Plant Soil (2016) 401:1–6

DOI 10.1007/s11104-016-2846-9

EDITORIAL

Phosphorus in soils and plants – facing phosphorus scarcity

Timothy S. George & Philippe Hinsinger &
Benjamin L. Turner

Received: 8 January 2016 / Accepted: 23 February 2016 / Published online: 3 March 2016
# Springer International Publishing Switzerland 2016

Abstract Conclusions The challenges associated with P sustain-

Introduction Phosphorus is a fundamental nutrient for ability are tackled from many different directions, in-
primary productivity of ecosystems and agricultural cluding plant genetics, soil microbiology, novel imaging
production, but its misuse impacts agricultural sustain- and modelling techniques, the development of new
ability and has important environmental consequences. technologies, and an improved understanding of how
Access to global reserves of phosphate rock is politically these technologies interact with agronomic manage-
sensitive and economically challenging. Phosphorus ac- ment. Integration of the various approaches will be
cumulates in agricultural soils, representing a financial necessary to deliver a truly effective solution to the
loss to farmers and increasing the risk of loss to water. challenge of attaining phosphorus sustainability.
The challenges facing phosphorus sustainability are var-
ied, but many solutions are to be found in the plant–soil Keywords Ecosystem dynamics . Environmental
system. impact . Phosphorus acquisition . Phosphorus forms .
Scope This special issue arises from the 5th International Phosphorus cycling . Phosphorus utilization .
Symposium on Phosphorus in Soils and Plants (PSP5), Phosphorus signalling . Sustainable use and management
held in Montpellier, France. Articles highlighted here
discuss ways to tackle food security, improve phosphorus
sustainability by understanding the imbalanced phospho- Phosphorus (P) is required for in many biochemical
rus cycle, use technology to reduce phosphorus demand processes in plants and is therefore crucial to the pro-
and recycle phosphorus in waste products, and consider ductivity of ecosystems, including agroecosystems.
how efforts to increase phosphorus efficiency interact However, the misuse of P in agriculture has important
with other sustainability challenges. environmental consequences and ultimately impacts ag-
ricultural sustainability. Access to geographically dis-
Responsible Editor: John Hammond. crete global reserves of phosphate rock is politically
sensitive and economically challenging (Godfray et al.
T. S. George (*) 2010). The use of mined rock phosphate as a principal P
The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
e-mail: [Link]@[Link]
source for chemical fertilisers was a major contribution
to the green revolution, but increased our dependence on
P. Hinsinger this non-renewable P source (Elser and Bennett 2011).
INRA, UMR Eco&Sols, Place Viala, 34060 Montpellier, France The biological availability of phosphate fertiliser is re-
B. L. Turner
duced by sorption and organic complexation in the soil,
Smithsonian Tropical Research Institute, Apartado 0843-03092, so fertiliser applications greater than the amount re-
Balboa, Ancon, Republic of Panama quired by the crop are used to counteract the strong
2 Plant Soil (2016) 401:1–6

binding of the phosphate to the soil matrix (MacDonald challenge of P limitation in agroecosystems and terres-
et al. 2011). This has greatly increased the P content of trial ecosystems.
managed soils, so soils in many regions of the world now
contain sufficient P reserves to potentially buffer threats
to food security in the coming decades. However, the Imbalanced P cycle
accumulation of soil P also has negative consequences: it
is a financial loss to the farmer, uses up a renewable The concentration of mined phosphate taken from a few
resource, and has important environmental conse- small areas and applied widely onto agricultural soils in
quences, because even small amounts of the excess P the form of soluble fertilisers has caused a geographical
leaking into watercourses can cause blooms of harmful imbalance in P distribution in agricultural systems in
algae and raise the trophic status of lakes for many years comparison to natural ecosystems. While this greatly
(Elser and Bennett 2011). expands the capacity for food production from a given
The challenges surrounding P sustainability have land area, it has had environmental consequences and
been addressed a number of times in the recent literature resulted in the human-induced alteration of the biogeo-
(Cordell and White 2011, 2014; Haygarth et al. 2014; chemical cycle of P over the past decades (Elser and
Sharpley et al. 1994; Stutter et al. 2012) and in a range of Bennett 2011; Penuelas et al. 2013). Biogeochemical P
international symposia, one of which led to a compre- flows now exceed the planetary boundaries as defined
hensive declaration on the issues surrounding P sustain- by Steffen et al. (2015), which is of particular concern in
ability (Wyant et al. 2013). In 2014, phosphate rocks regions of excess P fertiliser loads such as Western
were included in the list of twenty critical raw materials Europe, North America and China. To manage this
by the European Commission, and represent the only imbalance sustainably we must understand what hap-
one which primarily concerns agriculture and food pens to the forms, availability and mobility of P after
security. Declarations on P sustainability acknowl- fertiliser application to soils. A number of papers in this
edge that biological organisms need P to thrive special issue employ new techniques to examine the fate
and reproduce and that it is a limited resource. of P following application to agricultural soils.
They also state that there is an Imbalanced Cycle Phosphorus can be added to soils in a number of ways,
caused by agricultural inputs, but that getting access to including application of inorganic fertilisers or naturally
adequate P is essential for Food Security. To address from weathering of primary phosphate minerals (i.e.
some of these challenges, the global community needs apatite). However, P can also be added in organic forms,
to Recycle and Reuse more P, Reduce Demand and including as crop residues and manures.
understand how Interconnection with other sustain- Rivard et al. (2016) determined the distribution and
ability challenges works (Wyant et al. 2013). It is also speciation of P in cultivated soils developed on a tem-
stated that there are great opportunities to innovate in the perate calcareous loam developed in glacial till. They
domains of P supply, use, and cycling to deliver agri- employed micro-X-ray fluorescence (μ-XRF) to pro-
cultural sustainability. duce maps of undisturbed samples and X-ray absorption
This special issue contains a range of papers present- near edge structure (XANES) spectra were collected on
ed at the International Symposium on Phosphorus in points of interests selected from μ-XRF maps. Results
Soils and Plants (PSP5) held in 2014 in Montpellier, showed minor effects of cropping and fertiliser practices
France, which address some of the themes stated in the on P speciation in cultivated soils, suggesting that
global P challenge declaration. This meeting was the agronomic management had little impact on the forms
fifth international symposium of this successful series of P in soils at the microscale.
initiated in Beijing, China, in 2000 (see former special In an attempt to assess the fate of fertiliser P in
issues in Plant and Soil, volumes 237, 269 and 349) and pasture systems, McLaren et al. (2016) developed a
promoted a multidisciplinary approach, gathering to- novel method for tracing fertiliser P in the field using
gether 276 plant nutritionists (plant physiology, genetics single superphosphate granules radiolabelled with a 33P
and systems biology), agronomists, ecologists, radiotracer. The tracer was applied to the soil surface of
biogeochemists and soil scientists from 38 countries a clover pasture and recovery of fertiliser P was deter-
across the world, with the aim of fostering scientific mined in clover shoots, fertiliser granules and soil frac-
exchanges across discipline boundaries to face the tions. Recovery of fertiliser P by clover plants was up to
Plant Soil (2016) 401:1–6 3

35 % in the year of application. Much of the fertiliser P then grew a subset of 13 genotypes in low- and high-P
in soil fractions was inorganic P, which highlights the fields until maturity. Significant genotypic variation was
importance of inorganic P forms and dynamics in soils observed, although none of the genotypic groups
under pasture systems, despite many of the inputs in differed significantly in AMF colonization. The
these systems coming from organic residues. groups were also unrelated to shoot-P-content and grain
In contrast, Foyjunnessa et al. (2016) assessed the yield, despite contrasting in selection history and grain
contribution of crop residues to the soil P pool, specif- yield performance across multiple field trials. There
ically in the form of residual roots. Using a stem wick- were no significant genomic regions for AMF. This
feeding technique, 33P-labelled phosphoric acid was fed paper suggests that genotypic selection for AMF colo-
in-situ to oilseed rape (Brassica napus) and narrow-leaf nization in sorghum is not a promising approach due to
lupin (Lupinus angustifolius) grown in sandy or loamy low heritability and absence of positive relationship
soils in sealed pots. Recovery of 33P was 93 % in the between AMF and P acquisition.
plant − soil system, and significantly more 33P was In contrast, Vandamme et al. (2016) highlight a po-
allocated below-ground than to shoots for both species. tentially useful trait for selection of genotypes of soy-
Estimated total below-ground P accumulation by both bean. The authors evaluated how differences in seed
species was at least twice that of recovered root P and weight and seed P affected growth at low and high P
was a greater proportion of total plant P for narrow-leaf supply for forty-two soybean genotypes in a pot trial.
lupin than oilseed rape. This research suggests that a Correlations between seed weight and plant biomass,
large proportion of P taken up by plants remains in the shoot P content and root length were stronger at low
root system, which has been previously underestimated. than at high P supply. At low P supply, plant growth was
Roots of the previous crop are therefore a potentially correlated with seed weight up to the flowering stage.
important source of P for subsequent crop production. This research suggests that selecting large-seeded spe-
cies by seed size may be a way to improve P acquisition
in crops important to food security.
Food security In another study, Rose et al. (2016) present develop-
ments in the use of internal P use efficiency (PUE) as a
To achieve food security, farmers need access to reliable basis for selecting genotypes with the ability to enhance
and affordable sources of fertiliser to enhance and main- P sustainability. They investigated various soil and hy-
tain the productivity of their agricultural systems. This is droponic screening methods for their capacity to pro-
particularly important for resource poor farmers in the duce a consensus ranking of genotypes with regard to
developing world, such as in sub-Saharan Africa. In the PUE. Six rice genotypes identified previously in hydro-
absence of a reliable and affordable source of P fertiliser, ponic screening studies as being high, intermediate or
the available crop varieties must be able to tolerate (and low PUE were screened using hydroponic and soil-
be productive on) P-poor soils. A number of papers in based experiments with contrasting P levels. Overall,
this special issue tackle the problem of identifying the PUE was significantly influenced by genotype and P
genetic control of traits useful for P sustainability in crop supply, but there was no significant genotype × P supply
species important for resource poor farmers in the de- interaction. Hence, it was concluded that screening ge-
veloping world. Traits identified as having poten- notypes using hydroponics at one or two P supply levels
tial for delivering food security by enhancing P acqui- is the most cost- and time-effective way to screen large
sition and utilisation efficiency and examined in this numbers of rice genotypes for PUE.
issue include mycorrhizal symbiosis, seed size and sub-
sequent vigour and internal P use efficiency. Some of
these are shown to be effective and genetically tractable, Recycling and reuse of P
while others are not.
Leiser et al. (2016) aimed to determine whether sor- To reduce the reliance of agriculture on the use of
ghum breeding programs in West Africa should target inorganic fertilisers and the geopolitical uncertainties
greater colonization rates by arbuscular mycorrhizal associated with global phosphate reserves it is
fungi (AMF). They grew a sorghum diversity panel of important to promote technologies that attempt to
187 regional genotypes in low-P soil in a pot trial, and recycle some of the common waste products from
4 Plant Soil (2016) 401:1–6

agricultural and human consumption systems. This which plants access fertiliser P in soils and (2) the
requires an understanding of the ability of waste rhizosphere environment with respect to its ability to
products to act as effective fertilisers and replacements enhance access to organic forms.
for rock phosphate and the corresponding fertilisers. Ahmed et al. (2016) investigated how plant roots
Several articles in this special issue assess these interact with fertiliser granules in three-dimensional
technologies. space and with time. This understanding will help more
Christel et al. (2016) studied the impacts of slurry effectively utilise inorganic P fertilisers added to soils
acidification, separation technology and thermal pro- and therefore reduce demand for mineral P fertiliser.
cessing on the availability of P in soil amended with They used in-vivo, time resolved, microfocus X-ray
the solid fraction of pig slurry. Following addition of CT imaging (μCT) in three dimensions to visualise,
various treated pig slurries to soil, P availability was quantify and assess root–fertiliser interactions of wheat
determined over time using diffusive gradients in thin plants in an agricultural soil during the entire plant life
films (DGT). Application of separated pig slurry solids cycle. Two contrasting fertilisers – triple superphosphate
increased soil P availability initially, but this declined and struvite – were applied to the soil mesocosms.
with time. Chars and ashes on the other hand reduced P Lateral roots tended to pass within a few millimetres
availability initially, but availability remained constant of the P source and could therefore access the P diffus-
or increased slightly with chars, eventually yielding P ing from the granule. The authors also showed that
availability similar to biosolids. This research suggests rooting density was positively correlated with granule
that pig slurries treated in a number of ways are an volume-loss for a slow release struvite fertiliser.
effective replacement technology for conventional inor- In a complementary study, Heppell et al. (2016)
ganic fertilisers. developed a model to assess a range of P fertiliser and
In contrast, Talboys et al. (2016) demonstrate that soil management strategies for a cereal crop, to maxi-
struvite (a source of P extracted from wastewater) is mise plant P uptake under different climate conditions.
utilised more effectively when used in combination with The model was able to fit data from two barley field
relevant plant genotypes. They examined P release from trials with regard to P uptake by the crop, although the
commercial fertiliser-grade struvite and its uptake from model fits were better for early compared to late growth
a low-P sandy soil by two different crop types, in stages. Refinement of such models will allow more
comparison to more soluble inorganic P fertilisers (di- effective, site-specific recommendations for use of P
ammonium phosphate (DAP) and triple super phosphate fertilisers, thus reducing the demand for mineral P.
(TSP)). Struvite solubility was enhanced greatly in In a completely different approach, Sanguin
the presence of organic anions, where buckwheat, et al. (2016) investigated the potential for rhizo-
which exudes a high level of organic anions, was sphere microorganisms to reduce demand for min-
more effective at mobilising struvite P than spring eral P by enhancing the use of phytate (salts of
wheat, which exudes only low concentrations of myo-inositol hexakisphosphate), which can consti-
organic anions. However, struvite granules placed tute a considerable proportion of the organic P in
with the seed did not provide the same rate of P agricultural soils. In this study, the phytate-hydrolysing
supply as similarly placed DAP granules for early bacterial community was characterized in the rhizo-
growth of spring wheat. sphere of plants cultivated in the presence or absence
of phytate supplementation. Major changes in the bac-
terial community structure were observed with both
Reduced demand for P culture-dependent and culture-independent methods, in-
cluding the predominance of Proteobacteria and
Phosphorus sustainability can be improved by reducing Actinobacteria in phytate-treated soils. Phytase ac-
P demand in agricultural systems. This can be achieved tivity was detected for a range of rhizobacterial
in a number of ways, including improvements in the isolates and β-propeller phytases were detected in
efficiency of P use by crops and the enhanced use of P both isolates and soils. It is clear that a range of soil
that has accumulated in soils following decades of inor- microorganisms are endemic to the rhizosphere which,
ganic P additions. The special issue contains several if harnessed correctly, could enhance P sustainability
articles that help understand (1) the efficiency with and reduce demand for added P.
Plant Soil (2016) 401:1–6 5

Interconnection with global sustainability challenges Conclusions

In addition to P sustainability, there are a number of It is apparent from the information contained in this
other sustainability challenges facing global agriculture. special issue that the challenges associated with P sus-
These include (1) the sustainable use of water and other tainability are being tackled in a variety of ways, includ-
nutrients (specifically nitrogen), (2) the ability to pro- ing crop genetics, soil microbiology, novel imaging and
vide adequate nutritious food, particularly with refer- modelling techniques, technology development, and an
ence to zinc, iron and iodine nutrition, (3) the ability to understanding of how new technologies interact with the
mitigate global environmental change (specifically management environment. Obviously, additional solu-
carbon sequestration), and (4) the loss of biodiver- tions can be provided in the fields of crop physiology,
sity due the degradation of natural ecosystems. If agronomy, landscape management, to name but a few.
we consider the sustainability of P in the absence While it is clear that progress in being made, integration
of these other concerns, it is unlikely that any of the range of approaches will be necessary to deliver a
technology for improving food security will be truly effective solution to the challenge set out by P
effectively deployed. This special issue contains sustainability. Indeed, the life cycle of mined P, which is
two articles that look at how land-use change and now considered as a critical raw material for society,
management can impact the cycling of P in association demonstrates that major losses occur along the entire
with some other nutrients inherent in global sustainabil- production/consumption chain, from the phosphate rock
ity issues. mine to the consumer’s plate and beyond. Facing P
Somaweera et al. (2016) examined the impact of scarcity is a major challenge ahead of us, and will require
water saving management for rice production on the the identification of multiple solutions to reduce these
effective utilisation of both P and nitrogen. Rice was losses and use P more efficiently. Many of these solutions
grown in soil columns under four water management pertain to plants and soils, as major losses occur in
treatments. Moisture limitation substantially reduced agroecosystems of regions that can afford substantial
tissue P content and retranslocation of P to pani- application of P fertilisers. However, many regions of
cles, but nitrogen nutrition was little affected. This the developing world have limited access to P fertilisers,
research demonstrates that when managing crops which are becoming increasingly more expensive. In
with other sustainability issues in mind there are these regions, facing P scarcity is a major challenge,
significant impacts on the ability of the crops to and major research efforts in plant and soil sciences are
utilise nutrients, including P. Management packages that needed to solve this issue, which also poses the question
account for all the various demands on the system of global P stewardship. We anticipate that the sixth
should be considered. International Symposium on Phosphorus in Soils and
Likewise the impact of land-use change can have Plants (PSP6) to be held in Leuven, Belgium in 2018,
profound effects on the sustainability of use of P and will shed new light on the various solutions to improve P
other nutrients. This is highlighted by Spohn et al. sustainability atlocal, regional, and global scales.
(2016), who quantified changes in soil total P, nitrogen,
and carbon during secondary succession after abandon- Acknowledgments This work was supported by the Rural and
ment of vineyards on calcareous soils. Soil carbon and Environment Science and Analytical Services Division (RESAS)
of the Scottish Government, and by Agropolis Fondation
organic P concentrations increased after vineyard aban- (PHOSPHORUS 2014 project) under the reference ID 1202-019
donment in two chronosequences covering 200 years through the « Investissements d’avenir » programme (Labex
and differing in aspect and slope, while P availability Agro:ANR-10-LABX-0001-01).
determined by bicarbonate extraction diminished during
the first 50 years after abandonment. The study
demonstrates that the legacy of former cultivation References
persists for more than a century under these conditions,
indicating that our efforts to improve P sustainability in
Ahmed S, Klassen TN, Keyes S, Daly M, Jones DL, Mavrogordato
agricultural systems are unlikely to be short term solu- M, Sinclair I, Roose T (2016) Imaging the interaction of roots
tions but rather long term effort to develop systems that and phosphate fertiliser granules using 4D X-ray tomography.
are truly sustainable. Plant Soil. doi:10.1007/s11104-015-2425-5 (this Issue)
6 Plant Soil (2016) 401:1–6

Christel W, Bruun S, Magid J, Kwapinski W, Jensen LS (2016) Pig Rivard C, Lanson B, Cotte M (2016) Phosphorus speciation and
slurry acidification, separation technology and thermal micro-scale spatial distribution in North-American temperate
conversion affect phosphorus availability in soil agricultural soils from micro X-ray fluorescence and X-ray
amended with the derived solid fractions, chars or ashes. absorption near-edge spectroscopy. Plant Soil. doi:10.1007/
Plant Soil. doi:10.1007/s11104-015-2519-0 (this issue) s11104-015-2494-5 (this Issue)
Cordell D, White S (2011) Peak phosphorus: clarifying the key Rose TJ, Mori A, Julia CC, Wissuwa M (2016) Screening
issues of a vigorous debate about long-term phosphorus for internal phosphorus utilisation efficiency: compari-
security. Sustainability 3:2027–2049 son of genotypes at equal shoot P content is critical.
Cordell D, White S (2014) Life’s bottleneck: sustaining the Plant Soil. doi:10.1007/s11104-015-2565-7 (this Issue)
world’s phosphorus for a food secure future. Ann Rev Sanguin H, Wilson, NL, Kertesz MA (2016) Assessment of
Environ Res 39:161–188 functional diversity and structure of phytate hydrolys-
Elser J, Bennett EM (2011) A broken biogeochemical cycle. ing bacterial community in Lolium perenne rhizo-
Nature 478:29–31 sphere. Plant Soil. doi:10.1007/s11104-015-2512-7
Foyjunnessa, McNeill A, Doolette A, Mason S, McLaughlin, MJ (this Issue)
(2016) Quantifying total phosphorus accumulation below- Sharpley AN, Chapra SC, Wedepohl R, Sims JT, Daniel TC,
ground by canola and lupin plants using 33P-labelling. Reddy KR (1994) Managing agricultural phosphorus for
Plant Soil. doi:10.1007/s11104-015-2545-y (this Issue) protection of surface waters: issues and options. J Environ
Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Qual 23:437–451
Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C Somaweera KATN, Suriyagoda LDB, Sirisena DN, De Costa
(2010) Food security: the challenge of feeding 9 billion WAJM (2016) Accumulation and partitioning of biomass,
people. Science 327:812–881 nitrogen, phosphorus and potassium among different tissues
Haygarth PM, Jarvie HP, Powers SM, Sharpley AN, Elser JJ, Shen during the life cycle of rice grown under different water
J, Peterson HM, Chan NL, Howden NJK, Burt T, Worrall F, management regimes. Plant Soil. doi:10.1007/s11104-015-
Zhang F, Liu X (2014) Sustainable Phosphorus Management 2541-2 (this Issue)
and the need for a long-term perspective: the legacy hypoth- Spohn M, Novak, TJ, Incze J, Giani L (2016) Dynamics of soil
esis. Environ Sci Technol 48:8417–8419 carbon, nitrogen, and phosphorus in calcareous soils after
Heppell J, Payvandi S, Talboys P, Zygalakis KC, Fliege J, Landton land-use abandonment – A chronosequence study. Plant
D, Sylvester-Bradley R, Walker R, Jones DL, Roose, T Soil. doi:10.1007/s11104-015-2513-6 (this Issue)
(2016) Modelling the optimal phosphate fertiliser and soil Steffen W, Richardson K, Rockström J, Cornell SE, Fetzer I,
management strategy for crops. Plant Soil. doi:10.1007/ Bennett EM, Biggs R, Carpenter SR, de Vries W, de Wit
s11104-015-2543-0 (this Issue) CA, Folke C, Gerten D, Heinke J, Mace GM, Persson LM,
Leiser WL, Olatoye MO, Frederick H, Rattunde W, Neumann G, Ramanathan V, Reyers B, Sörlin S (2015) Planetary bound-
Weltzen E, Haussmann BIG (2016) No need to breed for aries: guiding human development on a changing planet.
enhanced colonization by arbuscular mycorrhizal fungi to Science 347:736–746. doi:10.1126/science.1259855
improve low-P adaptation of West African sorghums. Plant Stutter MI, Shand CA, George TS, Blackwell MSA, Bol R,
Soil. doi:10.1007/s11104-015-2437-1 (this issue) Mackay RL, Richardson AE, Condron LM, Turner BL,
MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Haygarth PM (2012) Recovering phosphorus from soil: A
Agronomic phosphorus imbalances across the world’s crop- root solution. Environ Sci Technol 46:1977–1978
lands. Proc Natl Acad Sci U S A 108:3086–3091 Talboys PJ, Heppell J, Roose T, Healey JR, Jones DL, Withers
Mclaren TI, McLaughlin MJ, McBeath TM, Simpson RJ, Smernik PJA (2016) Struvite: a slow-release fertiliser for sustainable
RJ, Guppy CN, Richardson AE (2016) The fate of fertiliser P phosphorus management? Plant Soil. doi:10.1007/s11104-
in soil under pasture and uptake by subterraneum clover – a 015-2747-3 (this Issue)
field study using 33P-labelled single superphosphate. Plant Vandamme E, Pypers P, Smolders E, Merckx R (2016) Seed
Soil. doi:10.1007/s11104-015-2610-6 (this issue) weight affects shoot and root growth among and within
Penuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, soybean genotypes beyond the seedling stage: implications
Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, for low P tolerance screening. Plant Soil. doi:10.1007/
Vicca S, Obersteiner M, Janssens IA (2013) Human- s11104-015-2564-8 (this issue)
induced nitrogen-phosphorus imbalances alter natural and Wyant KA, Corman JR, Elser JJ (2013) Phosphorus, food and our
managed ecosystems across the globe. Nature Comm 4:2934 future. Oxford University Press, New York