© 2014 American Society of Plant Biologists

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, J. (1699). Some thoughts and experiments concerning vegetation.PhilosophicalTransactions of the Royal Society, 21,193-227.

“Some thoughts and

experiments concerning

vegetation” (1699)

Spring

water

Rain

water

Thames River

water

Weight gain:

55% 62% 93%

Woodward concluded that mineral matter

nourishes plants, laying the foundation for

the study of plant mineral nutrition

Woodward compared plant

growth in water containing

different amounts of

“mineral matter” to test the

assumption that water is a

plant’s sole requirement

© 2014 American Society of Plant Biologists

“Law of the Minimum”: Nutrient in

least supply limits growth

Biodiversity Heritage Library

Justus von Liebig

1803 - 1873

Carl Sprengel

1787 - 1859

Growth is determined by

whichever nutrient is

present in shortest supply

Stamp issued 150

years after his birth

© 2014 American Society of Plant Biologists

Lawes & Gilbert began investigating

plant nutrition at Rothamsted 1843

Images used by permission of Rothamsted Research

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 chemically-

synthesized fertilizers

© 2014 American Society of Plant Biologists

Plants assimilate mineral nutrients

from their surroundings

K+

K+

PO43-

PO43-

PO43-

NO3-

NO3-

K+ K+

K+

K+

K+

K+

PO43-

PO43-

PO43-

NO3-

NO3-

Nutrient assimilation can

occur across the surface of

the plant or through the root

system of vascular plants

© 2014 American Society of Plant Biologists

Plants assimilate mineral nutrients

mainly as cations or anions

μmol / g (dry wt)

Element Assimilated form

250 Potassium (K) K+

1000 Nitrogen (N) NO3-, NH4

+

60 Phosphorus (P)

HPO42-,

H2PO4-

30 Sulfur (S) SO42-

80 Magnesium (Mg)

Mg2+

125 Calcium (Ca) Ca2+

μmol / g (dry wt)

Element Assimilated form

2 Iron (Fe) Fe3+, Fe2+

0.002 Nickel (Ni) Ni+

1 Manganese (Mn)

Mn2+

0.1 Copper (Cu) Cu2+

0.001 Molybdenum (Mo)

MoO42+

2 Boron (B) H3BO3

3 Chlorine (Cl) Cl-

0.3 Zinc (Zn) Zn2+

MACRONUTRIENTS MICRONUTRIENTS

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

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.

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

© 2014 American Society of Plant Biologists

Vascular plants assimilate mineral

nutrients mostly via roots

Barberon, M. and Geldner, N. (2014). Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiol. 166: 528-537.

By increasing surface area for

absorption, root hairs functionally

resemble microvilli of an animal’s

intestinal epithelium

Membrane transporters facilitate nutrient uptake

© 2014 American Society of Plant Biologists

Roots have several adaptations to

enhance nutrient capture

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.

Fungal symbiotic

partners

Prokaryotic

symbiotic

partners

Developmental

responses Biochemical

responses

© 2014 American Society of Plant Biologists

Nutrient uptake, assimilation and

utilization involve many processes Nutrient

uptake

efficiency

Nutrient

utilization

efficiency

Root system

architecture

Root

exudates

Rhizosphere

microbiota

Symbioses

P

P

N N

NH3

Transporters

and pumps

Intercellular

transport

efficiency

X R-X

Assimilation and

remobilization

efficiency

Regulatory and

control

networks

© 2014 American Society of Plant Biologists

Soil pH affects nutrient availability-

Some soils are acidic, others basic

Atlas of the biosphere, University of Wisconsin; FMoeckel

Strongly

acidic

Mildly

alkaline

© 2014 American Society of Plant Biologists

Physical and biological processes

affect nutrient availability

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.

Erosion, rainfall patterns,

cultural practices, soil

biodiversity, soil pH,

atmospheric gases etc. all

affect soil fertility

© 2014 American Society of Plant Biologists

Nutrients removed from soils can be

replenished with fertilizers

Total nutrient requirement

Typical fertilizer application

Corn

Soy W

he

at

Co

tto

n

Ric

e

Kg

/ha

K

g/h

a

1000

800

600

400

200

0

0

200

400

Nitrogen

Phosphate

Potash

Magnesium

Sulfur

Most fertilizers

contain nitrogen

(N), phosphorus

(P) and potassium

(K). Some include

other elements

Fertilizers can be

complex waste

products or

refined blends of

nutrient salts

Plants remove nutrients from the soil

Source: USGS

© 2014 American Society of Plant Biologists

Global mineral nutrient resources

are unevenly distributed

Supply > Demand

Supply < Demand

FAO (2011) Current world fertilizer trends and outlook to 2015.

N

P2O5

K2O

© 2014 American Society of Plant Biologists

The global trade in fertilizers is

worth billions of dollars annually

IFIA

Ammonium Urea Potash Diammonium

phosphate

Monoammonium

phosphate

Phosphate

rock

Sulfur Sulfuric

acid

© 2014 American Society of Plant Biologists

How much is the right amount of

fertilizer to apply to a field?

Photo by Michael Russelle.

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

Cultivation

practices: Is

unharvested

material removed,

or left to replenish

the soil?

Abiotic and biotic

factors: Temperature,

rain, stress and pests

or pathogens affect

nutrient needs

Developmental stage affects plant needs

Interactions between nutrients:

There are both positive and negative

interactions between various nutrients

Financial considerations:

Balancing the cost of fertilizers with

the gain reaped from their use

© 2014 American Society of Plant Biologists

Fertilizer use can cause

environmental and health problems Nitrogen fixation is

energy demanding

Phosphate and potash

mining is destructive

Image source: Lamiot; Alexandra Pugachevsky

Transport requires energy

Human and animal waste

can spread disease N O N

Nitrous oxide (N2O)

derived from fertilizer is a

major greenhouse gas

Nutrient runoff pollutes

waterways and can lead

to eutrophication

Plants need

nutrients, but their

application isn’t

always optimal or

sustainable – how

can plant science

contribute to

better practices?

© 2014 American Society of Plant Biologists

Fertilizer use is increasing to keep

pace with population growth

Rock weathering

Decaying matter

Organic matter

Inorganic matter

Fertilizers

Deposition

from

atmosphere

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

Nitrogen is one of

the three major

macronutrients found

in most fertilizers

N is in amino acids

(proteins), nucleic

acids (DNA, RNA),

chlorophyll, and

countless small

molecules

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,

ammonium ion -3

N2 Nitrogen 0

N2O Nitrous oxide +1

NO Nitric oxide +2

HNO2, NO2- Nitrous acid,

nitrite ion +3

NO2 Nitrogen dioxide +4

HNO3, NO3-

Nitric acid, nitrate ion +5

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.

NO2-

NO3-

NO2- NO

N2O

N2

NH3

Nitrate

reduction

Nitrogen

fixation

Nitrification

Anaerobic

reactions

Aerobic

reactions

© 2014 American Society of Plant Biologists

Plants are an important part of the

global nitrogen cycle Atmospheric pool of N2

Biological

fixation

Atmospheric

fixation Industrial

fixation

NO3-

NH4+

NO3-

NH4+

NO3-

NO2- NO3

- NH4

+

Nitrification by nitrifying bacteria

R-NH2

manure

Assimilation

by plants

decomposition

De

nitrifica

tio

n b

y

de

nitri

fyin

g b

acte

ria

Biological

fixation

(oceans)

120 Tg N / yr

(50%

agricultural)

120

Tg N / yr

140

Tg N / yr

5 Tg N / yr

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 nitrogen

taken up into

the plant?

How is inorganic

nitrogen

assimilated into

organic

molecules?

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 N-

utilization?

© 2014 American Society of Plant Biologists

Nitrogen metabolism: Uptake,

assimilation and remobilization

Uptake

NO3-

NH4+

NH4+

NO3-

Nitrate

reductase

NO2-

Nitrite

reductase

Glutamine

synthetase

(GS)

Glutamate

Glutamine

Incorporation into

amino acids and

other nitrogen-

containing

compounds

Amino acid

recycling,

photorespiration

Carbon pools

TCA cycle

2-oxoglutarate

Glutamate

Glutamine-2-

oxoglutarate

aminotransferase

(GOGAT)

Assimilation

Remobilization

Assimilation NH4

+

R-NH2

N2 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 NO3-

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.

Nitrate

reductase

Nitrite

reductase

NO2- NO3

- NH4

+

Nitrification by nitrifying prokaryotes

Energy

released

Energy

released

Many prokaryotes oxidize NH4+,

so soil NH4+ levels are often low

NO2- NH4

+ NO3

-

Energy

consumed

Energy

consumed

Plants use energy to reduce NO3- for

assimilation into organic compounds

R-NH3

Plant preferences for NH4+ vs NO3

- vary by species, other

metabolic processes, temperature, water, soil pH etc….

© 2014 American Society of Plant Biologists

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

HATS = high affinity

transporters

LATS = low affinity

transporters

© 2014 American Society of Plant Biologists

A major nitrate importer was the first

cloned: CHL1/ NRT1.1/ NPF6.3

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.

Chlorate (ClO3-)

mimics nitrate

(NO3-)

Nitrate

reductase

Chlorite

ClO2-

Wild-

type

Chlorate

uptake

mutant

(chl1-5)

Nitrate

reductase

mutant

+ + -

Growth on

chlorate

Nitrate

reductase

activity

The first nitrate

transporter was

identified using a

genetic selection for

chlorate resistance

1973

In 1993 the CHL1 gene was cloned and

found to be a nitrate transporter

(shown = current in Xenopus oocytes)

© 2014 American Society of Plant Biologists

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 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.

Specific transporters move nitrate

(or other N-containing

compounds) inwards and

outwards across the PM and

across the vacuolar membrane

Nitrogen uptake but also assimilation and

recycling depend on membrane transporters

© 2014 American Society of Plant Biologists

Primary N assimilation: NO3- is

reduced to NH4+ prior to assimilation

Uptake

NO3-

NH4+

NH4+

NO3-

Nitrate

reductase

NO2-

Nitrite

reductase

Glutamine

synthetase

(GS)

Glutamine

Assimilation

into organic

compounds

All other N-

containing

compounds

R-NH3

Glutamate

© 2014 American Society of Plant Biologists

Nitrate reductase is a large enzyme

with a complex catalytic scheme

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.

NO2- NO3

-

NADH NAD+

NADH

NO3-

Nitrate reductase

reduces nitrate to nitrate

with NADH acting as the

electron donor

The electrons move from

NADH to FAD to heme

to a molybdenum

cofactor (Moco) to NO3-

© 2014 American Society of Plant Biologists

GS/GOGAT assimilates inorganic

nitrogen into organic molecules

NH4+

Glutamine

synthetase

(GS)

Glutamate

Glutamine

Incorporation into

amino acids and

other nitrogen-

containing

compounds

Amino acid

recycling,

photorespiration

Carbon pools

TCA cycle

2-oxoglutarate

Glutamate

Glutamine-2-

oxoglutarate

aminotransferase

(GOGAT)

Assimilation

Remobilization

Uptake

© 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

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.

Leaves Roots, Cotyledons

Amino acids Amino acids

Glutamate Glutamate

Glutamate Glutamate Glutamine Glutamine

NH4+

NH4+

NADH-GOGAT Fdx-GOGAT

Chloroplast

localized GS2 Cytosolic GS1

Assimilation Assimilation

AA

catabolism Photo-

respiration

Each N atom may cycle through GS

many times as amino acids are recycled

during growth and senescence and

released due to photorespiration

uptake

assimilation

assimilation

remobilization

remobilization

© 2014 American Society of Plant Biologists

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.

In some plants, most grain N is

remobilized from vegetative tissues

The relative amount of N

taken up pre- and post-

flowering is important in

nitrogen use efficiency

Different crop rely more or

less on N remobilization

from vegetative tissues

© 2014 American Society of Plant Biologists

Summary: Plant nitrogen uptake and

assimilation

Uptake

NO3-

NH4+

NH4+

NO3-

Nitrate

reductase

NO2-

Nitrite

reductase

Glutamine

synthetase

(GS)

Glutamate

Glutamine

Incorporation into

amino acids and

other nitrogen-

containing

compounds

Amino acid

recycling,

photorespiration

Carbon pools

TCA cycle

2-oxoglutarate

Glutamate

Glutamine-2-

oxoglutarate

aminotransferase

(GOGAT)

Assimilation

Remobilization

Assimilation NH4

+

R-NH2

N2 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

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.

NITROGEN DEFICIT

Increase uptake

Metabolic adaptations to low-N

Accelerated senescence and nitrogen

remobilization

Activation of some NO3- and NH4

+ transporters

Preferential growth of root relative to shoot

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)

© 2014 American Society of Plant Biologists

Responses to NO3- can be separated

from those to N-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.

Nitrate

reductase

Nitrite

reductase

NO2- NH4

+ NO3

- R-NH3 X

Nitrate reductase mutants allow responses to NO3-

to be separated from responses to N-metabolites

Red indicates

nitrate-specific

genes

NR mutant can’t grow

on NO3-

Transcriptional responses

to nitrate (+ downstream

metabolites)

10% of the

genome responds

to nitrate, but only

some genes are

nitrate-specific

© 2014 American Society of Plant Biologists

CHL1/NRT1.1/NPF6.3 is a nitrate

transceptor (sensor)

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.

Lateral roots of

transceptor mutants

(chl1-10) fail to

respond to the HN

environment

In wild-type

plants (Ws),

lateral root

growth is

stimulated

in High

Nitrate (HN)

WT

chl1-5

Transceptor mutants

(chl1-5) also show

abnormal transcriptional

responses to nitrate

© 2014 American Society of Plant Biologists

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.

When nitrogen is abundant,

plants allocate less biomass

to their roots

When nitrogen

distribution is patchy,

roots proliferate in the

nutrient rich patches

Roots respond to local and systemic

nitrogen availability

© 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)

C.KCl plants

Both chambers

contain KCl (local

and systemic

signals indicate

NO3- deficiency)

Sp.NO3 roots

experience locally

high NO3- but also

N-deficiency

signals derived

from Sp.KCl roots

Sp.KCl roots

Experience locally

deficient NO3-

conditions but also

N-sufficient signals

from Sp.NO3 roots

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 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

Signals from the N-

deficient roots promote

elevated root growth in

Sp.NO3 as compared to

C.NO3, indicating that a

response to systemic N-

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. 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

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.

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

systemic N-

demand induced

increase in root

length

*

Growth augmentation

correlating to N-starvation

© 2014 American Society of Plant Biologists

Model of the effects of (some) local

and systemic signals

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.

Local NO3 effect

Systemic Systemic

Loss-of-function

receptor mutants for

root-derived peptides

do not downregulate

root growth when N is

abundant

WT LOF

Other factors that contribute

to local and systemic signals

include auxin, amino acids,

transcription factors and root-

derived peptides

© 2014 American Society of Plant Biologists

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.

NPF6.3

NO3-

Auxin NPF6.3

NO3-

Auxin

When NO3- is

low, NPF6.3

transports

auxin away

from the root

tip and growth

is inhibited

When NO3- is

high, auxin

transport

through

NPF6.3 is

suppressed

and growth is

promoted

© 2014 American Society of Plant Biologists

Strategies to improve nitrogen-use

efficiency and decrease N pollution

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

Nitrogen fixation is

energy demanding N O N

Nitrous oxide (N2O)

derived from fertilizer is a

major greenhouse gas

Unhealthful nitrate from agricultural

uses pollutes groundwater

Lake Erie

Cyanabacterial bloom

© 2014 American Society of Plant Biologists

Co-cropping and monitoring can

decrease the need for N application

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.

Co-cropping or

growing in rotation

with legumes enriches

soil N content

Chlorophyll can

be measured

the

transmission

ratio of 653 nm

to 931 nm light

N status can be

determined by

chlorophyll

content, measured

by reflected light

© 2014 American Society of Plant Biologists

Slow-release fertilizers can match

release to requirements

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

Traditional fertilizers don’t match

nitrogen availability to plant needs.

Slow release fertilizers can more

closely match plant needs

Traditional fertilizer –

one or two applications

Plant growth

requirements

Slow-release

fertilizer

Time

Am

ount

of

fert

ilize

r availa

ble

UREA N

N

N Time

Coated urea dissolves and releases

slowly, but it can be expensive

H2O

H2O

© 2014 American Society of Plant Biologists

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.

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

© 2014 American Society of Plant Biologists

Altering flux into amino acid pools

can increase NUE

NH4+

Glutamine

synthetase

(GS)

Glutamate

Glutamine

Incorporation into

amino acids and

other nitrogen-

containing

compounds

Amino acid

recycling,

photorespiration

Carbon pools

TCA cycle

2-oxoglutarate

Glutamate

Glutamine-2-

oxoglutarate

aminotransferase

(GOGAT)

Assimilation

Remobilization

Uptake Pyruvate

Alanine

Alanine

aminotransferase

(AlaAT)

Storage

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

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

Traits of an

idealized

plant with

high NUE

Glutamine synthetase

activity is an important

component of NUE

In rice, a subunit

of a heterotrimeric

G protein

contributes to N-

sensitive growth

and N assimilation

© 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)

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.

• 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

P has roles in cell structure,

energy and information

storage and energy and

information transfer

© 2014 American Society of Plant Biologists

Phosphorus is an essential nutrient

and found in many biomolecules Membrane phospholipids

DNA and RNA

ATP

Phosphorus (P) is

assimilated and used as

phosphate (Pi) which

depending on the pH is

H2PO4- ,HPO4

2- or PO43-

H H H

© 2014 American Society of Plant Biologists

Plants are part of the global

phosphorus cycle: Preindustrial

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.

Essentially NO atmospheric pool of P

manure

decomposition

Terrestrial

cycle: Plant /

Animal / Soil

Slow leaching of P to

lakes and oceans

Slow weathering of P from

rock reserves to soil

Aquatic

cycle

Sedimentation

Upwelling

© 2014 American Society of Plant Biologists

Plants are part of the global

phosphorus cycle: Postindustrial

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.

Essentially NO atmospheric pool of P

manure

decomposition

Terrestrial

cycle: Plant /

Animal / Soil

Mining and commercial

processing accelerates P

entry to biosphere

Aquatic

cycle Modern practices accelerate runoff

Sewage

Urbanization removes P

from terrestrial cycle and

accelerates entry to

waterways, causing toxic

algal blooms

(eutrophification)

© 2014 American Society of Plant Biologists

Is the current rate of phosphorus

use sustainable?

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.

United

States

8%

Morocco

38%

South Africa

10%

Jordan

6%

China

27%

Manure

Phosphate

rock Human excreta Guano

1800 1900 2000 1950

Phosphate usage has increased

dramatically in the past 70 years Some have argued that we

are approaching a period

of “peak phosphorus” as

deposits become depleted

90% of the world’s

phosphate rock reserves

are found in 5 countries

© 2014 American Society of Plant Biologists

Phosphorus in soil is in the form of

immobile, insoluble complexes

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

Depletion Zone

Ca-P

Mg-P

Al-P Cation-phosphate complexes

are relatively insoluble and

immobile in soil; these

include oxides and

hydroxides of Al and Fe

Organic

phosphates

Fe-P

Plants don’t

take up organic

phosphate

Roots growing in 31P-labeled soil. Only P

immediately next to roots is taken up

© 2014 American Society of Plant Biologists

Plant and microbial exudates can

increase Pi availability

Depletion Zone

Organic

phosphates

Pi

Phosphatases

(enzymes)

Pi

Low Molecular

Weight Organic

Acids (LMWOA)

Malate

Al-Malate

Al-P

Exudates from free-living and

symbiotic microbes also

contribute to P solubilization

Phytate

C6H18O24P6

Phytase-producing

bacteria

Pi

Pi

© 2014 American Society of Plant Biologists

Arbuscular mycorrhizal fungi

facilitate P-uptake in most plants

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).

~80% of plants associate

with mycorrhizal fungi;

these associations can

facilitate P uptake

© 2014 American Society of Plant Biologists

Root system architecture can optimize

foraging for phosphate

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.

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

© 2014 American Society of Plant Biologists

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.

Many species of the family

Proteaceae found throughout

the Southern Hemisphere make

short-lived “proteoid” or “cluster”

roots to facilitate P uptake

Simple and compound

Proteaceae root clusters

Banksia ericifolia flower

© 2014 American Society of Plant Biologists

Cluster roots increase surface area

and also root exudation

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.

White lupin

(Lupinus albus) is

a cluster-root

producing legume

that provides a

good genetic

model

© 2014 American Society of Plant Biologists

PHT1 phosphate transporters

mediate uptake and transport

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.

Most are

expressed in roots

and other tissues

PHT transporters are H+/

PO43- co-transporters

that have 12 membrane-

spanning domains

9 PHT1 genes in

Arabidopsis, 13 in rice,

12 in poplar. Some are

mycorrhiza inducible

© 2014 American Society of Plant Biologists

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.

Proteaceae show metabolic adaptions to P-

impoverished 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

© 2014 American Society of Plant Biologists

PSI (phosphate-starvation induced)

are upregulated 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.

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….

© 2014 American Society of Plant Biologists

Regulatory controls prevent Pi from

over accumulating

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.

PHO1 is a transporter that

moves Pi into xylem for

transport to the shoot

PHT transporters take up Pi

PHO1

PHO2

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

Too much

or too little

is bad Pi

Pi

xyle

m

root

shoot

PHT

PHO1

© 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

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.

PHO2

PHO2

mRNA

+ Pi

PHO1

P starvation induces

expression of miR399,

which targets PHO2 mRNA

for degradation

PHO1

PHO2

PHO2

mRNA

- Pi

Pi

xyle

m

Pi

PHO2

miR399

miR399

IPS1

A target mimic IPS1

fine-tunes the effects

of miR299; by binding

stably to miR399,

IPS1 supports PHO2

expression

When Pi is ample, PHO2

targets PHO1 for

degradation

PHO2

© 2014 American Society of Plant Biologists

P uptake & transport are regulated

by local and systemic signals

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.

Strigolactones

Phosphate

starvation

signal

(unknown) PHR1 (transcription factor)

PHT1 transporters

Phosphatases,

organic acid

synthases

miR399

Suppression of shoot

branching

Establishment of

plant – mycorrhizal

fungi symbiosis

Enhanced

uptake

PHO2 PHT1

(miR399 is a negative

regulator of a negative

regulator of P uptake) IPS1

PHO1

© 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

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.

Modifying

regulators of P

signaling network

Releasing Pi from

insoluble pools

(through organic acid

extrusion, proton

pumping, and

phosphatases)

Optimizing root

architecture

Enhancing high

affinity uptake

(PHT1 transporter)

Success has

been mixed

© 2014 American Society of Plant Biologists

Selection for root architecture traits

can lead to increased P uptake

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.

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

© 2014 American Society of Plant Biologists

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.

• The Pup1 (Phosphate Uptake 1)

major QTL was identified in aus-

variety 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

© 2014 American Society of Plant Biologists

Is it feasible to reuse, recapture and

recycle phosphate?

Urine-reclaiming toilet

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

N & P-rich

Wastewater in P

P

Mg

Mg

Struvite

(NH₄MgPO₄·6H₂O)

crystals harvested

for use as fertilizer

Cleaner

wastewater

out

P a

nd

N c

an

be

pre

cip

ita

ted

ou

t o

f w

aste

wate

r

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

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.

Timing of fertilizer application and

management of water flow from can decrease

the amount of P that enters waterways

Chemical and biological processes

including algal production can

effectively remove P from wastewaters

© 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