger, P. lycii) and crossed plant lines expressing both traits, were characterized for citrate efflux and phytase exudation. Monocultures and intercropped combinations of single-trait plants were grown in a low available P soil (12 weeks). Plant biomass, shoot P accumulation, rhizosphere soil pH and citrate-extractable-P fractions were determined. Land Equivalent Ratio and complementarity effect was determined in intercropped treatments and multiple-linear-regression was used to predict shoot P accumulation based on plant exudation and soil P depletion. Results Crossed plant lines with co-expression of citrate and phytase accumulated more shoot P than single-trait and intercropped plant treatments. Shoot P accumulation was predicted based on phytase-labile soil P, citrate efflux, and phytase activity (Rsq=0.58, P < .0001). Positive complementarity occurred between intercropped citrate- and phytase-exuding plants, with the greatest gains in shoot P occurring in plant treatments with A. niger phyA expression. Conclusions We show for the first time that trait synergism associated with the exudation of citrate and phytase by tobacco can be linked to the improved acquisition of P and the depletion of soil organic P.
Background and Aims: Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study investigated the interaction of citrate and phytase exudation in controlling the accumulation of P and depletion of soil organic P by transgenic Nicotiana tabacum plants. Methods: N. tabacum plant lines including wild-type, vector controls, transgenic plants with single-trait expression of a citrate transporter (A. thaliana frd3) or fungal phytases (phyA: A. niger, P. lycii) and crossed plant lines expressing both traits, were characterized for citrate efflux and phytase exudation. Monocultures and intercropped combinations of single-trait plants were grown in a low available P soil (12 weeks). Plant biomass, shoot P accumulation, rhizosphere soil pH and citrate-extractable-P fractions were determined. Land Equivalent Ratio and complementarity effect was determined in intercropped treatments and multiple-linearregression was used to predict shoot P accumulation based on plant exudation and soil P depletion. Results: Crossed plant lines with co-expression of citrate and phytase accumulated more shoot P than single-trait and intercropped plant treatments. Shoot P accumulation was predicted based on phytase-labile soil P, citrate efflux, and phytase activity (Rsq=0.58, P < .0001). Positive complementarity occurred between intercropped citrate-and phytase-exuding plants, with the greatest gains in shoot P occurring in plant treatments with A. niger phyA expression. Conclusions: We show for the first time that trait synergism associated with the exudation of citrate and phytase by tobacco can be linked to the improved acquisition of P and the depletion of soil organic P.
Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study investigated the interaction of citrate and phytase exudation in controlling the accumulation of P and depletion of soil organic P by transgenic Nicotiana tabacum plants. N. tabacum plant lines including wild-type, vector controls, transgenic plants with single-trait expression of a citrate transporter (A. thaliana frd3) or fungal phytases (phyA: A. niger, P. lycii) and crossed plant lines expressing both traits, were characterized for citrate efflux and phytase exudation. Monocultures and intercropped combinations of single-trait plants were grown in a low available P soil (12 weeks). Plant biomass, shoot P accumulation, rhizosphere soil pH and citrate-extractable-P fractions were determined. Land Equivalent Ratio and complementarity effect was determined in intercropped treatments and multiple-linear-regression was used to predict shoot P accumulation based on plant exudation and soil P depletion. Crossed plant lines with co-expression of citrate and phytase accumulated more shoot P than single-trait and intercropped plant treatments. Shoot P accumulation was predicted based on phytase-labile soil P, citrate efflux, and phytase activity (Rsq=0.58, P < .0001). Positive complementarity occurred between intercropped citrate- and phytase-exuding plants, with the greatest gains in shoot P occurring in plant treatments with A. niger phyA expression. We show for the first time that trait synergism associated with the exudation of citrate and phytase by tobacco can be linked to the improved acquisition of P and the depletion of soil organic P.
Background and Aims Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study investigated the interaction of citrate and phytase exudation in controlling the accumulation of P and depletion of soil organic P by transgenic Nicotiana tabacum plants. Methods N. tabacum plant lines including wild-type, vector controls, transgenic plants with single-trait expression of a citrate transporter ( A. thaliana frd3 ) or fungal phytases ( phyA : A. niger , P. lycii ) and crossed plant lines expressing both traits, were characterized for citrate efflux and phytase exudation. Monocultures and intercropped combinations of single-trait plants were grown in a low available P soil (12 weeks). Plant biomass, shoot P accumulation, rhizosphere soil pH and citrate-extractable-P fractions were determined. Land Equivalent Ratio and complementarity effect was determined in intercropped treatments and multiple-linear-regression was used to predict shoot P accumulation based on plant exudation and soil P depletion. Results Crossed plant lines with co-expression of citrate and phytase accumulated more shoot P than single-trait and intercropped plant treatments. Shoot P accumulation was predicted based on phytase-labile soil P, citrate efflux, and phytase activity (Rsq=0.58, P  < .0001). Positive complementarity occurred between intercropped citrate- and phytase-exuding plants, with the greatest gains in shoot P occurring in plant treatments with A. niger phyA expression. Conclusions We show for the first time that trait synergism associated with the exudation of citrate and phytase by tobacco can be linked to the improved acquisition of P and the depletion of soil organic P.
Audience Academic
Author Shand, Charles A.
Giles, Courtney D.
Cooper, Patricia
Stutter, Marc I.
Richardson, Alan E.
Zhang, Hao
Darch, Tegan
Lumsdon, David G.
Blackwell, Martin S. A.
Wearing, Catherine
Haygarth, Philip M.
Brown, Lawrie K.
Menezes-Blackburn, Daniel
George, Timothy S.
Wendler, Renate
Mezeli, Malika M.
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Cites_doi 10.1016/j.envdev.2013.09.003
10.1007/s11248-007-9138-3
10.1016/j.plantsci.2005.03.006
10.1080/00103629009368377
10.1023/B:PLSO.0000035579.39823.16
10.1104/pp.102.019661
10.1016/j.soilbio.2005.08.021
10.1128/AEM.67.10.4701-4707.2001
10.1007/s003740000249
10.1111/ppl.12150
10.1016/j.geoderma.2015.03.020
10.1071/FP02167
10.1016/j.soilbio.2015.02.019
10.1093/aob/mcu191
10.1016/j.soilbio.2009.12.002
10.1104/pp.15.00145
10.1016/S0168-9452(03)00286-3
10.1371/journal.pone.0060801
10.1111/j.1365-3040.2012.02547.x
10.1080/10643389.2011.627019
10.1046/j.1467-7652.2003.00033.x
10.1021/es2044745
10.1016/S0006-291X(03)00374-7
10.1007/BF00570634
10.1023/A:1022352229863
10.1023/A:1004656205144
10.1093/jxb/ers342
10.1023/A:1021523515707
10.1021/acs.jafc.5b01996
10.1105/tpc.001263
10.1104/pp.111.175414
10.1007/s11104-011-0950-4
10.1023/A:1022389707051
10.1097/SS.0b013e318272f83f
10.1111/j.1365-3040.2004.01225.x
10.1016/j.enzmictec.2004.03.010
10.1007/s11032-011-9628-0
10.1111/j.1365-2389.2006.00767.x
10.1046/j.1365-3040.2000.00557.x
10.1111/j.1467-7652.2004.00116.x
10.1007/s11104-004-1096-4
10.1111/ejss.12119
10.1128/aem.67.10.4701-4707.2001
10.1111/j.1574-6941.2009.00762.x
10.1079/9780851998220.0113
10.1016/j.soilbio.2006.09.029
10.1071/9780643101265
10.1128/AEM.65.2.367-373.1999
10.1023/a:1021523515707
10.21273/HORTSCI.42.5.1107
10.1111/j.1365-2389.2005.00767.x
10.1007/s11104-015-2392-x
ContentType Journal Article
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Springer International Publishing Switzerland 2016
COPYRIGHT 2017 Springer
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ISSN 0032-079X
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Issue 1/2
Keywords Citrate
Rhizosphere
Phytase
Complementarity
Soil organic phosphorus
Root exudation
Language English
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OpenAccessLink https://link.springer.com/content/pdf/10.1007/s11104-016-2884-3.pdf
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ProviderPackageCode CITATION
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PublicationDate 2017-03-01
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  text: 2017-03-01
  day: 01
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PublicationSubtitle An International Journal on Plant-Soil Relationships
PublicationTitle Plant and soil
PublicationTitleAbbrev Plant Soil
PublicationYear 2017
Publisher Springer
Springer International Publishing
Springer Nature B.V
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References Richardson, Hadobas, Hayes (CR39) 2000; 23
George, Gregory, Robinson, Buresh (CR10) 2002; 246
Irving, McLaughlin (CR24) 1990; 21
CR38
Wang, Ye, Ding, Xu (CR52) 2013; 8
Wyss, Brugger, Kronenberger, Rémy, Fimbel, Oesterhelt, Lehmann, van Loon (CR53) 1999; 65
Tang, Leung, Leung, Lim (CR48) 2006; 38
Ullah, Sethumadhavan (CR49) 2003; 303
Hayes, Richardson, Simpson (CR22) 2000; 32
Giaveno, Celi, Richardson, Simpson, Barberis (CR17) 2010; 42
Lynch (CR30) 2007; 42
CR2
CR8
CR7
Ma, Tudor, Butler, Ge, Xi, Bouton, Harrison, Wang (CR33) 2012; 30
Richardson, Lynch, Ryan, Delhaize, Smith, Smith, Harvey, Ryan, Veneklaas, Lambers, Oberson, Culvenor, Simpson (CR41) 2011; 349
CR9
George, Quiquampoix, Simpson, Richardson, Turner, Richardson, Mullaney (CR14) 2007
Stutter, Shand, George, Blackwell, Dixon, Bol, MacKay, Richardson, Condron, Haygarth (CR47) 2015; 257–258
Heffernan (CR23) 1985
George, Simpson, Hadobas, Richardson (CR12) 2005; 3
Ryan, Tibbett, Edmonds-Tibbett, Suriyagoda, Lambers, Cawthray, Pang (CR42) 2012; 35
Hauggaard-Nielsen, Jensen, Lambers, Colmer (CR21) 2005
Vats, Banerjee (CR50) 2004; 35
Shen, Li, Mi, Li, Yuan, Jiang, Zhang (CR45) 2013; 64
Schunmann, Surin, Waterhouse (CR44) 2003; 30
Greiner, Turner, Richardson, Mullaney (CR20) 2007
Giles, Cade-Menun, He, Zhang (CR18) 2014
George, Turner, Gregory, Cade-Menun, Richardson (CR13) 2006; 57
Ryan, James, Weligama, Delhaize, Rattey, Lewis, Bovill, McDonald, Rathjen, Wang, Fettell, Richardson (CR43) 2014; 151
CR16
CR15
Lynch, Ho (CR32) 2005; 269
Walker, Bais, Grotewold, Vivanco (CR51) 2003; 132
Giles, Richardson, Druschel, Hill (CR19) 2012; 177
Yan, Liu, Li, Liu, Feng, Sparks (CR54) 2014; 65
Clarholm, Skyllberg, Rosling (CR4) 2015; 84
Lung, Chan, Yip, Wang, Yeung, Lim (CR29) 2005; 169
Condron, Spears, Haygarth, Turner, Richardson (CR5) 2013; 8
Connolly, Fett, Guerinot (CR6) 2002; 14
Zimmermann, Zardi, Lehmann, Zeder, Amrhein, Frossard, Bucher (CR57) 2003; 1
Lassen, Breinholt, Østergaard, Brugger, Bischoff, Wyss, Fuglsang (CR25) 2001; 67
Chen, Xue, Chen, Yao, Yang, Ma, Fan, Zhao, Tarczynski, Shi (CR3) 2008; 17
Bolan, Naidu, Mahimairaja, Baskaran (CR1) 1994; 18
George, Richardson, Hadobas, Simpson (CR11) 2004; 27
Li, Tang, Rengel, Zhang (CR28) 2004; 261
Richardson, Hadobas, Hayes (CR40) 2001; 25
Li, Tang, Rengel, Zhang (CR27) 2003; 248
Lynch (CR31) 2011; 156
Stutter, Shand, George, Blackwell, Bol, MacKay, Richardson, Condron, Turner, Haygarth (CR46) 2012; 46
Li, Yang, Li, Zhang, Christie (CR26) 1999; 212
Zhang, Li (CR55) 2003; 248
Menezes-Blackburn, Jorquera, Greiner, Gianfreda, Mora (CR34) 2013; 43
Mudge, Smith, Richardson (CR37) 2003; 165
Zhang, Postma, York, Lynch (CR56) 2014; 114
Menezes-Blackburn, Gabler, Greiner (CR35) 2015; 63
Miguel, Postma, Lynch (CR36) 2015; 167
TS George (2884_CR12) 2005; 3
L Li (2884_CR26) 1999; 212
CD Giles (2884_CR19) 2012; 177
YP Yan (2884_CR54) 2014; 65
PR Ryan (2884_CR43) 2014; 151
MH Ryan (2884_CR42) 2012; 35
MI Stutter (2884_CR47) 2015; 257–258
Y Wang (2884_CR52) 2013; 8
L Li (2884_CR28) 2004; 261
MA Miguel (2884_CR36) 2015; 167
PHD Schunmann (2884_CR44) 2003; 30
CD Giles (2884_CR18) 2014
B Heffernan (2884_CR23) 1985
J Shen (2884_CR45) 2013; 64
2884_CR15
2884_CR16
NS Bolan (2884_CR1) 1994; 18
AE Richardson (2884_CR41) 2011; 349
P Vats (2884_CR50) 2004; 35
D Menezes-Blackburn (2884_CR35) 2015; 63
JP Lynch (2884_CR31) 2011; 156
SF Lassen (2884_CR25) 2001; 67
D Menezes-Blackburn (2884_CR34) 2013; 43
H Hauggaard-Nielsen (2884_CR21) 2005
TS George (2884_CR11) 2004; 27
JP Lynch (2884_CR32) 2005; 269
AE Richardson (2884_CR39) 2000; 23
MI Stutter (2884_CR46) 2012; 46
F Zhang (2884_CR55) 2003; 248
R Chen (2884_CR3) 2008; 17
M Clarholm (2884_CR4) 2015; 84
JE Hayes (2884_CR22) 2000; 32
J Tang (2884_CR48) 2006; 38
T George (2884_CR14) 2007
X-F Ma (2884_CR33) 2012; 30
C Zhang (2884_CR56) 2014; 114
EL Connolly (2884_CR6) 2002; 14
TS George (2884_CR10) 2002; 246
AHJ Ullah (2884_CR49) 2003; 303
L Li (2884_CR27) 2003; 248
AE Richardson (2884_CR40) 2001; 25
2884_CR2
GCJ Irving (2884_CR24) 1990; 21
C Giaveno (2884_CR17) 2010; 42
2884_CR7
2884_CR8
2884_CR9
R Greiner (2884_CR20) 2007
SR Mudge (2884_CR37) 2003; 165
2884_CR38
LM Condron (2884_CR5) 2013; 8
S-C Lung (2884_CR29) 2005; 169
P Zimmermann (2884_CR57) 2003; 1
TS George (2884_CR13) 2006; 57
M Wyss (2884_CR53) 1999; 65
JP Lynch (2884_CR30) 2007; 42
TS Walker (2884_CR51) 2003; 132
References_xml – volume: 8
  start-page: 147
  year: 2013
  end-page: 148
  ident: CR5
  article-title: Role of legacy phosphorus in improving global phosphorus-use efficiency
  publication-title: Environ Dev
  doi: 10.1016/j.envdev.2013.09.003
– volume: 17
  start-page: 633
  year: 2008
  end-page: 643
  ident: CR3
  article-title: Transgenic maize plants expressing a fungal phytase gene
  publication-title: Transgenic research
  doi: 10.1007/s11248-007-9138-3
– volume: 169
  start-page: 341
  year: 2005
  end-page: 349
  ident: CR29
  article-title: Secretion of beta-propeller phytase from tobacco and Arabidopsis roots enhances phosphorus utilization
  publication-title: Plant Sci
  doi: 10.1016/j.plantsci.2005.03.006
– ident: CR16
– volume: 21
  start-page: 2245
  year: 1990
  end-page: 2255
  ident: CR24
  article-title: A rapid and simple field test for phosphorus in Olsen and Bray no. 1 extracts of soil
  publication-title: Commun Soil Sci Plant Anal
  doi: 10.1080/00103629009368377
– year: 2005
  ident: CR21
  article-title: Facilitative root interactions in intercrops
  publication-title: Root physiology: from Gene to function
– volume: 261
  start-page: 29
  year: 2004
  end-page: 37
  ident: CR28
  article-title: Calcium, magnesium and microelement uptake as affected by phosphorus sources and interspecific root interactions between wheat and chickpea
  publication-title: Plant Soil
  doi: 10.1023/B:PLSO.0000035579.39823.16
– volume: 132
  start-page: 44
  year: 2003
  end-page: 51
  ident: CR51
  article-title: Root exudation and rhizosphere biology
  publication-title: Plant Physiol
  doi: 10.1104/pp.102.019661
– volume: 38
  start-page: 1316
  year: 2006
  end-page: 1324
  ident: CR48
  article-title: Hydrolysis of precipitated phytate by three distinct families of phytases
  publication-title: Soil Biol Biochem
  doi: 10.1016/j.soilbio.2005.08.021
– ident: CR8
– volume: 67
  start-page: 4701
  year: 2001
  end-page: 4707
  ident: CR25
  article-title: Expression, Gene cloning, and characterization of five novel Phytases from four basidiomycete fungi: Peniophora lycii, Agrocybe pediades, a Ceriporia sp., and Trametes pubescens
  publication-title: Appl Environ Microbiol
  doi: 10.1128/AEM.67.10.4701-4707.2001
– volume: 32
  start-page: 279
  year: 2000
  end-page: 286
  ident: CR22
  article-title: Components of organic phosphorus in soil extracts that are hydrolysed by phytase and acid phosphatase
  publication-title: Biol Fertil Soils
  doi: 10.1007/s003740000249
– volume: 151
  start-page: 230
  year: 2014
  end-page: 242
  ident: CR43
  article-title: Can citrate efflux from roots improve phosphorus uptake by plants? Testing the hypothesis with near-isogenic lines of wheat
  publication-title: Physiol Plant
  doi: 10.1111/ppl.12150
– volume: 257–258
  start-page: 29
  year: 2015
  end-page: 39
  ident: CR47
  article-title: Land use and soil factors affecting accumulation of phosphorus species in temperate soils
  publication-title: Geoderma
  doi: 10.1016/j.geoderma.2015.03.020
– volume: 30
  start-page: 453
  year: 2003
  end-page: 460
  ident: CR44
  article-title: A suite of novel promoters and terminators for plant biotechnology. II. The pPLEX series for use in monocots
  publication-title: Funct Plant Biol
  doi: 10.1071/FP02167
– volume: 65
  start-page: 367
  year: 1999
  end-page: 373
  ident: CR53
  article-title: Biochemical characterization of fungal Phytases (myo-inositol Hexakisphosphate Phosphohydrolases): catalytic properties
  publication-title: Appl Environ Microbiol
– volume: 84
  start-page: 168
  year: 2015
  end-page: 176
  ident: CR4
  article-title: Organic acid induced release of nutrients from metal-stabilized soil organic matter – The unbutton model
  publication-title: Soil Biol Biochem
  doi: 10.1016/j.soilbio.2015.02.019
– volume: 114
  start-page: 1719
  year: 2014
  end-page: 1733
  ident: CR56
  article-title: Root foraging elicits niche complementarity-dependent yield advantage in the ancient ‘three sisters’ (maize/bean/squash) polyculture
  publication-title: Ann Bot
  doi: 10.1093/aob/mcu191
– ident: CR15
– volume: 42
  start-page: 491
  year: 2010
  end-page: 498
  ident: CR17
  article-title: Interaction of phytases with minerals and availability of substrate affect the hydrolysis of inositol phosphates
  publication-title: Soil Biol Biochem
  doi: 10.1016/j.soilbio.2009.12.002
– volume: 42
  start-page: 1107
  year: 2007
  end-page: 1109
  ident: CR30
  article-title: Rhizoeconomics: the roots of shoot growth limitations
  publication-title: Hortscience
– volume: 167
  start-page: 1430
  year: 2015
  end-page: 1439
  ident: CR36
  article-title: Phene synergism between root hair length and basal root growth Angle for phosphorus acquisition
  publication-title: Plant Physiol
  doi: 10.1104/pp.15.00145
– volume: 165
  start-page: 871
  year: 2003
  end-page: 878
  ident: CR37
  article-title: Root-specific and phosphate-regulated expression of phytase under the control of a phosphate transporter promoter enables Arabidopsis to grow on phytate as a sole P source
  publication-title: Plant Sci
  doi: 10.1016/S0168-9452(03)00286-3
– volume: 8
  start-page: e60801
  year: 2013
  end-page: e60801
  ident: CR52
  article-title: Overexpression of phyA and appA genes improves soil organic phosphorus utilisation and seed Phytase activity in
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0060801
– volume: 35
  start-page: 2170
  year: 2012
  end-page: 2180
  ident: CR42
  article-title: Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition
  publication-title: Plant Cell Environ
  doi: 10.1111/j.1365-3040.2012.02547.x
– ident: CR9
– volume: 43
  start-page: 916
  year: 2013
  end-page: 954
  ident: CR34
  article-title: Phytases and Phytase-labile organic phosphorus in manures and soils
  publication-title: Crit Rev Environ Sci Technol
  doi: 10.1080/10643389.2011.627019
– volume: 1
  start-page: 353
  year: 2003
  end-page: 360
  ident: CR57
  article-title: Engineering the root–soil interface via targeted expression of a synthetic phytase gene in trichoblasts
  publication-title: Plant Biotechnol J
  doi: 10.1046/j.1467-7652.2003.00033.x
– volume: 46
  start-page: 1977
  year: 2012
  end-page: 1978
  ident: CR46
  article-title: Recovering phosphorus from soil: a root solution?
  publication-title: Environ Sci Technol
  doi: 10.1021/es2044745
– volume: 303
  start-page: 463
  year: 2003
  end-page: 468
  ident: CR49
  article-title: PhyA gene product of Aspergillus ficuum and Peniophora lycii produces dissimilar phytases
  publication-title: Biochem Biophys Res Commun
  doi: 10.1016/S0006-291X(03)00374-7
– volume: 18
  start-page: 311
  year: 1994
  end-page: 319
  ident: CR1
  article-title: Influence of low-molecular-weight organic acids on the solubilization of phosphate
  publication-title: Biology and Fertility of Soils
  doi: 10.1007/BF00570634
– volume: 248
  start-page: 305
  year: 2003
  end-page: 312
  ident: CR55
  article-title: Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency
  publication-title: Plant Soil
  doi: 10.1023/A:1022352229863
– volume: 212
  start-page: 105
  year: 1999
  end-page: 114
  ident: CR26
  article-title: Interspecific complementary and competitive interactions between intercropped maize and faba bean
  publication-title: Plant Soil
  doi: 10.1023/A:1004656205144
– volume: 64
  start-page: 1181
  year: 2013
  end-page: 1192
  ident: CR45
  article-title: Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China
  publication-title: J Exp Bot
  doi: 10.1093/jxb/ers342
– year: 2007
  ident: CR14
  article-title: Interactions Between Phytases and Soil Constituents: Implicatins for the Hydrolysis of Inositol Phosphates
  publication-title: Inositol Phosphates: Linking Agriculture and the Environment
– volume: 246
  start-page: 65
  year: 2002
  end-page: 73
  ident: CR10
  article-title: Changes in phosphorus concentrations and pH in the rhizosphere of some agroforestry and crop species
  publication-title: Plant and Soil
  doi: 10.1023/A:1021523515707
– ident: CR2
– volume: 63
  start-page: 6142
  year: 2015
  end-page: 6149
  ident: CR35
  article-title: Performance of seven commercial Phytases in an in vitro simulation of poultry digestive tract
  publication-title: J Agric Food Chem
  doi: 10.1021/acs.jafc.5b01996
– volume: 14
  start-page: 1347
  year: 2002
  end-page: 1357
  ident: CR6
  article-title: Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation
  publication-title: The Plant cell
  doi: 10.1105/tpc.001263
– volume: 156
  start-page: 1041
  year: 2011
  end-page: 1049
  ident: CR31
  article-title: Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops
  publication-title: Plant Physiol
  doi: 10.1104/pp.111.175414
– volume: 349
  start-page: 121
  year: 2011
  end-page: 156
  ident: CR41
  article-title: Plant and microbial strategies to improve the phosphorus efficiency of agriculture
  publication-title: Plant Soil
  doi: 10.1007/s11104-011-0950-4
– volume: 248
  start-page: 297
  year: 2003
  end-page: 303
  ident: CR27
  article-title: Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source
  publication-title: Plant Soil
  doi: 10.1023/A:1022389707051
– volume: 177
  start-page: 591
  year: 2012
  end-page: 598
  ident: CR19
  article-title: Organic anion-driven solubilization of precipitated and sorbed phytate improves hydrolysis by phytases and bioavailability to
  publication-title: Soil Sci
  doi: 10.1097/SS.0b013e318272f83f
– volume: 27
  start-page: 1351
  year: 2004
  end-page: 1361
  ident: CR11
  article-title: Characterization of transgenic L. wwhich expresses phyA and releases extracellular phytase: growth and P nutrition in laboratory media and soil
  publication-title: Plant, Cell & Environment
  doi: 10.1111/j.1365-3040.2004.01225.x
– volume: 35
  start-page: 3
  year: 2004
  end-page: 14
  ident: CR50
  article-title: Production studies and catalytic properties of phytases (myo-inositolhexakisphosphate phosphohydrolases): an overview
  publication-title: Enzym Micro Technol
  doi: 10.1016/j.enzmictec.2004.03.010
– volume: 30
  start-page: 377
  year: 2012
  end-page: 391
  ident: CR33
  article-title: Transgenic expression of phytase and acid phosphatase genes in alfalfa (Medicagosativa) leads to improved phosphate uptake in natural soils
  publication-title: Mol Breed
  doi: 10.1007/s11032-011-9628-0
– ident: CR38
– volume: 25
  start-page: 641
  year: 2001
  end-page: 649
  ident: CR40
  article-title: Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate
  publication-title: Plant J CellMol Biol
– volume: 57
  start-page: 47
  year: 2006
  end-page: 57
  ident: CR13
  article-title: Depletion of organic phosphorus from Oxisols in relation to phosphatase activities in the rhizosphere
  publication-title: Eur J Soil Sci
  doi: 10.1111/j.1365-2389.2006.00767.x
– year: 2007
  ident: CR20
  article-title: Phytate-degrading enzymes: regulation of synthesis in microorganisms and plants
  publication-title: Inositol phosphates: linking agriculture and the environment
– volume: 23
  start-page: 397
  year: 2000
  end-page: 405
  ident: CR39
  article-title: Acid phosphomonoesterase and phytase activities of wheat ( L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture
  publication-title: Plant Cell Environ
  doi: 10.1046/j.1365-3040.2000.00557.x
– ident: CR7
– volume: 3
  start-page: 129
  year: 2005
  end-page: 140
  ident: CR12
  article-title: Expression of a fungal phytase gene in improves phosphorus nutrition of plants grown in amended soils
  publication-title: Plant Biotechnol J
  doi: 10.1111/j.1467-7652.2004.00116.x
– year: 1985
  ident: CR23
  publication-title: A handbook of methods of inorganic chemical analysis for forest soils, foliage and water
– year: 2014
  ident: CR18
  article-title: Phytate in animal manure and soils: abundance, cycling and bioavailability
  publication-title: Applied manure and nutrient chemistry for sustainable agriculture and environment
– volume: 269
  start-page: 45
  year: 2005
  end-page: 56
  ident: CR32
  article-title: Rhizoeconomics: carbon costs of phosphorus acquisition
  publication-title: Plant Soil
  doi: 10.1007/s11104-004-1096-4
– volume: 65
  start-page: 308
  year: 2014
  end-page: 317
  ident: CR54
  article-title: Sorption and desorption characteristics of organic phosphates of different structures on aluminium (oxyhydr)oxides
  publication-title: Eur J Soil Sci
  doi: 10.1111/ejss.12119
– volume: 67
  start-page: 4701
  year: 2001
  ident: 2884_CR25
  publication-title: Appl Environ Microbiol
  doi: 10.1128/aem.67.10.4701-4707.2001
– volume: 32
  start-page: 279
  year: 2000
  ident: 2884_CR22
  publication-title: Biol Fertil Soils
  doi: 10.1007/s003740000249
– volume: 248
  start-page: 297
  year: 2003
  ident: 2884_CR27
  publication-title: Plant Soil
  doi: 10.1023/A:1022389707051
– volume: 261
  start-page: 29
  year: 2004
  ident: 2884_CR28
  publication-title: Plant Soil
  doi: 10.1023/B:PLSO.0000035579.39823.16
– ident: 2884_CR16
  doi: 10.1111/j.1574-6941.2009.00762.x
– volume: 349
  start-page: 121
  year: 2011
  ident: 2884_CR41
  publication-title: Plant Soil
  doi: 10.1007/s11104-011-0950-4
– volume: 14
  start-page: 1347
  year: 2002
  ident: 2884_CR6
  publication-title: The Plant cell
  doi: 10.1105/tpc.001263
– ident: 2884_CR2
  doi: 10.1079/9780851998220.0113
– volume: 257–258
  start-page: 29
  year: 2015
  ident: 2884_CR47
  publication-title: Geoderma
  doi: 10.1016/j.geoderma.2015.03.020
– volume: 8
  start-page: 147
  year: 2013
  ident: 2884_CR5
  publication-title: Environ Dev
  doi: 10.1016/j.envdev.2013.09.003
– volume-title: Root physiology: from Gene to function
  year: 2005
  ident: 2884_CR21
– volume: 25
  start-page: 641
  year: 2001
  ident: 2884_CR40
  publication-title: Plant J CellMol Biol
– volume: 21
  start-page: 2245
  year: 1990
  ident: 2884_CR24
  publication-title: Commun Soil Sci Plant Anal
  doi: 10.1080/00103629009368377
– volume: 35
  start-page: 3
  year: 2004
  ident: 2884_CR50
  publication-title: Enzym Micro Technol
  doi: 10.1016/j.enzmictec.2004.03.010
– volume-title: A handbook of methods of inorganic chemical analysis for forest soils, foliage and water
  year: 1985
  ident: 2884_CR23
– volume: 64
  start-page: 1181
  year: 2013
  ident: 2884_CR45
  publication-title: J Exp Bot
  doi: 10.1093/jxb/ers342
– volume: 165
  start-page: 871
  year: 2003
  ident: 2884_CR37
  publication-title: Plant Sci
  doi: 10.1016/S0168-9452(03)00286-3
– volume: 18
  start-page: 311
  year: 1994
  ident: 2884_CR1
  publication-title: Biology and Fertility of Soils
  doi: 10.1007/BF00570634
– ident: 2884_CR15
  doi: 10.1016/j.soilbio.2006.09.029
– ident: 2884_CR38
  doi: 10.1071/9780643101265
– volume: 17
  start-page: 633
  year: 2008
  ident: 2884_CR3
  publication-title: Transgenic research
  doi: 10.1007/s11248-007-9138-3
– volume: 63
  start-page: 6142
  year: 2015
  ident: 2884_CR35
  publication-title: J Agric Food Chem
  doi: 10.1021/acs.jafc.5b01996
– volume: 35
  start-page: 2170
  year: 2012
  ident: 2884_CR42
  publication-title: Plant Cell Environ
  doi: 10.1111/j.1365-3040.2012.02547.x
– volume: 46
  start-page: 1977
  year: 2012
  ident: 2884_CR46
  publication-title: Environ Sci Technol
  doi: 10.1021/es2044745
– volume: 65
  start-page: 367
  year: 1999
  ident: 2884_CR53
  publication-title: Appl Environ Microbiol
  doi: 10.1128/AEM.65.2.367-373.1999
– volume: 246
  start-page: 65
  year: 2002
  ident: 2884_CR10
  publication-title: Plant and Soil
  doi: 10.1023/a:1021523515707
– volume: 167
  start-page: 1430
  year: 2015
  ident: 2884_CR36
  publication-title: Plant Physiol
  doi: 10.1104/pp.15.00145
– volume: 8
  start-page: e60801
  year: 2013
  ident: 2884_CR52
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0060801
– volume: 1
  start-page: 353
  year: 2003
  ident: 2884_CR57
  publication-title: Plant Biotechnol J
  doi: 10.1046/j.1467-7652.2003.00033.x
– volume: 42
  start-page: 1107
  year: 2007
  ident: 2884_CR30
  publication-title: Hortscience
  doi: 10.21273/HORTSCI.42.5.1107
– ident: 2884_CR7
– volume: 30
  start-page: 453
  year: 2003
  ident: 2884_CR44
  publication-title: Funct Plant Biol
  doi: 10.1071/FP02167
– volume-title: Applied manure and nutrient chemistry for sustainable agriculture and environment
  year: 2014
  ident: 2884_CR18
– volume: 132
  start-page: 44
  year: 2003
  ident: 2884_CR51
  publication-title: Plant Physiol
  doi: 10.1104/pp.102.019661
– volume: 43
  start-page: 916
  year: 2013
  ident: 2884_CR34
  publication-title: Crit Rev Environ Sci Technol
  doi: 10.1080/10643389.2011.627019
– volume-title: Inositol Phosphates: Linking Agriculture and the Environment
  year: 2007
  ident: 2884_CR14
– volume: 57
  start-page: 47
  year: 2006
  ident: 2884_CR13
  publication-title: Eur J Soil Sci
  doi: 10.1111/j.1365-2389.2005.00767.x
– volume: 269
  start-page: 45
  year: 2005
  ident: 2884_CR32
  publication-title: Plant Soil
  doi: 10.1007/s11104-004-1096-4
– volume: 3
  start-page: 129
  year: 2005
  ident: 2884_CR12
  publication-title: Plant Biotechnol J
  doi: 10.1111/j.1467-7652.2004.00116.x
– volume: 84
  start-page: 168
  year: 2015
  ident: 2884_CR4
  publication-title: Soil Biol Biochem
  doi: 10.1016/j.soilbio.2015.02.019
– volume: 248
  start-page: 305
  year: 2003
  ident: 2884_CR55
  publication-title: Plant Soil
  doi: 10.1023/A:1022352229863
– volume: 27
  start-page: 1351
  year: 2004
  ident: 2884_CR11
  publication-title: Plant, Cell & Environment
  doi: 10.1111/j.1365-3040.2004.01225.x
– volume: 169
  start-page: 341
  year: 2005
  ident: 2884_CR29
  publication-title: Plant Sci
  doi: 10.1016/j.plantsci.2005.03.006
– volume: 23
  start-page: 397
  year: 2000
  ident: 2884_CR39
  publication-title: Plant Cell Environ
  doi: 10.1046/j.1365-3040.2000.00557.x
– volume: 156
  start-page: 1041
  year: 2011
  ident: 2884_CR31
  publication-title: Plant Physiol
  doi: 10.1104/pp.111.175414
– volume: 114
  start-page: 1719
  year: 2014
  ident: 2884_CR56
  publication-title: Ann Bot
  doi: 10.1093/aob/mcu191
– volume: 65
  start-page: 308
  year: 2014
  ident: 2884_CR54
  publication-title: Eur J Soil Sci
  doi: 10.1111/ejss.12119
– volume: 30
  start-page: 377
  year: 2012
  ident: 2884_CR33
  publication-title: Mol Breed
  doi: 10.1007/s11032-011-9628-0
– ident: 2884_CR8
  doi: 10.1007/s11104-015-2392-x
– volume: 42
  start-page: 491
  year: 2010
  ident: 2884_CR17
  publication-title: Soil Biol Biochem
  doi: 10.1016/j.soilbio.2009.12.002
– volume-title: Inositol phosphates: linking agriculture and the environment
  year: 2007
  ident: 2884_CR20
– volume: 212
  start-page: 105
  year: 1999
  ident: 2884_CR26
  publication-title: Plant Soil
  doi: 10.1023/A:1004656205144
– volume: 38
  start-page: 1316
  year: 2006
  ident: 2884_CR48
  publication-title: Soil Biol Biochem
  doi: 10.1016/j.soilbio.2005.08.021
– volume: 151
  start-page: 230
  year: 2014
  ident: 2884_CR43
  publication-title: Physiol Plant
  doi: 10.1111/ppl.12150
– volume: 303
  start-page: 463
  year: 2003
  ident: 2884_CR49
  publication-title: Biochem Biophys Res Commun
  doi: 10.1016/S0006-291X(03)00374-7
– ident: 2884_CR9
– volume: 177
  start-page: 591
  year: 2012
  ident: 2884_CR19
  publication-title: Soil Sci
  doi: 10.1097/SS.0b013e318272f83f
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Snippet Background and Aims: Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study...
Background and Aims Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study...
Background and Aims Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study...
Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study investigated the...
BACKGROUND AND AIMS: Plant acquisition of endogenous forms of soil phosphorus (P) could reduce external P requirements in agricultural systems. This study...
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SubjectTerms Accumulation
Agriculture
Biomedical and Life Sciences
citrates
Citric acid
Ecology
Environmental aspects
Enzymes
exudation
Farming systems
fungi
intercropping
Life Sciences
Monoculture
Nicotiana tabacum
Organic phosphorus
Phosphatase
Phosphatases
Phosphorus
Physiological aspects
phytases
phytomass
Plant biomass
Plant Physiology
Plant Sciences
Regular Article
Rhizosphere
Soil pH
Soil phosphorus
Soil Science & Conservation
Soils
Synergism
Tobacco
Tobacco (Plant)
Transgenic plants
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Title Does the combination of citrate and phytase exudation in Nicotiana tabacum promote the acquisition of endogenous soil organic phosphorus?
URI https://www.jstor.org/stable/44245252
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