FACULTY OF SCIENCE
Opportunities for improving
phosphorus-use efficiency in crop plants
Erik Veneklaas
School of Plant Biology - UWA

Perth

UWA
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New Phytologist 195:306-320

Phosphorus is an essential mineral nutrient for plants
Plants contain approximately 0.1% of P
1/100
1/1000
1/1000 – 1/100,000
P cannot be substituted by any other element
www.soil-net.com

P in agriculture: open systems requiring large P inputs
CROP
residues uptake
SOIL
fertilizer
product
runoff
drainage
unavailable P
Can we have more
product with less P?
Losses to the
environment need
to be minimized!
P needs to be used more efficiently: better yield, more recycling

Mohr & Evans (2013) http://www.philica.com
We are running out of P reserves
“Peak P”
1900 2000 2100 2200
Supply, Demand (Mt P per year)
Projected P supply, using optimistic estimates of P reserves and
assuming a stabilizing demand.
P cannot be “produced” like N (industrially or plant-mediated).

Fertilizer phosphorus will become scarce and expensive
Environmental impact of P is undesirable
Aim: produce more food with less P
= increase P use efficiency
Most food contains more P than we need.
• Most P in cereal and legume grains is phytate.
• Phytate cannot be used by humans and most animals, and
restricts the bioavailability of Fe and Zn.

PUE definitions
P acquisition efficiency (= P uptake efficiency):
P taken up by plant / P in soil
P use efficiency (= P utilization efficiency) = PUE:
dry mass production (or yield) / P taken up by the plant

Crops have high P (but higher N) compared to other plants
Crops are high in leaf N and P compared to non-crops
Crops are high in N/P compared to non-crops with high N and P
Presumably due to selection for fast growth and high N

What are the main P pools?
10
8
5
3
0
0 5 10 15
P fractions concentrations (mg g-1 DW)
Sum of P fractions (mg g-1 DW)
Pi
Nucleic acids
Lipid P
Ester P
1.0
0.8
0.6
0.4
0.2
0.0
<1 1-2 2-4 4-8 >8
Total P (mg g-1)
fractions
At high tissue P concentrations, much P is inorganic.
This 5 Pi is located in 10 vacuoles and is 15
not engaged in metabolism.
Sum of P fractions (mg g-1 DW)
Pi
Nucleic acids
Lipid P
Ester P
Sum of P fractions (mg g-1 DW)
P fraction concentration (mg g-1 DW)

Where is P in plants?
Inorganic phosphate (Pi)
• low and well-regulated concentrations in cytoplasm
• vacuole stores excess Pi, should be minimized
“Ester P”
•Water-soluble small molecules, e.g. sugar phosphates, ATP
• Small pool, can probably not be reduced
Nucleic acids
• DNA and RNA
Phospholipids
• membranes

Nucleic acid P
• represents ~40% of all organic P
• 85% is RNA
• RNA: ~90% is ribosomal (rRNA)
• Ribosomal RNA important for protein synthesis and thus
growth
• But rRNA and protein synthesis capacity stay very high in
fully developed tissue
• Functions include turnover, repair, senescence processes
• Reduction of rRNA may reduce adaptability and stress
tolerance?

Can rRNA levels be reduced?
Crops use a lot of RNA to produce proteins (more than trees)
Reduction of excess protein synthesis capacity may be
possible in well-managed crops
Protein / RNA
Algae Crops Trees

Lambers et al. (2012)
New Phytologist 196:1098-1108
Lipid P is mainly found in membranes
Phospholipids may be substituted by sulfolipids and
galactolipids (as in chloroplasts)
galactolipids
sulfolipids
phospholipids
This substitution is often found in P-starved plants
Implications for membrane properties are not fully known

Effects of low P are partly due to signalling, not just P deficiency
Rouached et al. (2011) Plant J. 65:557-570
Lower P status without a decrease of growth rate, presumably due
to lack of signalling
Unlinking Pi status and signalling may enable better growth at low P

Dissecting PUE
PUE =
biomass production per unit P per unit time X P residence time
Carbon balance and the role of P in it
Tissue longevity
Internal recycling of P
photosynthesis
high P
fast growth
time
low P
slow growth

Photosynthetic P-use efficiency = net photosynthesis per P present
Global patterns using the “leaf economics spectrum” dataset
(Wright et al. (2004) Nature 428:821-827)
1.0
0.5
0.0
-0.5
-1.0
-1.5
1.0 1.5 2.0 2.5 3.0 3.5
log [P] (mg g-1)
log LMA (g m-2)
3.0
2.5
2.0
1.5
1.0
0.5
0.0
1.0 1.5 2.0 2.5 3.0
log Amass (nmol g-1 s-1)
Higher Leaf Dry Mass per Area (LMA): thicker, denser leaves
Longer leaf lifespan
log LMA (g m-2)
P concentration Photosynthesis

Photosynthetic P-use efficiency: net photosynthesis per P present
3.0
2.5
2.0
1.5
1.0
0.5
0.0
1.0 1.5 2.0 2.5 3.0
log A/P (μmol g-1 s-1)
log LMA (g m-2)
PPUE = A / P
There is no clear trend with increasing LMA
There is an order-of-magnitude range at any LMA

Some of the variation in A/P at a given LMA is related with [N]
A/P (μmol g-1 s-1)
Leaf N/P > 15
“P-limited”
129.4
Leaf N/P < 15
“N-limited”
59.3
3.0
2.5
2.0
1.5
1.0
0.5
0.0
N/P < 15
N/P > 15
1.0 1.5 2.0 2.5 3.0
log A/P (μmol g-1 s-1)
log LMA (g m-2)
Much higher Photosynthetic P-use Efficiency in “P-limited” than “N-limited”
plants
Implication for agronomy: plant production is most efficient when all
resources are used optimally at all times

How does this work out over the life-time of a leaf?
Photosynthetic P use efficiency:
Rate of (maximum) net photosynthesis per amount of P present
Lifetime leaf PUE:
Amount of C (or dry matter) gained per amount of P used (= P
lost upon senescence)
photosynthesis
high P
fast growth
time
low P
slow growth

Modelling of leaf lifetime PUE based on:
• photosynthesis and respiration
• leaf construction cost
0.12
• leaf lifespan
• leaf P concentration
0.08
• P remobilization
0.04
0.00
40, 60 or 80% P remobilization
80%
40%
60%
0 200 400 600
A/P (g C mg-1 P)
LMA (g m-2)
Conclusions:
• Lifetime leaf PUE is very similar for leaves with very different
physiology and morphology
• Long lifespans compensate for low photosynthetic rates
• Fast growth is not incompatible with efficient P use
• P remobilization is vital for high lifetime leaf PUE

How do roots compare in terms of P economy?
Fine root P concentrations are high, like in leaves.
Fine roots have high turnover rates, like leaves.
Remobilization of P in roots is similar to that in leaves (?)
Variation in these traits is largely unexplored.
Temperate angiosperms Temperate gymnosperms Subtropical-tropical
Li et al. (2010)
Funct. Ecol. 24:224-232
Gill & Jackson (2000)
New Phytol. 147:13-31
Turnover (yr-1)
Root diameter (mm)

An extreme leaf-root contrast in PUE in a low-P environment
Trait Banksia leaf Banksia cluster root
[P], mg g-1 0.2 1
Life span, yr 3 0.1
P remobilisation, % 80 90
P cost, mg g-1 yr-1 0.01 1.0
P cost per unit standing crop per year may be 100X more for cluster roots than leaves

From leaf to plant scale – P remobilization in growing plants
Remobilization from a senescing leaf can
potentially supply P for a growing leaf
Relative growth rate (g g-1 d-1)
is proportional to
leaf replacement rate (d-1)
=
1/(leaf lifespan)
P
P

P recycling in the vegetative plant
60
50
40
30
20
10
0
remobilisation = 80%
0 10 20 30
% P from remobilisation
time
current
cumulative
Remobilization only starts
contributing to P economy
when there is senescing
tissue
Even with constant growth rate, senescence, [P] and remobilization:
• % P derived from remobilization increases only slowly over time
• total % P derived from remobilization for vegetative growth is
considerably less than the % P remobilized from senescing biomass

P recycling becomes important for later vegetative growth and grain filling
Shortlived species;
exponential growth followed
soon by senescence
Conclusions:
• P remobilization can reduce
dependency on soil P during later
stages of crop
• P remobilization during vegetative
growth is more important in crops
with long growing seasons and short
leaf life-spans, forming dense stands
100
80
60
40
20
0
biomass produced
biomass shed
live biomass
senesced
0 10 20 30 40 50
biomass
time
live
total
biomass
time
1500
1000
500
0
P taken up
P remobilised
total taken up
total remobilized
0 10 20 30 40 50
P
time
P
time

Transition to reproductive growth
In this period 30-90% of
plant P is remobilized
100
50
0
into the grain
whole
plant
vegetative
plant
0 20 40 60 80 100
P content (mg)
Time after sowing (d)
Plant P content (mg)
Time after sowing (d)
rice
wheat
lupin
canola
sunflower

Redistribution of P in the plant, from germination to maturity
Reducing the P flux to grain
• may allow for longer use of P for photosynthesis
• would help reduce P export from the field

P is very efficiently remobilized from plant to grain
PHI =
Grain P
Total P
?
Grain mass
Total mass
N/P = 6
N/P = 12
HI =
Grain is relatively enriched in P (compared to plant P and grain N).
Can this be reduced, for the benefit of PUE and nutrition?

[P] in grain has already been reduced through selection
0.6
0.4
0.2
0
Domestication of wheat Historic wheat cultivars
diploid tetraploid hexaploid
P concentration in grain (%)
high P
low P
Calderini et al. (1995) Ann. Bot. 76:315-322
Batten et al. (1986) Ann. Bot. 58:49-59
Mainly due to ‘dilution’ (more starch).
Further progress may be possible; physiological limits are unknown
but links with N and C are likely.

“Ideotype” for efficient use of P
Fast and early P uptake and efficient internal recycling of P
• P will be in plant for a longer time to be used
productively
High photosynthesis at low P
• No excess P in tissues (including roots and stems)
• More productive use of P
Low grain P • More P returns to the soil
• Less P is lost to the environment
• Improved nutritional value
[Need to watch possible early vigour penalty]

Where to invest scarce P? Soil P banks and P debts ...
yield
increased PUE
soil P
Yield benefit of high PUE will probably be highest in low-P soils

Where to invest scarce P? Soil P banks and P debts ...
yield
increased PUE
soil P
Fertilizer savings in high-P soils should be invested in low-P soils
(but only if there are no other major limitations to yield?)

CONCLUSIONS
Increased PUE and wiser use of P fertilizer is desirable and probably
vital to ensure P fertilizer availability for future generations
P is fundamentally different to N in its physiology, agroecology,
fertilizer management and environmental implications
PUE may be increased by decreasing certain P pools and by
improving remobilization to where it is used most productively
Use of all resources (P, N, water) is most efficient when they are
all balanced;
Decisions about the distribution of these resources have large
agronomical but also large socio-economical and political
implications

Acknowledgements
Hans Lambers, John Raven and
other co-authors of the review
Ian Wright/Peter Reich/Glopnet
and many others …
The University of Western Australia
Contact:
Erik.Veneklaas@uwa.edu.au

The University of Western Australia
P in ecosystems: tight cycling
VEGETATION
litter uptake
SOIL
weathering +
atmosphere
runoff
drainage
unavailable P
Nevertheless: old weathered soils are very low in soil P

The University of Western Australia
Sclerophyllous Banksia leaves have quite high
Photosynthetic P-use Efficiency
3.0
2.5
2.0
1.5
1.0
0.5
0.0
N/P < 15
N/P > 15
1.0 1.5 2.0 2.5 3.0
log A/P (μmol g-1 s-1)
log LMA (g m-2)
In blue: Banksia spp.
Foteini
Hassiotou
Banksia victoriae Banksia
Patrick Mitchell

PUE over the life-time of a leaf (in the context of
the Leaf Economic Spectrum)
C balance: High-LMA leaves live longer but have lower
rates of photosynthesis …
P balance: High-LMA leaves have lower [P] and may
have higher remobilisation …
The University of Western Australia
150
100
50
0
0 100 200 300 400
LL (mo)
LMA (g m-2)
500
400
300
200
100
0
0 100 200 300 400
Amass (nmol g-1 s-1)
LMA (g m-2)
5
4
3
2
1
0
0 100 200 300 400
[P] (mg g-1)
LMA (g m-2)
Data: glopnet database – Wright et al. (2004) Nature
428:821-827

The University of Western Australia
Assumptions for life-time C and P balance:
C balance = (mean daily net photosynthesis – respiration) X lifespan –
leaf C cost
Photosynthetic capacity (Amass) scales with mean net photosynthesis (daily
basis):
• Daily C balance accounts for suboptimal light conditions, respiration.
• Amass declines over lifetime of leaf.
Reich et al. (2009) New Phytol. 183:153–166
P balance = (1-remobilised fraction) X leaf P content
Remobilisation is typically 40 to 80%, not strongly correlated with LMA

Leaf photosynthetic capacity scales with daily C balance
Zotz & Winter (1993) Planta 191:409-
412
Gottsberger (2002)
PhD thesis Universität
Wien
The University of Western Australia
Reich et al. (2009)
300
200
100
Tropical rainforest
Mediterranean
sclerophyllous
woodland
0 New Phytol. 183:153-166
0 5 10 15 20
Daily C balance (mmol m-2 d-1)
Amax (μmol m-2 s-1)
Cloud forest

Lifetime PUE does not correlate strongly with LMA but
percentage remobilization has a large impact
80
%
40%
60
%
The University of Western Australia
0.2
0.1
0.0
remobilization=60
%
0 200 400 600
lifetime PUE (g C mg-1 P)
LMA (g m-2)
0.12
0.08
0.04
0.00
0 200 400 600
A/P (g C mg-1 P)
LMA (g m-2)
Conclusion: There is large variation in PPUE and lifetime leaf
PUE, which doesn’t scale clearly with the Leaf Economics
Spectrum;
P remobilization is vital for high lifetime leaf PUE.

Summary lifetime leaf PUE: comparing leaves with LMA 100 and 200 g
m-2
(P remobilisation 60%)
[P] X 0.57
lifetime P balance X 1.85
LMA 100 LMA 200
The University of Western Australia
30
20
10
0
LL X 3.3
LMA 100 LMA 200
100
50
0
Amax X 0.59
LMA 100 LMA 200
15
10
5
0
lifetime C balance X 2.01
LMA 100 LMA 200
1.5
1.0
0.5
0.0
LMA 100 LMA 200
200
150
100
50
0
0.06
0.04
0.02
0.00
lifetime PUE X 1.09
LMA 100 LMA 200
Despite large differences in morphology and physiology, PUE differs by
less than 10%

Remobilisation of P from senescing fine roots is
significant
Species from subarctic communities,
Sweden
Freschet et al. (2010)
New Phytol. 186:879-
889
Remobilisation of P from senescing roots has often been
claimed to be very small
Root N and P remobilisation rates and root life spans are
very poorly known but potentially very important
The University of Western Australia
Leaves
(n=40)
Stems (n=38)
Roots (n=11)

Banksia attenuata, observed at weekly intervals in a
minirhizotron
The University of Western Australia
Banksia root turnover and P remobilization
data are being quantified

P required to maintain biomass (e.g. mature perennial plants)
The University of Western Australia
1000
800
600
400
200
0
P
remobilisation
20%
40%
60%
80%
0 10 20 30
Annual P cost (% of P content)
Tissue lifespan (months)
No net growth – maintenance
only;
P uptake required to maintain
same amount of tissue with same
[P]

Reduction of rRNA levels in Arabidopsis
Sulpice et al (2014) PCE

Lessons from Nature?
Many of the traits identified are present in undomesticated plants
Plants on low-P soils have:
-Low tissue P concentrations
-Replace phospholipids by sulfo- and galactolipids
-Low levels of RNA
-Efficient internal P recycling
-Long tissue lifespans (often perennial plants)