Adapted from Xu, G., Fan, X. and Miller, A.J. (2012). Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 63: 153-182.
Most plants take up most of their nitrogen as nitrate
NO3-
Many prokaryotes oxidize NH4+, Plants use energy to reduce NO3- for
so soil NH4+ levels are often low assimilation into organic compounds
See Li, B., Li, G., Kronzucker, H.J., Baluška, F. and Shi, W. (2014). Ammonium stress in Arabidopsis: signaling, genetic loci, and physiological targets. Trends
Plant Sci. 19: 107-114; Britto, D.T. and Kronzucker, H.J. (2013). Ecological significance and complexity of N-source preference in plants. Ann. Bot. 112: 957-963.
Plants have specific transporters for NO3-, NH4+ and
other N forms
Nacry, P., Bouguyon, E. and Gojon, A. (2013). Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring
plant adaptation to a fluctuating resource. Plant Soil. 370: 1-29, With kind permission from Springer Science and Business Media
A major nitrate importer was the first cloned: CHL1/
NRT1.1/ NPF6.3
Nitrate Chlorate
Wild- In 1993 the CHL1 gene was cloned and
reductase uptake
found to be a nitrate transporter
1973 type mutant mutant
(shown = current in Xenopus oocytes)
(chl1-5)
Growth on
chlorate
Nitrate
reductase
activity
+ - +
Oostindiër-Braaksma, F.J. and Feenstra, W.J. (1973). Isolation and characterization of chlorate-resistant mutants of Arabidopsis thaliana. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis. 19: 175-185; Reprinted from Tsay,
Y.-F., Schroeder, J.I., Feldmann, K.A. and Crawford, N.M. (1993). The herbicide sensitivity gene CHL1 of arabidopsis encodes a nitrate-inducible nitrate transporter. Cell. 72: 705-713 with permission from Elsevier.
Other channels contribute to nitrate transport w/in
and between cells
Reprinted from Wang, Y.-Y., Hsu, P.-K. and Tsay, Y.-F. (2012). Uptake, allocation and signaling of nitrate. Trends Plant Sci. 17: 458-467; Tegeder, M. (2014). Transporters involved in source to sink
partitioning of amino acids and ureides: opportunities for crop improvement. J. Exp. Bot. 65: 1865-1878
Primary N assimilation: NO3- is reduced to NH4+
prior to assimilation
Glutamate
Uptake
NH4+
Assimilation
into organic
Nitrite NH4+ compounds
reductase
NO2-
Nitrate All other N-
reductase Glutamine Glutamine
synthetase containing
NO3- (GS) compounds
NO3-
R-NH3
Nitrate reductase is a large enzyme with a complex
catalytic scheme
NO3-
NADH
Lambeck, I.C., Fischer-Schrader, K., Niks, D., Roeper, J., Chi, J.-C., Hille, R. and Schwarz, G. (2012). Molecular
mechanism of 14-3-3 protein-mediated inhibition of plant nitrate reductase. J. Biol. Chem. 287: 4562-4571.
GS/GOGAT assimilates inorganic nitrogen into
organic molecules
Remobilization
Carbon pools
Amino acid
Assimilation TCA cycle
recycling,
photorespiration Glutamate 2-oxoglutarate
Glutamine-2-
oxoglutarate
NH4+ aminotransferase
(GOGAT)
Uptake
Glutamate
Glutamine Glutamine
synthetase
Incorporation into
(GS)
amino acids and
other nitrogen-
containing
compounds
Gln synthetase (GS) expression is regulated by many
factors
GS ac&vity is correlated
with nitrogen use
efficiency
Martin, A., et al., and Hirel, B. (2006). Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell. 18: 3252-3274.
Rebmobilization of N occurs during senescence and
photorespiration
Glutamate Glutamate
Fdx-GOGAT NADH-GOGAT
Avice, J.-C. and Etienne, P. (2014). Leaf senescence and nitrogen remobilization efficiency in oilseed rape (Brassica napus L.). J. Exp. Bot. 65: 3813-3824
In some plants, most grain N is remobilized from
vegetative tissues
Hirel, B., Le Gouis, J., Ney, B. and Gallais, A. (2007). The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for
genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 58: 2369-2387
Summary: Plant nitrogen uptake and assimilation
Adapted from Xu, G., Fan, X. and Miller, A.J. (2012). Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 63: 153-182.
Regulation: Nitrogen sensing, signalling and deficit
responses
NITROGEN DEFICIT
Increase uptake
Activation of some NO3- and NH4+ transporters
Preferential growth of root relative to shoot
See for example Scheible, W.-R., et al and Stitt, M. (2004). Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant
Physiol. 136: 2483-2499; Krapp, A. et al and Daniel-Vedele, F. (2011). Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiol. 157: 1255-1282. Schlüter, U., et al. and Sonnewald, U. (2012).
Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiol. 160: 1384-1406. Amiour, N. et al and Hirel, B. (2012). The use of metabolomics integrated
with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J. Exp. Bot. 63: 5017-5033. Balazadeh, S., et al. and Mueller-Roeber, B. (2014). Reversal of senescence by N
resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences. J. Exp. Bot. 63: 5017-5033.
Responses to NO3- can be separated from those to
N-metabolites
X
NR mutant can’t grow 10% of the
on NO3- NO3- NO2- NH4+ R-NH3 genome responds
Nitrate Nitrite to nitrate, but only
reductase reductase
some genes are
Nitrate reductase mutants allow responses to NO3- nitrate-specific
to be separated from responses to N-metabolites
Red indicates
nitrate-specific
genes
Transcriptional responses
to nitrate (+ downstream
metabolites)
Wang, R., Tischner, R., Gutiérrez, R.A., Hoffman, M., Xing, X., Chen, M., Coruzzi, G., Crawford, N.M. (2004). Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 136: 2512–2522; Canales, J.,
Moyano, T.C., Villarroel, E. and Gutiérrez, R.A. (2014). Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments. Front. Plant Sci. 5: 22.
CHL1/NRT1.1/NPF6.3 is a nitrate transceptor
(sensor)
WT
chl1-5
Remans, T., et al. and Gojon, A. (2006). The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc. Natl. Acad. Sci. 103: 19206-19211 © by the
National Academy of Sciences; Krouk, G., et al. and Gojon, A. (2010). Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Devel. Cell. 18: 927-937
Roots respond to local and systemic nitrogen
availability
Reprinted by permission from Wiley from Drew, M.C. (1975). Comparison of the effects of a localised supply of phosphate, nitrate and ammonium and potassium on the growth of the seminal
root system, and the shoot, in barley. New Phytol. 75: 479-490.. Reprinted from Bouguyon, E., Gojon, A. and Nacry, P. (2012). Nitrate sensing and signaling in plants. Sem. Cell Devel. Biol. 23:
648-654, with permission from Elsevier. See also Gersani, M. and Sachs, T. (1992). Development correlations between roots in heterogeneous environments. Plant Cell Environ. 15: 463-469.
The split-root system separates local and systemic
signals
All plants split with ½ root system in each of two chambers
Sp.NO3 roots Sp.KCl roots
C.NO3 plants experience locally Experience locally C.KCl plants
Both chambers high NO3- but also deficient NO3- Both chambers
contain KNO3 N-deficiency signals condiAons but also contain KCl (local
(local and systemic derived from Sp.KCl N-sufficient signals and systemic signals
signals indicate roots from Sp.NO3 roots indicate NO3-
NO3 available) deficiency)
Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011). Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N
supply vs. demand. Proc. Natl. Acad. Sci. USA 108: 18524-18529.
Evidence for a systemic signal of "
N-demand on root development
Signals from the N- Signals from the N-replete
deficient roots promote Sp.NO3 roots supress root
elevated root growth in growth in Sp.KCl as compared to
Sp.NO3 as compared to C.KCl roots, indicaAng that a
C.NO3, indicating that a response to systemic N-
response to systemic N- reple&on signals
starvation signals
Model: Systemic
signals promote root
growth and suppress
root growth
Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011). Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N
supply vs. demand. Proc. Natl. Acad. Sci. USA 108: 18524-18529.
Evidence for cytokinin-dependent and –independent
signals
*
A separate signal that promotes
root growth in plants with total N
deprivation (C.KCl) still operates
in CK-deficient plants, as shown
by increased growth in C.KCl as
compared to Sp.KCl conditions
In cytokinin
deficient plants,
there is no
Growth augmentation
systemic N-
correlating to N-starvation
demand induced
increase in root
length
Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011). Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N
supply vs. demand. Proc. Natl. Acad. Sci. USA 108: 18524-18529.
Model of the effects of (some) local and systemic
signals
Systemic Other factors that contribute
Systemic to local and systemic signals
include auxin, amino acids,
transcription factors and root-
derived peptides
Loss-of-funcAon receptor
mutants for root-derived
pepAdes do not
Local NO3 effect downregulate root
growth when N is
abundant
WT LOF
Ruffel, S., Krouk, G., Ristova, D., Shasha, D., Birnbaum, K.D. and Coruzzi, G.M. (2011). Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N
supply vs. demand. Proc. Natl. Acad. Sci. USA 108: 18524-18529. Guan, P., Wang, R., Nacry, P., Breton, G., Kay, S.A., Pruneda-Paz, J.L., Davani, A., and Crawford, N.M. (2014). Nitrate foraging by Arabidopsis roots is
mediated by the transcription factor TCP20 through the systemic signaling pathway. Proc. Natl. Acad. Sci. USA 111: 15267-15272. Tabata, R., Sumida, K., Yoshii, T., Ohyama, K., Shinohara, H., and Matsubayashi,Y.
(2014). Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346: 343-346.
Model for transceptor action: NO3- competes for
auxin transport
Beeckman, T. and Friml, J. (2010). Nitrate contra auxin: Nutrient sensing by roots. Devel. Cell. 18: 877-878 with permission from Elsevier. See also Krouk, G., et al and Gojon, A. (2010). Nitrate-regulated auxin transport by NRT1.1 defines a
mechanism for nutrient sensing in plants. Devel. Cell. 18: 927-937; Mounier, E., et al and Nacry, P. (2014). Auxin-mediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity
of nitrate availability. Plant Cell Environ. 37: 162-174; Forde, B.G. (2014). Nitrogen signalling pathways shaping root system architecture: an update. Curr. Opin. Plant Biol. 21: 30-36.
Strategies to improve nitrogen-use efficiency and
decrease N pollution
Nitrogen fixation is
energy demanding
Nitrous oxide (N2O)
N N O derived from fertilizer is a
major greenhouse gas
Cyanabacterial bloom
Nolan, B.T. and Hitt, K.J. (2006). Vulnerability of shallow groundwater and drinking-water wells to nitrate in the United
States. Environ. Sci. Technol. 40: 7834-7840. Image source: Lamiot; Alexandra Pugachevsky; NASA Earth Observatory
Co-cropping and monitoring can decrease the need
for N application
Co-cropping or
growing in rotation
with legumes enriches
soil N content
Apogee; N2Africa; Petr Kosina / CIMMYT. See also Muñoz-Huerta, R.F., Guevara-Gonzalez, R.G., Contreras-Medina, L.M., Torres-Pacheco, I., Prado-Olivarez, J., and
Ocampo-Velazquez, R.V. (2013). A review of methods for sensing the nitrogen status in plants: Advantages, disadvantages and recent advances. Sensors. 13:
10823-10843; Robertson, G.P. and Vitousek, P.M. (2009). Nitrogen in agriculture: Balancing the cost of an essential resource. Annu. Rev. of Environ. Res. 34: 97-125.
Slow-release fertilizers can match release to
requirements
Slow-release
fer9lizer
Time
H 2O N N
UREA
H 2O N
Plant growth
requirements Coated urea dissolves and releases
slowly, but it can be expensive
Time
Adapted from Timilsena, Y.P., Adhikari, R., Casey, P., Muster, T., Gill, H. and Adhikari, B. (2014). Enhanced efficiency fertilisers: a review of formulation and nutrient release patterns. J. Sci. Food Agric. DOI: 10.1002/jsfa.6812
Soil bacteria can be manipulated to decrease N2O
and NO3- pollution
Philippot, L. and Hallin, S. (2011). Towards food, feed and energy crops mitigating climate change. Trends Plant Sci. 16: 476-480 with permission from Elsevier. See also Subbarao, G.V., et al. 2009). Evidence for biological nitrification inhibition in
Brachiaria pastures. Proc. Natl. Acad. Sci. USA. 106: 17302-17307. Subbarao, G.V., et al., (2013). A paradigm shift towards low-nitrifying production systems: the role of biological nitrification inhibition (BNI). Ann. Bot. 112: 297-316; Schipper,
L.A., Robertson, W.D., Gold, A.J., Jaynes, D.B. and Cameron, S.C. (2010). Denitrifying bioreactors—An approach for reducing nitrate loads to receiving waters. Ecol. Engin. 36: 1532-1543.
Altering flux into amino acid pools can increase NUE
Remobilization
Carbon pools
Amino acid Storage
Assimilation TCA cycle
recycling,
photorespiration Glutamate 2-oxoglutarate
Alanine
Glutamine-2-
Alanine
oxoglutarate
aminotransferase
NH4+ aminotransferase
(AlaAT)
(GOGAT)
Uptake
Glutamate Pyruvate
Glutamine Glutamine
synthetase
Incorporation into
(GS)
amino acids and
other nitrogen-
containing
compounds
Good, A.G., Johnson, S.J., De Pauw, M., Carroll, R.T., Savidov, N., Vidmar, J., Lu, Z., Taylor, G. and Stroeher, V. (2007). Engineering nitrogen use efficiency with alanine aminotransferase. Can. J. Bot. 85: 252-262.
Breeding strategies for enhanced nitrogen use
efficiency
Glutamine synthetase
Traits of an acJvity is an important
idealized plant component of NUE
with high NUE
In rice, a subunit of a
heterotrimeric G
protein contributes
to N-sensiJve growth
and N assimilaJon
Chardon, F., Noël, V. and Masclaux-Daubresse, C. (2012). Exploring NUE in crops and in Arabidopsis ideotypes to improve yield and seed quality. J. Exp. Bot. 63: 3401-3412 by permission of Oxford University Press;
Martin, A., et al. and Hirel, B. (2006). Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell. 18: 3252-3274. Reprinted by permission from
Macmillan Publishers Ltd: Sun, H., et al. (2014). Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet. 46: 652-656. Hirel, B., Le Gouis, J., Ney, B. and Gallais, A. (2007). The challenge of
improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 58: 2369-2387
Summary: Improving N use efficiency in plants and
soils
9 PHT1 genes in
Arabidopsis, 13 in rice,
Most are 12 in poplar. Some are
expressed in mycorrhiza inducible
roots and other
tissues
Nussaume, L., Kanno, S., Javot, H., Marin, E., Pochon, N., Ayadi, A., Nakanishi, T.M. and Thibaud, M.-C. (2011) Phosphate import in plants: focus on the
PHT1 transporters. Front. Plant Sci. 2: 83. Pedersen, B.P., et al and and Stroud, R.M. (2013). Crystal structure of a eukaryotic phosphate transporter. Nature.
496: 533-536. Loth-Pereda, V.,et al. and Martin, F. (2011). Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal
Populus trichocarpa. Plant Physiol. 156: 2141-2154. See also Lapis-Gaza, H.R., Jost, R., and Patrick M Finnegan, P.M. (2014). Arabidopsis PHOSPHATE
TRANSPORTER1 genes PHT1;8 and PHT1;9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol. 14: 334.
P-Starvation Inducible responses increase P uptake
and recycling
Huang, T.-K., et al and Lucas, W.J. (2014). Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J. Integr. Plant Biol. 56: 192-220 by permission. Sulpice, R., et al and Lambers, H.
(2014). Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant Cell Environ. 37: 1276-1298. See also Lin, W.-Y., Huang, T.-K., Leong, S.J.
and Chiou, T.-J. (2014). Long-distance call from phosphate: systemic regulation of phosphate starvation responses. J. Exp. Bot. 65: 1817-1827.
PSI (phosphate-starvation induced) are up-regulated
by PHR1
Puga, M.I., Mateos, I., Charukesi, R., Wang, Z., Franco-Zorrilla, J.M., de Lorenzo, L., Irigoyen, M.L., Masiero, S., Bustos, R., Rodríguez, J., Leyva, A., Rubio, V., Sommer, H. and Paz-Ares, J. (2014). SPX1 is a phosphate-dependent inhibitor of
PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. Proc. Natl. Acad. Sci. USA 111: 14947-14952; Wang, Z., Ruan, W., Shi, J., Zhang, L., Xiang, D., Yang, C., Li, C., Wu, Z., Liu, Y., Yu, Y., Shou, H., Mo, X., Mao, C. and Wu, P. (2014). Rice
SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc. Natl. Acad. Sci. USA 111: 14953-14958.
Regulatory controls prevent Pi from over
accumulating
PHO1 is a transporter that PHO2 is an E2 ligase
moves Pi into xylem for In pho1 mutants, too
that targets much Pi accumulates
transport to the shoot
PHT transporters take up Pi
transporters for in the root and too
proteolysis little in the shoot
Pi In pho2 mutants,
shoot
too much Pi
accumulates in the
shoot and too little
in the root; transport
xylem
is out-of-control
PHO2
root
PHO1 PHO1
PHT Too much
or too little
Pi is bad
Delhaize, E., and Randall, P.J. (1995). Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol. 107: 207 – 213; Liu, T.-Y., Huang, T.-K., Tsenga, C.-Y., Lai, Y.-S., Lin, S.-I., Lin,
W.-Y., Chen, J.-W., Chiou, T.J. (2012). PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24: 2167 – 2183.
Mutants pho1 and pho2 show effects of altered Pi
transport
Liu, T.-Y., Lin, W.-Y., Huang, T.-K. and Chiou, T.-J. MicroRNA-mediated surveillance of phosphate transporters on the move. Trends Plant Sci. 19: 647-655
PHO2 accumulation is regulated by miR399
expression
xylem
PHO2 PHO2
PHO1 PHO1 miR399
Pi
IPS1
Redrawn from Franco-Zorrilla, J. M., Valli, A., Todesco, M., Mateos, I., Puga, M.I., Rubio-Somoza, I., Leyva, A., Weigel, D., García, J.A.,
and Paz-Ares, J. (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39: 1033–1037.
P uptake & transport are regulated by local and
systemic signals
Suppression of shoot
branching
Strigolactones
Establishment of
plant – mycorrhizal
fungi symbiosis
Phosphate Enhanced
starvation PHT1 transporters uptake
signal
(unknown) PHR1 Phosphatases,
(transcription factor) organic acid
synthases
PHO1 (miR399 is a negaAve
regulator of a negaAve
IPS1 miR399 PHO2 PHT1 regulator of P uptake)
Wu, P., Shou, H., Xu, G. and Lian, X. (2013). Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr. Opin. Plant Biol. 16: 205-212. Liu, T.-Y., Lin, W.-Y.,
Huang, T.-K. and Chiou, T.-J. (2014). MicroRNA-mediated surveillance of phosphate transporters on the move. Trends Plant Sci. 19: 647-655.
The auxin transport capacity in the primary shoot governs the
induction of shoot branching
An intimate crosstalk of different plant hormones regulates
shoot branching
Strategies to improve crop plant phosphorus use
efficiency
Vinod, K.K. and Heuer, S. (2012). Approaches towards nitrogen- and phosphorus-efficient rice. AoB Plants. 2012: pls028
Selection for root architecture traits can lead to
increased P uptake
P-uptake efficiency can be correlated P-efficient
to more efficient root traits root system
P-inefficient
root system
Lynch, J.P. (2011). Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiol. 156: 1041-1049; Wang, X., Yan, X. and
Liao, H. (2010). Genetic improvement for phosphorus efficiency in soybean: a radical approach. Ann. Bot. 106: 215-222.
Rice adapted to poor-soil regions revealed a key
protein kinase
Reprinted by permission from Macmillan Publishers Ltd : Gamuyao, R., Chin, J.H., Pariasca-Tanaka, J., Pesaresi, P., Catausan, S., Dalid, C., Slamet-Loedin, I., Tecson-Mendoza, E.M., Wissuwa, M. and Heuer, S. (2012).
The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature. 488: 535-539.See also Chin, J.H., Gamuyao, R., Dalid, C., Bustamam, M., Prasetiyono, J., Moeljopawiro, S., Wissuwa,
M. and Heuer, S. (2011). Developing rice with high yield under phosphorus deficiency: Pup1 sequence to application. Plant Physiol. 156: 1202-1216.
Is it feasible to reuse, recapture and recycle
phosphate?
Phosphate recovered
from human urine alone Human urine is rich
in phosphate, and it Cleaner
Mg
Mg
Urine can be
applied directly to
plants as liquid
fertilizer
N & P-rich
Wastewater in Struvite
P (NH MgPO ·6H O)
P crystals harvested
for use as fertilizer
Urine-reclaiming toilet
Pratt, C., Parsons, S.A., Soares, A. and Martin, B.D. (2012). Biologically and chemically mediated adsorption and precipitation of phosphorus from wastewater. Curr. Opin. Biotechnol. 23: 890-896; Mihelcic,
J.R., Fry, L.M. and Shaw, R. (2011). Global potential of phosphorus recovery from human urine and feces. Chemosphere. 84: 832-839.. Multiformharvest.com
Strategies have been developed to impede P from
entering waterways
McDowell, R.W. (2012). Minimising phosphorus losses from the soil matrix. Curr. Opin. Biotech. 23: 860-865 with permission from Elsevier; Pratt, C., Parsons, S.A., Soares, A. and Martin, B.D. (2012). Biologically
and chemically mediated adsorption and precipitation of phosphorus from wastewater. Curr. Opin. Biotech. 23: 890-896 Shilton, A.N., Powell, N. and Guieysse, B. (2012). Plant based phosphorus recovery from
wastewater via algae and macrophytes. Curr. Opin. Biotech. 23: 884-889 by permission from Elsevier, and others from the same issue. Rittmann, B.E., Mayer, B., Westerhoff, P. and Edwards, M. (2011). Capturing the
lost phosphorus. Chemosphere. 84: 846-853. Schipper, W. (2014). Phosphorus: Too big to fail. Eur. J. Inorgan. Chem. 2014: 1567-1571.
Summary: Phosphorus