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Organic Anion–Driven Solubilization of Precipitated and Sorbed Phytate Improves Hydrolysis by Phytases and Bioavailability to Nicotiana tabacum

Giles,, Courtney D.1; Richardson,, Alan E.2; Druschel,, Gregory K.3; Hill, Jane E.1

doi: 10.1097/SS.0b013e318272f83f
Technical Article

Improved plant access to native soil phosphorus (P) species such as phytate (metal ion derivatives of myo-inositol hexakisphosphate (IHP)) could minimize agricultural dependence on nonrenewable mineral phosphates and reduce surface water pollution. Nicotiana tabacum plant lines with unique organic anion (OA) and phytase production patterns were used to investigate the effect of OA-driven solubilization on the bioavailability of precipitated and sorbed IHP. Organic anions released IHP sorbed to goethite (Gt) by chelation or reductive dissolution mechanisms in the order: ascorbate > citrate > oxalate > pyruvate > acetate. Transgenic tobacco overexpressing Peniophora lycii phytase (PHY) and a MATE-type citrate transporter (CIT) exuded 2.2- to 2.6-fold higher OA compared with that of wild-type plants. The PHY plants had 33-fold higher exudate phytase activity (6.0 × 10−2 nkat plant−1 day−1) compared with those of wild-type and CIT plants, produced the largest zone of iron-IHP hydrolysis in agar media, and incorporated the most shoot P (2.3 μg) when grown on Gt-IHP. Plants grown on IHP at 2× Gt saturation (0.26 mmol/L) were 10-fold higher in shoot P compared with the 1× Gt condition (0.13 mmol/L IHP) with PHY plants approaching excess P status (1 % shoot P). The addition of Gt diminished shoot P in plants grown without P (−70 to −80 %) and with phosphate (−50 %) or IHP (−100 %); the exception was the high citrate–exuding plant line (21 nmol citrate plant−1 day−1), for which phosphate uptake was only 20 % reduced. Plant OA production mitigates P inhibition by Gt when weakly sorbing phosphate species are supplied or when high phytase production by plants can maximize the hydrolysis of IHP.

1School of Engineering, University of Vermont, Burlington, VT.

2CSIRO (Commonwealth Scientific and Industrial Research Organisation) Plant Industry, Black Mountain, Canberra, Acton, Australia.

3Department of Earth Sciences, Indiana University-Purdue University Indianapolis, Indianapolis, IN.

Address for correspondence: Dr. Jane E. Hill, 33 Colchester Avenue, Burlington, VT 05405. E-mail:

Financial Disclosures/Conflicts of Interest: C.D.G. was generously supported by a UVM Graduate Research Fellowship (2010–2011) from the James M. Jeffords Center (UVM) that also provided travel support to visit CSIRO (Commonwealth Scientific and Industrial Research Organisation).

Received May 28, 2012.

Accepted for publication September 5, 2012.

© 2012 Lippincott Williams & Wilkins, Inc.