This document summarizes a presentation about opportunities to improve phosphorus-use efficiency in crop plants. It discusses how phosphorus is essential for plants but finite reserves exist, creating a need to produce more food with less phosphorus input. Various strategies are presented to improve phosphorus acquisition and utilization efficiency, such as increasing phosphorus recycling within plants and reducing phosphorus concentrations in plant tissues like leaves, roots and grain.

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

2. Perth

3. UWA
• 20000 Undergraduate students
• 2000 PhD (Research) students
• 1500 academic staff
• Ranked 88 on the Academic Ranking of World Universities
• Ranked 24 for Life and Agricultural Sciences
• International collaboration
School of Plant Biology
• 20-25 academic staff
• 110 PhD (Research) students
• research strengths in terrestrial ecology, agriculture and marine science

4. New Phytologist 195:306-320

5. 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

6. 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

7. 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).

8. 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.

9. 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

10. 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

11. 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)

12. 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

13. 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?

14. 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

15. 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

16. 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

17. 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

18. 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

19. 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

20. 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

21. 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

22. 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

23. 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)

24. 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

25. 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

26. 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

27. 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

28. 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

29. 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

30. 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?

31. [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.

32. “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]

33. 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

34. 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?)

35. 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

36. 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

38. 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

39. 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

40. 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

41. 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

42. 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

43. 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.

44. 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%

45. 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)

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

47. 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]

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

49. 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)