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 in | Physiologia plantarum Vol. 163; no. 3; pp. 356 - 371 |
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Main Authors | , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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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. |
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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 |
Author_xml | – sequence: 1 givenname: Courtney D. orcidid: 0000-0003-2563-2920 surname: Giles fullname: Giles, Courtney D. email: cdgiles@uvm.edu organization: The James Hutton Institute – sequence: 2 givenname: Alan E. surname: Richardson fullname: Richardson, Alan E. organization: CSIRO Agriculture & Food – sequence: 3 givenname: Barbara J. surname: Cade‐Menun fullname: Cade‐Menun, Barbara J. organization: Agriculture and Agri‐Food Canada – sequence: 4 givenname: Malika M. surname: Mezeli fullname: Mezeli, Malika M. organization: The James Hutton Institute – sequence: 5 givenname: Lawrie K. surname: Brown fullname: Brown, Lawrie K. organization: University of Vermont – sequence: 6 givenname: Daniel surname: Menezes‐Blackburn fullname: Menezes‐Blackburn, Daniel organization: Lancaster University – sequence: 7 givenname: Tegan surname: Darch fullname: Darch, Tegan organization: North Wyke – sequence: 8 givenname: Martin S.A. surname: Blackwell fullname: Blackwell, Martin S.A. organization: North Wyke – sequence: 9 givenname: Charles A. surname: Shand fullname: Shand, Charles A. organization: The James Hutton Institute – sequence: 10 givenname: Marc I. surname: Stutter fullname: Stutter, Marc I. organization: The James Hutton Institute – sequence: 11 givenname: Renate surname: Wendler fullname: Wendler, Renate organization: The James Hutton Institute – sequence: 12 givenname: Patricia surname: Cooper fullname: Cooper, Patricia organization: The James Hutton Institute – sequence: 13 givenname: David G. surname: Lumsdon fullname: Lumsdon, David G. organization: The James Hutton Institute – sequence: 14 givenname: Catherine surname: Wearing fullname: Wearing, Catherine organization: Lancaster University – sequence: 15 givenname: Hao surname: Zhang fullname: Zhang, Hao organization: Lancaster University – sequence: 16 givenname: Philip M. surname: Haygarth fullname: Haygarth, Philip M. organization: Lancaster University – sequence: 17 givenname: Timothy S. surname: George fullname: George, Timothy S. organization: The James Hutton Institute |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29498417$$D View this record in MEDLINE/PubMed |
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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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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 |
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