Plant Nutrition 2: Macronutrients
(N, P, K, S, Mg and Ca)
© 2014 American Society of Plant Biologists
“Earth, and not water, is the matter
that constitutes vegetables”
Woodward compared plant
growth in water containing
different amounts of
“mineral matter” to test the
assumption that water is a
plant’s sole requirement
Spring
water
Rain
water
Thames River
water
Weight gain:
55%
“Some thoughts and
experiments concerning
vegetation” (1699)
62%
93%
Woodward concluded that mineral matter
nourishes plants, laying the foundation for
the study of plant mineral nutrition
Woodward, J. (1699). Some thoughts and experiments concerning vegetation.PhilosophicalTransactions of the Royal Society, 21,193-227.
© 2014 American Society of Plant Biologists
“Law of the Minimum”: Nutrient in
least supply limits growth
Carl Sprengel
1787 - 1859
Growth is determined by
whichever nutrient is
present in shortest supply
Justus von Liebig
1803 - 1873
Stamp issued 150
years after his birth
Biodiversity Heritage Library
© 2014 American Society of Plant Biologists
Lawes & Gilbert began investigating
plant nutrition at Rothamsted 1843
Joseph Henry Gilbert
1817 - 1901
John Bennett Lawes
1814 - 1901
Lawes’ estate is now Rothamsted
Research, the longest-running
agricultural experiment station
Lawes’ Superphosphate
factory pioneered the
production of chemicallysynthesized fertilizers
Images used by permission of Rothamsted Research
© 2014 American Society of Plant Biologists
Plants assimilate mineral nutrients
from their surroundings
Nutrient assimilation can
occur across the surface of
the plant or through the root
system of vascular plants
K+
NO3-
NO3-
NO3-
K+
K+
PO43-
K+
K+
PO43-
K+
PO43-
PO4
3-
PO43NO3
K+
-
PO43-
K+
© 2014 American Society of Plant Biologists
Plants assimilate mineral nutrients
mainly as cations or anions
MACRONUTRIENTS
μmol / g Element
Assimilated
(dry wt)
form
MICRONUTRIENTS
μmol / g Element
(dry wt)
Assimilated
form
250
Potassium (K)
K+
2
Iron (Fe)
Fe3+, Fe2+
1000
Nitrogen (N)
NO3-, NH4+
0.002
Nickel (Ni)
Ni+
60
Phosphorus
(P)
HPO42-,
H2PO4-
1
Manganese
(Mn)
Mn2+
30
Sulfur (S)
SO42-
0.1
Copper (Cu)
Cu2+
80
Magnesium
(Mg)
Mg2+
0.001
Molybdenum
(Mo)
MoO42+
125
Calcium (Ca)
Ca2+
2
Boron (B)
H3BO3
3
Chlorine (Cl)
Cl-
0.3
Zinc (Zn)
Zn2+
Charged ions require transport
proteins to cross membranes
See Taiz, L. and Zeiger, E. (2010) Plant Physiology. Sinauer Associates; Marschner, P. (2012) Mineral Nutrition of Higher Plants. Academic Press, London
© 2014 American Society of Plant Biologists
However, larger and more complex
nutrients also can be taken up
Carnivorous plants can
obtain nutrients by
digesting trapped
animals
Other, non-carnivorous
plants can obtain
nutrients from proteins
and even microbes,
although these
processes are very
inefficient
Schmidt, S., Raven, J.A. and Paungfoo-Lonhienne, C. (2013). The mixotrophic nature of photosynthetic plants. Funct. Plant Biol. 40: 425-438 by permission of CSIRO Publishing; Adlassnig, W., Koller-Peroutka, M.,
Bauer, S., Koshkin, E., Lendl, T. and Lichtscheidl, I.K. (2012). Endocytotic uptake of nutrients in carnivorous plants. Plant J. 71: 303-313. Hill, P.W., Marsden, K.A. and Jones, D.L. (2013). How significant to plant N
nutrition is the direct consumption of soil microbes by roots? New Phytol. 199: 948-955.
© 2014 American Society of Plant Biologists
Vascular plants assimilate mineral
nutrients mostly via roots
By increasing surface area for
absorption, root hairs functionally
resemble microvilli of an animal’s
intestinal epithelium
Membrane transporters facilitate nutrient uptake
Barberon, M. and Geldner, N. (2014). Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiol. 166: 528-537.
© 2014 American Society of Plant Biologists
Roots have several adaptations to
enhance nutrient capture
Biochemical
responses
Fungal symbiotic
partners
Developmental
responses
Prokaryotic
symbiotic
partners
Schmidt, S., Raven, J.A. and Paungfoo-Lonhienne, C. (2013). The mixotrophic nature of photosynthetic plants. Funct. Plant Biol. 40: 425-438 by permission of CSIRO publishing.
© 2014 American Society of Plant Biologists
Nutrient uptake, assimilation and
utilization involve many processes
Nutrient
uptake
efficiency
Root
exudates
Nutrient
utilization
efficiency
X
Root system
architecture
Intercellular
transport
efficiency
P
P
Symbioses
NH3
R-X
Assimilation and
remobilization
efficiency
Transporters
and pumps
Regulatory and
control
networks
N N
Rhizosphere
microbiota
© 2014 American Society of Plant Biologists
Soil pH affects nutrient availabilitySome soils are acidic, others basic
Strongly
acidic
Mildly
alkaline
Atlas of the biosphere, University of Wisconsin; FMoeckel
© 2014 American Society of Plant Biologists
Physical and biological processes
affect nutrient availability
Erosion, rainfall patterns,
cultural practices, soil
biodiversity, soil pH,
atmospheric gases etc. all
affect soil fertility
Reprinted from Scholes, M.C. and Scholes, R.J. (2013). Dust unto dust. Science. 342: 565-566; See also Tedersoo, L., et al., and Abarenkov, K. (2014). Global diversity and geography of soil fungi. Science. 346: 1256688.
© 2014 American Society of Plant Biologists
Nutrients removed from soils can be
replenished with fertilizers
Plants remove nutrients from the soil
Wheat
Soy
Kg/ha
600
Corn
800
Rice
Total nutrient requirement
Cotton
1000
Fertilizers can be
complex waste
products or
refined blends of
nutrient salts
400
Sulfur
Magnesium
Potash
200
Phosphate
Nitrogen
0
Kg/ha
400
200
Typical fertilizer application
Most fertilizers
contain nitrogen
(N), phosphorus
(P) and potassium
(K). Some include
other elements
0
Source: USGS
© 2014 American Society of Plant Biologists
Global mineral nutrient resources
are unevenly distributed
Supply > Demand
Supply < Demand
N
P2O5
K2O
FAO (2011) Current world fertilizer trends and outlook to 2015.
© 2014 American Society of Plant Biologists
The global trade in fertilizers is
worth billions of dollars annually
Ammonium
Urea
Potash
Diammonium Monoammonium
phosphate
phosphate
Phosphate
rock
Sulfur
Sulfuric
acid
IFIA
© 2014 American Society of Plant Biologists
How much is the right amount of
fertilizer to apply to a field?
Cultivation
practices: Is
unharvested
material removed,
or left to replenish
the soil?
Species / variety
of plant: Different
plants have
different needs
Soil
characteristics:
Residual nutrients,
rate of nutrient
leaching, pH,
particle size,
presence of
microbes etc. affect
optimal application
Abiotic and biotic
factors: Temperature,
rain, stress and pests
or pathogens affect
nutrient needs
Developmental stage affects plant needs
Financial considerations:
Balancing the cost of fertilizers with
the gain reaped from their use
Interactions between nutrients:
There are both positive and negative
interactions between various nutrients
Photo by Michael Russelle.
© 2014 American Society of Plant Biologists
Fertilizer use can cause
environmental and health problems
Nitrogen fixation is
energy demanding
Human and animal waste
can spread disease
Transport requires energy
Phosphate and potash
mining is destructive
Nutrient runoff pollutes
waterways and can lead
to eutrophication
N
N
O
Nitrous oxide (N2O)
derived from fertilizer is a
major greenhouse gas
Plants need
nutrients, but their
application isn’t
always optimal or
sustainable – how
can plant science
contribute to
better practices?
Image source: Lamiot; Alexandra Pugachevsky
© 2014 American Society of Plant Biologists
Fertilizer use is increasing to keep
pace with population growth
Deposition
from
atmosphere
Rock weathering
Decaying matter
Organic matter
Inorganic matter
Fertilizers
Vance, C.P. (2001). Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol. 127: 390-397.
© 2014 American Society of Plant Biologists
Summary: Overview of plant nutrient
requirements and fertilizers
• People eat plants (or eat animals or products from
animals that eat plants)
• Plants get C, H and O from water and carbon dioxide
• Plants get the rest of their nutrients as mineral nutrients
• Mineral nutrients are usually ions in soil solution
• Mineral nutrients are taken up across membranes and
moved throughout the plant as needed
• The nutrients that plants remove from the soil must be
replenished
• Fertilizer use can contribute to environmental problems
© 2014 American Society of Plant Biologists
Nitrogen: The most abundant
mineral element in a plant
•
•
•
The most abundant element in
the earth’s atmosphere
The 4th most abundant element
in a plant (after C, H and O)
Often the limiting nutrient for
plant growth
N is in amino acids
(proteins), nucleic
acids (DNA, RNA),
chlorophyll, and
countless small
molecules
Nitrogen is one of
the three major
macronutrients found
in most fertilizers
Blank, L.M. (2012). The cell and P: From cellular function to biotechnological application. Curr. Opin. Biotech. 23: 846 – 851.From: Buchanan,
B.B., Gruissem, W. and Jones, R.L. (2000) Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists.
© 2014 American Society of Plant Biologists
Nitrogen can be found in many
inorganic forms
Species
Name
Oxidation
State
R-NH2
Organic nitrogen, urea
-3
NH3, NH4+ Ammonia,
-3
ammonium ion
N2
Nitrogen
0
N2 O
Nitrous oxide
+1
NO
Nitric oxide
+2
HNO2, NO2- Nitrous acid,
+3
nitrite ion
NO2
Nitrogen dioxide
+4
HNO3, NO3- Nitric acid, nitrate ion
+5
NO2Nitrification
NO3-
NO2-
Nitrate
reduction
Aerobic
reactions
NO
N2O
Anaerobic
reactions
NH3
Nitrogen
fixation
N2
Adapted from Robertson, G.P. and Vitousek, P.M. (2009). Nitrogen in agriculture: Balancing the cost of an essential resource. Annu. Rev. Environ. Res. 34: 97-125.
© 2014 American Society of Plant Biologists
Plants are an important part of the
global nitrogen cycle
Atmospheric pool of N2
Atmospheric
fixation
5 Tg N / yr
Industrial
fixation
Biological
fixation
NH4+
120 Tg N / yr
(50%
agricultural)
NH4+
NO3120
Tg N / yr
manure
decomposition
NO3-
R-NH2
NH4+
Assimilation
by plants
NO2-
NO3-
Denitrification by
denitrifying bacteria
NO3-
Biological
fixation
(oceans)
140
Tg N / yr
Nitrification by nitrifying bacteria
Adapted from Fowler, D., et al. (2013). The global nitrogen cycle in the twenty-first century. Phil. Trans. Roy. Soc. B: 368: 20130164
© 2014 American Society of Plant Biologists
How do plants optimize their uptake
and utilization of nitrogen?
How is inorganic
nitrogen
assimilated into
organic
molecules?
How is nitrogen
taken up into
the plant?
How do plants
sense local soil
nitrogen levels
and plant
nitrogen status?
How do plants
respond to nitrogen
deficit? How do they
maximize uptake
through their roots?
How do plants
remobilize
nitrogen to
optimize Nutilization?
© 2014 American Society of Plant Biologists
Nitrogen metabolism: Uptake,
assimilation and remobilization
Remobilization
Amino acid
recycling,
photorespiration
Uptake
Assimilation
Glutamate
NH4+
Nitrite
reductase
Nitrate
reductase
NO3
-
NO3
NO2
N2
2-oxoglutarate
Glutamine-2oxoglutarate
aminotransferase
(GOGAT)
NH4+
Glutamate
-
Glutamine
synthetase
(GS)
-
R-NH2
NH4+
Carbon pools
TCA cycle
Assimilation
Glutamine
Incorporation into
amino acids and
other nitrogencontaining
compounds
Adapted from Xu, G., Fan, X. and Miller, A.J. (2012). Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 63: 153-182.
© 2014 American Society of Plant Biologists
Most plants take up most of their
nitrogen as nitrate NO3Many prokaryotes oxidize NH4+,
so soil NH4+ levels are often low
Energy Energy
released released
NH4+
NO2-
Plants use energy to reduce NO3- for
assimilation into organic compounds
Energy
consumed
NO3-
Nitrification by nitrifying prokaryotes
NO3-
Energy
consumed
NO2Nitrate
reductase
NH4+
R-NH3
Nitrite
reductase
Plant preferences for NH4+ vs NO3- vary by species, other
metabolic processes, temperature, water, soil pH etc….
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.
© 2014 American Society of Plant Biologists
Plants have specific transporters for
NO3-, NH4+ and other N forms
HATS = high affinity
transporters
LATS = low affinity
transporters
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
© 2014 American Society of Plant Biologists
A major nitrate importer was the first
cloned: CHL1/ NRT1.1/ NPF6.3
The first nitrate
transporter was
identified using a
genetic selection for
chlorate resistance
1973
Wildtype
Chlorate (ClO3-)
mimics nitrate
(NO3-)
Nitrate
reductase
Chlorite
ClO2-
Nitrate
reductase
mutant
Chlorate
uptake
mutant
(chl1-5)
-
+
In 1993 the CHL1 gene was cloned and
found to be a nitrate transporter
(shown = current in Xenopus oocytes)
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.
© 2014 American Society of Plant Biologists
Other channels contribute to nitrate
transport w/in and between cells
Nitrogen uptake but also assimilation and
recycling depend on membrane transporters
Specific transporters move nitrate
(or other N-containing
compounds) inwards and
outwards across the PM and
across the vacuolar membrane
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 with permission from Elsevier; 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 by permission of Oxford University Press.
© 2014 American Society of Plant Biologists
Primary N assimilation: NO3- is
reduced to NH4+ prior to assimilation
Glutamate
Uptake
NH4+
Nitrite
reductase
Nitrate
reductase
NO3-
NO3-
NH4+
Assimilation
into organic
compounds
NO2Glutamine
synthetase
(GS)
Glutamine
All other Ncontaining
compounds
R-NH3
© 2014 American Society of Plant Biologists
Nitrate reductase is a large enzyme
with a complex catalytic scheme
NADH
NO3-
NAD+
NO2-
Nitrate reductase
reduces nitrate to nitrate
with NADH acting as the
electron donor
NO3NADH
The electrons move from
NADH to FAD to heme
to a molybdenum
cofactor (Moco) to NO3-
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.
© 2014 American Society of Plant Biologists
GS/GOGAT assimilates inorganic
nitrogen into organic molecules
Remobilization
Amino acid
recycling,
photorespiration
Assimilation
Glutamate
Carbon pools
TCA cycle
2-oxoglutarate
Glutamine-2oxoglutarate
aminotransferase
(GOGAT)
NH4+
Uptake
Glutamate
Glutamine
synthetase
(GS)
Glutamine
Incorporation into
amino acids and
other nitrogencontaining
compounds
© 2014 American Society of Plant Biologists
Gln synthetase (GS) expression is
regulated by many factors
GS1 (GLN1 genes)
Cytosolic protein
GS2 (GLN2 genes)
Nuclear gene, plastid localized protein
GS activity is regulated transcriptionally
and post-transcriptionally by cell type,
light, [NH4+], circadian cycles, plant
carbon status etc.
GS activity 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.
© 2014 American Society of Plant Biologists
Rebmobilization of N occurs during
senescence and photorespiration
Each N atom may cycle through GS
many times as amino acids are recycled
during growth and senescence and
released due to photorespiration
Leaves
Fdx-GOGAT
Glutamine
Chloroplast
localized GS2
Photorespiration
remobilization
Glutamate
Glutamate
Glutamate
remobilization
Roots, Cotyledons
Amino acids
Amino acids
assimilation
NH4+
Assimilation
NADH-GOGAT
Glutamate
Glutamine
assimilation
Cytosolic GS1
AA
catabolism
NH4+
uptake
Assimilation
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 by permission of Oxford University Press.
© 2014 American Society of Plant Biologists
In some plants, most grain N is
remobilized from vegetative tissues
The relative amount of N
taken up pre- and postflowering is important in
nitrogen use efficiency
Different crop rely more or
less on N remobilization
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 by permission of Oxford University Press.
© 2014 American Society of Plant Biologists
Summary: Plant nitrogen uptake and
assimilation
Remobilization
Amino acid
recycling,
photorespiration
Uptake
Assimilation
Glutamate
NH4+
Nitrite
reductase
Nitrate
reductase
NO3
-
NO3
NO2
N2
2-oxoglutarate
Glutamine-2oxoglutarate
aminotransferase
(GOGAT)
NH4+
Glutamate
-
Glutamine
synthetase
(GS)
-
R-NH2
NH4+
Carbon pools
TCA cycle
Assimilation
Glutamine
Incorporation into
amino acids and
other nitrogencontaining
compounds
Adapted from Xu, G., Fan, X. and Miller, A.J. (2012). Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 63: 153-182.
© 2014 American Society of Plant Biologists
Regulation: Nitrogen sensing,
signaling and deficit responses
NITROGEN DEFICIT
Increase uptake
Activation of some NO3- and NH4+ transporters
Preferential growth of root relative to shoot
Metabolic adaptations to low-N
Decreased accumulation of N-rich chlorophyll
Increased accumulation N-free anthocyanins
Smaller pools of N-containing compounds (amino acids)
Larger pools of N-free compounds (starches, organic acids)
Accelerated senescence and nitrogen
remobilization
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.
© 2014 American Society of Plant Biologists
Responses to NO3- can be separated
from those to N-metabolites
NR mutant can’t grow
on NO3-
NO3-
X
NO2-
Nitrate
reductase
NH4+
R-NH3
Nitrite
reductase
Nitrate reductase mutants allow responses to NO3to be separated from responses to N-metabolites
10% of the
genome responds
to nitrate, but only
some genes are
nitrate-specific
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.
© 2014 American Society of Plant Biologists
CHL1/NRT1.1/NPF6.3 is a nitrate
transceptor (sensor)
In wild-type
plants (Ws),
lateral root
growth is
stimulated
in High
Nitrate (HN)
Lateral roots of
transceptor mutants
(chl1-10) fail to
respond to the HN
environment
Transceptor mutants
(chl1-5) also show
abnormal transcriptional
responses to nitrate
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 with permission from Elsevier.
© 2014 American Society of Plant Biologists
Roots respond to local and systemic
nitrogen availability
When nitrogen is abundant,
plants allocate less biomass
to their roots
When nitrogen
distribution is patchy,
roots proliferate in the
nutrient rich patches
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.
© 2014 American Society of Plant Biologists
The split-root system separates
local and systemic signals
All plants split with ½ root system in each of two chambers
C.NO3 plants
Both chambers
contain KNO3
(local and systemic
signals indicate
NO3 available)
Sp.NO3 roots
experience locally
high NO3- but also
N-deficiency
signals derived
from Sp.KCl roots
Sp.KCl roots
Experience locally
deficient NO3conditions but also
N-sufficient signals
from Sp.NO3 roots
C.KCl plants
Both chambers
contain KCl (local
and systemic
signals indicate
NO3- 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.
© 2014 American Society of Plant Biologists
Evidence for a systemic signal of
N-demand on root development
Signals from the Ndeficient roots promote
elevated root growth in
Sp.NO3 as compared to
C.NO3, indicating that a
response to systemic Nstarvation signals
Signals from the N-replete
Sp.NO3 roots supress root
growth in Sp.KCl as
compared to C.KCl roots,
indicating that a response to
systemic N-repletion 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. Li, Y., Krouk, G., Coruzzi, G.M. and Ruffel, S. (2014). Finding a nitrogen niche: a systems integration of local and systemic nitrogen signalling in
plants. J. Exp. Bot. 65: 5601-5610 by permission of Oxford University Press.
© 2014 American Society of Plant Biologists
Evidence for cytokinin-dependent
and –independent signals
*
In cytokinin
deficient plants,
there is no
systemic Ndemand induced
increase in root
length
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
Growth augmentation
correlating to N-starvation
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.
© 2014 American Society of Plant Biologists
Model of the effects of (some) local
and systemic signals
Systemic
Systemic
Other factors that contribute
to local and systemic signals
include auxin, amino acids,
transcription factors and rootderived peptides
Loss-of-function
receptor mutants for
root-derived peptides
do not downregulate
root growth when N is
abundant
Local NO3 effect
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.
© 2014 American Society of Plant Biologists
Model for transceptor action: NO3competes for auxin transport
When NO3- is
low, NPF6.3
transports
auxin away
from the root
tip and growth
is inhibited
NPF6.3
Auxin
NO3-
When NO3- is
high, auxin
transport
through
NPF6.3 is
suppressed
and growth is
promoted
NPF6.3
Auxin
NO3-
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.
© 2014 American Society of Plant Biologists
Strategies to improve nitrogen-use
efficiency and decrease N pollution
Nitrogen fixation is
energy demanding
N
N
O
Nitrous oxide (N2O)
derived from fertilizer is a
major greenhouse gas
Cyanabacterial bloom
Lake Erie
Unhealthful nitrate from agricultural
uses pollutes groundwater
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
© 2014 American Society of Plant Biologists
Co-cropping and monitoring can
decrease the need for N application
Co-cropping or
growing in rotation
with legumes enriches
soil N content
N status can be
determined by
chlorophyll
content, measured
by reflected light
Chlorophyll can
be measured
the
transmission
ratio of 653 nm
to 931 nm light
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: 1082310843; 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.
© 2014 American Society of Plant Biologists
Slow-release fertilizers can match
release to requirements
Amount of fertilizer available
Slow-release
fertilizer
Time
H2O
Plant growth
requirements
Time
UREA
N
H2O
N
N
Traditional fertilizer –
one or two applications
Traditional fertilizers don’t match
nitrogen availability to plant needs.
Slow release fertilizers can more
closely match plant needs
Coated urea dissolves and releases
slowly, but it can be expensive
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
© 2014 American Society of Plant Biologists
Soil bacteria can be manipulated to
decrease N2O and NO3- pollution
Inhibitors of bacterial nitrification cause
NH4+ to be retained in the soil, leading to
less leaching and less N2O production
Denitrifying bacteria cultivated in
a bioreactor downstream of a
fertilized field protect waterways
by converting NO3- in runoff to N2
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.
© 2014 American Society of Plant Biologists
Altering flux into amino acid pools
can increase NUE
Remobilization
Amino acid
recycling,
photorespiration
Assimilation
Glutamate
Carbon pools
TCA cycle
Storage
2-oxoglutarate
Alanine
Glutamine-2oxoglutarate
aminotransferase
(GOGAT)
NH4+
Uptake
Alanine
aminotransferase
(AlaAT)
Pyruvate
Glutamate
Glutamine
synthetase
(GS)
Glutamine
Incorporation into
amino acids and
other nitrogencontaining
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.
© 2014 American Society of Plant Biologists
Breeding strategies for enhanced
nitrogen use efficiency
Glutamine synthetase
activity is an important
component of NUE
Traits of an
idealized
plant with
high NUE
In rice, a subunit
of a heterotrimeric
G protein
contributes to Nsensitive growth
and N assimilation
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
© 2014 American Society of Plant Biologists
Summary: Improving N use
efficiency in plants and soils
•
•
•
•
N is abundant as N2, but often limiting for growth
N is fixed by biological or industrial means
N fertilization is economically and environmentally costly
N use efficiency involves uptake of NO3- and NH4+,
primary assimilation and recycling via GS / GOGAT
• Regulatory and signaling pathways are being identified
as opportunities for breeding improvements
• Monitoring of plant and soil N status can improve
fertilizer use efficiency
© 2014 American Society of Plant Biologists
Phosphorus
(note spelling – not phosphorous)
•
•
•
P has roles in cell structure,
energy and information
storage and energy and
information transfer
The 11th most abundant element
in the earth’s crust
The 5th most abundant element
in a plant
The 1st or 2nd most commonly
limiting nutrient for plant growth
Phosphorus is one of
the three major
macronutrients found
in most fertilizers
Reprinted from Blank, L.M. (2012). The cell and P: From cellular function to biotechnological application. Curr. Opin. Biotech. 23: 846 – 851 by permission of Elsevier.
© 2014 American Society of Plant Biologists
Phosphorus is an essential nutrient
and found in many biomolecules
Membrane phospholipids
DNA and RNA
Phosphorus (P) is
assimilated and used as
phosphate (Pi) which
depending on the pH is
H2PO4- ,HPO42- or PO43H
ATP
H H
© 2014 American Society of Plant Biologists
Plants are part of the global
phosphorus cycle: Preindustrial
Essentially NO atmospheric pool of P
Slow leaching of P to
lakes and oceans
Slow weathering of P from
rock reserves to soil
manure
decomposition
Aquatic
cycle
Upwelling
Terrestrial
cycle: Plant /
Animal / Soil
Sedimentation
Adapted from Smil, V. (2000). Phosphorus in the environment: Natural flows and human interference. Annu. Rev. Energy Environ. 25: 53–88 and Vaccari, D.A. (2000). Phosphorus:
A looming crisis. Sci. Am. June: 54 – 59; Fixen, P.E. and Johnston, A.M. (2012). World fertilizer nutrient reserves: a view to the future. J. Sci. Food Agricul. 92: 1001-1005.
© 2014 American Society of Plant Biologists
Plants are part of the global
phosphorus cycle: Postindustrial
Essentially NO atmospheric pool of P
manure
decomposition
Mining and commercial
processing accelerates P
entry to biosphere
Sewage
Modern practices accelerate runoff
Terrestrial
cycle: Plant /
Animal / Soil
Aquatic
cycle
Urbanization removes P
from terrestrial cycle and
accelerates entry to
waterways, causing toxic
algal blooms
(eutrophification)
Adapted from Smil, V. (2000). Phosphorus in the environment: Natural flows and human interference. Annu. Rev. Energy Environ. 25: 53–88 and Vaccari, D.A. (2000).
Phosphorus: A looming crisis. Sci. Am. June: 54 – 59. See also Elser, J. and Bennett, E. (2011). Phosphorus cycle: A broken biogeochemical cycle. Nature. 478: 29-31.
© 2014 American Society of Plant Biologists
Is the current rate of phosphorus
use sustainable?
Phosphate usage has increased
dramatically in the past 70 years
Guano
Human excreta
Phosphate
rock
Some have argued that we
are approaching a period
of “peak phosphorus” as
deposits become depleted
Manure
1800
1900
1950
90% of the world’s
phosphate rock reserves
are found in 5 countries
2000
United
States
8%
Jordan
6%
Morocco
38%
China
27%
South Africa
10%
Adapted from Cordell, D., Drangert, J.-O. and White, S. (2009). The story of phosphorus: Global food security and food for thought. Global Environmental Change. 19: 292-305, and Great Quest.
© 2014 American Society of Plant Biologists
Phosphorus in soil is in the form of
immobile, insoluble complexes
Depletion Zone
Cation-phosphate complexes
are relatively insoluble and
immobile in soil; these
include oxides and
Fe-P
hydroxides of Al and Fe
Al-P
Mg-P
Ca-P
Plants don’t
take up organic
phosphate
Organic
phosphates
Roots growing in 31P-labeled soil. Only P
immediately next to roots is taken up
Lewis, D.G. and Quirk, J.P. (1967). Phosphate diffusion in soil and uptake by plants. Plant nd Soil. 26: 445-453; With kind permission from Springer Science and Business Media
© 2014 American Society of Plant Biologists
Plant and microbial exudates can
increase Pi availability
Depletion Zone
Exudates from free-living and
symbiotic microbes also
contribute to P solubilization
Phytase-producing
bacteria
Phytate
C6H18O24P6
Low Molecular
Weight Organic
Acids (LMWOA)
Pi
Malate
Phosphatases
(enzymes)
Al-P
Organic
phosphates
Pi
Pi
Pi
Al-Malate
© 2014 American Society of Plant Biologists
Arbuscular mycorrhizal fungi
facilitate P-uptake in most plants
~80% of plants associate
with mycorrhizal fungi;
these associations can
facilitate P uptake
Karandashov, V. and Bucher, M. (2005). Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci. 10: 22-29 with permission from Elsevier; see also Smith, S.E., Jakobsen, I., Grønlund, M. and Smith,
F.A. (2011). Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and
manipulating plant phosphorus acquisition. Plant Physiol. 156: 1050-1057. (See also Teaching Tools in Plant Biology 19: Plants and their Microsymbionts).
© 2014 American Society of Plant Biologists
Root system architecture can optimize
foraging for phosphate
Root traits associated with enhanced
phosphate uptake:
• Reduced gravitropism
• Increased formation and elongation of
lateral roots and root hairs
• Aerenchyma (air spaces that allow
metabolically inexpensive growth)
Aerenchyma
Péret, B., Clément, M., Nussaume, L. and Desnos, T. Root developmental adaptation to phosphate starvation: better safe than sorry. (2011). Trends Plant Sci. 16: 442-450 with
permission from Elsevier; Lynch, J.P. (2011). Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiol. 156: 1041-1049.
© 2014 American Society of Plant Biologists
Many species of the family
Proteaceae found throughout
the Southern Hemisphere make
short-lived “proteoid” or “cluster”
roots to facilitate P uptake
Banksia ericifolia flower
Simple and compound
Proteaceae root clusters
Lambers, H., Finnegan, P.M., Laliberté, E., Pearse, S.J., Ryan, M.H., Shane, M.W. and Veneklaas, E.J. (2011).
Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: Are there lessons to be learned
for future crops? Plant Physiol. 156: 1058-1066.
© 2014 American Society of Plant Biologists
Cluster roots increase surface area
and also root exudation
White lupin
(Lupinus albus) is
a cluster-root
producing legume
that provides a
good genetic
model
Cheng, L., Bucciarelli, B., Shen, J., Allan, D. and Vance, C.P. (2011). Update on white lupin cluster root acclimation to phosphorus deficiency Plant Physiol. 156: 1025-1032. Lambers, H., Clements, J.C. and Nelson,
M.N. (2013). How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am. J. Bot.. 100: 263-288.
© 2014 American Society of Plant Biologists
PHT1 phosphate transporters
mediate uptake and transport
Most are
expressed in roots
and other tissues
9 PHT1 genes in
Arabidopsis, 13 in rice,
12 in poplar. Some are
mycorrhiza inducible
PHT transporters are H+/
PO43- co-transporters
that have 12 membranespanning domains
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.
© 2014 American Society of Plant Biologists
P-Starvation Inducible responses
increase P uptake and recycling
Proteaceae show metabolic adaptions to Pimpoverished soils such as very efficient use of P
Ribosomes (rRNA) are the major form of organic P.
Proteaceae maintain a very low copy number of
ribosomes, yet are photosynthetically efficient
Proteaceae also show delayed
greening; ribosomes first promote
growth, then chloroplast maturation
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.
© 2014 American Society of Plant Biologists
PSI (phosphate-starvation induced)
are upregulated by PHR1
PSI genes encode
phosphatases,
transporters,
regulatory factors….
SPX1 interferes with PHR1
binding to its DNA binding site
(P1BS). In yeast, SPX1 proteins
act as Pi sensors
The interaction between SPX1
and PHR1 is Pi-dependent….
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 phosphatedependent 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.
© 2014 American Society of Plant Biologists
Regulatory controls prevent Pi from
over accumulating
PHO1 is a transporter that
moves Pi into xylem for
transport to the shoot
PHT transporters take up Pi
Pi
xylem
shoot
root
PHO1
PHT
Pi
PHO2 is an E2 ligase
that targets
transporters for
proteolysis
In pho1 mutants, too
much Pi accumulates
in the root and too
little in the shoot
In pho2 mutants,
too much Pi
accumulates in the
shoot and too little
in the root; transport
is out-of-control
PHO2
PHO1
Too much
or too little
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.
© 2014 American Society of Plant Biologists
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 with permission from Elsevier.
© 2014 American Society of Plant Biologists
PHO2 accumulation is regulated by
miR399 expression
When Pi is ample, PHO2
targets PHO1 for
degradation
+ Pi
P starvation induces
expression of miR399,
which targets PHO2 mRNA
for degradation
- Pi
Pi
PHO2
mRNA
PHO2
PHO1
PHO2
A target mimic IPS1
fine-tunes the effects
of miR299; by binding
stably to miR399,
IPS1 supports PHO2
expression
xylem
PHO2
PHO2
mRNA
miR399
Pi
PHO1
PHO2
miR399
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.
© 2014 American Society of Plant Biologists
P uptake & transport are regulated
by local and systemic signals
Suppression of shoot
branching
Strigolactones
Phosphate
starvation
signal
(unknown)
Establishment of
plant – mycorrhizal
fungi symbiosis
PHT1 transporters
PHR1
(transcription factor)
Phosphatases,
organic acid
synthases
PHO1
IPS1
miR399
Enhanced
uptake
PHO2
PHT1
(miR399 is a negative
regulator of a negative
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.
© 2014 American Society of Plant Biologists
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
© 2014 American Society of Plant Biologists
Many different transgenic lines have
been tested for enhanced P uptake
Modifying
regulators of P
signaling network
Releasing Pi from
insoluble pools
(through organic acid
extrusion, proton
pumping, and
phosphatases)
Success has
been mixed
Optimizing root
architecture
Enhancing high
affinity uptake
(PHT1 transporter)
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 with permission from Elsevier.
© 2014 American Society of Plant Biologists
Selection for root architecture traits
can lead to increased P uptake
P-uptake efficiency can be correlated
to more efficient root traits
P-efficient
root system
P-inefficient
root system
P-efficient 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 by permission of Oxford University Press.
© 2014 American Society of Plant Biologists
Rice adapted to poor-soil regions
revealed a key protein kinase
• The Pup1 (Phosphate Uptake 1)
major QTL was identified in ausvariety rice adapted to poor soils
• Eventually this was revealed to
encode a protein kinase PSTOL1
not present in other rice genomes
• Overexpression of PSTOL1 leads
to enhanced root growth
Overexpressor
Control
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.
© 2014 American Society of Plant Biologists
Phosphate recovered
from human urine alone
could replace >20% of
phosphate demands
Human urine is rich
in phosphate, and it
can be separated
from other waste at
the point of origin
Urine can be
applied directly to
plants as liquid
fertilizer
Urine-reclaiming toilet
P and N can be precipitated out of wastewater
Is it feasible to reuse, recapture and
recycle phosphate?
Cleaner
wastewater
out
Mg
Mg
N & P-rich
Wastewater in
P
P
Struvite
(NH₄MgPO₄·6H₂O)
crystals harvested
for use as fertilizer
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
© 2014 American Society of Plant Biologists
Strategies have been developed to
impede P from entering waterways
Chemical and biological processes
including algal production can
effectively remove P from wastewaters
Timing of fertilizer application and
management of water flow from can decrease
the amount of P that enters 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.
© 2014 American Society of Plant Biologists
Summary: Phosphorus
• First or second most commonly limiting nutrient
• Very insoluble and immobile in soil
• Roots mine and forage for P through exudations and
symbioses
• Root system architecture is particularly sensitive to P
• Uptake involves positive and negative controls
• Strategies are available to minimize P pollution
© 2014 American Society of Plant Biologists