REVIEW

Fungicide impacts on photosynthesis in crop plants

Anne-Noelle Petit • Florence Fontaine •

Parul Vatsa • Christophe Clement •

Nathalie Vaillant-Gaveau

Received: 27 March 2011 / Accepted: 12 January 2012 / Published online: 1 February 2012

� 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

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. Clement �N. Vaillant-Gaveau (&)

Laboratoire de Stress, Defenses et Reproduction des Plantes,

URVVC EA 2069, Universite de Reims Champagne-Ardenne,

UFR Sciences Exactes et Naturelles, Batiment 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

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

Inhibit several enzymes involved in respiration and this multi-site action

(Leroux 2003)

Kumulus

Sx

Inhibit several enzymes involved in respiration and this multi-site action

(Leroux 2003)

Cuproxat

3Cu(OH)2CuSO4

Inhibit several enzymes involved in respiration and this multi-site action

(Leroux 2003)

Strobilurine

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 (Hanbler 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)

316 Photosynth Res (2012) 111:315–326

123

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

Clement 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 CO2 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

Fungicides,

Formules

Structures Primary mode of action in fungus

Hexaconazole

C14H17Cl2N3O

Sterol C-14 demethylation inhibitor (Debieu et al. 1995)

Propiconazole

C15H17Cl2N3O2

Sterol C-14 demethylation inhibitor (Gaitan 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)

Photosynth Res (2012) 111:315–326 317

123

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 CO2 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? 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 CO2 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. O2 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; PQplastoquinone; PQH2 plastoquinol

318 Photosynth Res (2012) 111:315–326

123

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 CO2 fixation

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

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 Clement 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 (Baron 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-1 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

Boger 1980). Copper alters the lipid chloroplast membrane

(Szalontai et al. 1999), affecting light reaction processes,

especially those associated with PSII (Baron 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

Boger 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

123

capacity (Caspi et al. 1999). Sensitivity of PSII was con-

firmed with increased PSII inactivation under photoinhib-

itory conditions (Patsikka 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], 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 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

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

ultrastructure

Copper Sandmann and Boger (1980), Baszynski et al. (1988),

Caspi et al. (1999), Szalontai et al. (1999)

PSII inactivation Copper Baron 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 Boger (1980), Uribe and Stark

(1982), van Assche and Clijsters (1990), Baron et al. (1995)

320 Photosynth Res (2012) 111:315–326

123

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 treatment with

5.6 kg ha-1 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 (Kohle 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; Kohle

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

123

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

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

123

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

CO2

Fig. 2 Site of action of

different class of fungicides

observed in fungi. EREndoplasmic reticulum

Photosynth Res (2012) 111:315–326 323

123

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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