Past, present and future of organic nutrients

Abstract

Slowing crop yield increases despite high fertiliser application rates, declining soil health and off-site pollution are testimony that many bioproduction systems require innovative nutrient supply strategies. One avenue is a greater contribution of organic compounds as nutrient sources for crops. That plants take up and metabolise organic molecules ('organic nutrients') has been discovered prior to more recent interest with scientific roots reaching far into the 19th century. Research on organic nutrients continued in the early decades of the 20th century, but after two world wars and yield increases achieved with mineral and synthetic fertilisers, a smooth continuation of the research was not to be expected, and we find major gaps in the transmission of methods and knowledge. Addressing the antagonism of 'organicists' and 'mineralists' in plant nutrition, we illustrate how the focus of crop nutrition has shifted from organic to inorganic nutrients. We discuss reasons and provide evidence for a role of organic compounds as nutrients and signalling agents. After decades of focussing on inorganic nutrients, perspectives have greatly widened again. As has occurred before in agricultural history, science has to validate agronomic practises. We argue that a framework that views plants as mixotrophs with an inherent ability to use organic nutrients, via direct uptake or aided by exoenzyme-mediated degradation, will transform nutrient management and crop breeding to complement inorganic and synthetic fertilisers with organic nutrients.

Full text

MARSCHNER REVIEW
Past, present and future of organic nutrients
Chanyarat Paungfoo-Lonhienne &Jozef Visser &
Thierry G. A. Lonhienne &Susanne Schmidt
today’s predominant application of mineral and syn-
thetic (urea) fertilisers in high-production cropping. In
recent decades, organic nutrients have been recognised
as nutrient sources of plants in natural ecosystems and
questions have been raised about what we know about
the form in which nutrients such as nitrogen (N) enter
roots (Näsholm et al. 2009). To consider organic
Plant Soil (2012) 359:1–18
DOI 10.1007/s11104-012-1357-6
J. Visser
Intrasoil Consultancy,
Aziëlaan 2, 3526 SB Utrecht, The Netherlands
T. G. A. Lonhienne
School of Chemistry and Molecular Biosciences,
The University of Queensland,
Brisbane, QLD 4072, Australia
Abstract
Background Slowing crop yield increases despite high
fertiliser application rates, declining soil health and
off-site pollution are testimony that many bioproduc-
tion systems require innovative nutrient supply strate-
gies. One avenue is a greater contribution of organic
compounds as nutrient sources for crops. That plants
take up and metabolise organic molecules (‘organic
nutrients’) has been discovered prior to more recent
interest with scientific roots reaching far into the 19th
century. Research on organic nutrients continued in
the early decades of the 20th century, but after two
world wars and yield increases achieved with mineral
and synthetic fertilisers, a smooth continuation of the
research was not to be expected, and we find major
gaps in the transmission of methods and knowledge.
Scope Addressing the antagonism of ‘organicists’and
‘mineralists’in plant nutrition, we illustrate how the
focus of crop nutrition has shifted from organic to
inorganic nutrients. We discuss reasons and provide
evidence for a role of organic compounds as nutrients
and signalling agents.
Conclusion After decades of focussing on inorganic
nutrients, perspectives have greatly widened again. As
has occurred before in agricultural history, science has
to validate agronomic practises. We argue that a
framework that views plants as mixotrophs with an
inherent ability to use organic nutrients, via direct
uptake or aided by exoenzyme-mediated degradation,
will transform nutrient management and crop breeding
to complement inorganic and synthetic fertilisers with
organic nutrients.
Keywords Sustainable agriculture .Organic
nutrients .Nitrogen .Phosphorus .Plant nutrition
Introduction
We review how practises and knowledge of plant
nutrition have changed over two centuries, from the
application of organic residues in early agriculture to
Responsible Editor: Philippe Hinsinger.
C. Paungfoo-Lonhienne (*):S. Schmidt
School of Agriculture and Food Sciences,
The University of Queensland,
Brisbane, QLD 4072, Australia
e-mail: chanyarat@uq.edu.au
Received: 7 November 2011 / Accepted: 28 June 2012 / Published online: 20 July 2012
#Springer Science+Business Media B.V. 2012

nutrients as directly contributing to crop nutrition may
seem unorthodox in the light of the vast body of
literature demonstrating that addition of mineral
nutrients successfully enhances crop growth and the
well-described mechanisms for their uptake and as-
similation. However, there is largely forgotten as well
as recent literature proposing a more comprehensive
view of plant nutrition. While many experiments in
controlled conditions (axenic agar culture, hydrocul-
ture) supplying inorganic nutrients show that plants
use these for growth (and organic C in the form of
sucrose as C source in agar culture systems), we
should be careful about interpreting this as proof that
only inorganic nutrients are acquired by soil-grown
plants. As stated by Phelan (2009)‘In its purest form,
reductionism searches for mechanisms among the
constituents of a system and holds that understanding
the constituents is sufficient to understanding the sys-
tem. …The beauty of reductionism is its simplicity and
the relative ease of experimentally demonstrating
cause and effect within system components. By con-
trolling the variables, interpreting experimental
results is relatively straightforward. On the other
hand, the weakness of reductionism derives from its
inability to predict system behaviour that arises from
interactions among components.’Expanding high
quality research on plant nutrition from tightly con-
trolled, inorganic nutrient-focused experimental sys-
tems to real-world systems in which plants interact
with soil, microbes and biota will advance plant nutri-
tion. Expanding the concept of mixotrophy to green
plants where it is currently considered an exception
(although it is a rule in photosynthetic algae, Raven et
al. 2009), provides innovation for crop nutrition.
Long-standing and recent concepts of plant nutrition
are worth exploring as we are seeking to improve
nutrient supply to crops.
Contemporary research on organic nitrogen
and phosphorus
Announcing a paradigm shift in plant nitrogen (N)
nutrition, Aerts and Chapin (2000) stated that miner-
alisation is only the end point of a long track of
conversions of plant-available organic compounds
from soil organic matter: ‘Since N is typically trans-
formed from insoluble organic N to soluble organic N
to ammonium to nitrate, with some uptake of these
forms by plants and/or microbes at each step, the
supply rate in any soil must be in the order: soluble
organic N greater than ammonium greater than ni-
trate. Thus the potential of plants to absorb soluble
organic N may be much more important than previ-
ously anticipated’. Since then a plethora of publications,
spanning from ecology to molecular biology, proved the
fruitfulness of the new paradigm (reviewed by Gardenas
et al. 2011; Näsholm et al. 2009; Rentsch et al. 2007;
Schimel and Bennett 2004; Tegeder and Rentsch 2010;
Waterworth and Bray 2006). It is worthy of note that the
rediscovery of organic nutrients as sources of essential
nutrients did not come from agriculture but ecology
(reviewed by Lipson and Näsholm 2001).
Tab le 1summarises recent research on organic
nutrients which shows that organic molecules have
confirmed functions as sources of essential elements
for plants and signalling agents. Organic monomers in
the form of amino acids are the best studied example
and are acquired by life forms that include monocot
sedges, grasses and grain crops, as well as dicot herbs,
shrubs and trees. Initially only considered as compo-
nents of root exudates (e.g. Kuo et al. 1982), the
molecular mechanisms of amino acid uptake have
been elucidated in Arabidopsis.
The seminal study alerting to amino acids and
generating subsequent studies showed that non-
mycorrhizal arctic sedge Eriophorum vaginatum
grows better with amino acids than nitrate and
achieves similar growth with amino acids and ammo-
nium, while barley (Hordeum vulgare) grows better
with inorganic N (Chapin et al. 1993). However, the
relevance of amino acids as plant N sources has been
questioned for reasons that include (i) microbes are
better competitors for amino acids than plants, (ii)
amino acids are a minor component of the soil N pool
and experimental systems use unrealistically high con-
centrations of amino acids, (iii) some amino acids
inhibit root growth (Forde and Walch-Liu 2009; Jones
et al. 2005; Näsholm et al. 2009). These issues have
been addressed in studies supplying mixtures of amino
acids rather than single amino acids and amino acids +
inorganic N at concentrations encountered in soil.
Barley, wheat and Arabidopsis take up amino acids
at soil relevant concentrations of 2–50 μM with sim-
ilar uptake kinetics as soil microbes (Hill et al. 2011a;
Jämtgård et al. 2008; Svennerstam et al. 2011), and
amino acids as N source result in similar or greater
biomass than inorganic N (Cambui et al. 2011; Soper
2 Plant Soil (2012) 359:1–18

Table 1 Examples of recent research on organic nutrient as nutrient sources and effects of organic nutrients on roots
Concept Approach References
Plants take up and metabolise amino acids at
field-relevant concentrations and in the
absence of fungal symbionts
15
N/
13
C-amino acids in controlled and field conditions Reviewed by Gardenas et al. 2011;
Jones et al. 2005; Näsholm et al. 2009;
Svennerstam et al. 2011
Amino acids depleted from sterile solution
Membrane transporters mediating uptake of amino acids into root cells
Arabidopsis with altered expression of amino acid transporters
Amino acids modulate root growth L-GLY and L-TRP with duckweed (Spirodela oligorrhiza) and Arabidopsis Bollard 1966; Vidal et al. 2010;
Walch-Liu et al. 2006a,b
L-GLN, L-GLU and nitrate with Arabidopsis sterile culture; several amino
acids with Arabidopsis and Lobelia anceps
Cambui et al. 2011; Forde and
Walch-Liu 2009; Soper et al. 2011
Plants acquire and metabolise di-, tri- and
tetra-peptides
Arabidopsis with altered peptide transporters expression Komarova et al. 2008
Arabidopsis,Hakea actites and Lobelia on sterile medium Paungfoo-Lonhienne et al. 2009;
Schmidt et al. 2003; Soper et al. 2011
Roots of oak (Quercus robur),wheat (Triticum aestivum) and Antarctic
plants in solution culture, the latter also in situ with stable isotope-
labelled peptides added to soil
Seegmüller and Rennenberg 2002;
Hill et al. 2011a,b
Di- to penta-peptides modulate biomass
allocation and increase root growth
Adventitious root formation in asparagus (Asparagus officinalis) and
cucumber (Cucumis sativus)
Matsubayashi and Sakagami 1996;
Yamakawa et al. 1998
Arabidopsis and Lobelia on sterile medium Soper et al. 2011
Plants exude proteases, incorporate protein
and use it as N source
Hakea and Arabidopsis on sterile medium with bovine serum albumen
(BSA) or fluorescent proteins
Paungfoo-Lonhienne et al. 2008
Wheat in sterile liquid medium with casein Adamczyk et al. 2008
Plants use organic P substrates for growth Wheat on sterile solid medium with inositol hexaphosphate Richardson et al. 2000
Arabidopsis with phytase gene from Aspergillus niger Richardson et al. 2001
Arabidopsis on sterile medium with nucleic acid Chen et al. 2000
DNA enters roots and increases length of
roots and root hairs
Arabidopsis on sterile solid and liquid media, nuclease-resistant S-DNA;
DNA and P
i
-replete growth medium
Paungfoo-Lonhienne et al. 2010a
Plant Soil (2012) 359:1–18 3

et al. 2011; Vinall et al. 2012). With the exception of
the initial period after N fertiliser application when inor-
ganic N concentrations are elevated, amino acids repre-
sent a significant proportion of exchangeable and soluble
N pools in agricultural soils (Holst et al. 2012; Jämtgård
et al. 2010) and dominate forest soil (Inselsbacher and
Näsholm 2012). Even if it remains unresolved how
much amino acids contribute to the N budget of crops,
all plants studied so far have the capacity to acquire and
metabolise amino acids and all soils studied in this
respect contain amino acids.
Here, we need to point out the main caveat that
dominates the debate of organic versus inorganic
nutrients. While ecologists tend to acknowledge that
amino acids are a source of N in ecosystems charac-
terised by slow mineralisation rates, crop physiologists
and agronomists generally view nitrate and ammoni-
um as main N sources for crops due to their prevalence
in N-fertilised soils. An alternative view is that ammo-
nium and nitrate are the end products of N depolymer-
isation and that organic precursor compounds are also
available for plant use. Which forms of N enter plant
roots remains a matter of debate due to the inherent
difficulty of measuring fluxes, simultaneous uptake,
release, immobilisation and conversion of N in the
soil–microbe–plant continuum (Näsholm et al. 2009).
Deducing from the plants’ability to acquire and
metabolise inorganic N that nitrate and ammonium
are the sole N sources is flawed since the same argu-
ment holds true for amino acids. Similarly, the argu-
ment that high soil concentrations of nitrate and
ammonium prove their role as sole N sources invites
the counter-argument that a prevalence of inorganic N
is indicative of a ‘left over’pool discriminated against
by crops (Hill et al. 2011a; Robinson et al. 2011).
Adding to the difficulties of discerning in which
form N enters roots is the presence of a large store N in
soils of ≈1 to 10 t of mostly proteinaceous N at root-
accessible depth. To advance knowledge of how much
amino acids—and other forms of organic N—contrib-
ute to the crop N budget, Jämtgård et al. (2010) argue
that plant growth should be compared in soils that
differ in N quality rather than quantity. Knowledge
of soil and microbial processes has to be integrated
with understanding of molecular and physiological
processes of plants, but to the best of our knowledge,
no study has yet made use of the full spectrum of
tools. New approaches include proteomic and metab-
olomic techniques to distinguish N assimilation
characteristics of plants grown with organic or inor-
ganic N (Thornton et al. 2007). Metabolite analysis
identified a shift from nitrate to asparagine in the
soluble N pool of roots of soil-grown sugarcane sup-
plied with amino acid versus inorganic N (Vinall et al.
2012). Combined imaging-mass spectrometry meth-
ods (Clode et al. 2009) hold promise for advancing
knowledge of N use by plants and soil organisms, as
do visualisation techniques such as fluorescent semi-
conductors (‘quantum dots’). Quantum dots conjugat-
ed to amino acids or chitosan (glucosamine-polymer)
were traced into saprophytic and arbuscular mycorrhi-
zal fungal hyphae, roots and shoots (Whiteside et al.
2009), elegantly demonstrating that organic mono-
mers and oligomers are acquired by fungi and plants.
Further size reductions will advance this technique as
the current size of quantum dots (5 nm) prevents
incorporation by soil bacteria. Soil microbes are being
investigated with modern sequencing tools and roots
contain many microbial taxa without known relation-
ships to plants (Vandenkoornhuyse et al. 2007). We
examined if plants use microbes as a source of nutrients
and found that non-symbiotic and non-pathogenic
microbes enter root cells and are digested (Fig. 1,
Paungfoo-Lonhienne et al. 2010b). Since plant growth
promoting bacteria (PGPB) are increasingly applied as
biofertilisers (reviewed by Vessey 2003), it is conceiv-
able that benefits of PGPB include a function as direct
nutrient sources for plants. Altogether, these examples
show that knowledge of plant nutrient sources is
expanding and question the notion that plants are wholly
dependent on soil biota for depolymerisation and min-
eralisation of organic matter.
Research on organic N has focussed on amino
acids, but N oligomers including di-, tri- and tetra-
peptides are also potential N sources for crops. Peptide
oligomers enter root cells via specialised transporter
proteins and enable plant growth when supplied as
sole N source (Table 1). Arabidopsis over-expressing
di-peptide transporters displayed enhanced growth with
di-peptides as N source which indicates that peptide
transport across membranes is a bottleneck (Komarova
et al. 2008). Peptide oligomers facilitate growth of axe-
nic Arabidopsis and naturally arbuscular-mycorrhizal
Lobelia (grown without fungal symbionts) to different
extent which demonstrates that species differ in response
and capacity to use single peptides (Soper et al. 2011).
Wheat acquired peptides at rates comparable to amino
acids and inorganic N at soil-relevant concentrations of
4 Plant Soil (2012) 359:1–18

10 μM or higher (Hill et al. 2011a). Thus there is evi-
dence that small peptides deserve to be added to the list
of crop N sources.
Organic polymers are the final frontier in organic N
research. Enabled by the proteolytic activity of mycor-
rhizal symbionts, ecto- or ericoid mycorrhizal species
access protein as N source (Read 1991), but this
exludes most crop species which form symbioses with
arbuscular mycorrhizal (AM) fungi. Hodge and Fitter
(2010) showed that AM fungi derive N from organic
matter, and it is therefore conceivable that crops indi-
rectly access proteinacous N via AM symbionts. Nat-
urally non-mycorrhizal species Arabidopsis and
Hakea derive N from protein and proposed mecha-
nisms include lysis of proteins at the root surface and
in the cortical apoplast via root-derived proteolytic
exoenzymes (Table 1). Root proteases, their sub-
strates and degradation products may be more
relevant for plant N acquisition than currently as-
sumed, and three of the 40 plant proteases for
which functions have been described are concerned
with roots (Kohli et al. 2012).
The presence of externally-supplied green fluo-
rescent protein (25 kDa GFP) in root hairs sug-
gests that intact protein can be incorporated into
cells (Paungfoo-Lonhienne et al. 2008). Rapid up-
take of polyguanidine peptoids (polyarginine-like)
into the cytosol of walled tobacco cells indicates that
this process is only partially driven by endocytosis
(Eggenberger et al. 2009,2011). We currently lack
insight of mechanisms and ecological significance of
the direct acquisition of N polymers by roots, but should
consider uptake of protein and degradation products as
one of several N acquisition strategies.
While research on organic N has been advanced in
recent years, research on organic P has been hampered
by routine soil-testing methods that miss the plant-
available soil organic pool. Organic phosphorus (P)
has received less attention than organic N, although
much of the soluble P pool in soils occurs in organic
form. Organic P, including phytates, phospholipids,
phosphoproteins, phosphoesters, sugar phosphates
and other (Tate 1984), is generally considered unavail-
able for direct uptake by roots, requiring microbial
conversion to inorganic phosphate (P
i
) (Raghothama
1999; Richardson et al. 2000) or depolymerisation of
organic phosphate-esters by root-derived phosphatases
(Marschner 1995; Neumann and Martinoia 2002).
Axenic Arabidopsis with elevated extracellular phy-
tase activity had improved P nutrition with phytate as
P source (Richardson et al. 2001). Secretion of nucle-
olytic enzymes by roots and subsequent breakdown of
nucleic acid to P
i
were considered the reason that Ara-
bidopsis grows with nucleic acid substrates as sole P
source (Chen et al. 2000;Richardsonetal.2000). How-
ever, DNA composed of 25-nucleotides (16.5 kDa)
enters Arabidopsis roots intact (Fig. 1, Paungfoo-
Lonhienne et al. 2010a) which raises the question
whether other forms of organic P also enter roots and,
if confirmed, how much organic P contributes to the P
nutrition of plants.
Together these studies illustrate that plants, includ-
ing non-mycorrhizal species, access and incorporate
organic nutrients. In addition to a role as nutrients,
Fig. 1 Plant nitrogen sour-
ces (adapted from Schimel
and Bennett 2004) expanded
to include N polymers and
oligomers. Root-derived
enzymes contribute to depo-
lymerisation, but organic
polymers and oligomers are
also directly incorporated
into roots. Light-field and
confocal microscopy images
(upper and lower panels,
respectively) show fluores-
cent polymers (protein,
DNA) and microbes in root
cells (Paungfoo-Lonhienne
et al. 2008,2010a,b)
Plant Soil (2012) 359:1–18 5

organic compounds affect root morphogenesis as has
been shown with inorganic N (e.g. Forde and Walch-
Liu 2009). Arabidopsis grown in P
i
replete conditions
supplemented with DNA displayed enhanced root
branching, root and root hair length (Paungfoo-
Lonhienne et al. 2010a), congruent with the concept
that organic compounds stimulate root proliferation in
organic-matter rich sites. Glutamine enhanced root
growth of Arabidopsisi and Lobelia (Cambui et al.
2011; Soper et al. 2011) and root length of Arabidop-
sis increased in response to protein concentration in
the growth medium (Paungfoo-Lonhienne et al. 2008).
These examples illustrate that, similar to inorganic
nutrients, roots exhibit measurable responses to organ-
ic nutrients. In the following we examine nutrients in
historic context and show that the recent debate on
organic nutrients has in fact a long history.
Lest we forget: research on organic nutrients
pre-World War I
Over much of the 20th century, plant nutrition research
has focussed on inorganic nutrients with foundations
laid by 19th century chemist Justus von Liebig who
identified the nutrients essential for plant growth and
promoted the use of mineral fertilisers. Yet organic
nutrients have a long history of use in agriculture,
and we argue that knowledge has been overlooked or
even doubted in modern agriculture. Since the 19th
century, organic compounds were studied for their role
in plant nutrition including substances in animal and
plant wastes (Table 2). Albrecht Thaër, the most influ-
ential agronomist of his time established the role of
humus as food for plants (Thaër 1809). The humus
theory appeared in his book on “The Principles of
Rational Agriculture”, which identified quantifiable
fertility indicators for crop systems (reviewed by Feller
et al. 2003; Manlay et al. 2007). Although Ingenhousz
had demonstrated in 1779 that plants photosynthesise, it
remained unclear how much of the plant’smassorigi-
nated from soil and air. This topic was of interest to 19th
century researchers and experiments aimed at determin-
ing if plants assimilate soil organic N (urea) had encour-
aging results (Cameron 1857). Several researchers
followed this line of study, evaluating asparagine as
anutrientsource(Baessler1884) and characterisinig
organic N forms in soil (Berthelot 1888; Lawes and
Gilbert 1887).
Rapid advances in organic chemistry informed
plant nutrition research, and researchers in the early
20th century tested organic compounds identified in
soils (Table 2). Organic C was identified as contribut-
ing to plant growth. Starch accumulated in plants
grown with organic carbon compounds ranging from
extracts of humus, glucose, saccharin to glycerine
(Acton 1889), and the role of organic C for supporting
plant growth was confirmed with plants grown in the
absence of light (Cailletet 1911; Mazé 1899). French
plant physiologist Molliard examined plant growth in
axenic conditions the presence of organic compounds,
concluding that sucrose is a source of carbon (C), and
asparagine and urea are sources of N and C for radish
plants (Molliard 1905,1909). He expanded research to
organic N substances present in soils and demonstrat-
ed that plant growth was supported in the order urate
(uric acid) > aspartate > asparagine > glycocoll
(glycine) > legumin > cyanide > amygdalin > hydro-
cyanic acid > leucine, while tyrosine, myronate and
alanine had toxic effects (Molliard 1910).
Oswald Schreiner, one of the USA
’s leading organic
chemists, analysed ‘The Organic Constituents of Soils
(Schreiner 1913). In his 1912 lecture to the American
Association for the Advancement of Science, Schreiner
gave an account of creatinine (2-Amino-1-methyl-1H-
imidazol-4-ol, a compound contained in urine) and ni-
trate as nutrient sources for wheat. According to
Schreiner’s research, creatinine and nitrate were present
in equal amounts in agricultural soils. In hydroculture,
wheat grew better with creatinine when supplied as sole
N source or together with small amounts of nitrate than
with nitrate only. At the 8th International Congress of
Applied Chemistry in Washington and New York
(1912) Schreiner presented a review of the ‘Organic soil
constituents in their relation to soil fertility’:‘The ni-
trogenous fertilizers, such as dried blood, tankage, fish
scrap, etc., as well as the leguminous crops as green
manure, are excellent sources of the compounds de-
scribed in this paper. ....such compounds are removed
from the soil with the greatest difficulty by drainage
waters, whereas nitrates are easily lost in this way, if
the plant does not remove them as fast as formed.
Nitrates do not last over from season to season but the
organic compounds can do so and yet be ready for
absorption and use by plants at any time. In this form
the nitrogen of the soil is conserved, while excessive
nitrification or even ammonification may result in actual
loss of soil nitrogen by leaching’.
6 Plant Soil (2012) 359:1–18

Table 2 Chronology of examples of early research on organic nutrients
Concept Approach References
Plants acquire and metabolise organic C compounds 20 plant species
a
in hydroculture and CO
2
-free air with organic C
sources (glucose, acetic aldehyde, aldehyde, glycerine, lævunilic
acid, others)
Acton 1889
Fern (Adiantum temoins) in sand culture and low light with burnt
fern biomass as C source
Mazé 1899
Bean (Vicia narbonensis) in the dark with glucose Cailletet 1911
Plants use organic N and C compounds for growth Radish (Raphanus sativus) in hydro- and pumice culture (aimed to
be sterile) with glucose as sole C source; asparagine, urea, and
other organic N compounds (see text) as N sources
Molliard 1905,1909,1910
Organic N compounds isolated from soil Arginine and histidine, pyrimidine derivatives and purine bases
extracted from soil
Schreiner and Shorey 1910a,b
Organic N compounds support shoot and roots
growth to different extent
Pea (Pisum arvense) in hydroculture (aimed to be sterile) (Fig. 2a) Hutchinson and Miller 1911
Soil N constituents have beneficial effect on plants
growth
Wheat in hydroculture (aimed to be sterile) with creatinine or
creatine, and histidine or arginine
Skinner Skinner 1912a,b
Plants grow equally well with soil organic N
constituents and nitrate
Wheat in hydroculture (aimed to be sterile) with nitrate or
creatinine. Soil constituents creatinine, hypoxanthine and
xanthine, arginine, histidine, and nucleic acid and glycine
(Fig. 2b)
Schreiner 1913;
Schreiner and Skinner 1915
Plants assimilate organic N compounds Maize (Zea mays) in sterile culture urea, peptone, guanin,
guanidin carbonate, casein, uric acid, linseed meal
Brigham 1917
Plants grow with organic C as sole C source Pea (Pisum spp.) and maize (Zea mays) in sterile hydroculture
with sucrose
Knudson 1920
a
Shoots (cut branches) of Acer pseudoplatanus,Phaseolus vulgaris,Ranunculus acris,Cheiranthus cheiri,Tilia europea,Scrophularia aquatica,Alisma plantago; whole plants
(seedlings) of Acer pseudoplatanus,Phaseolus vulgaris,Phaseolus multiflorus;Cheiranthus cheiri,Quercus robur,Campanula glomerata,Euphorbia helioscopia,Epilobium
hirsutum; water-plants (shoots) of Anacharis,Callitriche aquatica, and others
Plant Soil (2012) 359:1–18 7

Similarly, soil fertility researcher Skinner focussed
on histidine and arginine as nutrients and stressed that
N fertilisers derived from organic matter, ranging from
offal to green manure, support plant growth and have
the advantage of not being lost as easily from soil as
nitrate (Skinner 1912b). It seems ironic that N losses
from crop systems and possible solutions to this per-
vasive problem were already discussed a century ago.
In parallel with research on soil organic com-
pounds, microbiological studies examining biological
N
2
fixation culminated in the conclusive proof of N
2
fixation by the bacterial symbionts of legumes (Hell-
riegel and Wilfarth 1888). This discovery explained
earlier research by Gilbert and Lawes at Rothamsted
whose soil sterilisation experiments prevented N
2
fix-
ation (Lawes et al. 1860). Following the discovery of
legume symbionts, Winogradsky (1895) described
non-symbiotic N
2
fixing bacteria in soils, having pre-
viously discovered the bacteria responsible for N
transformations (Winogradsky 1890) and recognising
the fundamental importance of N-converting bacteria
for soil fertility (reviewed by Ackert 2006). Evidently
in the years leading up to World War I, high-level
research recognised the role of organic nutrients and
soil microbiology for plant nutrition.
Research on organic nutrients between and after
the World Wars
The year 1927 was a landmark in the recognition
of organic nutrients and microbiology as leading
soil microbiologist Winogradsky questioned the
increasing application of N fertilisers at two inter-
national chemical congresses (Winogradsky 1927a,
b). He warned that industrial fertiliser was dis-
abling effective biological N
2
fixation (BNF) and
related soil fertility-building microbiological pro-
cesses. Winogradsky argued that farmers had to
buy at a high price what could be obtained with
their own labour. Research into soil organics and
soil microbiology evidently had come of age and
held great promise to agriculture, but was counter-
acted by the use of synthetic N fertiliser. The first
synthetic N factory at Oppau (Gemany) produced
800tofammoniain1913andexpandedtopro-
duce 845,000 t in 1928; while reactive N was
initially produced for explosives manufacture, after
the war it was promoted as fertiliser (Smil 2004).
Agricultural research under government direction
had the industrialisation of agriculture assigned as
its chief task, and knowledge of soil biology and
organic nutrients was not transferred to the new
generation of researchers. In the interbellum and
after WWII, research on soil organics was acknowl-
edged but had only incidental follow-up (Table 3).
Schreiner et al. (1938) lamented in one of his last
publications, a contribution to the 1938 USDA
Yearbook of Agriculture: ‘The influence of the
World War I on the production of new fertiliser
materials was very marked. …The chief concern
of all belligerents, insofar as explosives were
concerned, was to have a plentiful supply of nitro-
gen…When the World War terminated, the huge
chemical plants, geared to capacity production of
wartime necessities, faced a difficult situation. In
order to avoid ruin, these plants turned to the
manufacture of nitrogen and other compounds for
fertilizer use’.
In 1953, Nobel Prize winner Virtanen stressed that
the way to agricultural intensification was not through
an increase in fertiliser application, but through in-
creasing BNF (Virtanen 1953). He showed that non-
leguminous plants growing in association with
legumes acquired amino acids released by legume
roots (Thornton and Nicol 1934; Virtanen and von
Hausen 1935;Table3). The research was well re-
ceived, and Virtanen’s lecture series was summarised
by the Editor of the journal Nature: ‘It is therefore
concluded that higher plants can take up and utilise
directly organic compounds present in soils before
their nitrogen is mineralised by bacteria or other
micro-organisms’(Nature 15 April 1933, p.535).
At least two alternatives to synthetic N fertilisers
were considered to intensify crop production (i) great-
er incorporation of biological N fixation in agricultural
production (Jensen 1950; Virtanen 1938) and (ii) fur-
ther development of the ‘organics’approach that pro-
motes restricted additions of mineral and synthetic
fertilisers (Hall 1919; Preston 1941). Both alternatives
were considered viable and included rotation with N
2
fixing crops and manure application.
By 1952, research into organic plant nutrition had
ceased in the institutes covered by the Agricultural
Research Centre of the USDA. The National Soil
and Fertilizer Research Committee was established in
1947 with a National Fertilizer Workgroup in 1951,
which issued its combined research in the 1954
8 Plant Soil (2012) 359:1–18

Table 3 Chronology of mostly post-World War II research on organic nutrients
Concept Approach References
Root-excreted amino acids are used by
companion plants
Nodulated legumes and companion plants in sterilised sand and agar culture Virtanen and von Hausen 1935
Adenine and phenylalanine incorporated
by roots
Onion roots (Allium cepa) with
14
C-labeled compounds Jensen 1957
DNA and derivatives are present in soil DNA from humic compounds extracted from agricultural soils Anderson 1958
Plants take up amino acids as intact
molecules
Roots of pea in nutrient solution with
14
C-amino acids Miettinen 1959
Sterile soil-grown bean (Phaseolus vulgaris) with
14
C-GLY or
14
C-ALA, analysis of free amino acids and tissue hydrolysate
Miller and Schmidt 1965
Straw extracts increase dry weight of
seedlings
Decomposed wheat straw extracted with distilled water, filtrates applied
to sand-grown rye seedlings
Flaig et al. 1960
Lignin degradation products are taken
up and metabolised by seedlings
Rye (Secale cereale) with
14
C-vanillin or vanillic acid in sterile closed-
chamber hydroculture, production of
14
CO
2
and
14
C distribution in plant
tissues
Flaig 1965
Exogenously supplied DNA or
nucleotides enter roots
Germinating barley with
3
H-labelled DNA and
3
H-labeled DNA in roots Ledoux 1965
Plants take up fractions of humic
substances
Sunflower (Helianthus annuus) in hydroculture with
14
C-labelled humic
fractions; control plants receive resultant CO
2
, uptake of
14
CO
2
determined
Führ and Sauerbeck 1966
Roots take up protein Fluorescein-labelled lysozyme and ferritin with barley, maize, onion and
other species
Seear et al. 1968
Plants take up and metabolise indole
14
C-labelled indole applied to mustard plants (Sinapis alba) in sterile agar,
radiograms of roots and shoots extracts and detection of intermediate of
indole metabolism
Scheffer et al. 1968
Externally supplied DNA enters roots and
increases desoxy-ribonuclease activity
Broad bean (Vicia faba) with salmon sperm or wheat germ DNA grown in
non-sterile hydroculture, cytochemical assay for DNAase
Gahan et al. 1974
Plant Soil (2012) 359:1–18 9

volume ‘Fertilizers and crop yields in the US’. The
volume’s focus on synthetic urea and inorganic fertil-
isers is evidence that organic compounds together with
green manures, manures and composts had disap-
peared from view. An example of this new vision is
demonstrated in Robert Salter, chief of the Bureau of
Plant Industry, Soils, and Agricultural Engineering
publication ‘World soil and fertilizer resources in re-
lation to food crops’, which fails to mention previous
research by scientists at the Bureau of Soils on organic
nutrients and biological N fixation: ‘Since nitrogen
fertilizers can be manufactured by fixation of nitrogen
from the atmosphere, world supplies are limited only
by the capacity of [industrial] plants to produce. This
plant capacity was expanded greatly in the last decade
because nitrates are a necessity of war’(Salter 1947).
By the mid-20th century plant nutrition was focussed
on mineral and synthetic fertilisers, but research on the
uptake of organic molecules established fundamental
knowledge of plant function. Since the 1950s, isotope-
labelling enabled tracing organic compounds and their
transformation products in plants (Table 3). The rela-
tionship between plants and humic compounds was
studied following observations that water extracts of
decomposed straw increased the dry weight of sand-
grown rye seedlings (reviewed by Flaig 1965,1968,
1984). Studies on
14
C-labelled lignin degradation prod-
ucts p-hydroxybenzoic, vanillic and syringic acid and
wheat seedlings in sterile hydroculture demonstrated
their uptake and metabolism in roots (Fig. 2c,reviewed
by Flaig 1968; Flaig and Harms 1977). Tryptophan, an
intermediate of indole metabolism, in root and shoot
extracts of mustard plants provided evidence that plants
take up and metabolise organic compounds (Scheffer et
al. 1968),
14
C-labelled glycine and β-alanine are assim-
ilated by bean plants (Miller and Schmidt 1965).
Nucleotides and DNA were reported to enter plant roots
(Jensen 1957;Ledoux1965; Ledoux and Huart 1972
and references cited) after supplying
3
H-DNA to barley
roots. Root autoradiographs showed that nuclei of root
Fig. 2 Examples of historic studies of organic plant nutrition. a
Experiment of Hutchinson and Miller (1911)ofpeaplants
grown in axenic solution culture with different organic N com-
pounds shows effects of the supplied N forms on shoot and root
growth (from Centralblatt für Bakteriologie, Parasitenkunde und
Infektionskrankenheiten, 30, p. 30, 1911). bExperimental set-
up of Schreiner and Skinner (1915) examining the ability of
wheat to use inorganic and organic N sources in hydroculture.
Plants grown with inorganic N (left panel) or with inorganic N
plus organic N (right panel) achieved similar growth (reprinted
from Botanical Gazette, Volume 59, p. 456, 1915 with permis-
sion of The University of Chicago Press). cApparatus used by
Flaig (1965) to demonstrate uptake and metabolism of
14
C-
labelled organic C compounds by roots of axenically cultivated
plants (Reprinted from The Use of Isotopes and Radiation in
Soil-Plant Nutrition Studies, p. 11, 1965 with permission of
International Atomic Energy Agency)
10 Plant Soil (2012) 359:1–18

cells were rapidly
3
H-labelled and radioactivity was
localised predominantly in the root elongation zone
and represented ~0.5 % of barley DNA. Further experi-
ments led to the conclusion that externally supplied
DNA or nucleotides were acquired and nucleotides in-
tegrated into plant DNA (Ledoux and Huart 1972).
Gahan et al. (1974)showedthatVi c i a f a b a plants in
aerated hydroculture amended with salmon sperm or
wheat germ DNA displayed up to ~7-fold increases in
DNAseactivityinresponsetoincubationtime(Table3).
A concomitant increase in the number of cytosolic
vesicles was detected containing acid deoxyribonucle-
ase activity; initially vesicles were observed in the root
epidermis but subsequently also in cortical cells. Gahan
et al. (1974) interpreted the findings that DNA enters the
roots via endocytosis as analogous to lysosomal diges-
tion in animal cells. Research on N compounds expand-
ed to fluorescent proteins demonstrating that lysozyme
entered root cortex cells while much larger ferritin
(450 kDa) did not penetrate cells and was observed only
in the epidermis of root cell walls (Seear et al. 1968).
Although these experiments did not determine whether
intact macromolecules or fragments enter root cells,
they provide evidence that plants acquire and metabolise
organic compounds and link to contemporary research.
A role for organic nutrients in modern crop
production
In addition to the discussed role of organic nutrients
for supplying essential nutrients, good arguments exist
for using organic nutrients in agriculture. Synthetic
and inorganic fertilisers are derived from finite natural
resources such as fossil fuels, phosphate rock, potas-
sium salts and others, whereas organic wastes are by-
products of various industries. In the USA alone ~1
billion tons of agricultural recyclables are generated
annually (Edwards and Someshwar 2000) and sustain-
able high-productivity crop systems will benefit from
knowledge of the effects of organic nutrients on soil,
plants and microbes for improved soil function and
plant health.
Organic wastes such as straw contain much C as
cellulose and hemicelluloses serve as substrates for
cellulolytic microorganisms and subsequently for oth-
er microbes including N
2
fixing bacteria (Roper and
Ladha 1995). Inorganic fertilisers can affect plant and
soil health by inhibiting mycorrhizal and N
2
fixing
symbionts (Larsen et al. 2007; Ryan and Graham
2002; Streeter 1988), and AM fungi were less abun-
dant in soil supplemented with inorganic fertilisers
than organic nutrients (Verbruggen et al. 2010). The
presence of organic nutrients may reduce soil-borne
diseases (reviewed by Bailey and Lazarovits 2003;
Hoitink and Boehm 1999; Janvier et al. 2007), and
long-term use of inorganic fertilisers can promote
incidence of plant diseases (Hoitink and Boehm
1999). Explanations include that organic amendments
have biological or chemical properties that affect dis-
ease agents directly or through stimulation of compet-
itor microorganisms, and/or induced plant resistance
(Ghorbani et al. 2005; Zhang et al. 1998). However,
disease suppressive effects of organic amendments are
often inconsistent and coincidental increases in dis-
ease incidence and severity can accompany organic
amendment application (reviewed by Bonanomi et al.
2010), warranting better knowledge of soil biology.
Inorganic or synthetic nutrients are used in modern
agriculture for reasons that include ease of application
and lack of organic materials available in specialised
agricultural enterprises. Globally, crop systems have a
low nutrient use efficiency with ~30–50 % and 45 %
of applied N and P fertilisers, respectively, used by
crops (Tilman et al. 2002). While some nutrients
remain in soils, others contribute to pollution, in-
cluding a growing pool of reactive P and N, which
are a pressing issue for reasons that include loss of
biota, and the integrity of ecosystems and global
biogeochemical cycles (Gruber and Galloway
2008; Rockström et al. 2009). Ingested nitrate
affects mammals as causal agent for carcinogenesis
and other diseases (Santamaria 2006), and expo-
sure to excessive quantities of reactive N shortens
our life expectancy (Sutton et al. 2011). In plants,
the effects of nitrate include a lower production of
UV-B protective anthocyanins (Chimphango et al.
2003) and quality and quantity of root exudates
(Coronado et al. 1995; Wojtaszek et al. 1993).
Organic nutrients, derived for example from an-
imal manures, may also result in N loss from soil
(Kirchmann 1985; Kristensen et al. 1995), but these
losses can be lower in systems receiving organic
than inorganic nutrients (Drinkwater et al. 1998;
Koepf 1973). Systems receiving organic nutrients
displayed less nitrate leaching over a cropping sea-
son per unit area than conventional systems
(Kirchmann and Bergström 2001) although reduced
Plant Soil (2012) 359:1–18 11

leaching may take effect only after several seasons
of organic amendment (Dourado-Neto et al. 2010;
Dufault et al. 2008). Evaluating inorganic and or-
ganic nutrients and their combined application will
produce the knowledge required to improve the
efficiency of nutrient use in agriculture.
As noted by Schreiner (1913), soil biota are affect-
ed by fertiliser salts that change the physical, chemical
and biochemical properties of soils. Reported soil
degradation associated with inorganic N fertiliser
includes loss of soil organic matter (SOM), declining
soil pH and declining crop yields (Guo et al. 2010;Ju
et al. 2009; Khan et al. 2007; Mulvaney et al. 2009).
Loss of SOM in degraded agricultural soils affects
aeration, structure, nutrient availability and microbial
ecology (Davey 1996). Preventing declining SOM has
been a challenge since the beginning of sedentary
agriculture, and returning organic residues to soil con-
tributes to replenishing SOM (McNeill and Winiwar-
ter 2004). Adverse effects of synthetic and inorganic
fertilisers have questioned their continued application,
aptly put by Dutch proverb “Fertiliser makes the fa-
ther rich and the son poor”. SOM is a key factor for
soil fertility due to its role for soil structure, biological
processes and nutrient cycling, providing sink and
source for nutrients and energy for soil organisms
and plants. Long-term trials have shown that yields
are often higher in soils with higher SOM (Johnston et
al. 2009; Manlay et al. 2007; Reeves 1997). Organic
cropping systems that supply predominantly organic
materials and legumes as nutrient sources have been
compared with conventional systems (Badgley et al.
2007), demonstrating that average yields are 5 to
34 % lower in organic compared with conventional
systems (Seufert et al. 2012). Compared to conven-
tional agriculture, organic systems are more likely
to be N limited (Seufert et al. 2012), which may
reduce off-site N losses.
Transformation of high-input/high-production crop
systems to systems with efficient resource use is need-
ed and ‘mineralist’and ‘organicist’ideologies are
being bridged—if not conceptually, then through the
increasing use of organic fertilisers in agriculture. This
is exemplified in Australian sugarcane production
where stagnating or declining yields in recent decades
defy high fertiliser applications and have led to the
adoption of ‘green cane trash blanketing’, the post-
harvest retaining of plant matter on the field that con-
tributes up to 60 kg N ha
−1
, as well as the increasing
use of organic materials such as mill wastes and com-
posts as soil amendments and nutrient sources.
Down to earth
Nutrient stoichiometry and optimal supply for maxi-
mum crop production were principal drivers of plant
nutrition research from the mid-20th century. Reasons
for the almost exclusive focus on inorganic nutrients
include the suggestion of precise and easy application
and quantification of nutrient availability with rela-
tively simple chemical assays. Due to ready dissolu-
tion of fertilisers, crop soils contain inorganic nutrients
in concentrations often exceeding those of natural
ecosystems by several orders of magnitude.
15
N-label-
ing methods (MacVicar 1957) have shown that in
some investigated systems, plants can derive a larger
proportion of N from soil organic matter than from
added fertiliser (Kudeyarov 1992; Dourado-Neto et al.
2010) although it is unknown whether this N is ac-
quired as organic or inorganic N.
It will be difficult to increase agricultural produc-
tion over the next 40 years to supply the growing
human population predicted to peak at ~9 billion
(United Nations; U.S. Census Bureau database,
http://www.census.gov/ipc/www/idb/). To meet the
projected demand for agricultural production, chal-
lenges associated with competition for land, water
and energy resources are amplified. Global use of N
and P fertiliser increased 7- and 3.5-fold between 1960
and 1995, and we experience the consequences of this
increase in greatly magnified ecological problems.
Clearly, we cannot just project the demand for N and
P fertiliser to triple by 2050 (Tilman et al. 2002) but
have to consider all means at our disposal for the
intensification of agricultural production and opt for
soil- and ecology-adapted versions.
Recognising the importance of healthy soils, it is
timely to draw on diverse nutrient sources to prevent
pollution and depletion of natural resources (FAO
2011). With food security as primary objectives,
Haber-Bosch (technology enabling synthesis of reac-
tive N) and The Green Revolution (initiatives advanc-
ing research, development and technology transfer that
resulted in increased crop yields during 1940s–1970
ties) saved us from famine; now environmental sus-
tainability is at the heart of innovation in crop produc-
tion. Next-generation crop systems will increasingly
12 Plant Soil (2012) 359:1–18

rely on nutrients that supplement or replace synthetic
N fertilisers and natural-deposit resources. Nutrient-
efficient crop systems have to integrate microbial sym-
bionts, appropriate soil biota and diverse nutrient sour-
ces. We have limited quantitative information on the
contribution of organic nutrients to crop nutrient budg-
ets, but the results from controlled experiments are
encouraging: axenic Arabidopsis supplied with subop-
timal amounts of inorganic N and supplemented with
protein produced the same biomass as plants supplied
with a non-limiting supply of inorganic N (Paungfoo-
Lonhienne et al. 2008).
Examples for yield-enhancing effects of combined
organic + inorganic nutrients includes maize cropping in
sub-Saharan Africa (Chivenge et al. 2011) and organic +
inorganic fertiliser in the System of Rice Intensification
to manage plants, soil, water and nutrients, and lowering
cost of production while enhancing crop yields (Thakur
et al. 2010;Zhaoetal.2010). Application of farmyard
manure along with inorganic fertilisers maintained
SOM and long-term productivity and increased micro-
bial biomass (Goyal et al. 1999;Kauretal.2005;Drink-
water and Snapp 2007).
Future research will identify how the use of organic
nutrients can be maximised in combination with in-
creased BNF and AM fungi. AM fungi enhance the
decomposition of organic material and retrieve organic
N and P for plants (reviewed by Hodge et al. 2010;
Hodge and Fitter 2010; Smith et al. 2011). The ability
of N
2
fixing plants to augment P availability in soil
(Houlton et al. 2008) can be exploited. Root exudation
of protons, organic acids and extracellular enzymes
deserve consideration for improved use of organic
nutrients. The combined function of soil, plants and
microbes (Dessaux et al. 2009; Hinsinger et al. 2009;
Lambers et al. 2009; Ryan et al. 2009) enabled by
agronomic practices, plant selection, rhizosphere en-
gineering and biotechnology will advance the use of
organic nutrients.
Conclusions
Although organic compounds have been considered as
nutrient sources and growth promoters for plants for
over a century, the focus of plant nutrition has
remained largely on inorganic nutrients. With the need
to improve nutrient efficiency of crop production and
recycling of nutrients contained in wastes from
agriculture and other industries, organic nutrients hold
promise for use in modern crop systems and warrant
new approaches to plant nutrition.
Acknowledgments We are grateful to Dr David Teakle for
discussions about the history of organic plant nutrition and his
critical comments that have improved the manuscript, to Prof
Peter Gahan for his advice on the section on DNA uptake, to Dr
Paul Scott for his thoughtful comments on this manuscript. Our
research is enabled with funding from the Australian Research
Council (Discovery Grant DP0986495 to SS) and The Univer-
sity of Queensland (Early Career Researcher grant to CPL). We
gratefully acknowledge the excellent facilities provided by the
ARC Centre of Excellence for Integrative Legume Research.
The authors acknowledge the following references in Fig. 2:
hydroponic pea plants (Centralblatt für Bakteriologie, Parasiten-
kunde und Infektionskrankenheiten, 30, page 30, 1911); hydro-
ponic wheat (reprinted from Botanical Gazette, Volume 59, page
456, 1915 with permission of The University of Chicago Press);
scheme apparatus (Reprinted from The Use of Isotopes and
Radiation in Soil-Plant Nutrition Studies, page 11, 1965 with
permission of International Atomic Energy Agency).
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