397
Plant rhizodeposition ± an important source for carbon turnover in soils
Birgit W. Hütsch1*, Jürgen Augustin2, and Wolfgang Merbach1
1
Institute of Soil Science and Plant Nutrition, Martin Luther University Halle-Wittenberg, Adam-Kuckhoff-Str. 17b,
D-06108 Halle (Saale), Germany
2
Center for Agricultural Landscape and Land Use Research (ZALF), Eberswalder Str. 84, D-15374 Müncheberg,
Germany
Accepted 31 May 2002
Summary ± Zusammenfassung
The soil organic matter plays a key role in ecological soil
functions, and has to be considered as an important CO2 sink on a
global scale. Apart from crop residues (shoots and roots), left over
on the field after harvest, carbon and nitrogen compounds are also
released by plant roots into the soil during vegetation, and undergo
several transformation processes. Up to now the knowledge about
amount, composition, and turnover of these root-borne compounds
is still very limited.
So far it could be demonstrated with different plant species, that
up to 20 % of photosynthetically fixed C are released into the soil
during vegetation period. These C amounts are ecological relevant.
Depending on assimilate sink strength during ontogenesis, the C
release varies with plant age. A large percentage of these root-
borne substances were rapidly respired by microorganisms (64±
86 %). About 2±5 % of net C assimilation was kept in soil. The
root exudates of maize were mainly water-soluble (79 %), and in
this fraction about 64 % carbohydrates, 22 % amino acids/amides
and 14 % organic acids could be identified. Plant species and in
some cases also plant cultivars varied strongly in their root
exudation pattern. Under non-sterile conditions the exuded com-
pounds were rapidly stabilized in water-insoluble forms and bound
preferably to the soil clay fraction. The binding of root exudates to
soil particles also improved soil structure by increasing aggregate
stability.
Future research should focus on quantification and character-
ization of root-borne C compounds during the whole plant
ontogenesis. Apart from pot experiments with 14CO2 labeling, it
is necessary to conduct model field experiments with 13CO2
labeling in order to be able to distinguish between CO2 originating
from the soil C pool and rhizosphere respiration, originating from
plant assimilates. Such a separation is necessary to assess if soils
are sources or sinks of CO2. The incorporation of root-borne C
(14C, 13C) into soil organic matter of different stability is also of
particular interest.
Key words: rhizodeposition / root exudates / 14CO2 pulse labeling /
root respiration / rhizomicrobial respiration / stabilization of SOM
* Correspondence: Priv.-Doz. Dr. B. Hütsch; E-mail: huetsch@landw.uni-
halle.de
J. Plant Nutr. Soil Sci. (2002), 165, 397±407 (2002)  WILEY-VCH Verlag GmbH, D-69451 Weinheim, 2002
Pflanzliche Rhizodeposition ± eine wichtige
Quelle für den Kohlenstoffumsatz in Böden
Die organische Bodensubstanz (OBS) nimmt eine Schlüsselrolle
bei den ökologischen Bodenfunktionen ein und stellt global
betrachtet eine wichtige CO2-Senke dar. Neben den auf dem Feld
verbleibenden Ernte- und Wurzelrückständen werden C- und N-
Verbindungen auch während des Pflanzenwachstums in den Boden
abgegeben und unterliegen dort vielfältigen Umsetzungsprozessen.
Der Kenntnisstand über die Menge, Zusammensetzung und den
Umsatz dieser wurzelbürtigen Verbindungen im Boden ist noch
sehr begrenzt. Daher beschäftigt sich die vorliegende Publikation
mit der Rhizodeposition als wichtiger Quelle des C-Umsatzes in
Böden, insbesondere mit den mobilen Wurzelabscheidungen.
Bisher konnte anhand verschiedener Pflanzenarten gezeigt werden,
dass bis zu 20 % des photosynthetisch fixierten C während der
Vegetation durch die Wurzeln freigesetzt werden. Es handelt sich
dabei um ökologisch relevante C-Mengen. In Abhängigkeit von der
Stärke des Assimilatsinks während der Ontogenese variiert die C-
Freisetzung mit dem Pflanzenalter. Ein hoher Anteil dieser
wurzelbürtigen Verbindungen (64±86 %) wurde schnell durch
Mikroorganismen veratmet. 2±5 % der Netto-C-Fixierung blieben
im Boden zurück. Dieser Bodenrückstand war bei Wurzelabschei-
dungen von Mais hauptsächlich wasserlöslich (79 %), und in dieser
Fraktion wurden 64 % Kohlenhydrate, 22 % Aminosäuren/Amide
und 14 % organische Säuren identifiziert. Pflanzenarten und
teilweise auch -sorten variierten stark in der Zusammensetzung
ihrer Wurzelexsudate. Unter insterilen Bedingungen wurden die
exsudierten Verbindungen schnell in nichtwasserlöslicher Form
stabilisiert und vor allem an die Tonfraktion des Bodens gebunden.
Die Bindung an Bodenpartikel verbesserte die Bodenstruktur durch
erhöhte Aggregatstabilität.
Zukünftige Forschungsarbeiten sollten sich auf die Quantifizierung
und Charakterisierung wurzelbürtiger C-Verbindungen während der
gesamten pflanzlichen Ontogenese konzentrieren. Abgesehen von
Gefäûversuchen mit 14CO2-Applikation ist es erforderlich, Feldmo-
dellversuche mit 13CO2-Applikation durchzuführen, um zwischen
der CO2-Emission aus dem Boden-C-Pool und derjenigen aus der
Rhizosphärenatmung (Ursprung sind Pflanzenassimilate) unter-
scheiden zu können. Eine solche Trennung ist zur Beurteilung, ob
Böden eine Quelle oder Senke für CO2 darstellen, zwingend
erforderlich. Von besonderem Interesse ist auch der Einbau des
wurzelbürtigen C (14C, 13C) in OBS-Fraktionen unterschiedlicher
Stabilität.
1436-8730/02/0408-397 $17.50+.50/0
398
1 Introduction
Soil organic matter plays a key role in ecological soil
functions as well as in conservation of soil fertility, and it is
on a global scale an important CO2 sink or source depending
on conditions. With crop residues, which are kept on the
field after harvest, considerable amounts of organic carbon
are incorporated into the soil. However, also during
vegetation and plant growth, C compounds are released by
the roots and undergo various transformation processes in
soil. This rhizodeposition has diverse functions in plant
nutrition and soil ecology. Some of these compounds are
able to improve nutrient availability, e.g. phytosiderophores,
mugineic acids, and malate for Fe (Treeby et al., 1989; Fan
et al., 2001), organic acids for phosphate and micronutrients
(Schilling et al., 1998; Gerke et al., 2000a, b; Hinsinger,
2001; Keller and Römer, 2001), others can relieve Al-
toxicity by chelating the phytotoxic metal (Pellet et al.,
1995; Heim et al., 2001). Additionally, root exudates act as
allelochemicals (Mahall and Callaway, 1992; Yu and
Matsui, 1994; Birkett et al., 2001), or as signaling substances
for the establishment of symbiotic relationships between
plant roots and microorganisms (Lerouge, 1994; Stacey et
al., 1995). Also they serve as an important carbon and energy
source for rhizosphere soil microorganisms (Cheng et al.,
1996; Qian et al., 1997). Despite the involvement in many
soil ecological functions, the knowledge about the amount,
composition, and dynamics of root-borne C compounds is
still very limited. So far in many investigations solution
culture experiments were conducted (e.g. Groleau-Renaud
et al., 2000; Nardi et al., 2000; Dousset et al., 2001) or quartz
sand was used as growth substrate (e.g. Shepherd and
Davies, 1993; Hodge et al., 1996; Paynel et al., 2001;
Yoshitomi and Shann, 2001); measurements under soil
conditions are rare (Merbach et al., 1999), particularly if
composition studies are considered. Thus, information about
the importance of rhizodeposition for production and
stabilization of soil organic matter is scarce.
Attempts were made to achieve total carbon balances for
the soil-plant system. For this purpose labeling of photo-
assimilates with 14CO2 was employed to trace the carbon
flow through the plant into the soil, and to monitor further
transformation processes (e.g. Keith et al., 1986; Helal and
Sauerbeck, 1989; Swinnen et al., 1994a, 1995; Rattray et al.,
1995; Kuzyakov et al., 1999; Nguyen et al., 1999; Warem-
bourg and Estelrich, 2000, 2001; Domanski et al., 2001;
Kuzyakov and Cheng, 2001; Van der Krift et al., 2001).
Swinnen et al. (1994a) found that, depending on the
development stage of wheat plants, between 15 % and
39 % of net 14C assimilation were translocated below-
ground, and of this 35 % to 48 % were respired by roots and
microorganisms in the rhizosphere. Experiments on peren-
nial bromegrass gave a belowground translocation as high as
56 % to 69 % of net 14C assimilation, and the main part of
this was bound in roots (52±62 %), 24 % to 31 % were
attributed to rhizosphere respiration, and 13 % to 21 % were
found in the soil matrix (Warembourg and Estelrich, 2000).
For determination of the total amount of plant released
organic compounds into the soil, the differentiation between
root and rhizomicrobial respiration is necessary. Several
Hütsch, Augustin, and Merbach
different approaches were used to separate both CO2 sources
in the rhizosphere, but the obtained results are not
unequivocal due to methodical limitations (see Chapters
2.1 and 2.2 for details).
At present there are still great uncertainties concerning the
quantification of rhizodeposition and the separation and
identification of individual compounds. Differentiation was
mainly achieved according to different solubility, e.g. water-
soluble, low molecular weight compounds like exudates and
lysates, and insoluble compounds with a high molecular
weight like mucilage and dead root residues. In most cases
the quantity of these compounds was not determined, and a
separation of root cell wall constituents from other
substances could not be achieved. Limited information is
available on the turnover of rhizodeposition as a whole and
of individual components, referring to the microbial
metabolism, the implementation into different organic
matter fractions during the vegetation period, and the
interaction with soil mineral particles.
Thus the aim of the investigations presented here was to
establish a carbon balance of the total amount of
rhizodeposits, including an estimation of rhizomicrobial
respiration. Furthermore, the composition of root-borne
compounds had to be identified as well as their trans-
formation and incorporation into soil organic matter and
their adsorption to the mineral soil matrix.
2 Quantification and characterization of rhizode-
position
14
2.1 C rhizodeposition balance
In order to trace the fate of CO2 assimilated by plants and to
distinguish between carbon originating from plants and soil-
borne carbon, commonly two compartments, plant shoots
and soil with roots, are established and gas-tightly separated.
Afterwards plant shoots are pulse-labeled with 14CO2. For
the carbon balance the total 14C rhizodeposition during plant
growth has to be determined, which is only possible after
distinguishing between root respiration and rhizomicrobial
respiration (ªsecondary microbial exudate respirationº). For
this purpose sterile treatments, using autoclaved soil, were
included in investigations of Merbach et al. (1996), and the
respiration under sterile and non-sterile growing conditions
was compared. These results can be used to calculate the
total 14C-rhizodeposition. The C balance in the plant-soil
system is given in Fig. 1 for spring wheat (4 to 6 leaves) and
alfalfa (6 to 8 leaves). It could be demonstrated that the
largest percentage of 14C was found in the plant material,
and total 14C released into the soil amounted between 14.4
and 18.3 % of the photosynthetically fixed 14C. Approx-
imately 86 % and 64 % of this root-borne 14C from wheat
and alfalfa, respectively, were respired by microorganisms
during three days. The residual 14C in soil was 2.5 % (wheat)
and 5.2 % (alfalfa) of the net 14CO2 assimilation. Com-
parable results were obtained in investigations of Barber and
Martin (1976) and Helal and Sauerbeck (1989).
An alternative experimental setup according to Swinnen
(1994) was also used to differentiate between root and
Plant rhizodeposition as source for carbon turnover
Figure 1: Quantification of C distribution in the plant/soil system of wheat
and alfalfa after 14CO2 labeling of plant shoots; calculation of root
respiration and total C release into soil using comparison of non-sterile and
sterile treatments (n = 5) (after Merbach et al., 1996).
Abbildung 1: Bilanzierung der C-Verwertung im System Pflanze/Boden
bei Weizen und Luzerne nach 14CO2-Begasung der Pflanzensprosse;
Berechnung der Wurzelatmung und Gesamtabgabe in den Boden durch
Vergleich unsteriler und steriler Varianten (n = 5) (nach Merbach et al.,
1996).
Figure 2: Model rhizodeposition method to separate root and microbial
14
C respiration after pulse-labeling of plants with 14CO2 (after Swinnen,
1994).
Abbildung 2: Schema der Modell-Rhizodepositionsmethode zur Tren-
nung von 14C Wurzel- und Mikrobenatmung nach Puls-Markierung der
Pflanzen mit 14CO2 (nach Swinnen, 1994).
rhizomicrobial respiration (Fig. 2). After the gastight
separation of soil and plant shoots, treatment (a) was
pulse-labeled with 14CO2, in treatment (b) a mixture of
finely ground maize roots and solved glucose, both labeled
with 14C, was applied to the soil as model rhizodeposits. It is
assumed that CO2 release in treatment (a) originates from
root respiration as well as from microbial exudate respira-
tion, whereas in treatment (b) the total CO2 production is
exclusively attributed to microbial activity. With the
equation given in Fig. 2 the microbial 14C-respiration in
the 14CO2-labeled treatment (a) was calculated (after
Swinnen, 1994).
399
Figure 3: Quantification of C distribution in the plant/soil system of maize
using the experimental setup after Swinnen (1994); comparison of 14CO2
labeling of plant shoots with application of 14C-labeled exudates (glucose)
and root residues to the soil (n = 4); soil respiration = respiration from
belowground; plants were harvested 2 weeks after labeling (Hütsch et al.,
unpublished).
Abbildung 3: Bilanzierung der C-Verwertung im System Pflanze/Boden
bei Mais im Versuchsansatz nach Swinnen (1994); Vergleich der 14CO2-
Begasung der Pflanzensprosse mit der Applikation von 14C-markierten
Exsudaten (Glucose) und Wurzelresten zum Boden (n = 4); Pflanzen
wurden 2 Wochen nach Markierung geerntet (Hütsch et al., unveröffent-
licht).
The 14C balance for maize plants is given in Fig. 3 (Hütsch
et al., unpublished data). The treatment with 14CO2 labeling
showed a 14C residue in soil of 4.0 % of net 14C assimilation,
which was comparable to our results of wheat and alfalfa
(Fig. 1). The microbial 14C respiration corresponds to 1.9 %
of the net 14CO2 assimilation and 32.4 % of the total
rhizodeposition (Hütsch et al., unpublished). In experiments
of Shepherd and Davies (1993) with oilseed rape 35 to 51 %
of root-borne 14C was respired by microorganisms. In own
investigations the microbial respiration contributed 5.6 % to
14
C soil respiration, and lay thus in the range given by
Swinnen and van Veen (1992; microbial respiration was 4±
9 % of 14C soil respiration). For the root respiration a value
of 32.7 % of net 14CO2 assimilation was determined, which
is remarkably higher than the values for wheat and alfalfa
(10 % and 25 %, respectively; Fig. 1).
If these discrepancies are caused by the different methods
employed or if they are attributable to the different plant
species, can only be answered with a direct comparison of
both methods using the same plant species and the same soil.
However, in this context one has to consider that both
methods have several disadvantages. On one hand plant
growth is inhibited under sterile conditions and a lower
amount of exudates is released than in a non-sterile growth
medium (Merbach and Ruppel, 1992; Meharg and Killham,
1995; Groleau-Renaud et al., 2000; Paynel et al., 2001;
Todorovic et al., 2001), where the rhizosphere micro-
organisms act as a sink for root deposits. In addition, the
microbial population in soil is only partly culturable, yet
non-observation of microbial growth on a culture medium is
considered as an index for sterility, thus the experimental
conditions can only be referred to as ªsemi-sterileº. On the
other hand, the method of Swinnen (1994) has also some
drawbacks. First of all it is impossible to apply the mixture
of glucose and root residues directly into the rhizosphere,
where microbial activity and proliferation are much higher
400 Hütsch, Augustin, and Merbach

than in the bulk soil. This can cause an underestimation of

the microbial respiration. Secondly, it is assumed that model
rhizodeposits and 14C rhizodeposition after pulse labeling
are equally transformed by the microorganisms. This
assumption is difficult to meet, as glucose is only one
compound among many different maize root exudates (see
Fig. 5). Additionally, the total amount of rhizodeposits is
normally not available at the same time, the date of
application, instead they are released continuously during
the vegetation period. A steady running nutrient source for
the microorganisms will certainly cause a stronger enhance-
ment of their activity than a single application. Additionally,
carbon is utilized differently in rhizosphere and in root-free
soil. These points should be considered for interpretation of
the results. Nevertheless, both methods showed that the total
C rhizodeposition can reach remarkable values and that its
importance for production and stabilization of soil organic Figure 4: Variation of 14CO2 evolution from soil immediately after pulse
matter has to be enlightened. labeling of maize shoots; dark columns are periods without light (night
cycles) (Hütsch et al., unpublished).
Abbildung 4: Variation der 14CO2-Abgabe aus dem Boden nach Puls-
Markierung der Sprosse von Maispflanzen; dunkle Säulen stehen für
2.2 Further attempts to separate root respiration from Perioden ohne Beleuchtung der Pflanzen (Nachtzyklen) (Hütsch et al.,
rhizomicrobial respiration unveröffentlicht).

As the estimate of microbial contributions to rhizosphere

respiration is still very vague and ranges from 5 % to 85 %
(see above and Todorovic et al., 2001), further attempts were
made in order to achieve more accurate values. A great
degree of uncertainty still exists with respect to its
determination because the works, including the studies
mentioned above, are based on assumptions that are difficult
to test. Thus, the quantification of rhizomicrobial respiration
still needs to receive consideration. In that framework, one
method is based on saturation of the soil solution with
unlabeled 12C-glucose immediately before 14C pulse label-
ing of growing plants (Cheng et al., 1993). It is assumed that
12
C-glucose addition dilutes 14C microbial respiration of
root-borne substances. This method of isotopic dilution
allowed to estimate root respiration (41 %) and rhizomicro-
bial respiration (59 %), as well as soluble C concentrations
in the rhizosphere of 3 weeks old wheat plants. Its
disadvantage, however, is that the allocation period is
necessarily kept short (4 h), which means that the 14C root
respiration as well as 14C rhizodeposition is incomplete.
With another method, based on the kinetics of 14CO2 efflux
from soil after 14C pulse labeling, similar results could be
achieved with Lolium perenne (Kuzyakov et al., 1999). For
the determination a model was used, which is based on the
assumption that the processes responsible for rhizosphere
respiration occur at different rates. The most rapid process is
CO2 efflux from root respiration. The CO2 evolution caused
by microbial respiration of root exudates is a slower process
than root respiration because it consists of a chain of
successive processes: synthesis by the plant and exudation
from the root, uptake and respiration by microorganisms.
Microbial respiration of dead roots is very slow and,
therefore, negligible in the first days after pulse labeling
(Kuzyakov et al., 1999). Already Warembourg and Billes
(1979) established, that a pulse labeling of wheat assimilates
resulted in two peaks of belowground respiratory activity,
attributing the second peak to microbial respiration of root
exudates. Meanwhile also Nguyen et al. (1999) and
ourselves (Fig. 4; Hütsch et al., unpublished) observed the
presence of two phases of 14C activity in the rhizosphere
respiration of maize plants. However, the second peak also
occurred under sterile conditions, thus being related to root
respiration (Todorovic et al., 2001). The authors suggested
that the second phase of activity resulted from the utilization
by roots and by microorganisms of stored 14C compounds,
which accumulated during the previous light period.
Other studies tried to achieve a separation of root
respiration and microbial respiration of root-borne com-
pounds by introduction of antibiotics into the growth
medium (e.g. Minchin and McNaughton, 1984; Helal and
Sauerbeck, 1991; Domanski et al., 2002). Also these
attempts have restrictions, as could be demonstrated by
Smart et al. (1995) after application of several antibiotics to
hydroponically grown wheat plants. Most antibiotics tested
reduced wheat growth rates substantially, and they acted
slowly, with maximum reductions in rhizoplane bacteria
occurring after more than 48 h of exposure. Additionally,
many viable bacteria remained on root surfaces (Smart et al.,
1995). In soil as growth medium an equal distribution of the
antimicrobial agents would be difficult to achieve, if this is
possible at all.
2.3 Water-soluble root exudates as affected by plant
species and cultivars
Fractionation of water-soluble root-borne C compounds
from different plant species revealed that in wheat, pea,
alfalfa, and Amaranthus retroflexus L. the largest portions
were carbohydrates (CH) and organic acids (OA), while
amino acids (AA) occurred only in small amounts (Tab. 1).
In contrast, organic acids and amino acids were dominant in
oil radish and Chenopodium album L. A more detailed
analysis was performed with maize plants. Water-soluble
root exudates were collected from quartz sand culture with
Plant rhizodeposition as source for carbon turnover 401

Table 1: Fractionation of water-soluble root-borne C compounds from the 5d). Likewise serine, together with glycine, were the most
rhizosphere of 14CO2-labeled plant shoots grown under soil conditions; OA abundant amino acids in clover and ryegrass root exudates
= organic acids (acid fraction), CH = carbohydrates (neutral fraction), AA (Paynel et al., 2001). Aulakh et al. (2001a) characterized root
= amino acids (basic fraction); mean of 10 replicates, recovery rate: 88± exudates of rice plants, and found that among organic acids,
94 % of specific 14C activity 22 kBq (mg C)±1 (after Merbach et al., 1999).
malic acid showed the highest concentration followed by
Tabelle 1: Fraktionierung wasserlöslicher wurzelbürtiger C-Verbindungen
tartaric, succinic, citric, and lactic acids. Thus, it can be
im wurzelnahen Boden nach 14CO2-Sprossbegasung verschiedener Pflan-
concluded that plant species vary strongly in their root
zenarten; OA = organische Säuren (saure Fraktion), CH = Kohlenhydrate
(neutrale Fraktion), AA = Aminosäuren (basische Fraktion); Mittel aus je
exudation pattern.
10 Wdh., Wiederfindungsrate: 88±94 % der spezifischen 14C-Radio- Results concerning variations in root exudation among
aktivität 22 kBq (mg C)±1 (nach Merbach et al., 1999). plant cultivars are not corresponding. Two pea cultivars
showed no significant differences in exudation of sugars,
Water-soluble % of total water-soluble amino acids, and carboxylic acids (Gransee and Witten-
Plant species exudates exudates mayer, 2000). However, the composition of root exudates
[mg C (g root DM)±1] OA CH AA
from two maize cultivars, grown under hydroponic con-
Wheat 11.6 34 49 6 ditions, varied strongly in the organic acid fraction with
Alfalfa 18.5 23 46 12 either tartaric or malic acid being the predominant
Oil radish 27.7 57 15 24 compound, followed by much smaller contributions of
Pea 16.0 9 52 7 oxalic, citric, and fumaric acid (Tab. 2; Nardi et al., 2002).
Chenopodium album L. 16.2 40 15 31 The results of Aulakh et al. (2001a) showed that significant
Amaranthus retroflexus L. 15.2 23 40 23 differences in the individual organic acids exuded exist
HSDTukey 0.05 3.7 between individual rice cultivars at a given growth stage. So
far no convincing explanation for differences in composition
of root exudates between plant cultivars can be given.
Cultivar differences in the total amount of root-released C
were attributed to root length (Xu and Juma, 1994) and root
the so-called ªdipping methodº, and subsequently the
dry matter production (Wang and Adachi, 2000). If these
constituents were separated with ion exchange resins and
parameters also affect the composition of root exudates still
quantified by HPLC. Details of the method are described by
needs to be investigated.
Gransee and Wittenmayer (2000). The maize root exudates
Based on the observed significant differences among rice
were mainly water-soluble (79 %), and in this fraction 64 %
cultivars, breeding of new, high-yielding varieties with low
carbohydrates, 22 % amino acids and amides, and 14 %
exudation rates was suggested (Wang and Adachi, 2000;
organic acids (without amino acids) were identified (Fig.
Aulakh et al., 2001a). As root exudates provide substrates for
5a). Particularly the carbohydrates are an easily available
methanogenesis in rice fields, this selection could offer an
carbon and energy source for the microorganisms in the
important option for mitigation of CH4 emission from rice
rhizosphere, and thus they are prone to fast turnover and
agriculture to the atmosphere as long as yields are not
probably incorporation into soil organic matter. Determi-
compromised (Aulakh et al., 2001b).
nation of the individual compounds showed, that the
carbohydrates consisted mainly of glucose, fructose, and
2.4 Rhizodeposition during ontogenesis
saccharose (Fig. 5b), citric and succinic acid made up 80 %
of the organic acids (Fig. 5c), and the amino acids/amides The amount and composition of water-soluble root
consisted mainly of glutamine, aspartate, and serine (Fig. exudates depended very much on the plant age. Inves-

Figure 5: Main fractions and relative composi-

tion of water-soluble, 14C-labeled maize root
exudates (a), detailed analysis of carbohydrates
(b), organic acids (c), and amino acids/amides
(d), values in [%], (n = 4); determination was
performed 15 days after sowing (Merbach et al.,
unpublished).
Abbildung 5: Hauptfraktionen und relative
Zusammensetzung der kaltwasserlöslichen,
14
C-markierten Maiswurzelabscheidungen (a)
sowie detaillierte Analyse der Kohlenhydrate
(b), Organischen Säuren (c) und Aminosäuren/
Amide (d); Angaben in [%], (n = 4); Bestim-
mung erfolgte 15 Tage nach Aussaat (Merbach
et al., unveröffentlicht).
402 Hütsch, Augustin, and Merbach

Table 2: Composition of root exudates from two maize (Zea mays L.)
cultivars, Mytos and Samantha (after Nardi et al., 2002).
Tabelle 2: Zusammensetzung der Wurzelexsudate von zwei Maissorten
(Zea mays L.), Mytos und Samantha (nach Nardi et al., 2002).

Organic acids [mM l±1] Maize cultivars

Mytos Samantha

Oxalic 12.69 5.98

Citric 11.73 10.32
Tartaric 93.90 11.98
L-Malic 5.15 62.07
Fumaric 3.98 0.77

Figure 6: Water-soluble root exudates of maize plants with different age;

4, 6, and 8 leaves refer to 20, 30, and 45 days after sowing, respectively (n
= 4); CH = Carbohydrates, AA = Amino acids, OA = Organic acids, Hws =
Hot water-soluble compounds, LSD = Least significant difference (partly
adopted from Gransee and Wittenmayer, 2000).
Abbildung 6: Wasserlösliche Wurzelabscheidungen bei Maispflanzen in
unterschiedlichen Entwicklungsstadien; 4, 6 bzw. 8 Blätter entsprechen 20,
30 bzw. 45 Tage nach Aussaat (n = 4); CH = Kohlenhydrate, AA =
Aminosäuren, OA = Organische Säuren, Hws = Warmwasserlösliche
Verbindungen, LSD = Grenzdifferenz (nach Gransee and Wittenmayer,
2000).

tigations of maize plants with 4, 6, and 8 leaves showed, that

the total release per g root dry matter decreased with
increasing plant age (Fig. 6; after Gransee and Wittenmayer,
2000). The decrease resulted from changes in carbohydrates
and amino acids/amides, the organic acids varied only
slightly. However, older plants released more hot-water-
soluble compounds than younger plants (Fig. 6).
These experiments and comparable studies, which traced
the incorporation of 14CO2 into plant matter and the release
of assimilates into soil, were frequently conducted with
young plants (Cheng et al., 1993; Shepherd and Davies,
1993; Hodge et al., 1996; Kuzyakov and Cheng, 2001).
However, depending on the plant age newly assimilated 14C
is preferably translocated into the shoot or root biomass
(Gregory and Atwell, 1991; Jensen, 1993, 1994). Young
plants show pronounced translocation into the roots, whereas
older plants preferably translocate into the shoot, which
could be demonstrated after pulse labeling of wheat plants
with 13CO2 (Palta and Gregory, 1997). In the shoots about
55 % of 13C recovered was maintained until stem elongation
(51 DAS = Days After Sowing) and then it increased to 67 %
at booting stage (64 DAS; Fig. 7). The percentage of the
excess 13C retained in the roots decreased from 36 % at the
Figure 7: Changes with time in the percentage of 13C recovered in (a)
shoots and roots, (b) respiration of roots and shoots, and (c) soil for wheat
plants. Bars indicate  SEM where these exceed the size of the symbols
(after Palta and Gregory, 1997).
Abbildung 7: Zeitliche Veränderung der 13C-Verteilung in (a) Spross und
Wurzeln, (b) Wurzel- und Sprossatmung und (c) im Boden bei
Weizenpflanzen. Mittelwerte  SEM sind angegeben; teilweise ist der
Fehler kleiner als das Symbol (nach Palta und Gregory, 1997).
two-leaf stage (28 DAS) to 25 % at tillering (36 DAS). This
value was maintained until stem elongation, and then it
decreased to 17 % at the booting stage. With time of
vegetation the excess 13C recovered as shoot respiration
increased continuously up to 6.9 % at booting stage. The 13C
recovered as root and microbial respiration increased rapidly
from 5.8 % to 13.7 % and then decreased to 7.7 %. Also the
Plant rhizodeposition as source for carbon turnover
percentage of 13C recovered in the soil (rhizodeposition)
increased first of all and decreased again later in the growing
period. Changes in C allocation between the different plant
organs were associated with changes in the activity of the
sinks. At least between stem elongation and booting stage
the decreased C translocation to the roots resulted in reduced
root and microbial respiration and less rhizodeposition. In
these experiments of Palta and Gregory (1997) the wheat
plants were investigated during the vegetative growth only.
Yet, Keith et al. (1986) and Swinnen et al. (1994a) could
demonstrate that particularly in the generative growth of
wheat ears are large assimilate sinks, and thus less C is
translocated belowground. This is also true for other plant
species, because the importance of reproductive plant organs
as large assimilate sinks has already been well-known for
many years (e.g. Römer, 1971; Merbach et al., 1994), and
could be confirmed recently (Warembourg and Estelrich,
2001). As these differences in distribution during onto-
genesis affect rhizodeposition, investigations during the
whole growing cycle are necessary in order to determine the
total plant-borne C input into the soil, thus achieving results
e.g. on a year basis.
3 Turnover of rhizodeposits (water-soluble exu-
dates and mucilage) in incubation studies
In order to determine the distribution and turnover of root-
borne compounds, small plexiglass containers (22 ´ 22.5 ´
12 mm3) were filled with soil (10 % clay, 70 % sand) and at
the open side water-soluble, 14C-labeled root exudates were
applied (Lezovic, 1999). D-glucose, L-aspartic acid, and
citric acid, the main components of the individual fractions
(see Fig. 5), were chosen. After a 3-days incubation at 20 oC
the soil blocks were deep frozen and afterwards cut into
slices. These soil slices were subsequently extracted with
distilled H2O, saturated CaSO4 solution, 4 % HCl and 14 %
HCl in the ratio 1:20 (soil : extraction solution); after
shaking for 1 h the extractable 14C amounts were deter-
mined. Part of the soil blocks were sterilized prior to the
experiment. More details can be obtained from Lezovic
(1999).
In Fig. 8a the recovered 14C amounts in relation to the
amount applied are given for the non-sterile experimental
conditions. The recovery rate was relatively small for all
three compounds tested and varied between 34 % and 64 %.
The microorganisms had obviously respired a considerable
part of the applied 14C, and they had also changed the
characteristics of the applied substances, as the solubility of
the originally water-soluble compounds was strongly
decreased. Only 7 to 25 % were water-extractable after 3
days. Between 10 and 25 % were fixed in the soil, either
bound to clay minerals or soil organic matter. With sterile
experimental conditions (Fig. 8b) the 14C recovery was
remarkable (87 to 96 %). The residual compounds in soil
were mainly water-soluble (61 to 80 %), and thus were still
in their originally applied form.
It can be assumed that the fixed 14C in soil was mainly
bound to clay minerals, as could be demonstrated in
investigations of different soil particle size fractions (1541
403
Figure 8: Recovery of 14C-labeled glucose, aspartic acid, and citric acid in
the soil block experiment; the relative contents in the individual extraction
solutions, the fixed and the totally recovered percentages are given,
determined under non-sterile (a) and sterile (b) conditions (after Lezovic,
1999).
Abbildung 8: Wiederfindung der als Glucose, Asparaginsäure oder
Citronensäure applizierten 14C-Menge im Bodenblockversuch, Angabe
der relativen Gehalte in den einzelnen Extraktionslösungen sowie der
festgelegten und insgesamt gefundenen Anteile [%], unsterile (a) bzw.
sterile (b) Bedingungen (nach Lezovic, 1999).
Bq (g clay)±1, 48 Bq (g silt)±1, 42 Bq (g sand)±1; Merbach et
al., 1993). The results of the incubation studies demonstrate,
that the water-soluble rhizodeposits are prone to fast
microbial turnover, which leads not only to 14CO2
respiration but also to fixation in more resistant microbial
metabolites. Eventually incorporation into less soluble soil
organic matter will occur as well as direct introduction into
the soil clay matrix, which tends to physically protect them
from microbial degradation. This is one important process,
which lowers the decay rate and increases the stabilization-
to-mineralization ratio of C in soils (Balesdent and
Balabane, 1996). In the experiments of Swinnen (1994)
the soil type had a significant effect on the proportion of 14C
respired from glucose model rhizodeposits, being 36.0 % on
a silt loam and 39.9 % on a loamy sand. Soils with finer
texture tend to be more ªpreservativeº than soils with
coarser texture (Swinnen, 1994). Investigations of Kaiser
and Zech (2000) indicated, that Al and Fe oxides/hydroxides
in the clay fraction are the main sorbents of dissolved
organic matter in soils.
The binding of root exudates to soil particles does not only
contribute to stabilization of soil organic matter, it also
improves soil structure by increasing aggregate stability.
Soil structure is either directly influenced by plant exudation
e.g. of sugars and mucilage, or indirectly by activity of
microorganisms, which produce polysaccharides as agents
for soil aggregation. In investigations of Traore et al. (2000)
the effect of a mixture of soluble exudates (MSE), glucose,
intact root mucilage (RM), and polygalacturonic acid (PGA)
on aggregate stability of a silty loam soil (25 % clay, 59 %
silt) was tested. During incubation at 25 oC for 30 days the
percentage of water-soluble aggregates decreased in the
control treatment (water application only), but increased
significantly in the MSE and the mucilage treatment (Fig. 9).
The soil aggregate stability decreased in the following order:
MSE=mucilage>PGA>glucose>control. Traore et al. (2000)
404
Figure 9: Percentage of water-stable aggregates during incubation of an
arable soil (25 % clay, 16 % sand). Letters indicate significant difference
between treatments at P < 0.05 (after Traore et al., 2000).
Abbildung 9: Anteile H2O-stabiler Aggregate während der Inkubation
eines Ackerbodens (25 % Ton, 16 % Sand). Die Buchstaben zeigen
signifikante Differenzen zwischen den Varianten an, P < 0.05 (nach Traore
et al., 2000).
suggested that various organic materials induced various
responses to rhizosphere microflora, and that those derived
from the root mucilage and MSE were the most effective.
These experiments, however, were done without the
presence of a plant. Nevertheless the authors concluded,
that plants have an adaptive mechanism to adverse soil
physical conditions. Certainly this has to be tested in further,
detailed studies including growing plants.
4 Distribution of rhizodeposits in experiments with
growing plants
The spatial distribution of root-borne 14C compounds in
soil was determined in experiments with growing spring
wheat plants (Merbach et al., 1999). For this purpose
rectangle cultivation pots were used. They consisted of a
central zone (1 cm), in which plants could grow, whereas
root growth into the neighboring zones was inhibited with a
nylon net (middle zone 1±1.5 cm, outer zone 1.5±2 cm, at
each side of the central zone). Root hairs could penetrate the
net. Wheat plants with 4 leaves were pulse-labeled with
14
CO2 (Merbach et al., 1999), and 14 days later the plants
were harvested and the relative distribution of 14C
compounds in the different zones was determined. The
largest percentage was found next to the root surface, the
compounds in this central zone being mostly water-soluble
(Tab. 3). However, with increasing distance from the roots
the water-soluble fraction decreased strongly, and the water-
insoluble fraction increased at the same time. This result is
attributable to microbial or chemical transformation proc-
esses, causing incorporation of rhizodeposits into soil
organic matter. Until now this is only a hypothesis, which
has to be tested in appropriate investigations.
Comparable results were obtained in experiments of Cheng
et al. (1996), who determined the water-soluble carbon in the
rhizosphere continuum of winter wheat plants without 14CO2
labeling of photoassimilates. Water-soluble C concentra-
tions radically declined from rhizoplane to rhizosphere soil
with a further reduction to bulk and root-free soil. Thus,
water-soluble C was inversely related to the relative distance
Hütsch, Augustin, and Merbach
Table 3: Relative distribution of 14C compounds in the root zone of wheat;
total 14C amount: 664 kBq (g DM)±1; ´ = significantly different from the
inner compartment with P = 0.05 (after Merbach et al., 1999).
Tabelle 3: Relative Verteilung von 14C-Verbindungen im Wurzelraum
von Weizen, absolute 14C-Menge: 664 kBq (g TS)±1; ´ = gegen inneres
Kompartiment mit P = 0.05 signifikant verschieden (nach Merbach et al.,
1999).
Parameter Inner Middle Outer
compartment compartment compartment
(é = 10 mm) (é = 5 mm) (é = 5 mm)
% of 14C 54.6 30.6x 14.8x
% H2O-soluble 74.6 5x 3x
% H2O-insoluble 25.4 95x 97x
from the root surface with several times higher concen-
trations in the rhizosphere soil.
5 Approaches to estimate rhizodeposition storage
potential of soils
For practical reasons most of the determinations of the
amount and composition of root-released C compounds were
conducted in pot experiments under controlled conditions,
which is certainly a suitable approach, as this kind of
investigation is very sophisticated and laborious. However,
for quantifications based on an area of land or even larger
scales, data have to be transferred to field conditions
somehow. Flessa et al. (2000) pronounced in their study,
that the lack of data on root production and the release of
root exudates is a large deficit in estimations of the
stabilization rate of plant-derived C into soil organic matter.
One possibility to fill this gap is to determine the root density
in the field, and to relate these results to the amount of
exudates per unit root biomass or root-C, found in the pot
experiments. Yet this can only be a rough approximation to
the actual release of C compounds under field conditions, as
the distribution of assimilates depends on many different
factors: climatic conditions like temperature (e.g. Meharg
and Killham, 1989), photo period (Whipps, 1984), light
intensity (Ryle and Powell, 1976; Kuzyakov and Cheng,
2001), as well as soil characteristics like moisture content
(e.g. Palta and Gregory, 1997), texture (Merckx et al., 1985),
nutritional status (Merckx et al., 1987; Gransee, 1993;
Hodge et al., 1996), pH and O2 partial pressure (Meharg and
Killham, 1990a, b). These influences were reviewed in more
detail by Kuzyakov (2002). The adjustment of soil character-
istics between pot and field experiments should be possible,
whereas the possibilities of adjusting the climatic conditions
are very restricted.
Field experiments with 14CO2 labeling of plant shoots are
rare (Swinnen et al., 1994a, b), because for safety reasons
they are frequently avoided. As an alternative labeling with
the stable 13C isotope can be used, which is not detrimental
to health and environment. Pulse-labeling with 13CO2, as
used by Palta and Gregory (1997) in pot experiments, can
also be employed under field conditions with acceptable
expenditures (Ostle et al., 2000). A disadvantage is the about
1000 times less detection sensitivity of 13C in soil in
comparison with 14C. Therefore the separate determination
Plant rhizodeposition as source for carbon turnover
of exudation and root residues is not possible, instead
rhizodeposition has to be considered as a whole. The
contribution of rhizomicrobial respiration to total soil
respiration could also be quantified under field conditions,
adding 13C-labeled compounds to the soil and compare the
13
CO2 emission with the treatment of 13CO2 plant shoot
labeling, a variation of the method of Swinnen (1994).
According to the strong dependence of microbial activity on
temperature, moisture, and redox conditions this approach is
of particular interest under field conditions. Additionally,
with the described field experiments it is possible to
distinguish between CO2 emission from the soil carbon
pool and the plant-borne CO2 release (rhizosphere respira-
tion). Root-derived CO2 is not part of soil C loss, and must
be separated from the total CO2 efflux in studies of soil C
sequestration. Other, more modern approaches to achieve
this separation are based on analyses of the natural
abundance of carbon-13 (Cheng, 1996; Rochette and
Flanagan, 1997; Rochette et al., 1999), or on the use of
CO2, strongly depleted in 13C, in Free Air Carbon dioxide
Enrichment (FACE) studies (Andrews et al., 1999). The
separation is necessary in order to estimate if soils are
sources or sinks of CO2 (Hanson et al., 2000; Kuzyakov and
Cheng, 2001).
Measurements of CO2 fluxes at the soil surface without
isotopic labeling give no information about C storage in soil,
as the rhizosphere respiration with its strong seasonal
variations is always included in the measurements. Using
different C tracer techniques, it has been shown that
rhizosphere respiration can contribute from 19 % (Ware-
mbourg and Paul, 1977) to 80 % (Martin and Merckx, 1992)
of the total CO2 efflux from planted soil. In a review by
Hanson et al. (2000) published estimates of the percent root/
rhizosphere contributions to total soil respiration varied
between 10 % and over 90 %, depending on vegetation and
season. The values for non-forest observations (e.g. arable,
pasture, tundra) lay mainly below 20 %. Of course, the
contribution of rhizosphere respiration is commonly much
higher during the growing season than during the dormant
periods of the year. However, for answering the question if
soils release or absorb CO2, exclusion of rhizosphere
respiration is essential, and predictions are necessary for
time spans of years or even longer (Hanson et al., 2000).
Future studies must involve repeated measurements
throughout an annual cycle to adequately characterize
seasonal variation driven by changing patterns of below-
ground root activity (Hanson et al, 2000). This will provide
valuable input to the discussions of soils as potential sinks or
sources for atmospheric CO2.
6 Conclusions and outlook
Plant rhizodeposition can reach remarkable values and its
importance for carbon turnover in soils has to be
enlightened. As differences in assimilate distribution during
ontogenesis strongly affect rhizodeposition, future research
should focus on the quantification and characterization of
root-borne C compounds during the whole growing cycle to
achieve more reliable estimates e.g. on a year basis. Until
now the role of the microbial biomass for turnover of plant-
405
borne C is still unclear. In order to put more light on that
issue, the combination of isotopic labeling with molecular-
biological methods could be advantageous (Boschker et al.,
1998; Killham and Yeomans, 2001), although they are very
laborious. According to Killham and Yeomans (2001) the
labeling of rhizobacteria with reporter genes enables to
distinguish between root and microbial C fluxes, and it is a
good completion of experiments using isotopes and other,
more traditional experimental setups, like e.g. comparison of
sterile and non-sterile conditions.
Of particular interest are investigations on the incorpo-
ration of rhizodeposits into soil organic matter fractions of
different stability, as well as their introduction into the
mineral soil matrix, which causes physical protection from
further degradation. The assumption, that plants can adapt to
adverse soil physical conditions by root exudation, has to be
tested in detailed studies including growing plants. Apart
from pot experiments with 14CO2 labeling it is necessary to
conduct model field experiments with 13CO2 labeling in
order to be able to distinguish between CO2 originating from
the soil C pool and rhizosphere respiration, originating
exclusively from plant assimilates. This will provide
valuable input to the discussions of soils as potential sink
or source for atmospheric CO2.
Acknowledgments
This work was financially supported by the German Research Foundation
(DFG) in frame of the priority program ªSoils as source and sink of CO2º
(SPP 1090). Thanks are due to Dr. J. Plugge and R. Remus, Center for
Agricultural Landscape and Land Use Research (ZALF), Müncheberg, for
helpful discussions and technical support.
References
Andrews, J. A., K. G. Harrison, R. Matamala, and W. H. Schlesinger
(1999): Separation of root respiration from total soil respiration using
carbon-13 labeling during Free-Air Carbon dioxide Enrichment (FACE).
Soil Sci. Soc. Am. J. 63, 1429±1435.
Aulakh, M. S., R. Wassmann, C. Bueno, J. Kreuzweiser, and H. Rennenberg
(2001a): Characterization of root exudates at different growth stages of
ten rice (Oryza sativa L.) cultivars. Plant Biol. 3, 139±148.
Aulakh, M. S., R. Wassmann, C. Bueno, and H. Rennenberg (2001b):
Impact of root exudates of different cultivars and plant development
stages of rice (Oryza sativa L.) on methane production in a paddy soil.
Plant Soil 230, 77±86.
Balesden, J., and M. Balabane (1996): Major contribution of roots to soil
carbon storage inferred from maize cultivated soils. Soil Biol. Biochem.
28, 1261±1263.
Barber, D. A., and J. K. Martin (1976): The release of organic substances
by cereal roots into soil. New Phytol. 76, 69±80.
Birkett, M. A., K. Chamberlain, A. M. Hooper, and J. A. Pickett (2001):
Does allelopathy offer real promise for practical weed management and
for explaining rhizosphere interactions involving higher plants? Plant
Soil 232, 31±39.
Boschker, H. T. S., S. C. Nold, P. Wellsbury, D. Bos, W. de Graaf, R. Pel, R.
J. Parkes, and T. E. Cappenberg (1998): Direct linking of microbial
populations to specific biogeochemical processes by C-13-labelling of
biomarkers. Nature 392, 801±805.
Cheng, W. (1996): Measurement of rhizosphere respiration and organic
matter decomposition using natural 13C. Plant Soil 183, 263±268.
406
Cheng, W., D. C. Coleman, C. R. Carroll, and C. A. Hoffman (1993): In situ
measurement of root respiration and soluble C concentrations in the
rhizosphere. Soil Biol. Biochem. 25, 1189±1196.
Cheng, W., Q. Zhang, D. C. Coleman, C. R. Carroll, and C. A. Hoffman
(1996): Is available carbon limiting microbial respiration in the
rhizosphere? Soil Biol. Biochem. 2, 1283±1288.
Domanski, G., Y. Kuzyakov, S. V. Siniakina, and K. Stahr (2001): Carbon
flows in the rhizosphere of ryegrass (Lolium perenne L.). J. Plant Nutr.
Soil Sci. 164, 381±387.
Domanski, G., Y. Kuzyakov, and K. Stahr (2002): Total and labelled CO2
emission and 14C partitioning as affected by streptomycin and benomyl.
In W. Merbach, B. W. Hütsch, and J. Augustin (eds.): Durchwurzelung,
Rhizodeposition und Pflanzenverfügbarkeit von Nährstoffen und Schwer-
metallen. 12. Borkheider Seminar zur Ökophysiologie des Wurzelraumes,
Vol. 12, B.G. Teubner, Stuttgart, Leipzig, Wiesbaden (im Druck).
Dousset, S., J. L. Morel, A. Jacobson, and B. Bitton (2001): Copper binding
capacity of root exudates of cultivated plants and associated weeds. Biol.
Fertil. Soils 34, 230±234.
Fan, T. W.-M., A. N. Lane, M. Shenker, J. P. Bartley, D. Crowley, and R. M.
Higashi (2001): Comprehensive chemical profiling of gramineous plant root
exudates using high-resolution NMR and MS. Phytochem. 57, 209±221.
Flessa, H., B. Ludwig, B. Heil, and W. Merbach (2000): The origin of soil
organic C, dissolved organic C and respiration in a long-term maize
experiment in Halle, Germany, determined by 13C natural abundance. J.
Plant Nutr. Soil Sci. 163, 157±163.
Gerke, J., L. Beissner, and W. Römer (2000a): The quantitative effect of
chemical phosphate mobilization by carboxylate anions on P uptake by
an single root. I. The basic concept and determination of soil parameters.
J. Plant Nutr. Soil Sci. 163, 207±212.
Gerke, J., W. Römer, and L. Beissner (2000b): The quantitative effect of
chemical phosphate mobilization by carboxylate anions on P uptake by
an single root. II. The importance of soil and plant parameters for uptake
of mobilized P. J. Plant Nutr. Soil Sci. 163, 213±219.
Gransee, A. (1993): Qualitative und quantitative Analyse von Wurzelab-
scheidungen bei Erbsen in Abhängigkeit vom Phosphaternährungszu-
stand. Ökophysiologie des Wurzelraumes, 4. wissenschaftliche
Arbeitstagung in Borkheide, ISSN 0945-2494, p. 56±59.
Gransee, A., and L. Wittenmayer (2000): Qualitative and quantitative
analysis of water-soluble root exudates in relation to plant species and
development. J. Plant Nutr. Soil Sci. 163, 381±385.
Gregory, P. J., and B. J. Atwell (1991): The fate of carbon in pulse-labelled
crops of barley and wheat. Plant Soil 136, 205±213.
Groleau-Renaud, V., S. Plantureux, A. Tebeileh, and A. Guckert (2000):
Influence of microflora and composition of root bathing solution on root
exudation of maize plants. J. Plant Nutr. 23, 1283±1301.
Hanson, P. J., N. T. Edwards, C. T. Garten, and J. A. Andrews (2000):
Separating root and soil microbial contributions to soil respiration: A
review of methods and observations. Biogeochemistry 48, 115±146.
Heim, A., I. Brunner, B. Frey, E. Frossard, and J. Luster (2001): Root
exudation, organic acids, and element distribution in roots of Norway
spruce seedlings treated with aluminum in hydroponics. J. Plant Nutri.
Soil Sci. 164, 519±526.
Helal, H. M., and D. Sauerbeck (1989): Carbon turnover in the rhizosphere.
Z. Pflanzenernähr. Bodenkd. 152, 211±216.
Helal, H. M., and D. Sauerbeck (1991): Short-term determination of the
actual respiration rate of intact plant roots. In B. L. McMichael and H.
Persson (eds.): Plant Roots and Their Environment, Elsevier, Amster-
dam, The Netherlands, pp. 88±92.
Hinsinger, P. (2001): Bioavailability of soil inorganic P in the rhizosphere as af-
fected by root-induced chemical changes: a review. Plant Soil 237, 173±195.
Hodge, A., S. J. Grayston, and B. G. Ord (1996): A novel method for
characterisation and quantification of plant root exudates. Plant Soil 184,
97±104.
Hütsch, Augustin, and Merbach
Jensen, B. (1993): Rhizodeposition by 14CO2-pulse-labelled spring barley
grown in small field plots on sandy loam. Soil Biol. Biochem. 25, 1553±
1559.
Jensen, B. (1994): Rhizodeposition by field-grown winter barley exposed
to 14CO2 pulse-labelling. Appl. Soil Ecol. 1, 65±74.
Kaiser, K., and W. Zech (2000): Dissolved organic matter sorption by
mineral constituents of subsoil clay fractions. J. Plant Nutr. Soil Sci. 163,
531±535.
Keith, H., J. M. Oades, and J. K. Martin (1986): Input of carbon to soil
from wheat plants. Soil Biol. Biochem. 18, 445±449.
Keller, H., and W. Römer (2001): Cu, Zn, and Cd acquisition by two
spinach cultivars depending on P nutrition and root exudation. J. Plant
Nutr. Soil Sci. 164, 335±342.
Killham, K., and C. Yeomans (2001): Rhizosphere carbon flow measure-
ment and implications: from isotopes to reporter genes. Plant Soil 232,
91±96.
Kuzyakov, Y. (2002): Factors affecting rhizosphere priming effects. J. Plant
Nutr. Soil Sci. 165, 382±396.
Kuzyakov, Y., and W. Cheng (2001): Photosynthesis controls of rhizosphere
respiration and organic matter decomposition. Soil Biol. Biochem. 33,
1915±1925.
Kuzyakov, Y., A. Kretzschmar, and K. Stahr (1999): Contribution of Lolium
perenne rhizodeposition to carbon turnover of pasture soil. Plant Soil
213, 127±136.
Lerouge, P. (1994): Symbiotic host-specificity between leguminous plants
and rhizobia is determined by substituted and acylated glucosamine
oligosaccharide signals. Glycobiol. 4, 127±134.
Lezovic, G. (1999): Wirkungen von Maiswurzelabscheidungen auf die
Phosphatmobilisierung im Boden. Ph D. thesis. Landw. Fakultät Univ.
Halle-Wittenberg, Germany.
Mahall, B. E., and R. M. Callaway (1992): Root communication
mechanisms and intracommunity distributions of 2 Mojave desert
shrubs. Ecology 73, 2145±2151.
Martin, J. K., and R. Merckx (1992): The partioning of photosynthetically
fixed carbon within the rhizosphere of mature wheat. Soil Biol.
Biochem. 24, 1147±1156.
Meharg, A. A., and K. Killham (1989): Distribution of assimilated carbon
within the plant and rhizosphere of Lolium perenne: influence of
temperature. Soil Biol. Biochem. 21, 487±489.
Meharg, A. A., and K. Killham (1990a): The effect of soil pH on
rhizosphere carbon flow of Lolium perenne. Plant Soil 123, 1±7.
Meharg, A. A., and K. Killham (1990b): Carbon distribution within the
plant and rhizosphere for Lolium perenne subjected to anaerobic soil
conditions. Soil Biol. Biochem. 22, 643±647.
Meharg, A. A., and K. Killham (1995): Loss of exudates from the roots of
perennial ryegrass inoculated with a range of micro-organisms. Plant
Soil 170, 345±349.
Merbach, W., and S. Ruppel (1992): Influence of microbial colonization on
14
CO2 assimilation and amounts of root-borne 14C compounds in soil.
Photosynthetica 27, 551±554.
Merbach, W., J. Augustin, and H. J. Jacob (1993): 14C-Verwertung von
Sommerweizen im Verlauf der Ontogenese. Ökophysiologie des
Wurzelraumes, 4. wissenschaftliche Arbeitstagung in Borkheide, ISSN
0945-2494, p. 64±67.
Merbach, W., F. Schumann, W. Römer, and E. Reining (1994): Appa-
rent CO2 assimilation, 14C incorporation, and 14C translocation in
spring barley influenced by sink manipulation. Photosynthetica 30, 593±
601.
Merbach, W., G. Knof, J. Augustin, H. J. Jacob, R. Jäger, and V. Toussaint
(1996): Ökophysiologische Wechselbeziehungen zwischen Pflanze und
Boden. In H. Mühle and S. Claus (eds.): Reaktionsverhalten von
agrarischen Ökosystemen homogener Areale. Teubner Verlag Stuttgart,
Leipzig, 195±207.
Plant rhizodeposition as source for carbon turnover
Merbach, W., E. Mirus, G. Knof, R. Remus, S. Ruppel, R. Russow, A.
Gransee, and J. Schulze (1999): Release of carbon and nitrogen
compounds by plant roots and their possible ecological importance. J.
Plant Nutr. Soil Sci. 162, 373±383.
Merckx, R., A. Den Hartog, and J. A. Van Veen (1985): Turnover of root-
derived material and related microbial biomass formation in soils of
different texture. Soil Biol. Biochem. 17, 565±569.
Merckx, R., A. Dijkstra, A. Den Hartog, and J. A. Van Veen (1987):
Production of root-derived material and associated microbial growth in
soil at different nutrient levels. Biol. Fertil. Soils 5, 126±132.
Minchin, P. E. H., and G. S. McNaughton (1984): Exudation of recently
fixed carbon by non-sterile roots. J. Exp. Bot. 35, 74±82.
Nardi, S., G. Concheri, D. Pizzeghello, A. Sturaro, R. Rella, and G. Parvoli
(2000): Soil organic matter mobilization by root exudates. Chemosphere
41, 653±658.
Nardi, S., E. Sessi, D. Pizzeghello, A. Sturaro, R. Rella, and G. Parvoli
(2002): Biological activity of soil organic matter mobilized by root
exudates. Chemosphere 46, 1075±1081.
Nguyen, C., C. Todorovic, C. Robin, A. Christophe, and A. Guckert (1999):
Continuous monitoring of rhizosphere respiration after labelling of plant
shoots with 14CO2. Plant Soil 212, 191±201.
Ostle, N., P. Ineson, D. Benham, and D. Sleep (2000): Carbon assimilation
and turnover in grassland vegetation using an in situ (CO2)-C-13 pulse
labelling system. Rapid Communications in Mass Spectrometry 14,
1345±1350.
Palta, J. A., and P. J. Gregory (1997): Drought affects the fluxes of carbon
to roots and soil in 13C pulse-labelled plants of wheat. Soil Biol.
Biochem. 9/10, 1395±1403.
Paynel, F., P. J. Murray, and J. B. Cliquet (2001): Root exudates: a path-
way for short-term N transfer from clover and ryegrass. Plant Soil 229,
235±243.
Pellet, D. M., D. L. Grunes, and L. V. Kochian (1995): Organic acid
exudation as an aluminium tolerance mechanism in maize Zea mays L.
Planta 196, 788±795.
Quian, J. H., J. W. Doran, and D. T. Walters (1997): Maize plant
contributions to root zone available carbon and microbial trans-
formations of nitrogen. Soil Biol. Biochem. 29, 1451±1462.
Rattray, E. A. S., E. Paterson, and K. Killham (1995): Characterization of
the dynamics of C-partitioning within Lolium-perenne and to the
rhizosphere microbial biomass using C-14 pulse-chase. Biol. Fertil. Soils
19, 280±286.
Rochette, P., and L. B. Flanagan (1997): Quantifying rhizosphere
respiration in a corn crop under field conditions. Soil Sci. Soc. Am. J.
61, 466±474.
Rochette, P., L. B. Flanagan, and E. G. Gregorich (1999): Separating soil
respiration into plant and soil components using analyses of the natural
abundance of carbon-13. Soil Sci. Soc. Am. J. 63, 1207±1213.
Römer, W. (1971): Untersuchungen über die Auslastung des Photo-
syntheseapparates bei Gerste (Hordeum distichon L.) und Weiûem Senf
(Sinapis alba L.) in Abhängigkeit von den Umweltbedingungen. Arch.
Bodenfruchtbark. Pflanzenprodukt. 15, 415±423.
Ryle, G. J. A., and C. E. Powell (1976): Effect of rate of photosynthesis on
the pattern of assimilate distribution in the graminaceous plant. J. Exp.
Bot. 27, 189±199.
Schilling, G., A. Gransee, A. Deubel, G. Lezovic, and S. Ruppel (1998):
Phosphorus availability, root exudates, and microbial activity in the
rhizosphere. J. Plant Nutr. Soil Sci. 161, 465±478.
Shepherd, T., and H. V. Davies (1993): Carbon loss from the roots of forage
rape (Brassica napus L.) seedlings following pulse-labelling with 14CO2.
Ann. Bot. 72, 155±163.
Smart, D. R., A. Ferro, K. Ritchie, and B. G. Bugbee (1995): On the use of
antibiotics to reduce rhizoplane microbial populations in root physiology
and ecology investigations. Physiol. Plant. 95, 533±540.
407
Stacey, G., J. Sanjuan, S. Luka, T. Dockendorff, and R. W. Carlson (1995):
Signal exchange in the Bradyrhizobium-soybean symbiosis. Soil Biol.
Biochem. 27, 473±483.
Swinnen, J. (1994): Evaluation of the use of a model rhizodeposition
technique to separate root and microbial respiration in soil. Plant Soil
165, 89±101.
Swinnen, J., and J. A. Van Veen (1992): Unterscheidung von Wurzel- und
mikrobieller Atmung im Boden durch Exsudatmarkierung. Berichte über
Landwirtschaft: Bodennutzung und Bodenfruchtbarkeit, Band 4:
Humushaushalt, Sonderheft 206, 114±116.
Swinnen, J., J. A. Van Veen, and R. Merckx (1994a): 14C pulse-labelling of
field-grown spring wheat: an evaluation of its use in rhizosphere carbon
budget estimations. Soil Biol. Biochem. 26, 161±170.
Swinnen, J., J. A. Van Veen, and R. Merckx (1994b): Rhizosphere carbon
fluxes in field-grown spring wheat: model calculations based on 14C
partitioning after pulse-labelling. Soil Biol. Biochem. 26, 171±182.
Swinnen, J., J. A. Van Veen, and R. Merckx (1995): Root decay and
turnover of rhizodeposits in field-grown winter wheat and spring barley
estimated by 14C pulse-labelling. Soil Biol. Biochem. 27, 211±217.
Todorovic, C., C. Nguyen, C. Robin, and A. Guckert (2001): Root and
microbial involvement in the kinetics of 14C-partitioning to rhizosphere
respiration after a pulse labelling of maize assimilates. Plant Soil 228,
179±189.
Traore, O., V. Groleau-Renaud, S. Plantureux, A. Tubeileh, and V. Búuf-
Tremblay (2000): Effect of root mucilage and modelled root exudates on
soil structure. Eur. J. Soil Sci. 51, 575±581.
Treeby, M., H. Marschner, and V. Römheld (1989): Mobilization of iron
and other micronutrients from a calcareous soil by plant-borne,
microbial, and synthetic metal chelators. Plant Soil 114, 217±226.
Van der Krift, T. A. J., P. J. Kuikman, F. Müller, and F. Berendse (2001):
Plant species and nutritional-mediated control over rhizodeposition and
root decomposition. Plant Soil 228, 191±200.
Wang, B., and K. Adachi (2000): Differences among rice cultivars in root
exudation, methane oxidation, and populations of methanogenic and
methanotrophic bacteria in relation to methane emission. Nutr. Cycl.
Agroecosyst. 58, 349±356.
Warembourg, F. R., and E. A. Paul (1977): Seasonal transfers of
assimilated 14C in grassland: plant production and turnover, soil and
plant respiration. Soil Biol. Biochem. 9, 295±301.
Warembourg, F. R., and G. Billes (1979): Estimating carbon transfers in the
plant rhizosphere. In J. L. Harley and R. S. Russel (eds.): The Soil-Root
Interface. Academic Press, London, pp. 183±196.
Warembourg, F. R., and H. D. Estelrich (2000): Towards a better
understanding of carbon flow in the rhizosphere: a time-dependent
approach using carbon-14. Biol. Fertil. Soils 30, 528±534.
Warembourg, F. R., and H. D. Estelrich (2001): Plant phenology and soil
fertility effects on below-ground carbon allocation for an annual
(Bromus madritensis) and a perennial (Bromus erectus) grass species.
Soil Biol. Biochem. 33, 1291±1303.
Whipps, J. M. (1984): Environmental factors affecting the loss of carbon
from the roots of wheat and barley seedlings. J. Exp. Bot. 35, 767±773.
Xu, J. G., and N. G. Juma (1994): Relations of shoot-C, root-C and root
length with root-released-C of 2 barley cultivars and the decomposition
of root-released-C in soil. Can. J. Soil Sci. 74, 17±22.
Yoshitomi, K. J., and J. R. Shann (2001): Corn (Zea mays L.) root exudates
and their impact on 14C-pyrene mineralization. Soil Biol. Biochem. 33,
1769±1776.
Yu, J. Q., and Y. Matsui (1994): Phytotoxic substances in root exudates of
cucumber Cucumis sativus L. J. Chem. Ecol. 20, 21±31.
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