Plant Soil (2013) 362:389–417

DOI 10.1007/s11104-012-1429-7

REVIEW ARTICLE

Redox potential (Eh) and pH as drivers

of soil/plant/microorganism systems: a transdisciplinary
overview pointing to integrative opportunities for agronomy
Olivier Husson

Received: 25 May 2012 / Accepted: 16 August 2012 / Published online: 8 September 2012
# The Author(s) 2012. This article is published with open access at Springerlink.com

Abstract homeostasis at the cell level. This new perspective

Background Oxidation-reduction and acid–base reac- could help in bridging several disciplines related to
tions are essential for the maintenance of all living agronomy, and across micro and macro-scales. It
organisms. However, redox potential (Eh) has received should help to improve cropping systems design and
little attention in agronomy, unlike pH, which is management, in conventional, organic, and conserva-
regarded as a master variable. Agronomists are probably tion agriculture.
depriving themselves of a key factor in crop and soil
science which could be a useful integrative tool. Keywords Cell homeostasis . ‘ideal’ soil . Nutrients .
Scope This paper reviews the existing literature on Eh Rhizosphere . Soil resistivity
in various disciplines connected to agronomy, whether
associated or not with pH, and then integrates this
knowledge within a composite framework. Introduction
Conclusions This transdisciplinary review offers evi-
dence that Eh and pH are respectively and jointly “What drives life is a little electric current, kept up by
major drivers of soil/plant/microorganism systems. In- the sunshine” was the elegant summary of Albert
formation on the roles of Eh and pH in plant and Szent-Gyorgyi (1960), a Nobel prize laureate in phys-
microorganism physiology and in soil genesis con- iology. Indeed, electrons are the essential reactants in
verges to form an operational framework for further inorganic, organic, and biochemical reactions (Bohn
studies of soil/plant/microorganism functioning. This 1971). The chemistry of living organisms relies even
framework is based on the hypothesis that plants more on oxidation-reduction reactions, i.e., transfer of
physiologically function within a specific internal electrons, than it does on acid–base reactions, which
Eh-pH range and that, along with microorganisms, are more focused on proton transfers (Clark 1960;
they alter Eh and pH in the rhizosphere to ensure Dietz 2003; Falkowski et al. 2008; Greenberg 1998).
It is worth reviewing that the main constituents of
living organisms, especially proteins, are just six ele-
Responsible Editor: Hans Lambers.
ments: (i) oxygen; the strongest oxidizing agent; (ii)
O. Husson (*) hydrogen; the strongest reducing agent; and (iii) the
CIRAD, UPR SIA, four elements that have the largest amplitude in redox
TA B01/07, Avenue Agropolis,
numbers: carbon (−IV in CH4 to+IV in CO2), nitrogen
34398 Montpellier Cedex 5, France
e-mail: olivier.husson@cirad.fr (−III in NH4+ to+V in NO3-), phosphorus (−III in PH3
URL: http://www.cirad.fr/ur/couverts_permanents to+V in PO43-), and sulfur (−II in H2S to+VI in SO42-).
390 Plant Soil (2013) 362:389–417

Oxidation-reduction conditions are classically for an a priori underestimation of the impact that high
assessed by measuring the redox potential (Eh), levels of Eh can have on soil//plant/microorganism
expressed in volts. The zero point for the Eh scale is functioning and on plant health and production.
set by the standard hydrogen electrode (SHE), involv- Agronomists are quite possibly missing a key factor
ing the redox couple H+/H2. Eh is commonly used in a in plant and soil science which, when associated sys-
large panel of disciplines dealing with living organ- tematically with pH, could help advance agronomic
isms, such as microbial ecology (Alexander 1964), knowledge for sustainable agriculture.
geochemistry, biogeochemistry, limnology (Bohn This paper undertakes: (i) to review the existing
1971; Falkowski et al. 2008; Reddy and DeLaune literature on redox potential (Eh) in various disciplines
2008), bioenergetics (Guérin 2004; Mathis 1995; connected to agronomy, associated or not with pH; and
Szent-Gyorgyi 1957), hydrobiology and the study of (ii) to integrate this knowledge to construct an opera-
marine ecosystems (Meadows et al. 1994), soil science tional perspective for bridging disciplines related to
(Chadwick and Chorover 2001), and physiology and agronomy and for linking micro and macro-scales, from
ecophysiology (De Gara et al. 2010; Dessaux et al. plant cells to plants, roots and soil on a field scale.
2009; Dietz 2003; Foyer and Noctor 2005; Lambers et The paper proceeds through five sections. First, I
al. 2008). According to the discipline, Eh and pH get review and underscore the importance of Eh at cell
measured on different scales and for various substrata: and plant levels in physiology. In the second section,
organelles, cells, plants, rhizosphere, bulk soil, sedi- the respective and combined influence of Eh and pH
ments, soil solution, or water. on microorganisms are explored. In the third section, I
However, in many disciplines, oxidation-reduction successively explore at field scale: (i) Eh and pH
conditions and electron fluxes have not received the ranges and variability; (ii) the influence of Eh and
same attention as have pH and proton fluxes. In soil pH on plant growth; (iii) the relationship between soil
science, for instance, despite the recognition of the Eh-pH and nutrient availability for plants; (iv) the
importance of Eh, pH is often regarded as the master impact of plants on soil Eh and pH; (v) the interactions
variable (Brady and Weil 2010; Simek and Cooper between Eh-pH and soil organic matter; (vi) the rela-
2002). This is also the case in plant physiology (Rengel tionship between Eh-pH and soil genesis; and (vii) the
2002). Surprisingly, and in contrast to pH, Eh is much influence of Eh and pH on greenhouse gas emissions,
less central in agronomy. Most studies on soil Eh have soil pollution, and bioremediation. The fourth section
remained limited to extreme situations leading to anaero- shows the impact of agricultural practices on soil Eh
biosis, as in paddy fields and submerged soils (Bartlett and pH. The fifth section synthesizes this knowledge,
and James 1993; De Mars and Wassen 1999; Gotoh and raising the hypothesis that plants, along with micro-
Yamashita 1966; Kludze and DeLaune 1999; Kogel- organisms, modify the Eh and pH in the rhizosphere to
Knabner et al. 2010; Ponnamperuma 1965; 1972; adjust for an optimum physiological level at which
Stepniewski and Stepniewska 2009; Yoshida 1981). they can function well. The questions this composite
The Eh of aerobic soils, which are the majority of perspective raises for agronomy are then discussed. I
cultivated soils, has received little attention in agrono- suggest that this perspective could help in assessing
my. Three methodological reasons might explain this agricultural practices, providing a conceptual frame-
lack of references in the literature: (i) the high variability work for developing tools for cropping systems design
of Eh in space and time, especially when compared to and management, in conventional, organic and con-
pH variability; (ii) the difficulties in measuring Eh in servation agriculture.
aerobic soils; and (iii) the dependence of Eh and pH.
Consequently, Eh measurements are difficult to repro-
duce and interpret, and results from various authors are Oxidation and reduction in cell and plant
difficult to compare (Snakin et al. 2001). physiology
Despite the paucity of redox potential (Eh) studies
in agronomy, especially for aerobic soils, this essential Oxidation-reduction reactions and energy
parameter should not be overlooked because it is dif-
ficult to measure or interpret. It is quite possible that In the plant kingdom, photosynthesis uses the light
the lack of studies of Eh on aerobic soils may account energy of photons to combine (reduce) carbon dioxide
Plant Soil (2013) 362:389–417 391

from the air with hydrogen taken from water (Govindjee redox states as mitochondria redox state, the tissue
and Krogmann 2004; Wurmser 1921). This reaction and even the organ redox states (Potters et al. 2010).
produces glucose and releases oxygen: Within a cell, the various organelles operate prop-
erly at a different redox state. For instance, mainte-
6 CO2ðgasÞ þ 12 H2 Oðliq:Þ þ hn ðlightÞ nance of a reduced nuclear redox state is critical for
transcription factor binding in transcriptional activa-
¼ C6 H12 O6ðaq:Þ þ 6 O2ðgasÞ þ 6 H2 Oðliq:Þ
tion (Hansen et al. 2006). Ordered by their redox
status, in a cell with no functional chloroplasts or a
It is an endothermic reaction, with a variation in
photosynthetic cell in the dark, mitochondria operate
enthalpy ΔH0+ 470 kJ per mol of CO2 at 25 °C
at the lowest Eh level, followed by, respectively, nuclei,
(Bisio and Bisio 1998).
cytosol, endoplasmic reticulum, and extracellular space
Nitrogen fixation also is an endothermic reduction
(Hansen et al. 2006).
of atmospheric nitrogen (Eagleson 1993), using energy
The redox situation is further complicated in plants
captured by photosynthesis in glucose which behaves as
by their highly reactive photosynthetic metabolism
an energy reservoir (Atkins and Jones 1997). The over-
(Dietz 2003). In plants, photosynthesis generates redox
all equation for the reduction of nitrogen by glucose
intermediates with extraordinarily negative redox poten-
(Bayliss 1956) is:
tials. Light-driven electron transport transfers electrons
from the acceptor site of photosystem I (mid-point
C6 H12 O6ðaq:Þ þ 4 N2ðgasÞ þ 6 H2 Oðliq:Þ
potential<−900 mV) to various acceptors, including
¼ 6 CO2ðgasÞ þ 8 NH3ðaq:Þ oxygen (Baier and Dietz 2005; Blankenship 2002).
Furthermore, photosynthesis in the chloroplasts
Similarly, proteosynthesis and liposynthesis in involves membrane-bound photosynthetic electron
plants are reduction reactions, with an accumulation transport, implying differences in Eh and pH: (i) be-
of chemical energy in the synthesized molecules. The tween the two sides of the membrane as the lumen and
energy released by the oxidation of these varied re- the stroma for the thylakoids; but also (ii) between
duced compounds in an oxygenated atmosphere is different areas of the membrane surface (Lambers et
used by cells (Lambers et al. 2008). The energy func- al. 2008). Similar processes are found in the Krebs
tioning of cells relies on the Krebs cycle in the mito- cycle in the mitochondria. Thus, compartmentalization
chondria: substrates imported into the mitochondrial and proper poising of the redox potential are critical
matrix are oxidized in a cyclical process, generating not only in establishing transfer kinetics in many
reducing power (Lambers et al. 2008). instances, but also in conserving the energy inherent
When these oxidation-reduction reactions are cata- in the potential gradients associated with electron
lyzed, this modifies their kinetics, but not their thermo- transport pathways (Chang and Swenson 1997).
dynamic conditions. Among the thermodynamically As a consequence, the redox state is a critical de-
possible reactions, those which predominate are deter- terminant of cell functioning, and any major imbalan-
mined by their redox kinetics. The thermodynamics and ces can cause severe damage or death (Dietz and
kinetics of oxidation-reduction reactions are therefore Scheibe 2004). In plants such as Nicotiana sylvestris,
essential for understanding the biochemical functioning leaf mitochondria modulate the whole cell redox ho-
of cells and living organisms. meostasis and determine antioxidant capacity (Dutilleul
et al. 2003).
Compartmentalization and redox state Peroxidation is particularly harmful to cells. For ex-
ample, peroxidation leads to disruption of membranes,
The myriad of inter-actions between redox-active oxidation of thiol groups, inhibition of thiol-containing
compounds, and the effect of environmental parame- enzymes, and DNA strand breaks (Ahmad 1992). Oxi-
ters on them, has been encapsulated in the concept of dation of mitochondrial glutathione jeopardizes mito-
‘cellular redox state’. Cellular redox state is envisaged chondrial integrity, causes oxidation of pyridine
as the sum of reducing and oxidizing redox-active nucleotides, and ultimately impairs energy production.
molecules (Potters et al. 2010). Derived from this Peroxidation of membrane lipids causes cell dysfunc-
concept of a cellular redox state are the organellar tion and ultimately cell death (Ahmad 1992).
392 Plant Soil (2013) 362:389–417

The production of reactive oxygen and reactive in a flexible way, depending on intensity and the type of
nitrogen species in plant cells can lead to an alteration impact (Scheibe et al. 2005). Cellular homeostasis will
of proteins through the oxidation of amino acid side be maintained as long as the mechanisms for acclima-
groups (Foyer and Noctor 2005). Peroxidation also tion are present in sufficiently high capacities. If an
inhibits a large variety of enzymes as they are regulat- impact is too rapid, and acclimation at the level of gene
ed by the oxidation-reduction state (Ahmad 1992; expression cannot occur, cellular damage and cell death
Chang and Swenson 1997; Ding et al. 1996; Ghezzi are initiated (Scheibe et al. 2005).
2005). Severe protein oxidation is costly to the cell In nodules harboring symbiotic rhizobia, legumi-
since oxidatively-damaged proteins need to be degrad- nous plants provide bacteria with energy and a micro-
ed by specific proteases (Sweetlove et al. 2009). Con- aerobic environment compatible with nitrogenase ac-
versely, dissipatory pathways are required to avoid any tivity (Marino et al. 2009). Oxygen can be either
detrimental effects caused by over-reduction of the beneficial or detrimental for diazotrophy in organisms
cellular redox state (Scheibe et al. 2005). capable of an aerobic catabolism. It supports the pro-
duction of a substrate for nitrogenase (ATP), but it can
Redox homeostasis also inhibit the activity and repress the synthesis of
this enzyme (Hill 1988). ROS are produced at every
Plants perform photosynthesis and assimilatory process- step of the symbiotic association: during symbiosis
es in a continuously changing environment. Rapidly establishment, during nitrogen fixation, and during
fluctuating environmental conditions can significantly nodule senescence. In order to deal with this ROS
stress organisms, particularly when fluctuations cross production, nodules are fitted with a large panel of
the thresholds of normal physiological tolerance enzymatic and non-enzymatic antioxidant mechanisms
(DeAngelis et al. 2010). To prevent these huge fluxes (Marino et al. 2009).
from causing catastrophic oxidative damage, there is an
extensive network of compensatory, buffering mecha- Redox regulation, redox signaling, plant phenology,
nisms (Dietz 2003; Hanke et al. 2009; Hansen et al. and global environment sensing
2006; Kandlbinder et al. 2003; Lambers et al. 2008;
Noctor et al. 2000). Redox compartmentalization also functions as a mech-
The simultaneous presence of strong oxidants and anism for specificity in redox signaling (Hansen et al.
strong reductants during oxygenic photosynthesis is 2006). Increasing evidence shows the importance of
the basis for regulation (Scheibe et al. 2005). Gluta- redox regulation and signaling in the context of trans-
thione, glutaredoxins and ascorbate are involved in a port activities, plant development, and programmed
large variety of cellular processes and play a crucial cell death; it also indicates involvement of redox inter-
role in response to oxidative stress and control of actions in proton pumping, membrane energization,
reactive oxygen species (ROS) (Foyer and Noctor ion channel regulation, iron reduction, nutrient uptake,
2003; Mullineaux and Rausch 2005; Noctor and signal transduction, and growth regulation (Dietz
Foyer 1998; Sanchez-Fernandez et al. 1997; Xing et 2003; Dietz and Pfannschmidt 2011; Kandlbinder et
al. 2006). Furthermore, proteins may have an over- al. 2004; Luthje et al. 1997; Noctor 2006; Pfannschmidt
representation of easily oxidizable amino acids (as 2003).
cysteine, tyrosine, and tryptophan) on their surface to Redox signals also regulate protein-DNA interac-
act as a decoy or as sacrificial residues, thus preventing tions and play a key role in gene expression, DNA
or postponing oxidation of residues that are more im- replication, and genome stability (Shlomai 2010;
portant for the function of the protein (Saurina et al. Turpaev and Litvinov 2004). Photosynthesis is also
2000; Sweetlove et al. 2009). governed by redox on essentially all levels, ranging
These buffering mechanisms must be integrated from gene transcription to translation, assembly and
with signaling cascades in a greater redox network, turnover, as well as short-term adaptation by state tran-
to ensure that short-term responses are adequate and sition and enzyme activity (Dietz 2003).
that, if buffering capacity is exceeded, there is a re- The redox regulation of many enzymes has a
sponse at transcript level (Hanke et al. 2009). Short- marked incidence on plant development. As early as
term and long-term mechanisms interact with each other 1949, Stout observed that induction of the reproductive
Plant Soil (2013) 362:389–417 393

development of sugar beet is correlated with changes in defense mechanism is the generation of ROS as a
the oxidation-reduction balance of certain regions of the hypersensitive response of plants to pathogens and
plant (Stout 1949). Root growth, flowering, develop- subsequent stress on the colonizing microbes or neigh-
ment of floral organs, leaf sectoring, and photoperiod- boring roots (Blokhina et al. 2003; Bolwell et al. 1995;
ism are regulated by the redox potential (Becker et al. Hartmann et al. 2009; Lamb and Dixon 1997; Mori
2006; Foreman et al. 2003; Rosso et al. 2009; Sanchez- and Schroeder 2004). Increased disease resistance is
Fernandez et al. 1997; Xing et al. 2006). Reactive oxy- very likely to be a combinatorial effect of redox sig-
gen species (ROS) are key actors in the regulation of nals triggered by salicylic acid, H2O2, glutathione, and
plants' dormancy and germination (Bailly et al. 2008). potentially additional yet unidentified compounds
Cellular antioxidants influence plant growth and devel- (Mateo et al. 2006). The ascorbate-glutathione (AsA-
opment by modulating processes from mitosis and cell GSH) cycle serves as the main antioxidant pathway in
elongation to senescence and death (Foyer and Noctor plant cells, linking protection against ROS to redox-
2005). regulated plant defenses (Kuzniak 2010). On this basis,
It is now well established that redox regulation is a hydrogen peroxide could be regarded as an 'offensive
central element in adjusting plant metabolism and weapon' of cells, and catalase as a 'defensive weapon,' as
development to the prevailing environmental condi- this enzyme degrades hydrogen peroxide into water and
tions (Dietz 2003). Redox sensing/signaling mecha- oxygen (Voisin 1959).
nisms may be primary sensors of environmental Oxidation-reduction processes are also involved in
change and are an important component for sensing interactions between herbivorous insects and plants.
abiotic stresses in general (Huner et al. 1996). For Plants produce pro-oxidant compounds as an allelo-
instance, cellular redox status, associated with cold- chemical defense, exacerbating the endogenous oxida-
stress sensing, can activate redox-responsive proteins tive stress of all aerobic organisms (Ahmad 1992). For
and might act as a signal for the reconfiguration of instance, host-plant phenolics have a widely recog-
gene expression (Yadav 2010). Chloroplastic redox- nized detrimental impact on gypsy moth (Lymantria
sensing affects chloroplastic and nuclear gene expres- dispar) (Meyer and Montgomery 1987; Rossiter et al.
sion in response, not only to light intensity, but to a 1988; Roth et al. 1994). It has been suggested that
myriad of abiotic stresses (Baier and Dietz 2005; oxidation of phenolics in the insect midgut produces
Wilson et al. 2006). toxic quinones, reducing food digestibility (Appel and
Finally, the nutritional status of a plant influences Maines 1995). Herbivorous insects cope with this
its redox status. N-, P- or S-nutrient deprivation trig- stress through direct detoxification of the prooxidants
gers distinct redox changes and induces oxidative or antioxidant compounds and antioxidant enzymes
stress with a rather defined pattern in the context of (Ahmad 1992; Appel 1993; Roth et al. 1997). How-
nutrient-specific alterations in metabolism. For instance, ever, high levels of allelochemicals in plant foliage
N-deprivation caused a five-fold increase in ascorbic may overload the detoxification capacity of insects
acid in Arabidopsis thaliana leaves (Kandlbinder et al. (Lindroth and Hemming 1990).
2004). P-starvation induced an increase in ascorbate and
glutathione levels. Sulfur depletion has been found to Redox potential, allelopathy, and recognition
cause a drop in glutathione levels to less than 25 % of by parasitic plants
the control (Kandlbinder et al. 2004).
Among the 20,000 allelopathic substances identified,
Redox signals, plant responses to biotic stresses, many are pro-oxidant and exert oxidative stress (Ahmad
and resistance to pathogens 1992; Downum 1986; Downum and Rodriguez 1986).
For instance, the phytotoxic action of Tagetes minuta is
Redox activity plays a role in the biocontrol of plant primarily the result of increased lipid peroxidation rates,
pathogens (Altomare et al. 1999). Reactive oxygen with the essential oils acting as an ‘oxidant’ agent
species (ROS) in plants are known to accumulate (Scrivanti et al. 2003).
during biotic stress, and different cellular compart- Similarities exist between allelopathic phenomena
ments respond to them by a distinct antioxidant reper- and those of plant recognition by parasitic plants
toire (Kuzniak 2010). A very widely-found local (Tomilov et al. 2006). Parasite perception of host
394 Plant Soil (2013) 362:389–417

factors by parasitic plants of the Scrophulariaceae of the mechanisms underlying root-induced pH

family such as Striga sp. occurs via a redox-associated changes (Hinsinger et al. 2003). As a consequence,
mechanism (Yoder 2001). Eh and pH are best analyzed concomitantly, in
interaction.
Redox potential and pH in plant cell and physiology:
the ignored Eh-pH interaction
Eh, pH, and microorganisms
Cell pH, regarded as the master variable in plant
physiology, has been extensively studied and reviewed The Eh and pH of a milieu largely determine the
(Kurkdjian and Guern 1989; Rengel 2002; Smith and metabolic types emergent in the bacterial community
Raven 1979). Hence, it is not reviewed in this paper. of that milieu, and they are therefore significant param-
Like Eh and electron transfers, pH and proton transfers eters for biological activity (Billen 1973; Stumm 1966).
are crucial in the energy functioning of cells and For instance, nitrogen fixation by Azospirillum spp. is
strongly affect plant metabolism and catabolism, as governed by soil redox fluctuations, pH and organic
for example, embryogenic cell division (Pasternak et matter (Charyulu and Rao 1980).
al. 2002). Water, as an active constituent in cell biology, Eh clearly influences the development of microorgan-
is structured in a network which facilitates electron isms. As early as 1934, Heintze proposed using varia-
transfers between proteins and other biomolecules, and tions in soil Eh to characterize groups of microorganisms
allows rapid proton diffusion (Ball 2008). As with Eh, (Heintze 1934). Bacterial growth is directly correlated to
compartmentalization and intracellular pH regulation changes in Eh (Kimbrough et al. 2006). Microbial and
are key features of cell physiology. Reactions in the enzymatic activity are negatively correlated with Eh in
cytosol are exquisitely sensitive to changes in pH (Taiz anaerobic soils (Brzezinska 2004; Kralova et al. 1992;
1992). pH regulation involves very complex processes Snakin and Dubinin 1980). Furthermore, the redox state
in interaction with each other (Felle 1988; Rengel 2002; of nodules is regarded as a referee of legume-rhizobium
Sakano 1998; Smith and Raven 1979). Cytosolic pH symbiosis (Marino et al. 2009).
can be regulated by pumping massive amounts of pro- Each microorganism type is adapted to specific
tons out of the cytosol into the lumen of the vacuole, in Eh conditions, and is characterized by its ability to
which pH varies according to plant species (Smith and develop within a wider or a narrower Eh-range. For
Raven 1979; Taiz 1992). Among the processes of pH instance, anaerobic bacteria can only develop within
regulation, Smith and Raven (1979) emphasize excretion a narrow range of very low Eh values. Aerobic
of excess protons or hydroxyl ions to the root medium. microorganisms such as Actinomyces sp. or Azoto-
As with Eh, pH-dependent signals regulate physiological bacter sp. require a higher Eh, but can develop over
processes as, for instance, root water transport during a much wider range (Rabotnova and Schwartz
anoxic stress (Tournaire-Roux et al. 2003). 1962). Fungi develop more than bacteria under
Surprisingly though, studies of Eh are generally moderately reducing conditions (Eh > + 250 mV),
disconnected from studies of pH; and Eh-pH interac- while bacteria are more abundant than fungi under
tions are ignored most of the time. This is clearly a highly reducing conditions (Eh < 0 mV) (Seo and
limitation of most studies as Eh and pH are not inde- DeLaune 2010).
pendent influences; for instance, (i) oxidation-reduction Frequent high-amplitude redox fluctuation may be
reactions can involve a transfer of protons, especially the a strong selective force on the phylogenetic and phys-
major chemical reactions involving changes in the oxi- iological composition of soil bacterial communities
dation state of Fe, Mn and N, which also imply the and may promote metabolic plasticity or redox-
consumption or production of H+, and thereby a cou- tolerance mechanisms (Pett-Ridge and Firestone
pling of the Eh and pH (Hinsinger et al. 2003); (ii) a 2005). For instance, indigenous soil bacteria are high-
redox system on the plasma membrane of plant cells has ly adapted to fluctuating redox regimens (Pett-Ridge
implications for cytoplasmic pH regulation (Rengel and Firestone 2005). Microbial community acclimation
2002); and (iii) in the rhizosphere, redox processes or avoidance strategies for survival will, in turn, shape
are intimately coupled with pH changes and thus microbial community diversity and biogeochemistry
need to be taken into account for understanding all (DeAngelis et al. 2010).
Plant Soil (2013) 362:389–417 395

Although studies on the impact of Eh on plant (Payne et al. 1994). Fusarium wilt of flax was sup-
pathogens are few, they all indicate that the develop- pressed when the soil pH was raised above seven and
ment of several plant pathogens could be related to a clay was added (Höper et al. 1995), and Fusarium of
high Eh. Four examples illustrate this hypothesis. Gerbera (Compositae) decreased when the pH was
First, the application of hydrogen peroxide to tobacco higher than six (Minuto et al. 2008).
plants, or inhibition of catalase by the application of Conversely, several studies have shown that virus
hydroxylamine (also leading to hydrogen peroxide development is slowed down by a low pH. In water,
accumulation in the cells), both induce development viruses are almost completely removed below a criti-
of the mosaic virus (Yamafuji and Cho 1948; Yamafuji cal pH (Guan et al. 2003). In sediments, a strong
and Fujiki 1947). Second, sclerotial differentiation in correlation between virus abundance and pH indicates
phytopathogenic fungi such as Rhizoctonia solani is virus susceptibility to a low pH (Kyle et al. 2008).
induced by oxidative stress (Patsoukis and Georgiou However, some viruses have been associated with
2007a, c). Third, it is known that soil-borne pathogens Archaea, organisms living in extreme conditions as
such as Fusarium sp. and Rhizoctonia solani can be acidic hot springs (Happonen et al. 2010).
controlled by a low Eh (Blok et al. 2000; Shinmura In plants, the activity of tomato spotted wilt and
2004; Takehara et al. 2004). Fourth, nitrogen fertilizer tobacco mosaic viruses, for instance, varied with pH
applied as NO3- (oxidized form of N) triggers severe (Best and Samuel 1936). Various explanations of the
attacks of rice blast, whereas application as NH4+ influence of low pH on virus development have been
(reduced form of N) does not induce rice blast proposed, such as: (i) a glycoprotein, playing a crucial
(Osuna-Canizalez et al. 1991). role in the capacity of the tomato spotted wilt virus to
Similarly, each microorganism is adapted to a def- bind to sensitive cells, undergoes pH-dependent confor-
inite pH range outside of which it cannot live. Most mational changes at a low pH (Pekosz and Gonzalez-
soil bacteria develop between pH 4.5 and 10 (Baas Scarano 1996; Whitfield et al. 2005); (ii) pH modifies
Becking et al. 1960). Diversity is highest in neutral the conductivity of the ion channel as has been observed
soils and minimum in acidic soils (Hinsinger et al. in southern cowpea mosaic virus (Helrich et al. 2001);
2009; Lauber et al. 2009) The ecological behavior of and (iii) pH induces RNA disaggregation and deg-
microbes is determined, among other ways, by their radation in the case of turnip yellow mosaic virus (Sam
ability to adapt themselves to wider or narrower pH et al. 1991).
ranges and by the limits of the pH range within which At the same time, microorganisms are known to be
multiplication is possible (Rabotnova and Schwartz able to modify the Eh and the pH of their surrounding
1962). For instance, thio-bacteria have a very wide medium, depending on their requirements; further,
potential environment, while algae are found literally they have this ability to a considerably greater degree
everywhere (Baas Becking et al. 1960). Saprophytic than other organisms (Rabotnova and Schwartz 1962).
bacteria, which are widespread in soil and water, can Potter (1911) was probably the first to draw attention
exist under very diverse conditions (Rabotnova and to the fact that microbial cultivation generates a low-
Schwartz 1962). Highly ubiquitous Actinomycetes in- ering of the Eh. In soils, widely-diffused saprophytes
crease in alkaline soils (Roger and Garcia 2001), while and pathogenic anaerobes lower the Eh (Rabotnova
Trichoderma prefer acid conditions (Steyaert et al. and Schwartz 1962). In aerobic soils, microorganisms
2010). Thus, pH has been proposed as the main factor consume oxygen and, as a consequence, lower the Eh
affecting the diversity and richness of soil microbial (Bohrerova et al. 2004; Kralova et al. 1992). When
communities (Fierer and Jackson 2006; Lauber et al. soil moisture content increases Eh decreases, leading
2009). to anaerobic soil conditions because of the rapid con-
Microorganisms that are adapted to special loca- sumption of oxygen by microbes and the resulting
tions and special ecological conditions, somewhat like partial or total loss of oxygen (Savant and Ellis 1964).
pathogenic bacteria, mostly have a narrow pH range In a culture medium, the pH value originally present
(Rabotnova and Schwartz 1962). Many pathogenic is changed and is regulated by the metabolism of the
fungi develop preferably at a slightly low pH. For microorganisms (Rabotnova and Schwartz 1962). Fungi
instance, development of Aphanomyces cochlioides can influence soil conditions such as the pH within the
et Pythium spp. was slowed down by a high pH microenvironment surrounding their hyphae (Garrett
396 Plant Soil (2013) 362:389–417

1963; Twining et al. 2004). Microorganism activity (Mansfeldt 2003; Snakin et al. 2001). Sabiene et al.
usually leads to acidification (Rabotnova and Schwartz (2010) also documented inter-annual variations in rela-
1962). In soils, this acidification can be compensated for tion to climatic conditions and soil moisture. Flooding
by the buffering capacity of the absorbing complex dramatically affects both Eh and pH, especially in or-
(Roger and Garcia 2001). ganic soils (Kashem and Singh 2001). Balakhnina et al.
(2010) reported a very rapid decrease in soil Eh from+
543 to +70 mV within a few hours after flooding, and a
Soil Eh and pH at the field scale restoration of the initial level within a few days after
drainage.
Soil Eh and pH variability Redox kinetics are largely governed by microbial
catalysis as soil microorganisms produce catalytic
Soil Eh fluctuates normally between −300 and enzymes (Fenchel et al. 1998). Microbial activity is
+900 mV. Waterlogged soils have an Eh below +350 itself influenced by Eh and pH. It is also promoted by
to +250 mV and dry soils above +380 to +400 mV, clay, which plays a role of surface catalyst (Filip 1973;
according to various authors (Pearsall and Mortimer Theng and Orchard 1995), retains organic matter used
1939; Pezeshki 2001). For Kaurichev and Shishova by microorganisms (Wardle 1992), and contributes to
(1967), four main classes of soil conditions can be the development of protective micro-habitats (Heijnen
determined according to Eh: Aerated soils have an and van Veen 1991). In a sandy soil a significant
Eh over+400 mV; moderately reduced soils between increase of the microbial biomass (bacteria and fungi)
+100 and +400 mV; reduced soils between −100 and was observed when it was enriched with clay (Davet
+100 mV; and highly reduced soils between −100 and 1996).
−300 mV. Cultivated soils are most frequently in the Faced with this high temporal variability, the ca-
range of +300 and +500 mV under aerobic conditions pacity of a soil to buffer Eh and pH is regarded as an
(Macías and Camps Arbestain 2010). However, Eh important parameter by various authors. Eh buffering
can reach +750 mV in podzols (Kaurichev and Shishova capacity determines the evolution of the soil's
1967). oxidation-reduction conditions, and especially the
Most cultivated soils have a pH between 4 and 9, speed and the amplitude of the response of a soil to
but a pH below 3 and above 10 can be measured in an input of electrons (Von de Kammer et al. 2000).
acid sulfate soils or sodic soils, respectively (Brady These previous authors proposed calculation of a pa-
and Weil 2010). Interestingly, pH and Eh are negatively rameter, total reducing capacity (TRC), as the number
correlated in soils (Bohrerova et al. 2004; Van Breemen of electrons that can be provided by the reduced com-
1987). ponent of a milieu. Similarly, Heron et al. (1994)
Soil Eh and pH can greatly vary at very short calculated an oxidation capacity (OXC) taking into
distances (Hinsinger et al. 2009; Yang et al. 2006). account the oxygen, nitrate, iron, manganese and sul-
For instance, the center of a humid soil aggregate of 6– fates available as the main electron acceptors. This
7 mm in diameter can have a redox potential 100 to oxidation capacity corresponds to the quantity of elec-
200 mV lower than its surface (Kaurichev and Tararina trons that can be accepted by a milieu.
1972). Various authors have also reported marked dif-
ferences in Eh and pH as a function of soil depth Soil Eh-pH and plant growth
(Bohrerova et al. 2004; Mansfeldt 2003; Rousseau
1959; Snakin et al. 2001). For instance, in a grey forest Eh has received little attention in the whole-plant
soil in Russia, in the A horizon at a depth of 7 cm, Eh context, apart from the influence of having very low
and pH were respectively measured at 80 mV lower and redox potential in submerged soils. Eh limits for plant
0.9 units higher than in the C horizon at a depth of growth are between +300 and +700 mV (Volk 1993).
116 cm (Snakin et al. 2001). In addition, the living Reduced conditions (< +350 mV) are particularly lim-
matter in soil creates significant Eh and pH heterogene- iting for many plants. For instance, the richness of
ity within a given soil horizon (Snakin et al. 2001). riparian plant species and total plant cover were pos-
Soil Eh and pH also exhibit high temporal variability, itively correlated with Eh at a depth of 10 and 25 cm
with a daily cycle and strong seasonal influences (Dwire et al. 2006). Five-year-old trees had greater
Plant Soil (2013) 362:389–417 397

vertical growth and higher survival rates in transition 1945) – represent stability areas of the various chem-
zones with Eh varying between +400 and +450 mV ical forms of an element in a solution as a composite
than in lowlands with Eh varying between +250 and function of Eh and pH. Among the reactions that are
+380 mV (Pennington and Walters 2006). Annual possible thermodynamically, those that predominate at
sugarcane yields decreased by 0.2 to 0.3 t/ha per day any given point in time are determined by redox
when Eh was lower than 332 mV (Carter 1980). In kinetics (Chadwick and Chorover 2001). Therefore,
acid sulfate soils in Vietnam, rice yields increased the complex kinetics of oxidation-reduction processes
sharply when Eh rose under reduced conditions, and in heterogeneous and changing soils should be con-
conversely decreased when Eh rose under oxidized sidered carefully (Sparks 2001). These kinetics are
conditions: the highest rice yield was obtained in soils also influenced by Eh and pH as they have an impact
forming jarosite around rice roots, indicating local Eh on microbial activity, which catalyzes these reactions
values of approximately +400 mV (Husson et al. (Fenchel et al. 1998).
2001; Husson et al. 2000b). Conversely, Eh and pH are influenced by the various
The tolerance of plants to changing redox condi- elements composing the soil, especially those having a
tions varies greatly. A study of riparian meadows high amplitude in their redox numbers, such as N, P or
suggests that the observed biological diversity is S, and those at high concentrations such as Fe.
strongly related to steep environmental gradients in
hydrology and soil Eh (Dwire et al. 2006). Similarly, Nitrogen
close associations were observed between distinct
plant community zones and Eh in created wetlands, The nitrogen cycle is related to Eh and pH as shown
suggesting that natural plant communities may be used by the Pourbaix diagram representing the predominant
to characterize the oxidation status of soils in a broad areas for the various forms of N in a water solution
range of wetland ecosystems (Pennington and Walters according to these parameters (Figure 1). In oxidized
2006). conditions (Eh>500 mV at pH 7), the thermodynami-
The pH of the soil solution is also a critical envi- cally stable form of N is NO3- ions, while under reduced
ronmental factor for plant growth (Brady and Weil or moderately oxidized conditions (Eh<400 mV at
2010). As for redox conditions, the tolerance of plants pH 7) and at a pH below 9.2, NH4+ ions will dominate.
to acid and/or alkaline conditions varies considerably; As both NO3- and NH4+ are soluble, Eh and pH
however, they all have a rather narrow range of opti- mainly influence the form under which N is assimilat-
mum pH conditions. Most cultivated crop plants grow ed by plants. The form of N assimilated by plants also
well on soils that are just slightly acid to near-neutral, has a marked effect on cellular regulation of pH
and only a few species can develop at a pH below 4.5 (Marschner 1995). Furthermore, as plants use NH4+
or above 9 (Brady and Weil 2010). Some plants such to synthesize proteins, the assimilation of NO3--N
as sweet potato (Ipomea batatas), cassava (Manihot induces a considerable energy cost for the plant to
esculenta), and tea (Camellia sinensis) are known for reduce NO3--N to NH4+-N (Marschner 1995). In ad-
their ability to grow under acid soil conditions. Strong dition, as NO3- is highly soluble, there is a risk of loss,
acidity or highly alkaline conditions affect plant and pollution. Finally, the form of nitrogen assimilated
growth, mainly because pH strongly influences nutri- by plants has a marked effect on rhizospheric pH and
ent availability and the risk of ion toxicity (Brady and on the assimilation by plants of other cations and
Weil 2010; Marschner 1991). anions (Hinsinger et al. 2003; Marschner 1995).

Soil Eh-pH, nutrient solubility, and assimilation Phosphorus

by plants
Under field conditions, plant roots absorb inorganic
Eh and pH are factors that strongly influence the phosphorus dissolved in the soil solution, mainly as
mobility of many nutrients in complex chemical and monovalent phosphate ions H2PO4- which can much
biological environments (Gambrell and Patrick 1978; more easily be transported through the plasma mem-
Laanbroek 1990). Based on thermodynamic laws, Eh- brane than divalent phosphate ions HPO42- (Hinsinger
pH diagrams – known as Pourbaix diagrams (Pourbaix et al. 2003). H2PO4- ions dominate in acid soils while
398 Plant Soil (2013) 362:389–417

Fig. 1 Pourbaix diagram of Eh (V)

nitrogen (N) representing 1.0
the various forms of N in a PO
2=
1ba
100 μM solution at 25 °C HNO 2 r
as a function of Eh (in V)
0.8 Acid and Alkaline and
and pH. Diagram adapted
oxidized oxidized
from MEDUSA Software.
Puigdomenech 2009–2011
0.6 NO 3-

0.4

0.2
NH 4+

0.0 NH 3 NO 2-
Acid and Alkaline and
PH reduced
2 =1b
ar
reduced
-0.2
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
pH

HPO42- ions are by far the dominant species in alkaline sulfur solubility is limited to waterlogged or sub-
soils. However, root apoplastic pH is normally less than merged fields. In these fields, especially when they
6, and the major form of P taken up across the mem- are rich in organic matter, a very low Eh leads to SO42-
brane by plants in high-pH soils would still be H2PO4- reduction into H2S, which is highly toxic to plants
(Hinsinger et al. 2003). Furthermore, rhizosphere acid- (Ponnamperuma 1972). At a higher Eh and pH, sulfur
ification as related to proton efflux from roots is well availability is also indirectly affected, as Eh and pH
known as a response of many plant species to phospho- influence the sulfate sorption capacity of the soil (Lefroy
rus deficiencies (Hinsinger et al. 2009). et al. 1993).
Eh and pH also indirectly affect P availability by Conversely, in natural environments sulfur is one of
affecting the solubility of metal ions as Mn, Al and Fe the main determinants of the Eh-pH characteristics
oxides and hydroxides or of CaCO3; these bind to or (Baas Becking et al. 1960). Furthermore, oxidation
adsorb phosphate ions and make them unavailable to of reduced sulfur (H2S or FeS2), most of the time by
plants (Brady and Weil 2010; Kemmou et al. 2006; autotrophic bacteria such as Thiobacillus spp., leads to
Phillips 1998; Sallade and Sims 1997; Vadas and Sims the production of sulfuric acid and, as a consequence,
1998). to acidification (Dent 1993).
In addition, the H2PO4-/ HPO42-system is known to
play a prominent role in the buffering of cytosolic pH Iron
(Gerendas and Schurr 1999; Hinsinger et al. 2003).
The solubility of iron is strongly influenced by both
Sulfur Eh and pH. Iron is absorbed by plants in its soluble
form as ferrous iron (Fe2+). High concentrations of
Sulfur deficiency is rare in agriculture, especially in ferrous iron in the soil solution are observed at a low
aerobic conditions. Under normal Eh-pH field condi- Eh, with a rapid decrease when the Eh rises above+
tions, the thermodynamically stable form of sulfur is 350 mV (at pH 5), in relation to the formation of iron
sulfate SO42- (Figure 2), which is transported and oxides and hydroxides (Frohne et al. 2011). Ferrous iron
easily assimilated by plants. As the reduction of toxicity is frequent at a low Eh and pH, and conversely,
SO42- to H2S occurs only at a low Eh and pH (around iron deficiency can occur at a high Eh and pH (Tanaka
−100 mV at pH 6), the direct impact of Eh-pH on et al. 1966).
Plant Soil (2013) 362:389–417 399

Fig. 2 Pourbaix diagram of Eh (V)

sulfur (S) representing the 1.0
various forms of S in a PO
2 =1b
100 μM solution at 25 °C ar
as a function of Eh (in V)
0.8 Acid
A and
a Alkaline
a aand
and pH. Diagram adapted
oxidized
o z oxidized
x d
from MEDUSA Software.
Puigdomenech 2009–2011 O 4-
HSO
0.6

0.4
SO 42-
S
0.2

Acid
c and
n
0.0 reduced
e d
Alkaline
a aand
PH
2 =1b
ar
H2 S reduced
d d
-0.2
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
pH

In natural environments, iron strongly influences lowering the permeability of the soil to air and water
the Eh-pH characteristics (Baas Becking et al. 1960), (Abrol et al. 1988), and altering the soil's Eh. High pH
and iron reduction–oxidation delineates an important induced by an excess of exchangeable sodium also
redox threshold in pedogenesis (Chadwick and Chorover indirectly affects other nutrient concentrations, as for
2001). P, Ca, Mg, Mn or Zn (Abrol et al. 1988).
Aluminum solubility is mainly governed by soil
Potassium, sodium, and aluminum pH, but also by soil organic matter and clay content.
Exchangeable aluminum rapidly increases when
Potassium, sodium, and aluminum solubility is not pH(KCl) decreases below 4.3. Aluminum plays a major
directly affected by Eh because these elements have role in soil acidity. The water molecules ligate to the
only one possible redox number, respectively+I in K+ aluminum ions forming Al(OH2)63+ ions, favoring
and Na+ and+III in Al3+, and they cannot exchange water dissociation which produces protons (Manahan
electrons. 2001). A single Al3+ can release up to three H+ (Brady
Potassium availability is mainly related to soil pH, and Weil 2010).
and to clay content and type. An increase in pH
increases potassium fixation as it makes it easier for Micronutrients
K+ ions to move closer to the colloidal surfaces. As they
move closer, K+ ions are more susceptible to fixation by The availability of several micronutrients, such as Mn,
2:1 clays, which fix potassium very readily and in large Cu or Zn, is strongly influenced by soil Eh and pH.
quantities (Brady and Weil 2010). There is evidence for direct or indirect biological
Sodic soils have high pH as H+ ions are adsorbed alterations in the availability, solubility, or oxidation-
on clay micelles in place of Na+, which results in reduction state of Mn, Zn, Cu, Mo, Co, Si, Ni, and
increased OH- concentration. Sodium Exchangeable various others (Reddy et al. 1986). For instance, the
Percentage (SEP), defined as Exchangeable Na/Cation Pourbaix diagram for manganese (Figure 3) shows
Exchange Capacity, is positively correlated to soil pH that solubilization as Mn2+ ions is a function of both
(Abrol et al. 1988). Excess exchangeable sodium in Eh and pH. In alkaline soil, Mn deficiency can occur
sodic soils has a marked influence on the physical soil under aerobic conditions. A decrease in Eh corresponds
properties, leading to breakdown of soil aggregates, to higher Mn bioavailability (Schwab and Lindsay
400 Plant Soil (2013) 362:389–417

Fig. 3 Pourbaix diagram of Eh (V)

manganese (Mn) represent- 1.0
ing the various forms of PO
2 =1b
Mn in a 100 μM solution
at 25 °C as a function of
ar
O 4-
MnO
M
0.8 Acid
A and
a Alkaline
k and
Eh (in V) and pH. Diagram
oxidized
o z oxidized
x e
adapted from MEDUSA MnO
Software. Puigdomenech 2
2009–2011 0.6

0.4
Mnn O
Mn
M n 2+ 2 3
0.2

Mnn O
0.0 Acid
A and
a 3 4
reduced
r e
Alkaline
a aand
PH
2 =1b reduced
d d
ar Mn(OH)
(
-0.2 2
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
pH

1982), and Mn toxicity is quite common in association oxygen transport through aerenchyma (Evans 2004;
with a low soil pH (Brady and Weil 2010). Gilbert and Frenzel 1998; Gotoh and Tai 1957). This
Similarly, Pourbaix diagrams for various micronu- ability to raise the Eh in their rhizosphere protects
trients (not shown) indicate that deficiency is more plants against phytotoxic concentrations of reducing
likely: (i) at a high pH and/or low Eh for Cu; (ii) at a substances. It is related to the nutritional state of the
high pH for Zn; (iii) at a very low Eh or a high pH for plant. For instance, K application on K-deficient soils
Ni; and iv) at a low Eh and pH for Mo. This is in paddy fields leads to an increase in the oxidizing
confirmed by field observations of Cu and Ni concen- power of rice roots, an increase in soil Eh and a decrease
tration, which increases in the soil solution with a in active reducing substances and ferrous iron, and a
rising Eh (Frohne et al. 2011). decrease in the number of oxygen-consuming micro-
organisms (Chen et al. 1997).
Plant impacts on soil Eh and pH In aerobic conditions, the rhizosphere of various
dicotyledonous cultivated plants (Pisum sativum, Vicia
Plants can quite dramatically alter the Eh and pH of sativa, Helianthus annuus) showed a decrease in Eh
their rhizosphere (Hartmann et al. 2009). Plant roots close to the root tip, probably due to the release of
create conditions allowing development of a unique reducing exudates (Flessa and Fischer 1992b).
microbial community in the rhizosphere, to such an The pH in the rhizosphere is also altered by plant
extent that evolution has shaped soil life to adapt to roots and soil microbes. Rhizosphere pH has been
this specific ecological niche (Hartmann et al. 2009; reported to be up to 1–2 pH units below or above the
Lambers et al. 2009; Sanon et al. 2009). This alteration bulk soil pH, and differences were detected up to 2–
can be a direct effect of root exudation or an indirect 3 mm from the root surface (Chaignon et al. 2002;
effect through preferential development of specific Hinsinger et al. 2009; Hinsinger et al. 2003; Youssef
microorganisms which also alter the Eh and pH. and Chino 1989). Miller et al. (1991a) in a study on
Roots of plants adapted to highly-reduced environ- barley (Hordeum vulgare) and white clover (Trifolium
ments obtain their essential oxygen through a system repens) showed that the rhizosphere at the root tip is
of air-filled intercellular space (Flessa and Fischer alkaline relative to that further from the tip. The form
1992a). Wetland plants, such as rice, have the ability under which plants absorb nutrients substantially
to raise the Eh in their rhizosphere, especially by affects rhizospheric pH, especially for nitrogen as
Plant Soil (2013) 362:389–417 401

NH4+ or NO3- ions amount to 80 % of the total anions decay may be looked upon as an electron-pump, sup-
and cations assimilated by plants (Marschner 1995). plying electrons to more oxidized species in the soil
Dramatic changes in pH can occur as a conse- (Chesworth 2004).
quence of the microbially-mediated oxidation of nitro- An increase in soil organic matter leads to a lower-
gen (Hinsinger et al. 2009). This is explained by: (i) ing of soil Eh: in soils rich in easily decomposable
the necessary release by plant roots of an H+ ion when organic matter, oxidation processes consume large
they absorb a NH 4 + ion to counterbalance the amounts of oxygen, which leads to the formation of
corresponding excess of positive charges (Hinsinger organic compounds with reducing properties (Lovley
et al. 2003; Raven and Smith 1976); (ii) conversely, et al. 1998). Fresh organic matter is the most reduced
the release of OH- ions when plants absorb NO3- ions fraction in soil, hence the most thermodynamically
to counterbalance the corresponding excess of nega- unstable, followed by necromass and most of the soil
tive charges, the excess OH- being also partly neutral- organic matter, with organic quinone molecules being
ized by the 'biochemical pH-stat' (Raven 1986; Raven the most resistant to oxidation (Macías and Camps
and Smith 1976). In addition to roots, many soil Arbestain 2010).
microbes, such as ectomycorrhizal and saprophytic Fresh straw was reported to have an Eh around
or pathogenic fungi, can produce organic acids and +150 mV (at pH 5.5 to 6). During composting the
acidify the rhizosphere (Hinsinger et al. 2009). Eh evolved from 0 (at pH 7.7) at the beginning of the
However, modifying the Eh and pH of the rhizo- process to +300-+400 mV at the end of composting
sphere has a cost for plants. In annual plant species, (Miller et al. 1991b). To summarize, the quality and
30-60 % of the photosynthetically-fixed carbon is the quantity of organic matter largely determine soil
translocated to the roots, and a large proportion of that Eh and its buffering capacity.
carbon (up to 70 %) can be released into the rhizo- Organic matter is also one of the main factors
sphere (Neumann and Römheld 2000). For instance, buffering soil pH (Magdoff and Bartlett 1984). It con-
cereals (wheat and barley) transfer 20-30 % of total tributes to the development of neutral to slightly acid
assimilated C into the soil, and pasture plants translo- soil pH (Brady and Weil 2010). At a low pH, soil
cate about 30-50 % of their assimilates below ground organic matter forms complexes with Al, which is a
(Kuzyakov and Domanski 2000). Thus, rhizodeposits, major pH-buffering process in soils (Skyllberg et al.
the organic compounds released by plant roots under 2001). At a high pH, organic matter contributes to
various forms, amount to 20 to 50 % of the total acidification through the formation of soluble com-
photosynthetic production, but can be as high as plexes with non-acid cations such as calcium or mag-
80 % (Gobat et al. 1998). nesium, which are easily lost by leaching (Brady and
Beside their short-term effect in the rhizosphere, Weil 2010).
plants also have an impact on soil Eh and pH in the On the other hand, soil Eh and pH are some of the
long term, as they are the main source of organic main factors regulating the speed and intensity of
matter in the soil. Whether or not their biomass is humification processes (Reddy et al. 1986; Rusanov
returned to the soil has a large and long-term effect and Anilova 2009). Organic matter degradation rates
on the structure and functioning of soil systems. are fastest under oxidizing conditions, in the presence
of free O2 (Macías and Camps Arbestain 2010). In the
Soil Eh and pH and soil organic matter absence of free O2 or inorganic oxidants as NO3-, Mn4+,
Fe3+ and SO42-, fermentation processes take place in
Organic matter is one of the main factors affecting soil which organic molecules are utilized as electron accept-
Eh (Oglesby 1997). Bioavailable organic matter as an ors (Reddy et al. 1986; Ugwuegbu et al. 2001).
electron reservoir constitutes the bulk of the soil's In the global carbon cycle, the length of time spent
reduction capacity (Chadwick and Chorover 2001; by the carbon in the soil as solid organic matter is a
Lovley et al. 1998). Organic matter can be partly, function of Eh. Organic matter represents a residence
and reversibly, reduced by microorganisms, and it time for carbon as short as a year in oxidized soils, and
plays the role of electron shuttle, i.e. a mobile carrier of thousands of years in highly reduced conditions
of electrons (Lovley et al. 1998). Organic matter is the (Chesworth 2004). The rate of organic matter decom-
most prolific source of electrons in soil and during position is also influenced by three parameters related
402 Plant Soil (2013) 362:389–417

to soil Eh and pH: (i) the type of microbial metabo- space, with three salients or dimensions, i.e. acidity,
lism; (ii) the bacterial efficiency; and (iii) the capacity alkalinity, and hydromorphism, the permanent or tem-
of the soil system to supply electron acceptors (Reddy porary state of water saturation in the soil. The acid
et al. 1986). salient represents the path of evolution of three major
types of soil genesis: podzolization, ferralitization, and
Soil Eh and pH and soil genesis andosolization (Chesworth and Macias 2004). Calcare-
ous, sodic and saline soils develop along the alkaline
The Eh and pH of the soil solution are key factors salient, while peat soils develop along the hydromorphic
influencing the trajectory of soil genesis (Chadwick salient, with excess moisture leading to suppression of
and Chorover 2001; Chesworth 2004; Chesworth et al. aerobic factors in soil-building.
2006; Chesworth and Macias 2004). This trajectory Such Eh-pH diagrams are particularly interesting
can be represented on Eh-pH diagrams (Figure 4). The for studying acid sulfate soils. In these soils, changes
chemical evolution of soils is essentially determined in Eh dramatically affect pH as they contain pyrite
by fluxes of protons and electrons. The electron flux (FeS2), which upon oxidation produces large amounts
takes place between organic matter as the major of sulfuric acid. Potential acid sulfate soils, with py-
source, and atmospheric oxygen as the principal sink rite, are found in reduced conditions. Upon oxidation
(Chesworth and Macias 2004). (> 50 mV at pH 4), actual acid sulfate soils develop as
The combined effect of proton and electron pumping pyrite oxidation leads to strong acidification (Dent
is to confine most soils within an envelope in Eh-pH 1993; Husson et al. 2000b).

Fig. 4 Pourbaix diagram

representing soil type
distribution as a function
of the pH and Eh. Adapted
from Chesworth et al.
(2004), Snakin et al. (2001),
Dent (1993), Husson et al.
(2000b) and Macias and
Camps Arbestain (2010)
Plant Soil (2013) 362:389–417 403

Eh, pH, and environmental issues dispersion, dilution, sorption, evaporation, and/or chem-
ical and biochemical stabilization of pollutants (Von de
In general, the concentration of heavy metals and Kammer et al. 2000).
pollutant metalloids in the soil solution is influenced In most soils, production or consumption of the three
by the combination of soil Eh and pH. Cadmium (Cd) major greenhouse gases (nitrous oxide N2O, methane
and lead (Pb) concentrations are low at a low Eh and CH4, carbon dioxide CO2) in oxidation-reduction reac-
rise when the Eh increases, which can be attributed to tions is regulated by interactions between the soil Eh,
interactions with dissolved organic carbon and man- the carbon source, and electron acceptors such as O2,
ganese and precipitations such as sulfides (Frohne et Mn4+, Fe3+, nitrate, sulfate or hydrogen (Li 2007). Other
al. 2011; Stepniewska et al. 2009). Cd solubility factors such as temperature, moisture, and pH can also
decreases with organic matter inputs because of the affect the biochemical or geochemical reactions related
induced decrease in Eh and the increase in pH to soil N2O, CH4 or CO2 emissions (Li 2007).
(Kashem and Singh 2001). Conversely, the concentra- The CH4 formation process and emission are con-
tions of the various forms of arsenic (As) and antimo- trolled by Eh and pH (Wang et al. 1993). N2O emis-
ny (Sb) sharply decrease when the soil Eh increases, sion is correlated with soil Eh (Kralova et al. 1992;
indicating that low Eh promotes the mobility of these Masscheleyn et al. 1993; Wlodarczyk et al. 2003; Yu
compounds (Frohne et al. 2011). and Patrick 2003), and with soil pH as pH influences
In its oxidized form (Hg2+ ions), mercury is highly the three most important processes that generate N2O
soluble but easily adsorbed by organic matter. In the and N2: nitrification, denitrification, and dissimilatory
presence of sulfur and at a low Eh (<−100 mV), Hg NO3- reduction to NH4+ (Simek and Cooper 2002). Eh
can precipitate as insoluble HgS. Hg is highly soluble and pH also interact in determining N2O and CH4
and toxic as methylmercury, which is only produced emission: the Eh range with minimum N2O and CH4
by methylating microorganisms, especially Clostridium production shifts to lower values of the Eh scale when
spp., which develop within a given Eh-pH range, with pH increases (Yu and Patrick 2003).
Eh between −400 mV and +100 mV (Billen 1973).
Furthermore, oxidation-reduction reactions control
the transformation and reactivity of Fe and Mn oxides, Soil Eh-pH and agronomy
which have a high capacity to adsorb heavy metals and
pollutant metalloids and are major sinks for these Eh and pH measurement
pollutants (Huang and Germida 2002).
Oxidation-reduction reactions largely drive biore- One of the major difficulties in using Eh and pH in
mediation processes. For instance, humic acids are agronomy lies in the measurement of these parame-
electron acceptors enabling anaerobic microbial oxi- ters, especially the Eh in aerobic soils. Literature on
dation of vinyl chloride and dichloroethene (Bradley the subject is sometimes controversial, as shown by
et al. 1998). Atrazine biotransformation is also oxida- numerous reviews (Bartlett and James 1993; De Mars
tion, enhanced by Mn and inhibited by antioxidants and Wassen 1999; Fiedler et al. 2007; Gantimurov 1969;
(Masaphy et al. 1996); this biotransformation is ex- Greenland and Hayes 1981; Kaurichev and Orlov 1982;
tremely rapid in oxidized soils (Eh>392 mV). It is Kovda 1973; Rabenhorst et al. 2009; Snakin et al. 2001;
much slower in reduced conditions (Eh<169 mV), Unger et al. 2008; Zakharievsky 1967).
such as in wetland soils where atrazine can persist These reviews reported two main problems: (i) the
for months (DeLaune et al. 1997). quality and the reliability of the equipment, especially for
Eh can be used as an indicator of soil health during Eh, as different types of electrodes have been developed
remediation processes and as an indicator of the rate of and as leaks or polarization of the electrodes can occur
remediation of a soil contaminated with polycyclic and distort the measurements; and (ii) the high spatial
aromatic hydrocarbons (Owabor and Obahiagbon and temporal variability of soil Eh and pH, and conse-
2009; Ugwuegbu et al. 2001). The redox poising ca- quently, the limited reliability of sampling and analysis
pacity can also be used as a tool for assessing long-term methods, which needs to be carefully addressed.
effects in natural attenuation/intrinsic remediation, Protocols are needed that ensure the reliability of
based on processes such as biological degradation, measurements and their sound interpretation, on the
404 Plant Soil (2013) 362:389–417

appropriate scale. Major progress has been made in the geochemistry or hydrobiology. In geochemistry, a study
development of Eh electrodes since Remezov mea- on over 6,200 pairs of measurements showed two inter-
sured the Eh in soil for the first time in 1929. Recom- esting results: (i) the Eh and pH of an environment such
mendations have been developed for the selection and as soil or water can be used to characterize that environ-
utilization of Eh electrodes (Fiedler et al. 2007; Snakin ment in many ways; and (ii) the Eh-pH characteristics of
et al. 2001). However, careful attention should still be natural environments are determined mainly by photo-
given to minimize the risk of measurement distortion synthesis, respiration, and redox couples of iron and
and proper characterization of the variability of Eh and sulfur (Baas Becking et al. 1960).
pH is still needed to standardize sampling and mea- In agronomy, Eh-pH diagrams are classically used
suring methods on various scales. for studies of submerged soils, especially paddy fields.
Furthermore, Eh and pH are not independent. For In such rapidly changing environments, Eh and pH are
example, in anaerobic soils, soil Eh increases with essential parameters, and Pourbaix diagrams are useful
acidification, and decreases with alkalinization (Van tools for understanding their chemistry (Ponnamperuma
Breemen 1987). On this basis, the pH at which this Eh 1972). In contrast, studies of Eh in aerobic soils are rare.
has been measured should be systematically mentioned. Despite their scarcity, studies of Eh in aerobic soil
A striking feature of this Eh literature review was that conditions have shown that Eh could be a useful
studies only occasionally associate the Eh with the pH, agronomic tool for characterizing field conditions. In
and they rarely pay attention to the possible interaction one of the few studies, Snakin et al. (2001) used the Eh
between Eh and pH in the processes studied. Under such and pH of the soil liquid phase as ecological indica-
conditions, comparisons between studies are difficult, tors. Using Eh-pH diagrams, these authors were able
which partly explains why Eh has not received sufficient to separate environmental entities into various groups
attention in agronomic studies. by: (i) ecosystem type: agricultural, grassland, and
Finally, Eh does not uniquely reflect electron activ- forest communities; (ii) vegetation type: coniferous,
ity, as it is also linked to proton activity (Fougerousse broad-leaved, meadow, meadow-steppe, and steppe
1996; Orszagh 1992). For a more effective character- vegetation; and (iii) soil type: podzolic, grey forest,
ization of oxidation-reduction, the chemical notion of chernozem, and chestnut soils (separately for agricul-
rH2 has been used in various disciplines linked to tural and natural communities). They also used Eh-pH
living organisms, including biological physics diagrams to characterize the distance between agricul-
(Deribere 1949; Fougerousse 1996; Huybrechts 1939; tural soils and the initial virgin milieu, represented by
Orszagh 1992; Rabotnova and Schwartz 1962; Vincent a vector.
1956; Vlès 1927; 1929). rH2 is defined in analogy with
pH, as –log[H2] , where [H2] is the thermodynamic Impacts of agricultural practices on soil Eh and pH
activity of molecular hydrogen that would be formed
following electron exchanges between water and solute Four main agricultural practices can affect soil Eh and
species (Orszagh 1992). In agronomy, some authors pH: application of soil amendments (organic or chem-
proposed using the pe concept (electronic potential), icals), water management, land preparation, and crop
defined as –log[e-] where [e-] is the hypothetical activity rotation. Amendments with lime and/or organic matter
of electrons (Lindsay 1979; Sillen and Martell 1964; are commonly used to alter soil pH (Brady and Weil
Sposito 1989; Stumm and Morgan 1981; Truesdell 2010; Whalen et al. 2000). Various methods have been
1969). pe+pH was also proposed as a redox parameter proposed to correct soil pH by liming, especially in
for soils (Lindsay 1983). The most appropriate way to response to Al toxicity (Dietzel et al. 2009). Herbel et
characterize oxidation-reduction is still a question which al. (2007) proposed to poise soil Eh using chemicals
needs to be addressed. such as NaNO3 or Mn oxyhydroxides.
In addition to practices specifically designed to
The application of Eh-pH diagrams correct undesirable soil chemical characteristics, the
use of agrochemicals has an influence on the Eh and
Since their first application to the earth sciences by pH. For instance, fertilizers such as superphosphate
Krumbein and Garrels (1952), Pourbaix diagrams have are acidifying, and others such as Thomas slag are
been used in other sciences such as soil chemistry, alkalinizing. Oxidation of urea or ammonium sulfate
Plant Soil (2013) 362:389–417 405

by microbes produces strong inorganic acids (Brady soil they grow in, and given the cross-species corre-
and Weil 2010). Herbicides also induce oxidative spondence of green leaf pH and leaf litter pH, plant
stress (Blokhina et al. 2003): for instance, paraquat species can alter the pH of the soil they grow in
(1,1'-dimethyl-4,4'-bipyridinium dichloride) is an oxi- (Cornelissen et al. 2011).
dant herbicide, operating by stimulation of superoxide
production in organisms (Cocheme and Murphy 2009).
Irrigation and drainage greatly affect soil Eh and Possible modification of rhizosphere Eh and pH
pH. Soil saturation reduces oxygen diffusion through by plants and microorganisms towards an
soils as the diffusion coefficient of oxygen through optimum physiological level
solution is about 10,000 times slower than diffusion in
the gaseous phase (Stolzy and Letey 1964). When It has been recognized for many years that plant energy
microorganisms consume oxygen for respiration, this use and metabolism contributes to internal pH homeo-
leads to a rapid decrease in soil Eh (Flessa and Fischer stasis (Kurkdjian and Guern 1989; Rengel 2002). A
1992a; Lambers et al. 2008). The pH tends toward recent ecological study of 23 herbaceous plant species
neutral conditions under continuous flooding: the pH showed that leaf pH is independent of bulk soil pH and
of acidic soils will increase whereas the pH of alka- suggested that tissue pH itself is tightly controlled for
line soils decreases (Glinski and Stepniewski 1985; any given species, because of its direct or indirect func-
Ponnamperuma 1972). tions in the plant (Cornelissen et al. 2011). From the
Land preparation also affects soil Eh and pH, mainly perspective of this review, I can put forward a wider
because by altering soil structure. Bulk density and ag- hypothesis: since physiological processes in plant cells
gregate size greatly influence soil water desorption and only operate properly within a fairly narrow and specific
the depth of soil to which O2 could diffuse (Grable and Eh-pH range, plants develop mechanisms to ensure their
Siemer 1967). Soil management affects pores' continuity cells' homeostasis at an optimum Eh-pH level. Alter-
and the hydraulic, gas, and heat fluxes (Horn and Peth ation of the Eh and pH conditions in their near environ-
2009). Reduction in the number of conducting coarse ment, i.e., in the rhizosphere, is part of the complex
pores leads to anoxic conditions (Horn and Peth 2009). interacting processes that have evolved to ensure plants'
On grey soils, Snakin et al. (2001) measured a significant internal Eh and pH homeostasis and, consequently, their
Eh gradient between horizons in natural forests, but not cell physiological processes.
in cultivated fields. Using an Eh-pH diagram, these The available literature already indicates that the Eh
authors could separate agricultural land from grassland and pH values in the rhizosphere converge toward 'ideal'
and from forest communities. In four soils, from sand to Eh-pH values, especially around root tips. For instance, in
loam, Czyz (2004) showed that soil compaction reduced conditions, rice roots were able to raise the Eh
decreases soil aeration and lowers the Eh. Soil tillage from +120 mV in bulk soil to +420 mVat the root surface,
modifies soil aeration and affects the Eh in the surface influencing the soil Eh up to 4 mm from the root surface
soil horizon, but also below the tilled zone, in interaction (Flessa and Fischer 1992a). Conversely, in oxidized con-
with rainfall (Clay et al. 1992; Olness et al. 1989). ditions, the root tips of soil-grown faba bean (Vicia faba
The type of plants cultivated and their sequence in L.) induced an Eh decrease from +700 mV to +380 mV
the crop rotation influences soil Eh and pH for two when they reached the microelectrode (Fischer et al.
reasons: (i) plants and their associated microorganisms 1989). For pH also, it is noteworthy that plants behave
play a crucial role in the formation and alteration of as if their roots are avoiding either too low or too high a
soil (Lambers et al. 2009); and (ii) plant biomass pH level around themselves (Hinsinger et al. 2003). A pH
production and inputs to the soil influence soil organic rise in the rhizosphere as compared to bulk soil can be up
matter content, which buffers the Eh and pH of the to 2 pH units in acid soils (Hinsinger et al. 2003). Con-
bulk soil (Paustian et al. 1997). In the surface horizon versely, in alkaline soils, Chaignon et al. (2002) reported a
(0–30 cm) of an aerobic soil, Bohrerova et al. (2004) decrease in rhizosphere pH to 6.9.
measured significant soil Eh differences between crop- Unfortunately, Eh and pH are rarely studied in
ping systems, with a higher Eh on an alfalfa/wheat association, and information on initial soil Eh and
rotation than on a sugar beet/barley rotation. Further- pH is never given in studies on root exudation and
more, by creating a different leaf pH from that of the respiration. As a result, this hypothesis can neither be
406 Plant Soil (2013) 362:389–417

confirmed nor rejected from the available literature: plant species and the soil pH and other characteristics.
but it certainly needs to be tested. However, I believe that at a pH of 6.5 to 7, an Eh above
+450 mV to +500 mV is unfavorable, with a risk of
mineral deficiency (P, Mn, Fe), heavy metal toxicity
Issues for agronomists (Cd, Pb), and pathogen development.
These optimum Eh-pH values correspond to the
Characterization of an 'ideal' soil by its Eh and pH transition between the two major forms of N in the
soil, NO3- and NH4+ (Figure 1). It is well known that
I propose that Eh and pH can be used, in interaction, as for most plants, the highest growth is obtained with
relevant primary parameters to characterize a soil and mixed NO3- and NH4+ nutrition (Marschner 1995).
define what is an 'ideal' soil for a given crop. These Eh-pH values also correspond to a high avail-
The concept of an 'ideal' soil is not new. Various ability of all major plant nutrients and micronutrients
disciplines related to agronomy have proposed to char- (N, P, Mg, Mn, etc.), and to a minimum risk of toxicity
acterize an 'ideal' soil either (i) according to individual by heavy metals, metalloids, Al, or Fe. A soil with
parameters such as base-cation saturation ratio (Kopittke such 'ideal' Eh-pH characteristics would be in accor-
and Menzies 2007), moisture (Keen 1924), and capillary dance with optimum plant physiological conditions
pull (Hackett and Strettan 1928), or (ii) through integrat- and would provide all nutrients in a readily available
ed parameters (De Orellana and Pilatti 1999; Janssen and form, with a low risk of mineral toxicity. This 'ideal'
de Willigen 2006; Pilatti and de Orellana 2000). soil would also provide favorable conditions for de-
This review makes it possible to estimate an Eh-pH velopment of 'useful' soil microorganisms, and unfa-
domain of optimum conditions for plant growth vorable conditions for pathogens.
(Figure 5). The optimum pH for most cultivated plants In such an 'ideal' soil, energy use efficiency is at a
is 6.5 to 7, and rather favorable conditions for plant maximum to ensure cell homeostasis. Most photosyn-
growth are found between 5.5 and 8. The optimum Eh thetic products can thus be used for the metabolism
for plant growth is probably in the range of +400 to and growth of plants and associated microorganisms.
+450 mV. Below +350 mV, plant growth rapidly Plant production is optimized, given that the resulting
decreases. The upper Eh limit is difficult to determine high biomass production generates C fluxes in the soil,
with available information, but also it may vary with more humus formation, and development of useful

Fig. 5 Synthesis of agro- Eh (V)

nomic constraints and 1.0
estimation of optimum PO
2=
1ba
conditions for plant growth r
depending on soil Eh
and pH 0.8
Acid
i andd Alkaline
A n andd
d d
oxidized Cd, NNi, Zn, Pb toxicity
i i
oxidized
Insects
n NO3 --N
N
0.6 Pathogenic
g fungi
u Viruss
& bbacteriaa
Favorable
F
All toxicity
t
ty
0.4 o
conditions

NH4+-N

0.2 Mn, Fe,

F As, S toxicity
i

i and
Acid d N2O emission A l
Alkaline n
and
d d
reduced u
reduced
0.0 CH
H4, H2S toxicity

PH
2=
1ba
r
-0.2
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
pH
Plant Soil (2013) 362:389–417 407

microorganisms. These fluxes and microorganisms law analogy is used in many situations in biology and
contribute to the buffering of the soil's Eh and pH at ecology as for example Fick’s law of diffusion.
favorable levels. The soil/plant/microorganism system By analogy, in soil/plant/microorganism systems the
is thus efficient and stable. electrical resistivity can be regarded as the resistance in
It can be expected that the more distant that soil Eh- Ohm’s law. Electrical conductivity (EC), the inverse of
pH is from an optimum physiological Eh-pH, the the resistivity, can be regarded as the diffusivity in Fick’s
higher will be the energy cost for plants to ensure their law.
cells' homeostasis. When soil Eh-pH is very different Soil electrical resistivity has been used for over a
from the optimum physiological Eh-pH, the capacities century to characterize a milieu, and its use has inten-
of the plant to maintain the soil Eh and pH at a sified since the 1970’s. Today, it is used in precision
favorable level can be overloaded. agriculture as a very attractive indicator to characterize
Physiological dysfunctions in reduced environ- soil (Samouëlian et al. 2005). This non-invasive mea-
ments have been widely recognized and studied, espe- suring technique enables researchers to characterize
cially for rice crops (Ponnamperuma 1972; Yoshida various soil properties, such as the cation exchange
1981). What has less been acknowledged is that two capacity (CEC), salinity, nutrients, residual humidity
processes sustain and increase these reduced condi- and preferred water flows, soil texture and properties
tions in a vicious circle: (i) very slow mineralization in related to texture (sand layers, impermeable clay
the absence of oxygen and under unfavorable condi- layers, etc.), bulk density, and compaction areas or
tions for the microorganisms involved in mineraliza- organic matter (Paillet et al. 2010; Samouëlian et al.
tion processes; and (ii) buffering of the Eh at low 2005). For instance, soil resistivity decreases when
levels by anaerobic microorganisms which preferen- bulk density increases, especially when soil water
tially develop in these conditions. content is low (Richard et al. 2006; Seladji et al.
Similarly, above an Eh threshold estimated at+ 2010). Electrical resistivity is also used to estimate
450 mV to+500 mV, four processes sustain and increase the level of soil weathering (Son et al. 2010).
the Eh in a reinforcing circle: (i) low energy efficiency at This suggests that using soil electrical resistivity in
high Eh leads to slow plant growth and low biomass addition to Eh and pH could be very useful. The
production; (ii) consequently, leaf area and solar energy description and the understanding of the functioning
interception are limited, and the reduction capacity of of soil/plant/microorganism systems could be im-
the plant is kept low; (iii) low biomass production also proved by calculating derived parameters such as in-
leads to losses in organic matter, all the more so as tensity. In animal production, the use of resistivity to
highly oxidized conditions favor mineralization calculate an intensity proved to be successful to ana-
(Chesworth 2004; Macías and Camps Arbestain 2010); lyze farm animals by analogy with electrical circuits
and finally (iv) low organic matter content in the soil (Aneshansley and Gorewit 1991; Rigalma et al. 2009).
leads to a low poising capacity and a rise in Eh. In aquaculture, it is appreciated that Eh, pH, and
resistivity are strong drivers for fish, shellfish, or oys-
Use of resistivity to characterize a soil ter production. They have been integrated in a soft-
ware (Vortex 2008–2011, designed by the French firm
This review makes clear the importance of Eh, an elec- Idee-aquaculture) used on a large scale to pilot aquacul-
trical potential, in soil/plant/microorganism systems, in ture ponds. This raises two questions for agronomists:
accordance with the perception of Szent-Gyorgyi (1960) (i) is such an analogy valid for plant production? and (ii)
that “what drives life is a little electric current.” It do Eh, pH, and resistivity capture the essential informa-
suggests that soil/plant/microorganism functioning tion needed to characterize systems as complex as soil/
could be regarded as an electrical circuit. plant/microorganism systems?
In physics, the functioning of an electrical circuit
cannot be described using only its voltage (V, in Volts). An Eh-pH-resistivity perspective: new insight
Its resistance (R, in Ohms) is also needed. Ohm’s law in agronomy
(I0V/R) allows to calculate the intensity (I, in Amperes),
an essential parameter characterizing the flow of elec- This integrated review had brought together converg-
trons in a conductor or ions in an electrolyte. An Ohm’s ing evidence from several disciplines that Eh, pH, and
408 Plant Soil (2013) 362:389–417

resistivity are fundamental parameters that can be leading to consequent yield decline. The good results
integrated into a revealing conceptual model of soil/ obtained by SRI techniques (System of Rice Intensi-
plant/microorganism system functioning. If this model fication) may also be explained by the maintenance of
is validated, and it becomes accepted that an 'ideal' soil a favorable soil Eh-pH when alternating irrigation and
can be defined by Eh, pH, and resistivity for a drainage (Stoop et al. 2002).
given crop, this analytical perspective could open Furthermore, this new perspective could help ex-
up avenues for new investigations and could gen- plain an increase in fungal diseases when pesticides
erate scientific advances in various disciplines are used, as reported for Fusarium sp. pathogens with
connected to agronomy. glyphosate (Fernandez et al. 2009). Pesticide applica-
For instance, this framework could be used to tion leads to oxidative stress in plants, which may
analyze Genotype x Environment x Management create favorable conditions for pathogenic fungi. This
(GxExM) interactions. Under this perspective, framework also supports the trophobiosis theory of
GxExM interactions could be explained by assess- Chaboussou (1985) that physiological dysfunction in-
ing varietal differences under optimum physiolog- duced by hydric stress and/or application of chemical
ical Eh-pH, considering their ability to sustain inputs favors insect or pathogens attack: these stresses
homeostasis in relation with the initial bulk soil are related to pH and/or to oxidative stresses as
Eh-pH and management practices. most chemical fertilizers and pesticides are oxi-
This conceptual model of soil/plant/microorganism dants (Bressy 1996).
systems could also provide a sound framework to In addition, this new framework for analysis of soil/
explain the high variability of rhizodeposition found plant/microorganism systems could help in bridging
in the literature: it predicts that rhizodeposition should the gap between chemistry-physics and biology and
be a function of initial bulk soil Eh-pH and of man- may be a useful tool for the integration between dis-
agement practices, which are not considered so far in ciplines, which is needed for the development of new
studies on rhizodeposition. perspectives in agronomy (Jones et al. 2004). Sparks
Furthermore, this conceptual model proposes some (2001), for instance, regards the studies of microbe-
new insights on the role and importance of soil organic driven redox reactions and redox transformations of C,
matter, especially in upland agriculture: organic matter N, P, and S according to various redox limits as new
poises the Eh and pH at favorable levels, which reduce frontiers of research at the interface between chemistry
the energy cost for plants to ensure their Eh-pH ho- and biology.
meostasis. This could also explain the variability in Similarly, this new framework could help in tran-
fertilizer efficiency and the phenomenon of hysteresis scending the constraints of scale. The lack of perspec-
during soil productivity restoration (Tittonell et al. tive across scales is a major limit for research, and
2008). Low organic matter content, and thus oxidized major progress will be achieved if scientists are able to
soil conditions, leads to low fertilizer efficiency in the bridge across micro and macro scales, from the rhizo-
short term because plants have to release a large share sphere of individual roots to soils at field scale and
of their photosynthetic production as root exudates to larger (Hinsinger et al. 2009). In a systemic approach,
adjust the Eh in the rhizosphere and ensure cell an average value of a parameter for a system (studied
homeostasis. at one particular scale) is determined by interactions of
This integrative perspective on the importance of the various sub-systems composing that system (on a
the Eh in soil/plant/microorganism systems may also finer scale).
help explain both: (i) the success of the Green Revo- Understanding the structure and the origin of the
lution in Asia under the reduced conditions of flooded variability of essential parameters such as Eh and pH
paddy fields because the oxidizing practices (land can help for scale transfers and also for understanding
preparation and soil aeration, mineral fertilization, processes across scales. For instance, understanding
chemical pesticide applications, etc.) rapidly raised the structure and the function of cell compartmentali-
Eh to a more favorable level; and (ii) the trend of zation for Eh and pH was crucial to understanding
declining yields in long-term experiments (Ladha et fundamental processes in cell physiology (Hansen
al. 2003) because the continued oxidizing practices et al. 2006; Scheibe et al. 2005). At another scale,
over long time periods may generate over-oxidation, Hinsinger et al. (2009) consider that it is urgent to
Plant Soil (2013) 362:389–417 409

improve the methodology for describing the physical microorganism interactions. The definition of opti-
architecture of the rhizosphere on a micro-scale and to mum ranges of soil Eh-pH-resistivity would help with
express these findings to interpret the data in respect of the design and management of cropping systems. The
their functional relevance. creation of a cropping system could then be based on
At a considerably larger scale, understanding the identifying plant species, microorganisms, and crop-
structure and the origin of the tremendous soil vari- ping practices that allow the development of favorable
ability in acid sulfate soils in Vietnam, in relation to soil conditions, using this optimum soil Eh-pH-
Eh and pH, proved to be a major step for designing resistivity as a 'target' zone.
more efficient cropping systems (Husson et al. 2000a; Insights from this analytical perspective could es-
Husson et al. 2000b). Furthermore, in environmental pecially contribute to planning 'ecological intensifica-
biotechnology, following electrons as they move tion' of agriculture, which is defined as the use of
through the ecosystem is regarded as the surest way biological regulation in agroecosystems both to
of translating knowledge about structure and function achieve a high level of food production and to provide
into practice (Rittmann 2006). ecosystem services (Dore et al. 2011). For instance,
Eh-pH-resistivity parameters might be used to develop
Translating soil Eh, pH, and resistivity into production rhizosphere-driven selection of microbes to improve
potential the development and health of plants, which has been
suggested as a major challenge for agronomy for the
Is it possible to translate the information provided by future of sustainable agriculture (Hartmann et al.
the three parameters Eh, pH, and resistivity of the soil 2009).
into a production potential for plants, in relation to Such an approach has been rarely, and only very
plant physiology? The production potential of a given partially, used by agronomists to correct the soil Eh for
crop is mainly determined by climatic factors such as various purposes. Carter (1980) used Eh assessments
temperature, water and sunlight, and by soil character- to pilot drainage for sugarcane production; Savich et
istics. I believe that Eh, pH, and resistivity can con- al. (1980) proposed to use oxidants such as KMnO4,
siderably improve the characterization of a milieu, and NaClO4 or Fe2O3 to regulate the Eh; Patsoukis and
thus produce a useful evaluation of the production Georgiou (2007b) used sulfites and nitrites as cytotox-
potential of a soil. However, a major challenge for ic oxidants to sustain fungi in their undifferentiated
agronomy will be to determine the optimum Eh-pH- hyphal stage, in which they are more vulnerable to
resistivity of a soil, to maximize the production poten- degradation by soil microorganisms; Blok et al. (2000)
tial of a plant as a function of climate. and Shinmura (2004) introduced easily decomposable
One major question remains regarding the relation- organic material and flooded or covered the soil with
ship between these parameters and a production poten- airtight plastic to reduce the Eh and control Fusarium
tial for a given soil. Interactions between the climate and oxysporum and Rhizoctonia solani. Takehara et al.
these parameters have to be assessed, particularly tem- (2004) used allelopathic plants to lower the soil Eh
perature, as it affects the Eh, pH, resistivity and kinetics and control soil-borne pathogens.
of biochemical reactions, and microorganism develop- Such practices could be largely improved if Eh, pH,
ment probably has a major impact. Optimum soil Eh- and resistivity were integrated to improve soil charac-
pH-resistivity for plant production is very likely to be a terization and identify optimum conditions, which
function of temperature, and to vary according to cli- could be used as 'target' zones, as is done in aquacul-
mate, with rainfall affecting not just water but also ture. Scientific development of such approaches will
oxygen availability in the soil. require intensive knowledge on specific optimum soil
Eh-pH-resistivity values for plants and microorgan-
isms, and on how the various species alter these
Conclusions: Eh, pH, and resistivity as tools parameters. If this proposed framework for soil/plant/
for designing and managing cropping systems microorganism systems is validated, a major challenge
for agronomists of different disciplinary orientations
This framework and the improved soil characterization will be to develop such knowledge further and trans-
it provides could be a tool for modeling soil/plant/ late it into sound agricultural practices.
410 Plant Soil (2013) 362:389–417

Acknowledgements I would like to thank Prof. Alain Capillon, Bayliss NS (1956) The thermochemistry of biological nitrogen
Prof. Norman Uphoff, Fabrice Dreyfus and Cécile Fovet-Rabot for fixation. Aust J Biol Sci 9:364–370
their support and the many comments that they made to improve Becker B, Holtgrefe S, Jung S, Wunrau C, Kandlbinder A, Baier
the manuscript, and also my colleagues in the SIA research unit at M, Dietz KJ, Backhausen JE, Scheibe R (2006) Influence
CIRAD for enduring the many discussions on redox potential. of the photoperiod on redox regulation and stress responses
Thanks also go to Peter Biggins for revising the English. Finally, I in Arabidopsis thaliana L. (Heynh.) plants under long- and
deeply thank the anonymous reviewers for their very constructive short-day conditions. Planta 224:481–481
comments. Best EJ, Samuel G (1936) The reaction of the viruses of tomato
spotted wilt and tobacco mosaic to the pH value of media
Open Access This article is distributed under the terms of the containing them. Ann Appl Biol 23:509–537
Creative Commons Attribution License which permits any use, Billen G (1973) Etude de l'écométabolisme du mercure dans un
distribution, and reproduction in any medium, provided the milieu d'eau douce. Aquat Ecol 7:60–68
original author(s) and the source are credited. Bisio G, Bisio A (1998) Some thermodynamic remarks on
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