Glyphosate interactions with physiology, nutrition, and diseases of plants: Threat to agricultural sustainability?

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Europ. J. Agronomy 31 (2009) 111–113
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Preface
Glyphosate interactions with physiology, nutrition, and diseases of plants: Threat
to agricultural sustainability?
The transition from biologically based to intensive, chemical-
based agricultural production systems advanced in North America
and Europe soon after World War II as inorganic fertilizers and
organically synthesized pesticides became widely available. This
modern or conventional-type agriculture was adopted by other
major crop production areas throughout the world with a sharp
increase in adoption generated by the input-intensive “Green Rev-
olution” of the 1960s and 1970s. In general, conventional cropping
systems are characterized as large-scale production enterprises
that utilize high-yielding crop varieties often in monoculture or
short-term rotations planted on the most fertile, productive soils
available with high inputs of chemical fertilizers and pesticides. Lit-
tle emphasis is given to managing soil organic matter through use
of traditional legume-based rotations, cover crops, or organic soil
amendments that are central to maintaining the biological activity
and inherent fertility of soils in biologically based cropping systems.
By abandoning the biological management component, many con-
ventionally managed fields have experienced severe disease, insect,
and weed infestations (Drinkwater et al., 1995); serious declines
in soil organic matter, nitrogen, and carbon contents (Khan et al.,
2007); and alterations in the balance of beneficial and detrimental
biological activities due to drastic changes in soil and rhizosphere
microbial communities (Dunfield and Germida, 2004).
One of the most significant inputs necessary for successful
conventional crop production are herbicides for management of
the variety of weed infestations especially encountered in row-
cropping systems. This technology was rapidly adopted because
most weeds could be controlled when matched with selective her-
bicides, which were compatible with the crop, and was considered
more cost-effective than cultural methods of weed management.
Glyphosate, the active ingredient in the herbicide Roundup, became
very popular after introduction in the 1970s for non-selective
weed control in fallowed fields and non-cropped areas of orchards,
vineyards, and timber plantations. The development of no-tillage
systems (“no-till”) for row-cropping systems greatly expanded
the use of glyphosate as it became standard practice to apply
glyphosate to growing vegetation in fields prior to planting. This
“burndown” application eliminated the need for tillage and allowed
farmers to plant crop seeds directly into soil beneath a mulch of
dead plant residues. The no-till practice contributed to reductions
in soil erosion and energy consumption for field preparation and
to expansion of grain production (primarily corn and soybean) in
many areas suitable for row-cropping throughout the world.
Although glyphosate is the most widely used herbicide
worldwide (Woodburn, 2000), several problems associated with
glyphosate interactions with plant nutrient availability, transfer
to and effects on susceptible crops, indirect effects on rhizo-
sphere microorganisms and plant pathogens, and development of
glyphosate-resistant weeds have raised serious concerns regard-
ing the sustainability of cropping systems in which glyphosate is
the primary weed management strategy. Within this context it
was our mandate to assemble a selection of papers for submis-
sion to European Journal of Agronomy. This Special Issue contains
peer-reviewed papers based on contributions presented at the
international symposium on “Mineral Nutrition and Disease Prob-
lems in Modern Agriculture: Threats to Sustainability?” held in
Piracicaba-SP, Brazil, 20–21 September 2007. The symposium,
organized by Dr. T. Yamada of the International Plant Nutrition
Institute-Brasil (IPNI) continued discussions of issues presented
in a previous symposium on herbicide impacts on plant nutrition
and disease convened in 2005 and was held under the auspices
of IPNI, The Agrisus Foundation – Sustainable Agriculture, ESALQ-
University of Sao Paulo, and European Society of Agronomy.
The strategic location of Piracicaba was ideal for convening a
symposium on experiences with nutrition and disease problems in
modern agriculture. Sao Paulo is among Brazil’s leading states in
land use devoted to sugarcane, citrus, and coffee plantations; the
majority of these enterprises are managed following modern and
intensive management, which include use of glyphosate to man-
age vegetation in these perennial crops. To the south, in subtropical
southern Brazil, no-till agriculture was developed to reduce exten-
sive soil erosion resulting from intensive row-cropping; adoption
of no-till accelerated with the introduction of glyphosate to Brazil
in the mid-1970s. To the north in the tropical savannah region
(cerrado) of central Brazil, no-till was introduced in the 1980s as
large farms devoted to soybean, cotton, and maize were established
(Bolliger et al., 2006). After many years of frequent applications
of glyphosate in both plantation and row crops in Brazil, several
problems in plant health and productivity developed, which are
representative of similar situations encountered in conventional
cropping systems all over the world.
A basic understanding of the behavior of glyphosate in plants
and the environment is necessary to set the foundation for the
investigations upon which the Symposium was based. The mode
of action, or the sequence of events leading to plant injury
and/or destruction after herbicide treatment, has been described
in numerous reports as the binding of glyphosate with and inacti-
vation of 5-enolpyruvoylshikimate-3-phosphate synthase (EPSPS),
the critical enzyme in the shikimate pathway required for synthesis
of a variety of aromatic plant metabolites including essential amino
1161-0301/$ – see front matter. Published by Elsevier B.V.
doi:10.1016/j.eja.2009.07.004

112 Preface / Europ. J. Agronomy 31 (2009) 111–113
acids, phenylalanine, tryptophan and tyrosine (Franz et al., 1997).
Tryptophan is necessary for the synthesis of indolylacetic acid (IAA),
the main growth promoter, that can explain the widespread field
observation of reduced in depth root growth of plants. Because a
single, specific enzyme restricted to one plant metabolic pathway
is inactivated by the herbicide resulting in eventual plant death,
glyphosate was proclaimed as environmentally friendly (Franz
et al., 1997). Additional standard assays identified other general
properties of glyphosate including immobilization by soil colloids
and organic matter and rapid degradation by soil microorganisms,
which suggested the herbicide posed no adverse impacts on the
environment or toward desirable plants.
More intensive evaluations revealed that glyphosate was
translocated within plants, accumulated in roots, and was even-
tually released into the rhizosphere (Coupland and Casely, 1979).
Subsequent research on glyphosate interactions with soil microor-
ganisms demonstrated that although glyphosate was metabolized
by a segment of the microbial population, it was also toxic to sev-
eral bacteria and fungi; the net effect of glyphosate appeared to
be a disruption of soil and root microbial community composition
because selected components of the microbial community were
stimulated while others were suppressed (Wardle and Parkinson,
1992; Busse et al., 2001). Interestingly, many studies showed that
glyphosate was not entirely and immediately immobilized by soil
colloids because a portion was available for metabolism by soil and
rhizosphere microorganisms (Haney et al., 2000). In the 1980s, Rahe
and coworkers documented that severe root infection associated
with glyphosate-treated plants was due to disruption of synthesis
of plant defense compounds, or phytoalexins, through the shiki-
mate pathway thereby predisposing plants to attack by soilborne
fungal pathogens (Johal and Rahe, 1988; Lévesque et al., 1987).
Thus, infection by soilborne pathogens caused by the inability of
plants to synthesize phytoalexins contributed to the overall her-
bicidal efficacy of glyphosate and was considered a “secondary
mode of action” of glyphosate. These findings were significant
because the release of glyphosate into the environment was found
to have considerably more and far-reaching effects than the orig-
inal notion that was limited to only the localized disruption of a
specific metabolic pathway within a target plant. As glyphosate use
increased in a number of agricultural systems, substantial evidence
accumulated on multiple adverse effects on crop health and pro-
ductivity and soil–plant–microorganism interactions mediated by
this herbicide.
Based on the concerns of multiple agricultural and environmen-
tal effects associated with widespread use of glyphosate during the
past decades, the Symposium was convened to present and dis-
cuss up-to-date research on problems of plant nutrition and disease
linked to glyphosate use, present and critique sustainable alterna-
tive management strategies, and propose future research efforts.
Key themes of the Symposium included interactions of glyphosate
with nutrient availability to crop plants; interactions of glyphosate
with plant pathogens and disease development in crop plants; and
impacts of glyphosate on plant nutrition and microbial interactions
in transgenic, glyphosate-resistant cropping systems (i.e., Roundup
Ready).
Each presenter addressed one or more of the key themes of the
Symposium. Römheld (Tesfamariam et al., 2009) reviewed the con-
sequences of glyphosate transfer to non-target (crop) plants via the
rhizosphere after herbicide application to target plants (undesir-
able vegetation). Evidence is provided that such transfer occurs
in orchards when weeds in alleys are sprayed with glyphosate,
which is subsequently released through the dying roots to be taken
up through the living roots of trees. This was demonstrated with
glyphosate-killed grass mulch simultaneously grown with citrus
saplings, which contained significantly high contents of shikimate
indicating glyphosate uptake by citrus from the dying grass roots
(Neumann et al., 2006). The cation-chelating ability of glyphosate,
which previously received little attention regarding impacts on
plant nutrition, was highlighted by several presenters as a criti-
cally important factor in nutrient deficiencies of crops observed in
production systems heavily reliant on glyphosate for weed man-
agement. Römheld and Cakmak (Cakmak et al., 2009; Senem Su et
al., 2009; Tesfamariam et al., 2009) discussed impaired micronu-
trient uptake and transport in plants exposed to glyphosate either
through root transfer or by simulated drift of sub-herbicidal rates
was due to the ability of glyphosate to form immobile stable com-
plexes with Fe and Mn (Eker et al., 2006; Neumann et al., 2006). The
possibility of interactive effects of glyphosate with other micronu-
trients was presented by Wood who suggested that the occurrence
of Ni deficiency in pecan (Bai et al., 2006) and other orchard replant
diseases might be exacerbated by release of glyphosate from killed
vegetation in orchards, which then complexes with Ni making it
unavailable for root uptake by trees.
Based on extensive field surveys and large-scale experiments,
Fernandez et al. (2009) demonstrated that previous glyphosate
applications (ranging from 18 to 36 months prior to planting) was
the most important agronomic factor in development of diseases,
primarily Fusarium head blight, in wheat and barley crops. Higher
Fusarium colonization of wheat and barley roots was also asso-
ciated with glyphosate burndown applications prior to planting
(Fernandez et al., 2007). An unknown but interesting aspect of
these observations is the apparent persistent effect of glyphosate
on plant growth two or more years after application. Huber (Johal
and Huber, 2009) reviewed various microbial interactions with
glyphosate including those documented for toxicity toward ben-
eficial microorganisms (i.e., rhizobia, Mn-reducers, mycorrhizae)
and stimulation of detrimental microorganisms (Mn-oxidizers,
pathogenic fungi). Through these interactions, glyphosate changes
nutrient availability and alters pathogen virulence to plants. Some
of the more notable diseases in which glyphosate might be impli-
cated include Corynespora root rot in soybean, Marasmius root
rot of sugarcane, citrus variegated chlorosis (Xylella fastidiosa),
and take-all (Gaeumannomyces graminis) in cereal crops. Many
of the pathogens causing these diseases are stimulated either by
glyphosate exuded from roots, by the altered composition of root
exudates caused by glyphosate treatment, or through a combina-
tion of both exudation processes.
The final key symposium theme addressed the impacts
of glyphosate on plant nutrition and microbial interactions,
and development of herbicide-resistant weeds in transgenic,
glyphosate-resistant (GR) cropping systems (i.e., Roundup Ready).
One of the most significant advancements in intensive agriculture is
the introduction of GR crops in the mid-1990s. By 2008 GR-resistant
soybean occupied 65.8 million ha (53% of the global area planted to
biotech crops), followed by maize (37.3 million ha at 30% of global
area), and cotton (15.5 million ha at 12% of global area) (James,
2008). The GR cropping system provided a more cost-effective
option for farmers, allowing them to spray a broad spectrum of
weeds with glyphosate on “as needed” basis and reducing the need
for pre and post emergence herbicides. However, the repetitive
and dedicated use of glyphosate within a growing season and over
the past decade has resulted in selection for resistance in several
weed species (Johnson et al., 2009) and development of similar crop
nutrition and health problems as those observed in non-GR sys-
tems. Previous findings that glyphosate and high concentrations
of soluble carbohydrates and amino acids were released in root
exudates of glyphosate-treated GR soybean (Kremer et al., 2005)
suggested that impacts on micronutrient uptake and root microbial
interactions might mirror those described for glyphosate interac-
tions in non-transgenic cropping systems. Indeed, presentations
at the Symposium indicated decreased uptake of micronutrients
and subsequent development of deficiency symptoms in some

Preface / Europ. J. Agronomy 31 (2009) 111–113 113
GR soybean cultivars (Tesfamariam et al., 2009; Johal and Huber,
2009); only limited information has been previously reported on
depressed uptake of Mn and Fe in GR soybean (Gordon, 2007; Jolley
et al., 2004), suggesting that genetic modification in the GR soybean
and/or glyphosate released into the rhizosphere affected micronu-
trient uptake. Valuable information on increased colonization by
potential fungal pathogens, increases in Mn-oxidizing microorgan-
isms, and decreases in beneficial bacterial populations (fluorescent
pseudomonads, rhizobia) in the rhizosphere of GR crops is pre-
sented to aid in understanding some of the production problems
often reported for GR-cropping systems (Johal and Huber, 2009;
Kremer and Means, 2009).
In summary, the Symposium provided a forum to bring together
a current understanding of the numerous factors – physiologi-
cal, nutritional, soil chemical, phytopathological, and biological
– that interact with glyphosate management whether situated
in conventional (plantation, orchard, row crops) or in transgenic
agroecosystems. This understanding is essential for developing
alternative approaches within management systems to overcome
the constraints to crop productivity and health. Some of the recom-
mendations that emerged from the Symposium included reducing
the use of glyphosate in perennial culture by using mulching sys-
tems to suppress weeds, which has been successful in many citrus
plantations in Brazil. Development of efficient methods for using
cover crops in annual crops for weed suppression and possible
increased availability of soil micronutrients was discussed. Sev-
eral approaches for improving productivity in GR cropping systems
included selection of cultivars with high Mn-uptake efficiency,
delayed application of micronutrients (Mn, Zn, Fe and Cu) after
glyphosate treatment, and cultural practices, including the use of
gypsum + Mo, and roller knife mulching that minimize glyphosate
impact on crops. The use of biological products such as those con-
taining the plant defense compound salicylic acid and amino acids
by foliar application to improve resistance to root pathogens was
also suggested. We trust that the articles in this Special Issue will
serve as valuable information sources for those interested in a bet-
ter understanding of the interactions of glyphosate with crop plants
and that this information will be used to develop more sustainable
agricultural production systems.
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Tsuioshi Yamada1(Guest Editor)
AgriNatura Agronomic Consulting, Piracicaba-SP, Brazil
Robert J. Kremer∗(Managing Guest Editor)
Cropping Systems & Water Quality Unit, USDA-ARS,
302 Natural Resources Bldg., University of Missouri,
Columbia, MO 65211, USA
Paulo Roberto de Camargo e Castro (Guest Editor)
ESALQ, University of Sao Paulo, Piracicaba-SP, Brazil
Bruce W. Wood (Guest Editor)
Southeast Fruit & Tree Nut Laboratory, USDA-ARS,
Byron, GA 31008, USA
∗Corresponding author.
E-mail address: kremerr@missouri.edu (R.J. Kremer)
1Retired from International Plant Nutrition
Institute, Brazil.