Fungicide impacts on photosynthesis in crop plants.

Abstract

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.

Full text

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REVIEW
Fungicide impacts on photosynthesis in crop plants
Anne-Noe ¨lle Petit•Florence Fontaine•
Parul Vatsa•Christophe Cle ´ment•
Nathalie Vaillant-Gaveau
Received: 27 March 2011/Accepted: 12 January 2012/Published online: 1 February 2012
? Springer Science+Business Media B.V. 2012
Abstract
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.
Fungicides are widely used to control pests in
Keywords
Photosynthesis ? Photosystems ? Physiology ?
Phytotoxicity ? Stomatal closure ? Stress
Chlorophyll ? Crop plants ? Fungicides ?
Introduction
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
fungicides.
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 ´ment ?
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 ˆtiment 18, Moulin de la
Housse, BP 1039, 51687 Reims Cedex 2, France
e-mail: nathalie.vaillant-gaveau@univ-reims.fr
123
Photosynth Res (2012) 111:315–326
DOI 10.1007/s11120-012-9719-8

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Table 1 Basic chemical characteristics of fungicides (data from International Union of Pure Applied Chemistry)
Fungicides,
Formules
Structures Primary mode of action in fungus
Copper and/or sulfate
Bordeaux mixture
CuSO4?3Cu(OH)2
3CaSO4
Kumulus
Inhibit several enzymes involved in respiration and this multi-site action
(Leroux 2003)
Sx
Cuproxat
Inhibit several enzymes involved in respiration and this multi-site action
(Leroux 2003)
3Cu(OH)2CuSO4
Strobilurine
Inhibit several enzymes involved in respiration and this multi-site action
(Leroux 2003)
Kresoxim-methyl
C18H19NO4
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)
Azoxystrobin
C22H17N3O5
Inhibits spore germination and mycelial growth (Zhang et al. 2010)
Pyrrole
Fludioxonil
C12H6F2N2O2
Perturbe the osmo-regulatory signal transmission pathway (Pillonel and
Meyer 1997)
Inhibits spore germination and mycelial growth (Leroux et al. 2002)
Anilides
Fenhexamid
C19H15FN2O4
Inhibits germ-tube elongation and mycelial growth (Ha ¨nbler and Pontzen
1999)
A sterol biosynthesis inhibitor: inhibits the 3-keto reductase involved in the
enzymatic complex of the sterol C-4 demethylation (Debieu et al. 2001)
Phthalimide
Folpet
C9H4Cl3NO2S
Inhibits spore germination and mycelial growth
Multi-site action (Teisseire et al. 1999)
Azoles
Cyazofamid
C13H13ClN4O2S
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)
Paclobutrazol
C15H20ClN3O
Inhibition of sterol biosynthesis at the 14a-demethylation step (Haughan
et al. 1988)
Triadimefon
C14H16ClN3O2
Sterol C-14 demethylation inhibitor (Debieu et al. 1995)
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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
Cle ´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 CO2 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 CO2availability (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
Fungicides,
Formules
StructuresPrimary mode of action in fungus
Hexaconazole
C14H17Cl2N3O
Sterol C-14 demethylation inhibitor (Debieu et al. 1995)
Propiconazole
C15H17Cl2N3O2
Sterol C-14 demethylation inhibitor (Gaita ´n et al. 2005)
Epoxiconazole
C17H13ClFN3O
Sterol C-14 demethylation inhibitor (Debieu et al. 1995)
Benzimidazoles
Carbendazim
C9H9N3O2
Inhibition of microtubule assembly which is due to their binding to tubulin, the main
protein of microtubules (Leroux and Descotes 1996)
Benomyl
C14H18N4O3
Inhibition of microtubule assembly which is due to their binding to tubulin, the main
protein of microtubules (Leroux and Descotes 1996)
Pyrimethanil
C12H13N3
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)
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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.
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
LHCproteins bindto
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 CO2fixation. 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?electrochemical
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 CO2
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 CO2into 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. O2can 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; PQH2plastoquinol
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inhibition. ATP and NADPH are then necessary for the
second step, i.e., the energy-consuming reductive conver-
sion of CO2 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 CO2fixation
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-
cides have also been reported to be toxic to nitrogen-fixing
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
synthesiswasnoticed.Phytoremediationwithmicroalgaehas
beenutilizedforareaspollutedwithnutrientsorheavymetals
(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
andis reflected byboth photosyntheticrate 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 lg g-1in 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
Bo ¨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
Bo ¨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
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capacity (Caspi et al. 1999). Sensitivity of PSII was con-
firmed with increased PSII inactivation under photoinhib-
itory conditions (Pa ¨tsikka ¨ 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 Mg2?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-1). The reduction in Pn is
always accompanied by reduced stomatal conductance.
The phytotoxicity of cuproxat (copper sulfate at 0.54 g l-1)
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],
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
contentsandcarotenoids
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 CO2 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
a phenyl-
afterfungicidetreatments
Table 2 Effects of contact fungicides on crop physiology
Affected parametersMolecules References
Inhibition of PnCopperVinit-Dunant et al. (2002)
Sulfur (kumulus)Ferree (1979), Ferree et al. (1999), Palmer et al. (2003)
Copper sulfate (cuproxat) Xia et al. (2006)
FludioxonilSaladin et al. (2003), Petit et al. (2008a, b)
Stomatal closure CopperVinit-Dunant et al. (2002)
Sulfur (kumulus)Palmer et al. (2003)
Copper sulfate (cuproxat)Xia et al. (2006)
Inhibition of CiCopper sulfate (cuproxat)Xia et al. (2006)
Inhibition of Rubisco Coppervan Assche and Clijsters (1990)
Decreased of chlorophyll
(synthesis or content)
CopperStiborova ´ et al. (1986)
FludioxonilSaladin et al. (2003)
Modification on chloroplast
ultrastructure
CopperSandmann and Bo ¨ger (1980), Baszynski et al. (1988),
Caspi et al. (1999), Szalontai et al. (1999)
PSII inactivationCopperBaro ´n et al. (1995), Caspi et al. (1999), Vinit-Dunant et al. (2002)
PSI inactivationCopperSamuelsson and Oquist 1980
Inhibition of other sites of
electron transport chain
CopperShioi et al. (1978), Sandmann and Bo ¨ger (1980), Uribe and Stark
(1982), van Assche and Clijsters (1990), Baro ´n et al. (1995)
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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-1), 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-N0-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-1, 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
5.6 kg ha-1DBU 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 ¨hle
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
treatment with
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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-3)
applications in radish crops (Panneerselvam et al. 1997)
and elephant foot yam (Gopi et al. 2005). By contrast,
cyazofamid (0.22 g l-1) 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
AnilidesInhibition of Pn FenhexamidPetit et al. (2008b)
Repression of Rubisco genes Fenhexamid Petit et al. (2008b)
Azoles Inhibition of PnCyazofamid Xia et al. (2006)
Stimulation of PnPaclobutrazol Hong et al. (1995)
TriadimefonKasele et al. (1995), Panneerselvam et al. (1997),
Gopi et al. (2005)
Stomatal opertureTriadimefon 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)
TriadimefonKasele et al. (1995)
Increased chlorophyll and
chloroplast contents
PaclobutrazolKishorekumar et al. (2006)
TriadimefonBuchenauer 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
EpoxiconazoleBenton and Cobb (1997)
BenzimidazolesInhibition of PnDibutylurea Shilling et al. (1994), Querns et al. (1998)
Chlorophyll declined Carbendazim Mihuta-Grimm et al. (1990), Garcia et al. (2002)
Carotenoids increasedCarbendazimGarcia et al. (2002)
Disorganization of chloroplasts DibutylureaShilling et al. (1994)
PSII inactivationDibutylurea Shilling et al. (1994)
Inhibition of electron transportDibutylureaQuerns et al. (1998)
Pyrimidines Inhibition of Pn PyrimethanilSaladin et al. (2003)
Modifications of pigment concentrations PyrimethanilSaladin et al. (2003)
StrobilurineStomatal closureKresoxim-methylGrossmann et al. (1999)
Increased chlorophyllKresoxim-methylGrossmann et al. (1999)
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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-1) 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
O2
CO
2
Fig. 2 Site of action of
different class of fungicides
observed in fungi. ER
Endoplasmic reticulum
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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.
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