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Fungicide impacts on photosynthesis in crop plants


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Fungicides are widely used to control pests in crop plants. However, it has been reported that these pesticides may have negative effects on crop physiology, especially on photosynthesis. An alteration in photosynthesis might lead to a reduction in photoassimilate production, resulting in a decrease in both growth and yield of crop plants. For example, a contact fungicide such as copper inhibits photosynthesis by destroying chloroplasts, affecting photosystem II activity and chlorophyll biosynthesis. Systemic fungicides such as benzimidazoles, anilides, and pyrimidine are also phytotoxic, whereas azoles stimulate photosynthesis. This article focuses on the available information about toxic effects of fungicides on photosynthesis in crop plants, highlighting the mechanisms of perturbation, interaction, and the target sites of different classes of fungicides.
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Fungicide impacts on photosynthesis in crop plants
lle Petit
Florence Fontaine
Parul Vatsa
Christophe Cle
Nathalie Vaillant-Gaveau
Received: 27 March 2011 / Accepted: 12 January 2012 / Published online: 1 February 2012
Ó Springer Science+Business Media B.V. 2012
Abstract Fungicides are widely used to control pests in
crop plants. However, it has been reported that these pes-
ticides may have negative effects on crop physiology,
especially on photosynthesis. An alteration in photosyn-
thesis might lead to a reduction in photoassimilate pro-
duction, resulting in a decrease in both growth and yield of
crop plants. For example, a contact fungicide such as
copper inhibits photosynthesis by destroying chloroplasts,
affecting photosystem II activity and chlorophyll biosyn-
thesis. Systemic fungicides such as benzimidazoles, ani-
lides, and pyrimidine are also phytotoxic, whereas azoles
stimulate photosynthesis. This article focuses on the
available information about toxic effects of fungicides on
photosynthesis in crop plants, highlighting the mechanisms
of perturbation, interaction, and the target sites of different
classes of fungicides.
Keywords Chlorophyll Crop plants Fungicides
Photosynthesis Photosystems Physiology
Phytotoxicity Stomatal closure Stress
Fungicides remain a vital solution to the effective control
of plant diseases, which are estimated to cause yield
reductions of almost 20 percent in major food and cash
crops worldwide. The great variety of known fungicides
can be classified into two main categories: contact and
systemic. Contact fungicides, such as copper or sulfur have
a preventive action by killing fungi as their spores germi-
nate, before mycelia can grow and develop within plant
tissues (Yuste and Gostincar 1999). Since their introduc-
tion in the 1960’s, systemic fungicides have gradually
replaced older non-systemic products, establishing higher
levels of disease control and developing new fungicide
markets. Systemic fungicides, known as curative or eradi-
cation fungicides, can also kill the fungus when mycelia
have penetrated into the parenchyma, stopping the dis-
persal or infection within the plant (Table 1, Yuste and
Gostincar 1999). Among systemic fungicides, benzimi-
dazoles are a group of organic fungicides that are exten-
sively used in agriculture along with the other classes of
All these types of compounds control a broad range of
fungi at relatively low application rates. However, the
effects of fungicides on crop growth depend on various
factors. Application of fungicides may affect crop physi-
ology by various disruptions such as growth reduction,
perturbation in the development of reproductive organs,
alteration of nitrogen, and/or carbon metabolism leading to
a lower nutrient availability for plant growth. The sensi-
tivity of some plant species may depend on the develop-
mental stage (i.e. more sensitive to the treatments at young
stages or during critical events such as reproduction) or the
type of pesticides used.
It has been previously reported that in response to a
stress, plants often mobilize nutrients and metabolite pro-
duction to develop defense mechanisms in detriment to
growth (Smith and Moser 1985). Under stress conditions,
plants firstly trigger their defence response for their sur-
vival because of the energetic cost of resistance and
A.-N. Petit F. Fontaine P. Vatsa C. Cle
N. Vaillant-Gaveau (&)
Laboratoire de Stress, De
fenses et Reproduction des Plantes,
URVVC EA 2069, Universite
de Reims Champagne-Ardenne,
UFR Sciences Exactes et Naturelles, Ba
timent 18, Moulin de la
Housse, BP 1039, 51687 Reims Cedex 2, France
Photosynth Res (2012) 111:315–326
DOI 10.1007/s11120-012-9719-8
Table 1 Basic chemical characteristics of fungicides (data from International Union of Pure Applied Chemistry)
Structures Primary mode of action in fungus
Copper and/or sulfate
Bordeaux mixture
Inhibit several enzymes involved in respiration and this multi-site action
(Leroux 2003)
Inhibit several enzymes involved in respiration and this multi-site action
(Leroux 2003)
Inhibit several enzymes involved in respiration and this multi-site action
(Leroux 2003)
Inhibits spore germination and mycelial growth (Leroux et al. 2002)
QoI inhibitors, which act to inhibit the respiratory chain at the level of
Complex III (Grossmann et al. 1999)
Inhibits spore germination and mycelial growth (Zhang et al. 2010)
Perturbe the osmo-regulatory signal transmission pathway (Pillonel and
Meyer 1997)
Inhibits spore germination and mycelial growth (Leroux et al. 2002)
Inhibits germ-tube elongation and mycelial growth (Ha
nbler and Pontzen
A sterol biosynthesis inhibitor: inhibits the 3-keto reductase involved in the
enzymatic complex of the sterol C-4 demethylation (Debieu et al. 2001)
Inhibits spore germination and mycelial growth
Multi-site action (Teisseire et al. 1999)
Inhibit mycelial growth
Indirect effect against germination of zoosporangia, zoospore motility,
cystospore germination, and oospore formation
Impairment of the ATP energy generation system
Inhibit several enzymes involved in respiration (Mitani et al. 2001)
Inhibition of sterol biosynthesis at the 14a-demethylation step (Haughan
et al. 1988)
Sterol C-14 demethylation inhibitor (Debieu et al. 1995)
316 Photosynth Res (2012) 111:315–326
growth. The intensity of the stress induced by pesticide
application and the intensity of plant response will thus
have a subsequent impact on the growth process if the
crops overcome the stress. According to the growth
reductions observed after agrochemical exposures, plants
may react by developing this kind of metabolite reorien-
tation. Therefore, the plant carbon and/or nitrogen primary
metabolism, which regulates the plant growth rate, appears
necessary to be investigated in order to understand more
precisely how pesticides can affect the crops (Saladin and
ment 2005).
Carbon metabolism is of particular importance for crop
culture and is reflected by both crop’s photosynthetic rate
and its management of carbohydrate reserves. Indeed,
photosynthesis alteration may lead to a decrease in pho-
toassimilate production and thus to plant yield and vigour.
A negative effect of sulfur-containing fungicides (particu-
larly lime sulfur) was revealed on apple production by a
loss of fruits and a delay in harvest (Palmer et al. 2003).
However, spray treatments did not influence shoot growth,
leaf area development or increment in trunk cross-sectional
area. Fungicide application programme containing Kocide
or slaked lime or use of both together, demonstrated that
Black spot incidence (caused by Venturia inaequalis), on
fruit at harvest was significantly higher on trees treated
with either Kocide or slaked lime compared to the controls.
When used together, however, control of Black spot was as
good as in the control. Dry eye rot incidence (caused by
Botrytis cinerea) was significantly higher on the trees
treated with lime sulfur (Palmer et al. 2003). Another study
about the effect of lime sulfur applied at different stages to
apple trees reported leaf phytotoxicity, revealed as necro-
sis, and a reduction of yield in terms of first class fruits
(Holb et al. 2003).
As stress increases, various photosynthetic processes
may be impaired, leading to a decrease in net photosyn-
thesis (Pn), equivalent to CO
assimilation (Fig. 1).
Stomatal closure, caused by a reduction in stomatal con-
ductance (gs), is often considered as an early physiological
response to stress, resulting in decreased Pn through lim-
ited CO
availability (Ci) in the mesophyll (Krause and
Weis 1991). Photosynthesis is one of the most studied and
best understood physiological process. Detailed biochem-
ical models of photosynthesis, including light reactions,
electron and proton transport, enzymatic reactions, and
regulatory functions have been recently developed (Laisk
et al. 2006). Life on earth is driven essentially by photo-
synthetic solar energy conversion. Photosynthetic organ-
isms use light energy for the synthesis of organic
molecules. In the case of plants, algae, and cyanobacteria,
oxygen is emitted into the atmosphere as a by-product of
photosynthesis. Fundamental to the photosynthetic process
Table 1 continued
Structures Primary mode of action in fungus
Sterol C-14 demethylation inhibitor (Debieu et al. 1995)
Sterol C-14 demethylation inhibitor (Gaita
n et al. 2005)
Sterol C-14 demethylation inhibitor (Debieu et al. 1995)
Inhibition of microtubule assembly which is due to their binding to tubulin, the main
protein of microtubules (Leroux and Descotes 1996)
Inhibition of microtubule assembly which is due to their binding to tubulin, the main
protein of microtubules (Leroux and Descotes 1996)
Inhibits germ tube elongation and initial mycelial
Inhibit biosynthesis of methionine affecting cystathionine-b-lyase
Prevention of fungal secretion of hydrolytic enzymes (Fritz et al. 1997)
Photosynth Res (2012) 111:315–326 317
is the ability of plants to absorb light energy that is then
converted into chemical energy. Light energy is captured
by pigments in the light-harvesting complex (LHC) pro-
teins and transferred to the reaction centers of the chloro-
plast thylakoid membrane. LHC proteins bind to
chlorophyll a, chlorophyll b, and carotenoids with weak
non-covalent bonds. LHC are assembled into two separate
yet biophysically linked photosystems: photosystem I (PSI)
and photosystem II (PSII) (Hillier and Babcock 2001). PSII
catalyzes light-induced electron transfer from water to
plastoquinone. The oxygen-evolving complex, located on
the luminal side of PSII is responsible for water oxidation
and produces protons, electrons, and molecular oxygen as a
by-product (Krause and Weis 1991). The protons are
involved in the formation of adenosine triphosphate (ATP),
the plant stock of energy, through the ATPase. The elec-
trons run along a complex transfer chain ending with the
formation of another energetic molecule, nicotinamide
adenine dinucleotide phosphate (NADP). Then ferredoxin
is reduced by a photochemical reaction at the level of PSI,
and the ferredoxin–NADP
reductase enzyme mediates
electron transfer from this reduced protein to NADP with
the formation of NADPH necessary for CO
fixation. An
alteration of any one of these processes can lead to Pn
Fig. 1 Schematic representation showing the interactions of the main
processes in C3 photosynthesis in higher plants (according to Baker
and Rosenqvist 2004) and impacts of fungicides (North east increase
and South east decrease). Photophosphorylation starts with the
absorption of light by the light-harvesting antenna complexes (LHCI
and LHCII) associated with photosystem II (PSII) and photosystem I
(PSI) in the chloroplast thylakoid membrane. This drives electron
transport from water via a series of electron carriers to NADP,
producing reducing power (NADPH) and a H
potential difference across the membrane. Dissipation of this proton
motive force by the passage of H
back across the membrane through
the ATPase drives the production of ATP. Ribulose 1,5-bisphosphate
carboxylase/oxygenase (Rubisco) catalyses the assimilation of CO
with ribulose 1,5-bisphosphate (RubP) in the carboxylation reaction
of the Calvin–Benson cycle in the stroma of the chloroplast. The
diffusion of atmospheric CO
into the leaf is regulated by the stomata
in the epidermis. Other reactions of the Calvin–Benson cycle utilize
NADPH and ATP to produce triose phosphates, which are required
for the synthesis of carbohydrates. NADPH and ATP are also used in
a range of other metabolic activities (e.g. nitrogen and sulfur
metabolism, lipid and pigment synthesis) in the chloroplast. Rubisco
can also catalyse the photorespiratory oxygenation of RubP, which
involves consumption of NADPH and ATP by the Calvin–Benson
cycle. O
can also be directly photoreduced by electron transfer from
PSI to produce superoxide, which is then rapidly dismutated to
hydrogen peroxide, which in turn is detoxified to water; this process is
often termed the Mehler-peroxidase reaction or the water–water
cycle. Cyt b/f cytochrome b6/f complex; PC plastocyanin; PQ
plastoquinone; PQH
318 Photosynth Res (2012) 111:315–326
inhibition. ATP and NADPH are then necessary for the
second step, i.e., the energy-consuming reductive conver-
sion of CO
into carbohydrates. These latter reactions
follow a cyclic sequence called the Calvin cycle. The key
enzyme of the cycle, Ribulose 1,5-bisphosphate carboxyl-
ase/oxygenase (Rubisco), is a prerequisite for CO
and catalyzes the carboxylation of ribulose 1,5-bisphos-
phate (RuBP). There is a strong evidence that Pn might
thus be limited by other biochemical processes occurring in
the mesophyll, such as Rubisco activity and RuBP regen-
eration (Krause and Weis 1991).
Apart from affecting wide variety of crop plants, fungi-
cyanobacteria (blue-green algae). The effect of pesticides on
cyanobacterial populations has been considered to be stim-
ulatory at low concentrations and inhibitory at high doses.
The rates of photosynthesis and respiration along with
chlorophyll content have been shown to decline in the
presence of Bavistin, a broad spectrum fungicide, containing
50% WP carbendazim (Rajendran et al. 2007). Previously, it
has been demonstrated that carbendazim 50% WP is effec-
tive against a wide range of pathogenic fungi and is highly
specific in its control of important plant pathogens on a
variety of crops, ornamental plants and plantation crops.
Dewez et al. (2005) demonstrated that when alga Scenedes-
mus obliquus was exposed to different copper concentrations
significant inhibition on the growth rate and chlorophyll
synthesis was noticed. Phytoremediation with microalgae has
been utilized for areas polluted with nutrients or heavy metals
(Perales-Vela et al. 2006); however, increasing environ-
mental pollution by pesticides might lead to consider mic-
roalgae as good candidates to remove these contaminants
from water at low cost (Dosnon-Olette et al. 2010).
The aim of this review is to make a thorough account of
the current available information about impacts of fungi-
cides on different crop varieties in relation to the photo-
synthetic process, relating different families of fungicides,
crop varieties, and photosynthetic parameters that are
affected. A large number of papers on the topic covered by
this review have been published since 1978. This review
summarizes the main findings in the field of agriculture,
photosynthesis, and fungicides. Furthermore, many articles
have reported negative effects of these products, but it does
not mean that all fungicides have negative effects.
Effect of contact fungicides on photosynthesis
Application of fungicides alters the crop physiology, in
terms of growth and development along with nitrogen, and/
or carbon metabolism (Saladin and Cle
ment 2005). This
former physiological trait is fundamental for crop culture
and is reflected by both photosynthetic rate and
mobilization of carbohydrate reserves. Indeed, as plants
rely on their ability to assimilate carbon through photo-
synthesis for their growth and overall vigor, photosynthesis
disruption may decrease both the yield and the vigor.
Several works on photosynthesis fluctuations after fungi-
cide application on various crops report modifications of
both photosynthetic activity and chlorophyll fluorescence
(Krugh and Miles 1996; van Iersel and Bugbee 1996;
Untiedt and Blanke 2004; Xia et al. 2006).
Several chemical compounds, based mainly on copper,
sulphur or fludioxonil, are used to prevent crop plant dis-
ease through non-systemic control programs. Copper is
commonly used both as a pesticide (e.g. Bordeaux mixture)
and as an algicide in agriculture. Copper is also an essential
plant micronutrient as a component of various proteins,
particularly those involved in both photosynthetic (plasto-
cyanin) and the respiratory (cytochrome oxidase) electron
transport chain (Baro
n et al. 1995). However, an excess is
strongly phytotoxic for crops. Toxicity symptoms were
observed in cucumber leaves by a pronounced inhibition of
Pn in mature leaves exposed to 20 lgg
in soil for 5 days
(Table 2). Although Pn decline which is associated with a
parallel decrease in gs, stomatal closure does not account
for Pn inhibition (Vinit-Dunant et al. 2002).
Inhibition of photosynthesis in the leaves of stressed
plants is most likely a consequence of an altered source-
sink relationship. Indeed, growth inhibition decreases car-
bohydrate export from leaves, causes both starch and
sucrose accumulations, and finally leads to a feedback
inhibition of photosynthesis (Vinit-Dunant et al. 2002).
However, Pn inhibition after copper exposure may be
due to a disturbance of other processes in photosynthesis.
Copper has a pronounced effect on chloroplast ultrastruc-
ture (Baszynski et al. 1988). In addition, chloroplast
destruction was observed in green algae exposed to copper
with enhanced peroxidative processes (Sandmann and
ger 1980). Copper alters the lipid chloroplast membrane
(Szalontai et al. 1999), affecting light reaction processes,
especially those associated with PSII (Baro
n et al. 1995).
Copper inhibits pigment accumulation and retards chloro-
phyll integration into the photosystems of barley (Caspi
et al. 1999). It inhibits both the synthesis of the chlorophyll
precursor, delta aminolevulinic acid and the activity of
protochlorophyllide reductase, an enzyme that catalyzes
the reductive formation of chlorophyllide from protochlo-
rophyllide during chlorophyll biosynthesis (Stiborova
et al.
1986). Most of the in vitro studies using isolated chloro-
plasts or excised leaves have reported an inhibition of the
photosynthetic electron transport both at the reducing side
of PSI and at the oxidizing side of PSII (Sandmann and
ger 1980). Another effect of copper-based fungicides
used in the treatment of plant disease is the suppression of
oxygen evolution, inducing a decrease in photosynthetic
Photosynth Res (2012) 111:315–326 319
capacity (Caspi et al. 1999). Sensitivity of PSII was con-
firmed with increased PSII inactivation under photoinhib-
itory conditions (Pa
et al. 1998). Action has also been
localized within the compounds of the thylakoid membrane
such as PSI (Samuelsson and Oquist 1980), the coupling
factor (Uribe and Stark 1982) and the ferredoxin-dependent
reactions (Shioi et al. 1978). Finally, a direct inhibition of
Rubisco by Mg
substitution or by interaction with SH-
groups of the ATPase may also account for the inhibition
of photosynthesis following exposure (van Assche and
Clijsters 1990).
A decrease in the disease severity and improvement in
the foliage colour and retention has been observed by
treatment with sulfur, which acts both as a plant nutrient
and a fungicide (Stone et al. 2004). Despite its efficiency,
treatments containing sulfur also cause phytotoxicity on
crops (Holb and Schnabel 2005). In his review, Ferree
(1979) summarized works in the 1930’s and 1940’s
reporting that sulfur and lime sulfur reduce leaf Pn. Ferree
et al. (1999) later found that a single spray of sulfur results
in a significant decrease in Pn of greenhouse grown apple
trees. Similarly, Palmer et al. (2003) reported that leaf
photosynthesis of Braeburn apple trees was significantly
reduced by almost 50% following sulfur treatments (lime
sulfur or Kumulus i.e. 800 g kg
). The reduction in Pn is
always accompanied by reduced stomatal conductance.
The phytotoxicity of cuproxat (copper sulfate at 0.54 g l
on photosynthesis was investigated in a cucumber crop
after using it as a pesticide treatment; the result was a
decreased Pn accompanied by a decreased stomatal con-
ductance and Ci, indicating that Pn inhibition is mostly
attributed to stomatal factors. However, cuproxat had no
significant effects on PSII activity (Xia et al. 2006).
The fungicide fludioxonil (fdx) [4-(2,2-difluoro-1,3-
benzodioxol-4-yl)-1H-pyrrole-3-carbonitrile], a phenyl-
pyrrole compound, is commonly used as a botryticide in
the vineyards (Rosslenbroich and Stuebler 2000). Fdx is a
non-systemic molecule and acts by inhibiting spore ger-
mination, germ-tube elongation, and the mycelium growth
of Botrytis cinerea (Table 1). It increases the glycerol
content in the fungus, leading to a perturbation of the
osmoregulation potential (Pillonel and Meyer 1997). Fdx
applied during flower and berry development, may thus
have significant consequences on yield. In grapevine, a
decrease in Pn was noticed 8 days after treatment although
fdx is not associated with a reduction in gs at 6 mM, the
recommended concentration (Saladin et al. 2003, Petit
et al. 2008a). In parallel studies, decrease in chlorophyll
contents and carotenoids after fungicide treatments
appeared to be dose-dependent (Saladin et al. 2003). It was
shown that fdx effects on Pn, were related neither to
inactivation of both Rubisco and other key enzymes of the
Calvin cycle, nor, to modification of CO
diffusion to
Rubisco. Pn recovered 10 days post-treatment, which
would mean that either fdx had only a slight deleterious
effect on plant photosynthesis or that grapevine has greater
capacity to overcome this temporary stress (Saladin et al.
2003; Petit et al. 2008a, b). Petit et al. (2009) suggest a
relationship between the application of the fungicide fdx
and the circadian rhythm of a plant’s photosynthesis.
Interpreting the effect of fdx spraying on grapevine pho-
tosynthesis, these authors showed a phenomenon of gating
Table 2 Effects of contact fungicides on crop physiology
Affected parameters Molecules References
Inhibition of Pn Copper Vinit-Dunant et al. (2002)
Sulfur (kumulus) Ferree (1979), Ferree et al. (1999), Palmer et al. (2003)
Copper sulfate (cuproxat) Xia et al. (2006)
Fludioxonil Saladin et al. (2003), Petit et al. (2008a, b)
Stomatal closure Copper Vinit-Dunant et al. (2002)
Sulfur (kumulus) Palmer et al. (2003)
Copper sulfate (cuproxat) Xia et al. (2006)
Inhibition of Ci Copper sulfate (cuproxat) Xia et al. (2006)
Inhibition of Rubisco Copper van Assche and Clijsters (1990)
Decreased of chlorophyll
(synthesis or content)
Copper Stiborova
et al. (1986)
Fludioxonil Saladin et al. (2003)
Modification on chloroplast
Copper Sandmann and Bo
ger (1980), Baszynski et al. (1988),
Caspi et al. (1999), Szalontai et al. (1999)
PSII inactivation Copper Baro
n et al. (1995), Caspi et al. (1999), Vinit-Dunant et al. (2002)
PSI inactivation Copper Samuelsson and Oquist 1980
Inhibition of other sites of
electron transport chain
Copper Shioi et al. (1978), Sandmann and Bo
ger (1980), Uribe and Stark
(1982), van Assche and Clijsters (1990), Baro
n et al. (1995)
320 Photosynth Res (2012) 111:315–326
for the first time, i.e. external stimuli of equal strength
applied at different times of the day can result in different
intensities of response. The time period for spraying also
was an important parameter in stress response. These data
suggest that a morning treatment results in a non-stomatal
limitation of Pn, while a midday treatment is more suitable
to treat grapevine because it is the time period that least
disrupts photosynthesis.
Folpet, used to control mildew and other fungal diseases
in grape (Table 1), is an uncoupling fungicide (uncouple
oxidative phosphorylation in mitochondria). The folpet
phytotoxicity was only investigated on duckweed (Lemna
minor L.), an aquatic macrophyte regularly used as a model
for non-target species in ecotoxicological studies (Teisseire
et al. 1999). Within the range of tested folpet concentra-
tions (0–30 mg l
), no significant effect of total chloro-
phyll content was observed. No data is available on the
cultivated plants.
Systemic fungicides: for better or for worse
A group of organic fungicides called benzimidazoles is
widely used in agriculture for pre- and post-harvest pro-
tection of crops against many fungal diseases, such as
anthracnose, fruit rot, or grey mould. Its key compound,
benomyl, is especially effective because it penetrates into
plants faster than carbendazim (methyl 2-benzimidazolec-
arbamate), its active metabolite (Upham and Delp 1973).
Benomyl is a broad spectrum fungicide currently employed
in agriculture, and many studies on the interaction between
fungi and vascular plants (for example mycorrhizae) use
benomyl as a systemic fungicide in order to get uninfected
plants (Carey et al. 1992; Merryweather and Fitter 1996). It
is possible that these fungicides may be phytotoxic to crops
(Table 3). Moreover, benomyl breaks down to n-butyl
isocyanate which may subsequently react to produce
n-butylamine or N-N
-dibutylurea (DBU). Products of
degradation of benomyl also contribute to the phytotoxicity
of the fungicide (van Iersel and Bugbee 1996). It was also
demonstrated that at a rate of 2.8 kg ha
, DBU reduces
cucumber biomass 3 weeks after treatment and inhibits Pn
of hydrilla 1 day after treatment (Shilling et al. 1994).
Benlate (50% benomyl) caused a seven-to-ten day decrease
in Pn of petunia and impatiens (van Iersel and Bugbee
1997) and DBU may be partly responsible for byside
benomyl deleterious effects on plant growth. Crops have
various sensitivities to DBU. Greenhouse studies revealed
that corn is unaffected by DBU, whereas DBU is phyto-
toxic when applied as a soil drench to cucumber (Shilling
et al. 1994). Indeed, physical symptoms in cucumber begin
with chlorosis at the leaf margins then extend to the whole
leaf and finally lead to necrosis (Shilling et al. 1994).
Similarly, Mihuta-Grimm et al. (1990) noted chlorosis and
stunting in tomato plants following applications of high
benomyl concentrations. Ultra structural examination of
cucumber chloroplasts 10 days after treatment with
5.6 kg ha
DBU showed dilation and a disorganization of
granal membranes (Shilling et al. 1994). Moreover, DBU
affects PSII; it causes elevated chlorophyll fluorescence in
cucumber leaf discs and inhibits photosynthetic oxygen
evolution in hydrilla. In isolated spinach chloroplasts, DBU
also reduces oxygen production and causes photo-induced,
ferricyanide reduction by PSII alone as well as NADP
reduction from a site in the electron transport chain prior to
oxidation of plastohydroquinone, explaining Pn reduction
(Querns et al. 1998).
Carbendazim applications result in changes to foliar
pigment concentrations (Garcia et al. 2002). The applica-
tion of doses lower than the recommended 2.6 mM
increases carotenoid concentrations, whereas a higher rate
([2.6 mM) of carbendazim causes a decrease in all foliar
pigments 2 weeks after treatment. These treatments with
carbendazim may trigger a photoprotection mechanism in
plants via carotenoids, which would interact with light to
alleviate damages caused by the fungicide application
(Garcia et al. 2002; Skillman and Osmond 1998).
Strobilurins, are another class of fungicides which are
considered as a very valuable tool for managing diseases.
Strobilurin fungicides are beta-methoxyacrylate com-
pounds that inhibit respiration in fungi by binding to the Qo
site of the cytochrome bc1 complex located in the inner
mitochondrial membrane (Bartlett et al. 2002; Wiggins and
Jager 1993). This blocks electron transport and so reduces
ATP synthesis. Strobilurin fungicides inhibit respiration in
cytochrome bc1 isolated from yeast, fly, rat, and corn
(Roehl and Sauter 1993) and wheat (Ko
hle et al. 1997).
They also inhibit respiration in intact wheat plants and in
spinach (Spinacia oleracea L.) leaf discs (Glaab and Kaiser
1999). When a fungicide preparation containing the stro-
bilurin kresoxim-methyl is applied to the wheat plants, a
reduction in the stomatal aperture is observed along with an
increase in Pn rate (Fig. 2; Grossmann et al. 1999;Ko
et al. 1997). This result was quite surprising, because a
direct relationship between Pn and gs is well established
where the stomatal aperture increases Pn by increasing
diffusive transport of carbon dioxide (Yu et al. 2001). In an
interesting work, Nason et al. (2007) demonstrated that
strobilurin fungicides reduced the rate of gs to water in the
leaves of wheat, barley and soya plants. Coincidently,
plants treated with strobilurin fungicides have a lower rate
of transpiration (T), a lower Ci and a lower Pn compared
with control plants or plants treated with a epoxiconazole
which is a triazole fungicide. Azoxystrobin is an uncou-
pling strobilurin fungicide. The only data concerning
impact of azoxystrobin on photosynthesis showed that
Photosynth Res (2012) 111:315–326 321
azoxystrobin does not affect the chlorophyll content in
winter wheat, however its application delayed the increase
of AOS, thus delaying the senescence of wheat and pro-
longing the duration of flag leaf photosynthesis (Zhang
et al. 2010).
Triazole compounds such as triadimefon (TDM), prop-
iconazole, hexaconazole, and paclobutrazol are the largest
and most important group of systemic compounds devel-
oped for control of crop fungal diseases caused by
Fusarium sp and Erysiphe necator. These fungicides may
present phytotoxicity for crops as well as stimulant effects
on plant physiology. Pn increased after triazole applica-
tions in rice seedlings and bhendi (Guirong et al. 1995;
Sujatha et al. 1999), after paclobutrazol applications in
apple (Hong et al. 1995) and after TDM (15–20 g m
applications in radish crops (Panneerselvam et al. 1997)
and elephant foot yam (Gopi et al. 2005). By contrast,
cyazofamid (0.22 g l
) inhibits Pn in cucumber crops, but
no effect was measured with flusilazole on the same plants
(Xia et al. 2006) (Table 3). Gas exchange analysis dem-
onstrated that the suppression of Pn induced by cyazofamid
is associated with an increase of Ci, suggesting that Pn
alteration is mostly attributed to non-stomatal factors (Xia
et al. 2006). TDM also increases Pn along with Ci and gs in
maize (Kasele et al. 1995). To contrast, TDM treatments
induce stomatal closure in bean (Fletcher and Hofstra
1988), wheat (Sairam et al. 1989), elephant foot yam (Gopi
et al. 2005), radish (Panneerselvam et al. 1997), and mul-
berry plants (Sreedhar 1991). TDM treatments increased
the level of abscisic acid content in various plants, inducing
stomatal closure (Fletcher and Hofstra 1988; Panneersel-
vam et al. 1997; Gopi et al. 2005).
In the mesophyll, the number of cells per unit area in
both palisade and spongy layers and chloroplast number
per cell in the leaves of Chinese potato increased with
hexaconazole and paclobutrazol treatments (Kishorekumar
et al. 2006). The use of triazoles enhanced chlorophyll and
carotenoid contents in rice seedlings (Guirong et al. 1995)
Table 3 Effects of systemic fungicides on crop physiology
Family Affected parameter Active ingredient References
Anilides Inhibition of Pn Fenhexamid Petit et al. (2008b)
Repression of Rubisco genes Fenhexamid Petit et al. (2008b)
Azoles Inhibition of Pn Cyazofamid Xia et al. (2006)
Stimulation of Pn Paclobutrazol Hong et al. (1995)
Triadimefon Kasele et al. (1995), Panneerselvam et al. (1997),
Gopi et al. (2005)
Stomatal operture Triadimefon Kasele et al. (1995)
Stomatal closure Triadimefon Fletcher and Hofstra (1988), Sairam et al. (1989),
Sreedhar (1991), Panneerselvam et al. (1997),
Gopi et al. (2005)
Increased Ci Cyazofamid Xia et al. (2006)
Triadimefon Kasele et al. (1995)
Increased chlorophyll and
chloroplast contents
Paclobutrazol Kishorekumar et al. (2006)
Triadimefon Buchenauer and Rohner (1981), Gao et al. (1988),
Muthukumarasamy and Panneerselvam (1997),
Gopi et al. (1999)
Hexaconazole Kishorekumar et al. (2006)
Reduced oxygen evolution
and electron transport
Epoxiconazole Benton and Cobb (1997)
Benzimidazoles Inhibition of Pn Dibutylurea Shilling et al. (1994), Querns et al. (1998)
Chlorophyll declined Carbendazim Mihuta-Grimm et al. (1990), Garcia et al. (2002)
Carotenoids increased Carbendazim Garcia et al. (2002)
Disorganization of chloroplasts Dibutylurea Shilling et al. (1994)
PSII inactivation Dibutylurea Shilling et al. (1994)
Inhibition of electron transport Dibutylurea Querns et al. (1998)
Pyrimidines Inhibition of Pn Pyrimethanil Saladin et al. (2003)
Modifications of pigment concentrations Pyrimethanil Saladin et al. (2003)
Strobilurine Stomatal closure Kresoxim-methyl Grossmann et al. (1999)
Increased chlorophyll Kresoxim-methyl Grossmann et al. (1999)
322 Photosynth Res (2012) 111:315–326
and bhendi (Sujatha et al. 1999). TDM treatments
increased chlorophyll content in the leaves of the tomato
(Buchenauer and Rohner 1981), radish (Muthukumarasamy
and Panneerselvam 1997), cowpea (Gopi et al. 1999), and
wheat (Gao et al. 1988). Triazole compounds increase the
level of cytokinin, which might stimulate chlorophyll
biosynthesis (Jaleel et al. 2008). Triazoles accelerate
chloroplast differentiation, and chlorophyll production,
enlarged chloroplasts while also protecting the integrity of
chlorophyll (Fletcher et al. 2000; Jaleel et al. 2008). By
contrast, foliar application of epoxiconazole retards the
growth of cleavers (Benton and Cobb 1997). In addition,
7 days after treatment, epoxiconazole clearly reduces
oxygen evolution, determined as electron flow from water
to ferricyanide, and thus the associated electron transport
capability of isolated thylakoids (Benton and Cobb 1997).
Use of fungicides in the vineyards leads to an effective
protection against a wide variety of pathogens but at the
same time, generates long term residues in food and the
environment. Photosynthesis alteration was revealed by
reduction in Pn accompanied by changes in gs and Ci
including modifications of dark respiration after fungicide
treatment (van Iersel and Bugbee 1996; Untiedt and Blanke
2004; Xia et al. 2006). Considering fluorescence, the rel-
ative quantum yield of PSII (UPSII) and the maximal
quantum efficiency of PSII (Fv/Fm) were reduced by some
fungicides and were attributed to decrease in photochemi-
cal quenching (qP) (Krugh and Miles 1996). Fungicides of
the anilide family (pyrimethanil) and pyrimidine family
(fenhexamid) are newly synthesized pesticides used for
chemical control of Botrytis cinerea in viticulture.
Regarding pyrimethanil, the effects differ according to the
studied model. Using in vitro grown plantlets of grapevine,
6 mM pyrimethanil causes a decline in Pn and in photo-
synthetic pigment concentrations 7 days after application
(Saladin et al. 2003). In cuttings, pyrimethanil also inhibits
Pn but without reduction in chlorophyll concentrations.
In the vineyard, differences have been observed according
to cultivars. Pyrimethanil increases Pn and pigment con-
centrations in Chardonnay, whereas a decrease of these
parameters is observed in Pinot noir and Pinot Meunier
(Saladin et al. 2003). Petit et al. (2008b) demonstrated a
decrease in Pn following fenhexamid (1.5 kg ha
) 7 days
after treatment in the vineyard. Pn modification is mostly
attributed to non-stomatal limitation since the reduction of
photosynthesis is associated with few changes in Ci despite
gs decline. However, PSII activity is not affected. Addi-
tionally, decreased Pn is coupled with repression of genes
encoding Rubisco small and large subunits.
Conclusions and prospects
Fungicides constitute one of the most effective and inte-
grative method to control diseases against phytopathogenic
fungus in agriculture. However, the toxicity and the
Fig. 2 Site of action of
different class of fungicides
observed in fungi. ER
Endoplasmic reticulum
Photosynth Res (2012) 111:315–326 323
pollution generated by fungicides cannot be neglected. The
toxic effect of a given pesticide on seeds depends on its
distribution, persistence, metabolism, its active form, and
its concentration. Some pesticides interfere with the met-
abolic pathways of plants and some interfere specifically
with the photosynthetic process.
This review examines the toxic effects of a number of
different classes of fungicides on photosynthesis. They are
of importance in modern agriculture and in crop protection
but the modes of action are still not known indeed. How-
ever, this review does refer to the relevant literature and
illustrates the need for further research in this area to
mitigate against the deleterious effects. This is particularly
important for some of the older treatments such as copper.
Many findings indicate that some fungicides may affect the
photosynthetic process. Some pesticides lead to Pn alter-
ation through stomatal closure, while others affect the
structure and the functioning of chloroplasts. Certain
molecular compounds have no effect, whereas a few of
them, such as the azoles, stimulate Pn. Triadimefon and
hexaconazole could be used as a potential tool to manip-
ulate carbohydrate metabolism (Gomathinayagam et al.
2007). Photosynthesis is a complex physiological process.
More research highlighting and decoding each component
of the photosynthetic electron transport chain for example
PSI, PSII, Cyt b/f, and ATP synthase would be necessary.
In addition to damages caused by pesticides to crops, all
pesticides are potentially harmful to human health and
environment. Therefore taking into consideration the nega-
tive effects due to the use of chemicals for disease control, it
is of great importance to develop new active ingredients,
which could be used at such a dose where it shows high
specific toxicity to the target fungi and low toxicity to rest of
the species and have a curative effect. Among other desired
properties, having a low runoff potential and a rapid bio-
degradation potential might be good from an environmental
perspective. In addition to this, designing and testing active
ingredients that are less exposed to the risk of pathogen
resistance development and that do not present a risk during
experimental process would be very useful for the human
health and environment as well. New axes of research in this
area require attention. It would be indispensible to look for
new targets for example functional genomics. The diversi-
fication of chemical structures, along with combinatorial
chemistry and screening systems are some approaches that
will confer their benefits in the coming times.
Moreover, pesticide applicability can be compromised
by the emergence of resistant pathogen strains. Thus, the
need exists to curtail pesticide use, which will reduce the
environmental impact of this cultural practice. To this
purpose, there is an increasing demand to develop alter-
native methods for plant disease control. Another alterna-
tive strategy commonly used to control fungi is the
activation of plant defence mechanisms using a variety of
biotic and abiotic inducers.
Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluores-
cence can improve crop production strategies: an examination of
future possibilities. J Exp Bot 55:1607–1621
n M, Arellano JB, Gorge
L (1995) Copper and photosystem II: a
controversial relationship. Physiol Plant 94:174–180
Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-
Dobrzanski B (2002) Review: the strobilurin fungicides. Pest
Manag Sci 58:649–662
Baszynski T, Tukendorf A, Skorzynska E, Maksymiec W (1988)
Characteristics of the photosynthetic apparatus of copper non-
tolerant spinach exposed to excess copper. J Plant Physiol
Benton JM, Cobb AH (1997) The modification of phytosterol profiles
and in vitro photosynthetic electron transport of Galium aparine
L. (cleavers) treated with the fungicide, epoxiconazole. Plant
Growth Regul 22:93–100
Buchenauer H, Rohner E (1981) Effects of Triadimefon and
Triadimenol on growth of various plant species as well as on
gibberellin content and sterol metabolism in shoot of barley
seedlings. Pestic Biochem Phys 15:58–70
Carey PD, Fitter AH, Watkinson AR (1992) A field study using the
fungicide benomyl to investigate the effect of mycorrhizal fungi
on plant fitness. Oecologia 90:550–555
Caspi V, Droppa M, Horvath G, Malkin S, Marder JB, Raskin V
(1999) The effect of copper on chlorophyll organization during
greening of barley leaves. Photosynth Res 62:165–174
Debieu D, Corio-Costet M-F, Steva H, Malosse C, Leroux P (1995)
Sterol composition of the vine powdery mildew fungus, Uncin-
ula necator: comparison of triadimenol-sensitive and resistant
strains. Phytochemistry 39(2):293–300
Debieu D, Bach J, Hugon M, Malosse C, Leroux P (2001) The
hydroxyanilide fenhexamid, a new sterol biosynthesis inhibitor
fungicide efficient against the plant pathogenic fungus Botryoti-
nia fuckeliana (Botrytis cinerea). Pest Manag Sci 57:1060–1067
Dewez D, Geoffroy L, Vernet G, Popovic R (2005) Determination of
photosynthetic and enzymatic biomarkers sensitivity used to
evaluate toxic effects of copper and fludioxonil in alga Scene-
desmus obliquus. Aquat Toxicol 74:150–159
Dosnon-Olette R, Trotel-Aziz P, Couderchet M, Eullaffroy P (2010)
Fungicides and herbicide removal in Scenedesmus cell suspen-
sions. Chemosphere 79:117–123
Ferree DC (1979) Influence of pesticides on photosynthesis of crop
plants. In: Marcelle R, Clijsters H, van Poucke M, Junk W (eds)
Photosynthesis and plant development. The Netherlands, The
Hague, pp 331–341
Ferree DC, Hall FR, Krause CR, Roberts BR, Brazee RD (1999)
Influence of pesticides and water stress on photosynthesis and
transpiration of apple. Res Circ Ohio Agric Res Dev Cent 299:
Fletcher RA, Hofstra G (1988) Triazole as potential plant protectants.
In: Berg D, Plempel M (eds) Sterol biosynthesis inhibitors in
plant production. Ellis Horwood Ltd, Cambridge, pp 321–331
Fletcher RA, Gilley A, Davis TD, Sankhla N (2000) Triazoles as plant
growth regulators and stress protectants. Hortic Rev 24:55–138
Fritz R, Lanen C, Colas V, Leroux P (1997) Inhibition of methionine
biosynthesis in Botrytis cinerea by the anilinopyrimidine fungi-
cide pyrimethanil. Pestic Sci 49:40–46
324 Photosynth Res (2012) 111:315–326
n MAG, Wen S, Fetcher N, Bayman P (2005) Effects of
fungicides on endophytic fungi and photosynthesis in seedlings
of a tropical tree, Guarea guidonia (Meliaceae). Acta Biolo
Colombiana 10:41–47
Gao J, Hofstra G, Fletcher RA (1988) Anatomical changes induced by
triazoles in wheat seedlings. Can J Bot 66:178–1185
Garcia PC, Ruiz JM, Rivero RM, Luis R, Pez-Lefebre L, Sa
nchez E,
Romero L (2002) Is the application of carbendazim harmful to
healthy plants? Evidence of weak phytotoxicity in tobacco.
J Agric Food Chem 50:279–283
Glaab J, Kaiser WM (1999) Increased nitrate reductase activity in leaf
tissue after application of the fungicide kresoxim-methyl. Planta
Gomathinayagam M, Jaleel CA, Lakshmanan GMA, Panneerselvam
R (2007) Changes in carbohydrate metabolism by triazole
growth regulators in cassava (Manihot esculenta Crantz); effects
on tuber production and quality. C R Biol 330:644–655
Gopi R, Sujatha BM, Rajan SN, Karikalan L, Panneerselvam R
(1999) Effect of Triadimefon in the NaCl stressed cowpea
(Vigna ungiculata) seedlings. Indian J Agr Sci 69:743–745
Gopi R, Sridharan R, Somasundaram R, Lakshmanan GMA,
Panneerselvam R (2005) Growth and photosynthetic character-
istics as affected by triazoles in Amorphophallus campanulatus
Blume. Gen App Plant Physiol 31:171–180
Grossmann K, Kwiatkowski J, Caspar G (1999) Regulation of
phytohormone levels, leaf senescence, and transpiration by the
strobilurin kresoxim-methyl in wheat (Triticum aestivum).
J Plant Physiol 154:805–808
Guirong C, Lin X, Kaijiun W, Yan ZA, Yijiu P, Yuming I, Xiang
WM (1995) The physiological and yield increasing effects of
multi-effect triazole treatment of green house rice seedling.
Henan Nongye Kexue, No.2, 2–4. (ch, 5 ref). Xinyang Higher
Agriculture Training School, China
nßler G, Pontzen R (1999) Effect of fenhexamid on the develop-
ment of Botrytis cinerea. Pflanzen Nach Bayer 52:158–176
Haughan PA, Lenton JR, Goad LJ (1988) Sterol requirements and
paclobutrazol inhibition of a celery cell culture. Phytochemistry
Hillier W, Babcock GT (2001) Photosynthetic Reaction Centers. Plant
Physiol 125:33–37
Holb IJ, Schnabel G (2005) Effect of fungicide treatments and
sanitation practices on brown rot blossom blight incidence,
phytotoxicity, and yield for organic sour cherry production. Plant
Dis 89:117–1164
Holb IJ, De Jong PF, Heijne B (2003) Efficacy and phytotoxicity of lime
sulfur in organic apple production. Ann Appl Biol 142:225–233
Hong Y, Zhimim Y, Jingyl Y (1995) Biological response of Hosta
plantaginea to mepiquat chloride and paclobutrazole. J Nanjing
Agric University China 18:18–22
IUPAC (International Union of Pure Applied Chemistry). Pesticide
properties database. Integr Pest Manag. http://agrochemicals. Accessed 2 April 2010
Jaleel CA, Gopi R, Panneerselvam R (2008) Growth and photosyn-
thetic pigments responses of two varieties of Catharanthus
roseus to triadimefon treatment. C R Biol 331(4):272–277
Kasele IN, Shannahan JF, Nielsel DC (1995) Impact of growth
retardants on corn leaf morphology and gas exchange traits. Crop
Sci 35:190–194
Kishorekumar A, Jaleel CA, Manivannan P, Sankar B, Sridharan R,
Somasundaram R, Panneerselvam R (2006) Differential effects
of hexaconazole and paclobutrazol on the foliage characteristics
of Chinese potato (Solenostemon rotundifolius Poir., J.K.
Morton). Acta Biol Szegediensis 50:127–129
hle H, Grossmann K, Retzlaff G, Akers A, Limburgerhof G (1997)
Physiological effects of the new fungicide Juwel
on yield in
cereals. Gesunde Pflanzen 49:267–271
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosyn-
thesis: the basics. Annu Rev Plant Physiol Plant Mol Biol
Krugh BW, Miles D (1996) Monitoring the effects of five ‘nonher-
bicidal’ pesticide chemicals of terrestrial plants using chloro-
phyll fluorescence. Environ Toxicol Chem 15:495–500
Laisk A, Eichelmann H, Oja V (2006) C
photosynthesis in silico.
Photosynth Res 90:45–66
Leroux P (2003) Mode of action of agrochemicals towards plant
pathogens. C R Biol 326:9–21
Leroux P, Descotes A (1996) Resistance of Botrytis cinerea to
fungicides and strategies for its control in the Champagne
vineyards. In: Proceeding of the 1996 Brighton crop protection
conference pests and diseases, pp 131–136
Leroux P, Frita R, Debiu D, Albertini C, Lanen C, Bach J, Gredt M,
Chapeland F (2002) Mechanisms of resistance to fungicides in
field strains of Botrytis cinerea. Pest Manag Sci 58:876–888
Merryweather J, Fitter A (1996) Phosphorous nutrition of an
obligately mycorrhizal plant treated with the fungicide benomyl
in the field. New Phytol 132:307–311
Mihuta-Grimm L, Erb WA, Rowe RC (1990) Fusarium crown and
root rot of tomato in greenhouse rock wool systems: sources of
inoculum and disease management with benomyl. Plant Dis
Mitani S, Araki S, Yamaguchi T, Takii Y, Ohshima T, Matsuo N
(2001) Antifungal activity of the novel fungicide Cyazofamid
against Phytophthora infestans and other plant pathogenic fungi
in vitro. Pestic Biochem Phys 70(2):92–99
Muthukumarasamy M, Panneerselvam R (1997) Triazole induced
protein metabolism in the salt stressed Raphanus sativus
seedlings. J Indian Bot Soc 76:39–42
Nason MA, Farrar J, Bartlett D (2007) Strobilurin fungicides induce
changes in photosynthetic gas exchange that do not improve
water use efficiency of plants grown under conditions of water
stress. Pest Manag Sci 63:1191–1200
Palmer JW, Davies SB, Shaw PW, Wu
nsche JN (2003) Growth and
fruit quality of ‘Braeburn’ apple (Malus domestica) trees as
influenced by fungicide programmes suitable for organic
production. New Zeal J Crop Hort Sci 31:169–177
Panneerselvam R, Muthukumarasamy M, Karikalan L (1997) Triadime-
fon enhances growth and net photosynthetic rate in NaCl stressed
plants of Raphanus sativus L. Photosynthetica 34:605–609
E, Aro E-M, Tyystja
rvi E (1998) Increase in the quantum
yield of photoinhibition contributes to copper toxicity in vivo.
Plant Physiol 117:619–627
Perales-Vela HV, Pena-Castro JM, Canizares-Villanueva RO (2006)
Heavy metal detoxification in eukaryotic microalgae. Chemo-
sphere 64:1–10
Petit A-N, Fontaine F, Cle
ment C, Vaillant-Gaveau N (2008a)
Photosynthesis limitations of grapevine after treatment with the
fludioxonil fungicide. J Agric Food Chem 56:6761–6767
Petit A-N, Fontaine F, Cle
ment C, Vaillant-Gaveau N (2008b) Two
botryticide effets on leaf photosynthesis grapevine. In: Sanchez
A, Gutierrez SJ (eds) Photochemistry Research Progress. Nova
Science Publishers Inc, NY, pp 1–12
Petit A-N, Fontaine F, Cle
ment C, Vaillant-Gaveau N (2009) Gating
in grapevine: relationship between application of the fungicide
fludioxonil and circadian rhythm on photosynthesis. Environ
Pollut 157:130–134
Pillonel C, Meyer T (1997) Effect of phenylpyrroles on glycerol
accumulation and protein kinase activity of Neurospora crassa.
Pestic Sci 49:229–236
Querns R, MacDonald GE, Gaffney JF, Chase CA, Moye HA,
Shilling DG, Bewick TA (1998) Effects of N, N
-dibutylurea on
photosynthetic electron transport reactions in isolated chloro-
plasts. Pestic Biochem Phys 59:129–135
Photosynth Res (2012) 111:315–326 325
Rajendran UM, Kathirvel E, Narayanaswamy A (2007) Effects of a
fungicide, an insecticide, and a biopesticide on Tolypothrix
scytonemoides. Pestic Biochem Phys 87:164–171
Roehl F, Sauter H (1993) Species dependence of mitochondrial
respiration inhibition by strobilurin analogues. Biochem Soc
Trans 22:63S
Rosslenbroich HJ, Stuebler D (2000) Botrytis cinerea—History of
chemical control and novel fungicides for its management. Crop
Prot 19:557–561
Sairam RK, Desmukh PS, Shukla DS, Wasnik KG, Kushwaha SR
(1989) Effect of abscisic acid and triadimefon on photosynthesis
and nitrate reductase activity during water stress in wheat. Indian
J Plant Physiol 32:51–56
Saladin G, Cle
ment C (2005) Physiological effects of pesticides on
cultivated crops. In: Livingston JV (ed) Agriculture and Soil
Pollution. New Research. Nova Science Publishers, USA, pp 53–86
Saladin G, Magne
C, Cle
ment C (2003) Effects of fludioxonil and
pyrimethanil, two fungicides used against Botrytis cinerea,on
carbohydrate physiology in Vitis vinifera L. Pest Manag Sci
Samuelsson G, Oquist G (1980) Effects of copper chloride on
photosynthetic electron transport and chlorophyll-protein com-
plexes of Spinacia oleracea. Plant Cell Physiol 21:445–454
Sandmann G, Bo
ger P (1980) Copper-mediated lipid peroxidation
processes in photosynthetic membranes. Plant Physiol 66:797–800
Shilling DG, Aldrich HC, Moye HA, Gaffney JF, Tolson JK, Querns
R, Mossler MA, Russell BL (1994) N, N’-Dibutylurea from n-
butyl isocyanate, a degradation product of benomyl. 2. Effects on
plant growth and physiology. J Agric Food Chem 42:1209–1212
Shioi Y, Tamai H, Sasa T (1978) Effects of copper on photosynthetic
electron transport systems in spinach chloroplasts. Plant Cell
Physiol 19:203–209
Skillman JB, Osmond CB (1998) Influence of nitrogen supply and
growth irradiance on photoinhibition and recovery in Heuchera
americana (Saxifragaceae). Physiol Plant 103:563–573
Smith GA, Moser HS (1985) Sporophytic-gametophytic herbicide
tolerance in sugar beet. Theor Appl Genet 71:231–237
Sreedhar VM (1991) Proline accumulation and reduced transpiration
in leaves of triazole treated mulberry plant. Indian Bot Report
M, Doubravova
M, Brezinova
A, Friedrich A (1986) Effect
of heavy metal ions on growth and biochemical characteristics of
photosynthesis of barley Hordeum vulgare L. Photosynthetica
Stone J, Chastagner G, Kanaskie A (2004) Control of Swiss needle
cast in forest plantations by aerially applied elemental sulfur
fungicide. In: Mainwaring D (ed) Swiss Needle Cast Coopera-
tive Annual report. Oregon State University, Corvallis, pp 49–56
Sujatha BM, Gopi R, Karikalan L, Rajan SN, Panneerselvam R
(1999) Effect of triadimefon treatment on bhendi (Abelmoschus
esculantus (L.) moench.) seedlings under salinity condition.
Indian J Plant Physiol 4:307–310
Szalontai B, Horvath LI, Debreczeny M, Droppa M, Horvath G
(1999) Molecular rearrangements of thylakoids after heavy metal
poisoning, as seen by Fourier transform infrared (FTIR) and
electron spin resonance (ESR) spectroscopy. Photosynth Res
Teisseire H, Couderchet M, Vernet G (1999) Phytotoxicity of diuron
alone and in combination with copper or folpet on duckweed
(Lemna minor). Environ Pollut 106:39–45
Untiedt R, Blanke MM (2004) Effects of fungicide and insecticide
mixtures on apple tree canopy photosynthesis, dark respiration
and carbon economy. Crop Prot 23:1001–1006
Upham PM, Delp CJ (1973) Role of benomyl in the systemic control
of fungi and mites on herbaceous plants. Phytopathology 63:
Uribe EG, Stark B (1982) Inhibition of photosynthetic energy
conversion by cupric ion-evidence for Cu2 -coupling factor 1
interaction. Plant Physiol 69:1040–1045
van Assche F, Clijsters H (1990) Effects of metals on enzyme activity
in plants. Plant Cell Environ 13:195–206
van Iersel MW, Bugbee B (1996) Phytotoxic effects of benzimidazole
fungicides on bedding plants. J Am Soc Hortic Sci 121:
van Iersel MW, Bugbee B (1997) Dibutylurea reduces photosynthesis,
growth and flowering of petunia and impatiens. J Am Soc Hortic
Sci 122:536–541
Vinit-Dunant F, Epron D, Alaoui-Sosse
B, Badot P-M (2002) Effects
on copper on growth and photosynthesis of mature and
expanding leaves in cucumber plants. Plant Sci 163:53–58
Wiggins TE, Jager BJ (1993) Mode of action of the new methoxy-
acrylate antifungal agent ICIA5504. Biochem Soc Trans 22:68S
Xia XJ, Huang YY, Wang L, Huang LF, Yu YL, Zhou YH, Yu JQ
(2006) Pesticides-induced depression of photosynthesis was
alleviated by 24-epibrassinolide pretreatment in Cucumis sativus
L. Pestic Biochem Physiol 86:42–48
Yu Q, Goudriaan J, Wang TD (2001) Modelling diurnal courses of
photosynthesis and transpiration of leaves on the basis of
stomatal and non-stomatal responses, including photoinhibition.
Photosynthetica 39:43–51
Yuste MP, Gostincar J (1999) Handbook of agriculture. Marcel
Dekker, New York
Zhang Y-J, Zhang X, Chen C-J, Zhou M-G, Wang H-C (2010) Effects
of fungicides JS399-19, azoxystrobin, tebuconazloe, and carb-
endazim on the physiological and biochemical indices and grain
yield of winter wheat. Pestic Biochem Physiol 98:151–157
326 Photosynth Res (2012) 111:315–326
... Most contact fungicides are not absorbed by the plant and remain on the plant tissue surface. However, the frequency of application must be carefully monitored, since contact fungicides can become phytotoxic in the rare cases when they are absorbed [14]. Because contact fungicides usually remain on the plant surface, protection is temporary and can be quickly lost due to rainfall or other weather conditions [15,16]. ...
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Fungal pathogens pose a major threat to food production worldwide. Traditionally, chemical fungicides have been the primary means of controlling these pathogens, but many of these fungicides have recently come under increased scrutiny due to their negative effects on the health of humans, animals, and the environment. However, the use of fungicides with less of an environmental impact tends to result in the development of resistance in populations of phytopathogenic fungi. Therefore, new environmentally friendly alternatives that provide adequate levels of disease control are needed to replace chemical fungicides—if not completely, at least partially. A number of alternatives to conventional chemical fungicides have been developed, including plant defence elicitors (PDEs), biological control agents (fungi, bacteria and mycoviruses), biofungicides, RNA interference (RNAi) methods, and resistance breeding. This article reviews the conventional and alternative methods available to manage fungal pathogens, discusses their strengths and weaknesses, and identifies potential areas for future research.
... According to Wyszkowska and Kucharski [11], frequent applying of fungicides has a threat to the environment because it increases the buildup of toxic substances in ecosystems and has a detrimental effect on soil microorganisms. For instance, copper fungicide inhibits photosynthesis, which has a negative impact on photosystem activity, the environmental balance and public health [12][13][14].This is another challenge to use hazardous and safe natural products to control root rot disease using mycorrhiza and nanoparticles. In this regard, Arbuscular mycorrhizal fungi (AMF) and chitosan nanoparticles were used as a trial to allow protection of VF against Rhizocotinia root rot disease. ...
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Background The spreading of root rot disease of faba bean plant ( Vichia faba L, VF) in Egypt is still of great challenge faced researchers since VF is an important legume in Egypt, because their seeds are used for human feeding. Fungicides are used for treatment of either seeds or soil; unfortunately they cause environmental pollution. Therefore, there is a need to continue research to find out safe natural solutions. In this regard, Arbuscular mycorrhizal fungi (AMF) and chitosan (micro or nanoform) were used as an inhibitory product against Rhizoctonia solani OM918223 ( R.solani ) either singly or in combinations. Results The results employed herein have exhibited that R.solani caused root rot disease of VF plants in more than 80% of the plants under investigation. Chitosan nanoparticles (Chitosan NPs) were prepared by ionic gelatin method and characterized by using dynamic light scattering (DLS), transmission electron microscopy (TEM) imaging and Fourier transform infra-red (FTIR). Chitosan NPs are spherical with a diameter of 78.5 nm and exhibited the presence of different functional groups. The inhibitory natural products against R.solani were arranged according to their ability to inhibit the pathogen used in the following descending manner; combination of AMF with Chitosan NPs, AMF with micro chitosan and single AMF, respectively. Where, Chitosan NPs showed a potent influence on R.solani pathogen and reduced the pre-and post-emergence of R. solani . In addition, Chitosan NPs reduced Disease Incidence (DI %) and Disease Severity (DS %) of root rot disease and are widely functional through mixing with AMF by about 88% and 89%. Further, Chitosan NPs and micro chitosan were proved to increase the growth parameters of VF plants such as nutritional status (mineral, soluble sugar, and pigment content), and defense mechanisms including total phenol, peroxidase, and polyphenol oxidase in mycorrhizal plants more than non-mycorrhizal one either in infected or healthy plants. Moreover, activity of AMF as an inhibitory against R.solani and improvement natural agent for VF growth parameters was enhanced through its fusing with Chitosan NPs. Conclusions The use of AMF and Chitosan NPs increased faba bean plant resistance against the infection of root rot R. solani , with both prevention and cure together. Therefore, this research opens the door to choose natural and environmental friendly treatments with different mechanisms of plant resistance to disease.
... Plants 2023, 12, 2974 ...
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Potato (Solanum tuberosum) is one of the most important food crops worldwide, and Rhizoctonia solani infection is one of the most common diseases. The objective of this study was to evaluate the antifungal activity of Vitis vinifera byproducts (VIDES) and flesh-coloured potato (FCP) extracts against Rhizoctonia sp. in potato crops. Photosynthetic traits, phenolic profiles, and antioxidant and enzymatic activities were determined. The VIDES extract showed a 151.4% improvement in stomatal conductance and a 258.5% improvement in the photosynthetic rate compared to the plants without infection. Regarding the enzymatic antioxidant activity, the best response was found in the FCP treatments with 30 min of application, with increases of 25%, 161%, and 450% in ascorbate peroxidase, catalase (CAT), and glutathione reductase (GR) activities, respectively, compared to plants without infection. For the VIDES extract, a 15 min application produced an 83% increase in CAT activity, whereas a 181% increase in GR activity compared to plants without infection was produced after a 30 min application. A similar behaviour was observed for antioxidant compounds, where FCP had a higher concentration of compounds and antioxidant activity. This finding suggests that FCP and VIDES promote the synthesis of plant-defence compounds against Rhizoctonia sp. in potato crops, in which the application time is a determining factor.
... Autre exemple, les fongicides affectent un large panel de microorganismes (Brühl et Zaller, 2019) en ciblant les fonctions membranaires de transmission du signal, la respiration, la division cellulaire, et la synthèses nucléique. Beaucoup de fongicides (dont le cuivre), sont par ailleurs préjudiciables à la photosynthèse des plantes (Petit et al., 2012) alors que d'autres de la famille des triazoles, la stimulent. ...
... Benomyl soil application also strongly affected plant performance by decreasing shoot dry weight, total dry weight, shoot phosphorus concentration, total number of pods, and seed germination rate. This maybe related to a possible direct phytotoxic effects of Benomyl due to the nbutyl isocyanate byproduct (Petit et al., 2012). However, another explanation of the reduced plant performance after Benomyl soil application maybe indirectly related to the inhibition and disruption of the mycorrhizal vetch association. ...
Soil microorganisms play a key role in plant growth and health, and honey bees depend on plant pollen and nectar for their nutrition. Despite this clear above- and belowground connection, our knowledge about bee-plant-soil interactions is yet limited. Also, how these multitrophic interactions are affected by agricultural practices like pesticide applications is not well understood. Here we investigated possible non-target effects of soil application of the fungicide Benomyl on bee-plant-soil interactions in a greenhouse experiment with vetch (Vicia sativa L.). When plants were flowering honey bees were confined to their respective experimental soil treatments (untreated control, Benomyl and soil disinfection) in tents made from anti-insect mesh and micro-hives for foraging. At harvest, results showed that Benomyl and soil disinfection strongly affected key root and soil microorganisms essential for plant nutrition, such as mycorrhiza and rhizobia, and Gram-positive and Gram-negative bacteria, which coincided with phenotypic alterations in plant development and subsequently significant effects on honey bee nutrition and health, and finally honey production. In conclusion, our results show that soil application of the fungicide Benomyl strongly impact on bee-plant-soil multitrophic interactions, calling for further investigation on non-target effect of pesticides including multitrophic studies when evaluating environmental impacts of pesticides.
Plants are essential for life on earth, and agricultural crops are a primary food source for humans. For the One Health future, crop health is crucial for safe, high-quality agricultural products and the development of future green commodities. However, the overuse of pesticides in modern agriculture raises concerns about their adverse effects on crop resistance and product quality. Recently, biostimulants, including microecological bacteria agents and nanoparticles, have garnered worldwide interest for their ability to sustain plant health and enhance crop resistance. This review analyzed the effects and mechanisms of pesticide stress on crop health. It also investigated the regulation of biostimulants on crop health and the multiomics mechanism, combining research on nanoselenium activating various crop health aspects conducted by the authors' research group. The paper helps readers understand the impact of pesticides on crop health and the positive influence of various biostimulants, especially nanomaterials and small molecules, on crop health.
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Triazole fungicides can threaten plants as abiotic stressors but can also positively affect plant defense by inducing priming. Thus, plant yield is also both protected and endangered by triazoles that may influence several metabolic pathways during maturation processes, such as the biosynthesis of saccharides or secondary metabolites. Here, Solanum lycopersicum L. plants were exposed to foliar and soil applications of penconazole, tebuconazole, or their combination, and their resulting effect on tomato fruits was followed. The exposure to the equimolar mixture of both triazoles influenced the representation of free proteinogenic amino acids, especially Gln, Glu, Gly, Ile, Lys, Ser and Pro, saccharide content, and led to a significant increase in the contents of total phenolics and flavonoids as well as positive stimulation of the non-enzymatic antioxidant system. Among the identified secondary metabolites, the most abundant was naringenin, followed by chlorogenic acid in tomato peel. In turn, all triazole-treated groups showed a significantly lower content of rosmarinic acid in comparison with the control. Foliar application of penconazole affected the fruit more than other single triazole applications, showing a significant decrease in antioxidant capacity, the total content of secondary metabolites, and the activities of total membrane-bound peroxidases and ascorbate peroxidase.
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Among the mycoparasites, Ampelomyces strains are studied in detail, particularly regarding their use as biocontrol agents (BCAs) of powdery mildew (PM) fungi, including their potential to replace conventional agrochemicals. Ampelomyces strains are characterized morphologically; their ribosomal DNA internal transcribed spacer (rDNA-ITS) regions and actin gene (ACT) fragments were sequenced and their mycoparasitic activity was analyzed. In the interaction between Ampelomyces strains and PM fungi, the spores of the mycoparasites germinate on plant leaves, and their hyphae then penetrate the hyphae of PM fungi. Ampelomyces hyphae continue their growth internally, initiating the atrophy of PM conidiophores and eventually their complete collapse. Following the successful destruction of PM hyphae by Ampelomyces, the mycoparasite produces new intracellular pycnidia in PM conidiophores. The progeny spores released by mature pycnidia become the sources of subsequent infections of intact PM hyphae. As a result, the number of Ampelomyces-inoculated PM colonies gradually declines, and the conidial release of PM colonies is inhibited after the first treatment. Almost all conidiophores of 5- and 10-day-old Ampelomyces-inoculated PM colonies undergo complete atrophy or collapse. Methodological advances and in-depth analyses of the Ampelomyces–PM interaction were recently published. In this review, we summarize the genetic and phylogenetic diversity, the timing of mycoparasitism and pycnidiogenesis, the results of quantitative and visual analyses using electrostatic and digital microscopy technologies, the PM biocontrol potential of Ampelomyces, and the potential commercialization of the mycoparasites. The information provided herein can support further biocontrol and ecological studies of Ampelomyces mycoparasites.
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Various treatments resulting in physical stress to leaves of apple ( Malus domestica Borkh.) were tested for their influence on net photosynthesis (Pn) and transpiration (Tr). Brushing to simulate handling or wind rubbing reduced both Pn and Tr in one study and had little effect in another. Shaking 1 min/day had no influence on Pn or Tr. Six or more 1-cm cuts/leaf reduced Pn and had no effect on Tr. Removal of 20% of the leaf area and twenty-four 1-cm cuts/leaf reduced Pn in young expanding leaves; the amount of cut surface exposed by injury was more important than the amount of leaf area removed. Scoring and feeding of two-spotted spider mites [ Tetranychus urticae (Koch)] reduced Pn.
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Dibutylurea (DBU), a breakdown product of benomyl, may be partially responsible for the previously reported phytotoxicity of the fungicide Benlate DF. We quantified the effect of DBU on the growth of two popular bedding plant species, petunia ( Petunia × hybrida ) and impatiens ( Impatiens wallerana Hook. f.). DBU reduced photosynthesis of both species, and its effect strongly depended on the amount of DBU applied. The effects of DBU were most apparent 2 to 4 days after treatment, at which time 1.20 g·m ⁻² (corresponding to 10% DBU in Benlate DF at maximum labeled drench rate) inhibited photosynthesis completely. DBU also decreased flower number and caused marginal necrosis. DBU effects were more pronounced in low relative humidity. Benlate DF containing 3.1% DBU and an equivalent amount of reagent grade DBU had similar effects on photosynthesis and petunia necrosis. Our results showed that DBU is responsible for at least part of the phytotoxic symptoms that can be caused by Benlate DF. However, other ingredients or breakdown products may also contribute to the phytotoxic symptoms of Benlate DF.
Juwel®, a new fungicide developed by BASF Aktiengesellschaft combines two active ingredients: the strobilurin compound Kresoxim-methyl and the triazol compound Expoxiconazole. In addition to its excellent and long lasting fungicidal activity against all important cereal crop pathogens, Juwel® has influence on the C- and N-assimilation of the plant as shown in test systems free of pathogens. The contents of ethylene and other plant hormones are also modified, which may be the reason for enhanced stress resistance and greening effects of plants after treatment with Juwel®. Since these special metabolic and regulatory changes are independant of fungal attack, the physiological effects of Juwel® are discussed to be the most likely cause for the superieur increase in yield compared to other fungicides.
The effect of copper on photoinhibition of photosystem II in vivo was studied in bean (Phaseolus vulgaris L. cv Dufrix). The plants were grown hydroponically in the presence of various concentrations of Cu²⁺ ranging from the optimum 0.3 μm(control) to 15 μm. The copper concentration of leaves varied according to the nutrient medium from a control value of 13 mg kg⁻¹ dry weight to 76 mg kg⁻¹ dry weight. Leaf samples were illuminated in the presence and absence of lincomycin at different light intensities (500–1500 μmol photons m⁻² s⁻¹). Lincomycin prevents the concurrent repair of photoinhibitory damage by blocking chloroplast protein synthesis. The photoinhibitory decrease in the light-saturated rate of O2 evolution measured from thylakoids isolated from treated leaves correlated well with the decrease in the ratio of variable to maximum fluorescence measured from the leaf discs; therefore, the fluorescence ratio was used as a routine measurement of photoinhibition in vivo. Excess copper was found to affect the equilibrium between photoinhibition and repair, resulting in a decrease in the steady-state concentration of active photosystem II centers of illuminated leaves. This shift in equilibrium apparently resulted from an increase in the quantum yield of photoinhibition (ΦPI) induced by excess copper. The kinetic pattern of photoinhibition and the independence of ΦPI on photon flux density were not affected by excess copper. An increase in ΦPI may contribute substantially to Cu²⁺ toxicity in certain plant species.
Individual spinach plants (Spinacia oleracea L., c.v. Matador) sensitive to excess copper were grown on a nutrient medium containing toxic amounts of the metal, and the characteristics of its photosynthetic apparatus were examined. In chloroplasts isolated from Cu-treated plants the accumulation of plastid pigments and lipoquinones was lower than in controls and it decreased with the increase of copper toxicity. The loss of photochemical activity of photosystem I and photosystem II was observed at the late stage of leaf degradation (the leaves turned yellow). The loss of photosystem II activity was faster than that of photosystem I. Consequently, changes in chlorophyll distribution of light harvesting chlorophyll-protein complexes were observed. The CPa level, being the presumable reaction center of photosystem II, decreased significantly. The fine structure of chloroplasts revealed degradation of grana stacks and stroma lamellae depending on the stage of their degeneration, an increase in the number and size of plastoglobuli and intrathylakoidal inclusions. The results obtained have been discussed with regard to direct or indirect effects of copper in chloroplasts of plants sensitive to excess copper.