Phosphorus acquisition by citrate‐ and phytase‐exuding Nicotiana tabacum plant mixtures depends on soil phosphorus availability and root intermingling

Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced in a P‐deficient soil. To test the importance of root intermingling in the interaction of citrate and phytase exudates, Nicotiana tabacum plan...

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Published inPhysiologia plantarum Vol. 163; no. 3; pp. 356 - 371
Main Authors Giles, Courtney D., Richardson, Alan E., Cade‐Menun, Barbara J., Mezeli, Malika M., Brown, Lawrie K., Menezes‐Blackburn, Daniel, Darch, Tegan, Blackwell, Martin S.A., Shand, Charles A., Stutter, Marc I., Wendler, Renate, Cooper, Patricia, Lumsdon, David G., Wearing, Catherine, Zhang, Hao, Haygarth, Philip M., George, Timothy S.
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LanguageEnglish
Published Oxford, UK Blackwell Publishing Ltd 01.07.2018
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Abstract Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced in a P‐deficient soil. To test the importance of root intermingling in the interaction of citrate and phytase exudates, Nicotiana tabacum plant‐lines with constitutive expression of heterologous citrate (Cit) or fungal phytase (Phy) exudation traits were grown under two root treatments (roots separated or intermingled) and in two soils with contrasting soil P availability. Complementarity of plant mixtures varying in citrate efflux rate and mobility of the expressed phytase in soil was determined based on plant biomass and P accumulation. Soil P composition was evaluated using solution 31P NMR spectroscopy. In the soil with limited available P, positive complementarity occurred in Cit + Phy mixtures with roots intermingled. Root separation eliminated positive interactions in mixtures expressing the less mobile phytase (Aspergillus niger PhyA) whereas positive complementarity persisted in mixtures that expressed the more mobile phytase (Peniophora lycii PhyA). Soils from Cit + Phy mixtures contained less inorganic P and more organic P compared to monocultures. Exudate‐specific strategies for the acquisition of soil P were most effective in P‐limited soil and depended on citrate efflux rate and the relative mobility of the expressed phytase in soil. Plant growth and soil P utilization in plant systems with complementary exudation strategies are expected to be greatest where exudates persist in soil and are expressed synchronously in space and time.
AbstractList Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced in a P deficient soil. To test the importance of root intermingling in the interaction of citrate and phytase exudates, Nicotiana tabacum plant-lines with constitutive expression of heterologous citrate (Cit) or fungal phytase (Phy) exudation traits were grown under two root treatments (roots separated or intermingled) and in two soils with contrasting soil P availability. Complementarity of plant mixtures varying in citrate efflux rate and mobility of the expressed phytase in soil was determined based on plant biomass and P accumulation. Soil P composition was evaluated using solution P NMR spectroscopy. In the soil with limited available P, positive complementarity occurred in Cit+Phy mixtures with roots intermingled. Root separation eliminated positive interactions in mixtures expressing the less mobile phytase (Aspergillus niger PhyA) whereas positive complementarity persisted in mixtures that expressed the more mobile phytase (Peniophora lycii PhyA). Soils from Cit+Phy mixtures contained less inorganic P and more organic P compared to monocultures. Exudate-specific strategies for the acquisition of soil P were most effective in P-limited soil and depended on citrate efflux rate and the relative mobility of the expressed phytase in soil. Plant growth and soil P utilization in plant systems with complementary exudation strategies are expected to be greatest where exudates persist in soil and are expressed synchronously in space and time.
Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced in a P‐deficient soil. To test the importance of root intermingling in the interaction of citrate and phytase exudates, Nicotiana tabacum plant‐lines with constitutive expression of heterologous citrate (Cit) or fungal phytase (Phy) exudation traits were grown under two root treatments (roots separated or intermingled) and in two soils with contrasting soil P availability. Complementarity of plant mixtures varying in citrate efflux rate and mobility of the expressed phytase in soil was determined based on plant biomass and P accumulation. Soil P composition was evaluated using solution 31P NMR spectroscopy. In the soil with limited available P, positive complementarity occurred in Cit + Phy mixtures with roots intermingled. Root separation eliminated positive interactions in mixtures expressing the less mobile phytase (Aspergillus niger PhyA) whereas positive complementarity persisted in mixtures that expressed the more mobile phytase (Peniophora lycii PhyA). Soils from Cit + Phy mixtures contained less inorganic P and more organic P compared to monocultures. Exudate‐specific strategies for the acquisition of soil P were most effective in P‐limited soil and depended on citrate efflux rate and the relative mobility of the expressed phytase in soil. Plant growth and soil P utilization in plant systems with complementary exudation strategies are expected to be greatest where exudates persist in soil and are expressed synchronously in space and time.
Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced in a P‐deficient soil. To test the importance of root intermingling in the interaction of citrate and phytase exudates, Nicotiana tabacum plant‐lines with constitutive expression of heterologous citrate (Cit) or fungal phytase (Phy) exudation traits were grown under two root treatments (roots separated or intermingled) and in two soils with contrasting soil P availability. Complementarity of plant mixtures varying in citrate efflux rate and mobility of the expressed phytase in soil was determined based on plant biomass and P accumulation. Soil P composition was evaluated using solution 31 P NMR spectroscopy. In the soil with limited available P, positive complementarity occurred in Cit + Phy mixtures with roots intermingled. Root separation eliminated positive interactions in mixtures expressing the less mobile phytase ( Aspergillus niger PhyA ) whereas positive complementarity persisted in mixtures that expressed the more mobile phytase ( Peniophora lycii PhyA ). Soils from Cit + Phy mixtures contained less inorganic P and more organic P compared to monocultures. Exudate‐specific strategies for the acquisition of soil P were most effective in P‐limited soil and depended on citrate efflux rate and the relative mobility of the expressed phytase in soil. Plant growth and soil P utilization in plant systems with complementary exudation strategies are expected to be greatest where exudates persist in soil and are expressed synchronously in space and time.
Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced in a P‐deficient soil. To test the importance of root intermingling in the interaction of citrate and phytase exudates, Nicotiana tabacum plant‐lines with constitutive expression of heterologous citrate (Cit) or fungal phytase (Phy) exudation traits were grown under two root treatments (roots separated or intermingled) and in two soils with contrasting soil P availability. Complementarity of plant mixtures varying in citrate efflux rate and mobility of the expressed phytase in soil was determined based on plant biomass and P accumulation. Soil P composition was evaluated using solution ³¹P NMR spectroscopy. In the soil with limited available P, positive complementarity occurred in Cit + Phy mixtures with roots intermingled. Root separation eliminated positive interactions in mixtures expressing the less mobile phytase (Aspergillus niger PhyA) whereas positive complementarity persisted in mixtures that expressed the more mobile phytase (Peniophora lycii PhyA). Soils from Cit + Phy mixtures contained less inorganic P and more organic P compared to monocultures. Exudate‐specific strategies for the acquisition of soil P were most effective in P‐limited soil and depended on citrate efflux rate and the relative mobility of the expressed phytase in soil. Plant growth and soil P utilization in plant systems with complementary exudation strategies are expected to be greatest where exudates persist in soil and are expressed synchronously in space and time.
Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced in a P deficient soil. To test the importance of root intermingling in the interaction of citrate and phytase exudates, Nicotiana tabacum plant-lines with constitutive expression of heterologous citrate (Cit) or fungal phytase (Phy) exudation traits were grown under two root treatments (roots separated or intermingled) and in two soils with contrasting soil P availability. Complementarity of plant mixtures varying in citrate efflux rate and mobility of the expressed phytase in soil was determined based on plant biomass and P accumulation. Soil P composition was evaluated using solution 31 P NMR spectroscopy. In the soil with limited available P, positive complementarity occurred in Cit+Phy mixtures with roots intermingled. Root separation eliminated positive interactions in mixtures expressing the less mobile phytase (Aspergillus niger PhyA) whereas positive complementarity persisted in mixtures that expressed the more mobile phytase (Peniophora lycii PhyA). Soils from Cit+Phy mixtures contained less inorganic P and more organic P compared to monocultures. Exudate-specific strategies for the acquisition of soil P were most effective in P-limited soil and depended on citrate efflux rate and the relative mobility of the expressed phytase in soil. Plant growth and soil P utilization in plant systems with complementary exudation strategies are expected to be greatest where exudates persist in soil and are expressed synchronously in space and time.Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced in a P deficient soil. To test the importance of root intermingling in the interaction of citrate and phytase exudates, Nicotiana tabacum plant-lines with constitutive expression of heterologous citrate (Cit) or fungal phytase (Phy) exudation traits were grown under two root treatments (roots separated or intermingled) and in two soils with contrasting soil P availability. Complementarity of plant mixtures varying in citrate efflux rate and mobility of the expressed phytase in soil was determined based on plant biomass and P accumulation. Soil P composition was evaluated using solution 31 P NMR spectroscopy. In the soil with limited available P, positive complementarity occurred in Cit+Phy mixtures with roots intermingled. Root separation eliminated positive interactions in mixtures expressing the less mobile phytase (Aspergillus niger PhyA) whereas positive complementarity persisted in mixtures that expressed the more mobile phytase (Peniophora lycii PhyA). Soils from Cit+Phy mixtures contained less inorganic P and more organic P compared to monocultures. Exudate-specific strategies for the acquisition of soil P were most effective in P-limited soil and depended on citrate efflux rate and the relative mobility of the expressed phytase in soil. Plant growth and soil P utilization in plant systems with complementary exudation strategies are expected to be greatest where exudates persist in soil and are expressed synchronously in space and time.
Author Shand, Charles A.
Giles, Courtney D.
Cooper, Patricia
Stutter, Marc I.
Richardson, Alan E.
Zhang, Hao
Darch, Tegan
Cade‐Menun, Barbara J.
Lumsdon, David G.
Wearing, Catherine
Haygarth, Philip M.
Brown, Lawrie K.
Blackwell, Martin S.A.
Wendler, Renate
George, Timothy S.
Mezeli, Malika M.
Menezes‐Blackburn, Daniel
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  fullname: Stutter, Marc I.
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  organization: Lancaster University
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  surname: Zhang
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  organization: Lancaster University
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  surname: Haygarth
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  organization: Lancaster University
– sequence: 17
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  surname: George
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  organization: The James Hutton Institute
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2014; 221
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2014; 78
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Snippet Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced...
Citrate and phytase root exudates contribute to improved phosphorus (P) acquisition efficiency in Nicotiana tabacum (tobacco) when both exudates are produced...
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crossref
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StartPage 356
SubjectTerms Aspergillus niger
citrates
Citric acid
Complementarity
Efflux
Exudates
Exudation
fungi
gene expression
inorganic phosphorus
Magnetic resonance spectroscopy
Mobility
Monoculture
Nicotiana tabacum
NMR spectroscopy
nuclear magnetic resonance spectroscopy
nutrient availability
Peniophora
Phosphorus
Phytase
phytases
phytomass
Plant biomass
Plant growth
root exudates
Roots
soil
soil enzymes
Soil mixtures
soil nutrients
Soil testing
Soils
space and time
stable isotopes
Tobacco
Title Phosphorus acquisition by citrate‐ and phytase‐exuding Nicotiana tabacum plant mixtures depends on soil phosphorus availability and root intermingling
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fppl.12718
https://www.ncbi.nlm.nih.gov/pubmed/29498417
https://www.proquest.com/docview/2071008107
https://www.proquest.com/docview/2010374026
https://www.proquest.com/docview/2116884534
Volume 163
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