Phenolic Compounds and their Role in Bio-control and ... - Iresa

Review Article 

Phenolic Compounds and their Role in Bio-control and 

Resistance of Chickpea to Fungal Pathogenic Attacks 

Mohamed Chérif, Arbia Arfaoui, and Azza Rhaiem, Laboratoire de 

Phytoapthologie, INAT, 43 Avenue Charles Nicolle, 1082 Cité Mahrajène, Tunis, 

Tunisia 

__________________________________________________________________________ 

ABSTRACT 

Chérif, M., Arfaoui, A., and Rhaiem, A. 2007. Phenolic compounds and their role in bio-control 

and resistance of chickpea to fungal pathogenic attacks. Tunisian Journal of Plant Protection 2: 

7-21. 

Chickpea is a major source of human and domestic animal food, particularly in developing countries. 

Chickpea may be attacked by different fungal diseases including Ascochyta blight, caused by 

Ascochyta rabiei, Fusarium wilt, caused by Fusarium oxysporum f. sp. ciceris (Foc), Botrytis grey 

mold, caused by Botrytis cinerea, rust, caused by Uromyces ciceris-arietini, collar rot, caused by 

Sclerotium rolfsii… These pathogens are difficult to control with cultural practices and chemical 

control is one of the most used approaches. Biological control and plant resistance, however, provide 

an environmentally and economically appropriate means for disease control that can be easily included 

within an integrated disease management strategy. In fact, the use of natural resistance for the 

management of fungal diseases in chickpea may be enhanced by means of biological control using 

either bacterial or fungal antagonists. Different biocontrol agents, including bacteria belonging to the 

genera Bacillus, Pseudomonas and Rhizobium and fungi such as nonpathogenic and nonhost Fusarium 

species, have been used successfully and resulted in significant reduction in both pathogenic fungal 

growth in vitro and disease development in planta. Different studies showed that induced resistance, 

through the accumulation of various phenolic compounds and phytoalexins, as well as the activation of 

peroxidases, polyphenoloxidases and key enzymes in phenylpropanoid and isoflavonoid pathways, may 

play a crucial role in the biological control and resistance of chickpea to pathogenic attacks. For 

instance, recent investigations revealed that the pre-treatment of chickpea seedlings with selected 

Rhizobium isolates before challenge with Foc, increased significantly the levels of total phenolics and 

the constitutive isoflavonoids, formononetin, and biochanin A. Protection of chickpea against Fusarium 

wilt by the nonpathogenic and nonhost Fusarium species was shown to be associated with the 

induction of the synthesis of the phytoalexins medicarpin and maachiain and the related isoflavones 

formononetin and biochanin A. Maakiain and medicarpin exhibited potent anti-fungal activity towards 

Fusarium spores, by inhibiting their germination and hyphal growth. Studies on phytoalexin tolerance 

in chickpea pathogenic fungi have also shown a relationship between virulence and the ability of these 

fungi to detoxify phytoalexins. This was examplified by the fact that the fungus Nectria heamatococca 

can metabolise and detoxify maakiain and medicarpin and that these reactions are required for 

pathogenesis by this fungus on chickpea. Among the other phenolic compounds studied, gallic, 

cinnamic, ferulic, and chlorogenic acids were also associated with the protection of chickpea from 

fungal attacks through induced resistance. Of the induced defenses, phenolics and phytoalexin 

production have received a particular attention in chickpea. However, more efforts are needed to 

provide good evidence that these compounds accumulate at the right time, concentration, and location 

and to elucidate the regulatory genes involved in their rapid and coordinated induction in response to 

fungal attack. 

Keywords: Chickpea, phenolics, phytoalexins, biocontrol, resistance, fungal diseases. 

__________________________________________________________________________ 

Tunisian Journal of Plant Protection 7 

Vol. 2, No. 1, 2007

Chickpea (Cicer arietinum L.) is, 

after soybean and pea, the third most 

important grain legume crop in the world 

and, along with French bean, soybean and 

alfalfa, one of the legume plants the most 

studied at the biochemical level for 

phenolics and phytoalexin responses (4, 

27). This plant is native of Syria, Southeastern 

Turkey and around the 

Mediterranean Basin, and constitutes a 

very important legume crop in North 

Africa (56, 73). In developing countries, 

it is an important source of high-quality 

protein for the poorer inhabitants. 

Chickpea is able to grow under poor soil 

conditions and can therefore be grown on 

marginal lands, where, owing to its 

capacity to fix nitrogen, it improves soil 

fertility (64). Chickpea occupies more 

than 10 million hectares of the cultivated 

areas in the world, with a total production 

of approximately 7 million tons and an 

average yield of 700 kg/ha (65, 66). Low 

yields are attributed to different factors, 

among which pathogenic microorganisms 

and insect attacks are 

considered the most serious. Nene and 

Reddy (57), reported many chickpea 

natural enemies, including 47 pathogens 

and 50 insects. Ascochyta blight of 

chickpea caused by Ascochyta rabiei, 

grey mould caused by Botrytis cinerea, 

rust caused by Uromyces ciceris-arietini 

and Alternaria alternata and Stemphylium 

sarciniforme attacks are considered as the 

most important and destructive foliar 

diseases of chickpea (60). As soil-borne 

fungi, Fusarium oxysporum f. sp. Ciceris 

(Foc), the causal agent of Fusarium wilt 

of chickpea, F. solani, F. eumartii, 

Rhizoctonia bataticola, Scleritium rolfsii, 

Pythium ultimum and Verticillium albo- 

Corresponding author: M. Chérif 

cherif.mohamed@inat.agrinet.tn 

Accepted for publication 30 July 2007. 

atrum are reported to be the most 

pathogenic (57). Besides these fungal 

enemies, chickpea may be attacked by 

more than 16 viruses and different 

pathogenic bacteria, including 

Xanthomonas campestris pv. cassiae, 

which is especially destructive on earlysown 

chickpea, and nematodes, such as 

Meloidogyne incognita, M. javanica, M. 

artiellia and Pratylenchus thornei (15, 

57). Despite the important number of 

chickpea natural enemies, Ascochyta 

blight and Fusarium wilt are always 

considered as respectively the first and 

the second most destructive diseases of 

chickpea (33, 59). Seeds infected by these 

pathogens are one of the main sources of 

inoculum and can be responsible of the 

introduction of these pathogens into 

disease-free areas. Therefore, planting 

pathogen free seed is the primary means 

to limit the introduction of these 

pathogens into a field and prevent the 

establishment of these diseases (64). 

Nevertheless, uninfected or treated seeds 

are not sufficient to prevent plants 

infection during the growing season. In 

fact, diseased debris and infected crop 

residues overwintering in and on the soil 

represent an efficient mechanism for the 

survival of these fungi from one season to 

another (35, 55). Cultural practices, such 

as planting date, sowing density and crop 

rotation proved to be very effective in 

reducing fungal attacks, but they are 

insufficient under high disease pressure, 

especially when weather conditions are 

particularly conducive to disease 

development. Among other control 

measures, such as fungicide treatments 

which are prohibitively expensive besides 

the problems relative to environmental 

pollution, chemical toxicity to humans 

and animals and fungal resistance, the use 

of resistant cultivars is probably the best 

way to manage these diseases (57). Many 

breeding and screening programs have 

been undertaken in order to obtain 

chickpea varieties with high levels of 

resistance to the major diseases of 

chickpea (18, 33, 40). However, the 


Vol. 2, No. 1, 2007

effectiveness of host resistance is 

curtailed by the presence or the 

appearance of virulent races of the 

pathogen, which is the case of Foc (14, 

39), or by the absence of complete 

resistance to the pathogen, case of 

Ascochyta blight where cultivars range in 

susceptibility to the disease (58). 

Biological control of chickpea 

major diseases. The use of resistant 

cultivars for management of chickpea 

diseases may be enhanced by biological 

control using either bacterial or fungal 

antagonists. Effective biocontrol of 

Ascochyta blight and Fusarium wilt of 

chickpea was achieved in our laboratory 

by using bacteria belonging respectively 

to the genera Bacillus and Rhizobium (1). 

Seventy-eight Bacillus isolates, most of 

which isolated from salty soils in Tunisia, 

were assessed in planta for their 

antagonistic activity against Ascochyta 

rabiei. Fungicides, such as Azoxystrobin 

(Quadris), Chlorothalonil (Banko) and 

Kresoxym-Methyl (Flint), were included 

in these experiments for comparison. 

Eleven of the tested isolates of Bacillus 

spp. appeared to be the most effective in 

reducing disease severity. Disease attack 

and severity recorded on the plants 

inoculated with these bacteria were 

significantly lower than those of the 

tested fungicides and the inoculated 

control. Moreover, these antagonists 

improved plant growth parameters, 

including the percentage of seedling 

emergence, plant height and plant weight. 

Arfaoui et al. (1) studied the 

antagonistic activities of 21 Rhizobium 

isolates in vitro in dual culture, and in 

vivo under greenhouse and field 

conditions against Foc race 0. In dual 

culture, 19 of these isolates inhibited the 

mycelial growth of the pathogen resulting 

in the case of the most effective isolates 

in a percentage of growth inhibition 

higher than 50%. Greenhouse and field 

experiments undertaken by these authors, 

using the susceptible ILC482 and the 

moderately resistant INRAT 87/1 

cultivars of chickpea, revealed the 

effectiveness of some of these isolates in 

reducing the percentage of wilted plants. 

In the greenhouse, the most effective 

Rhizobium isolate PchDMS reduced the 

percentage of wilted plants from more 

than 79% in the inoculated control to 

12.5% in the susceptible cultivar ILC482 

and from more than 54% to 8.3% in the 

moderately resistant cultivar INRAT 

87/1. Field experiments showed that in 

presence of the susceptible chickpea 

cultivar, although most of the studied 

Rhizobium isolates reduced the 

percentage of wilted plants, these 

reductions were not significantly 

different. However, very interesting 

results were achieved in presence of the 

moderately resistant cultivar INRAT 

87/1. For instance, Rhizobium isolate 

Pch43, which was very effective under 

greenhouse conditions, reduced the 

percentage of diseased plants from more 

than 48.6% in infected control plants to 

less than 8% in plants inoculated with the 

bacteria and infected with the pathogen. 

The best protection against disease was 

obtained with isolates Pch43 and Rh4, 

which reduced the percentage of wilted 

plants to less than 8%. Besides their 

beneficial effects on disease control, these 

studies showed that Rhizobium isolates 

may improve plant growth and yield. 

Biological control by using nonhost F. 

oxysporum isolates and incompatible 

races of the same forma specialis 

constitutes also a promising strategy for 

the management of Fusarium wilt of 

chickpea (14, 36, 37). Prior inoculation of 

germinated chickpea seeds with nonhost 

F. oxysporum isolates or incompatible 

Foc races protected effectively chickpea 

plants against a highly virulent isolate of 

Foc race 5 (36). These results were 

confirmed by the studies of Cachinera et 

al. (14), who showed that inoculation of 

germinated seeds with these antagonists 

delayed the onset of symptoms and 

significantly reduced the final amount of 

Fusarium wild caused by race 5. 


Vol. 2, No. 1, 2007

A growing body of evidence from 

several studies revealed that different 

mechanisms may be involved in the 

biological control of plant diseases by 

bacterial and fungal antagonists. These 

mechanisms may include antibiosis, 

direct parasitism, saprophytic competition 

for nutrients, competition for infection 

sites, and induced or enhanced host 

resistance (19, 22, 23, 30). These 

different modes of action are not 

necessarily exclusive of one another, and 

many of these mechanisms may be 

synergistically active and used by the 

same bio-control agent (22, 48). As far as 

chickpea is concerned, different 

investigations showed that induced 

resistance, through the accumulation of 

various phenolic compounds and 

phytoalexins, de novo synthesis of 

pathogenesis-related proteins as well as 

the activation of different enzymes such 

as chitinases, ß-1,3-glucanases, 

peroxidases, polyphenoloxidases and key 

enzymes in phenylpropanoid and 

isoflavonoid pathways, may play a crucial 

role in the biological control of chickpea 

diseases by antagonistic microorganisms 

(2, 3, 4, 6, 13, 14). In this bibliographic 

study we will focus on the roles of 

induced phenolic compounds and 

phytoalexins in the interaction of 

chickpea with bacterial and fungal 

antagonistic agents which should lead to 

biological control of the major diseases of 

this plant. 

Phenolic compounds in plants. 

Plants have the ability to synthesize a 

large number of aromatic substances, 

most of which are phenols or their 

oxygen-substituted derivatives (24). Most 

are secondary metabolites, which may be 

in the form of simple phenols and 

phenolic acids, quinones, flavones, 

flavonoids, flavonols, tannins, terpenoids, 

essential oils, alkaloids… All of the 

phenolics have one or more benzene rings 

with one or more hydroxyl groups that 

may be variously elaborated with methyl, 

methoxyl, amino or glycosyl groups. 

Some, such as terpenoids, give plants 

their odors and flavor; many compounds, 

like tannins and quinones, are responsible 

for plant pigment, and others, such as 

some alkaloids, may be toxic to the 

consumer. In many instances, these 

substances serve as plant defense 

mechanisms against predation by insects, 

herbivores and microorganisms (11, 24, 

74). Different studies showed that there 

are often large increases in phenolic 

synthesis in plants after attack by plant 

pathogens (26, 49). Phenolics that occur 

constitutively and function as preformed 

inhibitors are generally referred to as 

phytoanticipins, and those that are 

produced in response to infection by the 

pathogen are called phytoalexins and 

constitute an active defense response. In 

resistant plants, phenolic based defense 

responses are characterized by the early 

and rapid accumulation of phenolics at 

the infection site resulting in the effective 

isolation of the pathogen (20, 21, 28, 29). 

These physical responses may include the 

elaboration of cell wall thickenings and 

appositions, such as papillae, as well as 

the occlusion of plant vessels. These 

reactions are usually accompanied by the 

synthesis and deposition of lignin, a 

polymer of aromatic phenolics. Results 

from many studies suggest that 

esterification of phenols to cell wall 

materials and the accumulation and 

deposition of phenols in and on cell walls 

is usually considered as an increase in 

resistance to fungal hydrolytic enzymes 

as well as a physical barrier against 

fungal penetration. 

Phenolics present in healthy, 

uninfected plant tissues, as preformed 

antimicrobial compounds, that inhibit the 

growth of fungi may include simple 

phenols, phenolic acids, flavonols, some 

isoflavones… Those that are induced in 

response to fungal infection include 

phenolic phytoalexins, isoflavonoids, 

pterocarpans, furocoumarins, flavans, 

stilbenes, phenanthrenes… (43). All the 

above mentioned compounds originate 

through different branches of the general 


Vol. 2, No. 1, 2007

phenylpropanoid pathway, leading to the 

elaboration of various hydroxycinnamic 

acids and derivatives with antifungal 

activity. Confrontation of many of these 

compounds with fungi in vitro revealed 

their effectiveness in reducing fungal 

growth (Table 1). These studies seem also 

to indicate that hydroxycinnamaldehydes 

are more fungitoxic than 

hydroxycinnamic acids and 

hydroxycinnamyl alcohols (9). Among 

the cinnamics, caffeic and coumaric acids 

are widely distributed in plants occurring 

naturally in combination with other 

compounds, usually in the form of esters. 

For instance chlorogenic acid, the ester of 

caffeic with quinic acid, and ferulic acid 

were shown to be strong inhibitors of 

different fungal pathogens (43). Benzoic 

derivatives, such as 2,5- 

Dihydroxybenzoic acid and 2,5- 

dimetoxybenzoic acid, were very 

effective in inhibiting both spore 

germination and mycelial growth of 

different pathogenic fungi, including B. 

cinerea, Sclerotinia sclerotiorum, F. 

oxysporum, and Penicillium digitatum, 

Gleosporium album, in vitro, and in 

controlling disease development in vivo 

(44). Phenolics seem to inhibit disease 

development through different 

mechanisms involving the inhibition of 

extracellular fungal enzymes (cellulases, 

pectinases, laccase, xylanase,…), 

inhibition of fungal oxidative 

phosphorylation, nutrient deprivation 

(metal complexation, protein 

insolubilisation), and antioxidant activity 

in plant tissues (38, 47, 67). Lipophilic 

properties and the presence of a hydroxyl 

group in phenolics seem to play a major 

role in their antifungal activity, allowing 

respectively the penetration of biological 

membranes and oxidative 

phosphorylation uncoupling. 

Table 1. Phenolic compounds active in vitro against some plant pathogenic fungi 

Compound Target organism References 

Essential oils 

Penicillium spp., Botrytis cinerea, 

Fusarium oxysporum, Alternaria 

spp. 

Arras and Usai (7), Arras et al. (8), 

Reddy et al. (63) 

Cinnamic derivatives 

Cinnamic acid; 4-Coumaric acid; 3- 

Coumaric acid; Dihydrocaffeic acid; 

Ferulic acid; Sinapic acid. 

Sclerotinia sclerotirum; Alternaria 

spp; B. cinerea; Penicillium 

digitatum 

Lattanzio et al. (42) 

Flavonoids 

Apigenin-7-glucoside; (+)-Catechin; 

Luteollin-7-glucoside; Myricetin; 

Quercetin-3-rhamnoside; Quercetin- 

3-rutinoside. 

Alternaria spp.; Penicillium 

digitatum 


Benzoic derivatives 

Gallic acid; Syringic acid; 4- 

Hydroxybenzoic acid; 2,3-; 3,4- and 

2,5-Dihydroxybenzoic acid; 2,3-; 2,4- 

and 2,5- Dimethoxybenzoic acid. 

Alternaria spp.; B. cinerea; 

Penicillium digitatum 


Benzaldehyde; Methyl salicylate; 

Ethyl benzoate. 

Monilia fructicola; M. laxa; B. 

cinerea 

Tonini and Caccioni (72), Wilson et 

al. (75) 


Vol. 2, No. 1, 2007

Major phenolic compounds in 

legumes. The isoflavonoids, unlike most 

other flavonoids, show a very limited 

distribution in the plant kingdom, being 

largely confined to the legumes. Most of 

the biologically active isoflavonoids have 

been isolates from the legumes but this 

not preclude finding them in other plant 

families. Isoflavonoids are synthesized as 

part of the phenylpropanoid pathway and 

they show a wide range of biological 

activities. The three most important are 

the oestrogenic activities of simple 

isoflovonoids and coumestans, the 

insecticidal properties of rotenoids, and 

the antifungal and antibacterial properties 

of phytoalexins (73). Isoflavonoids play a 

key role in plant-microbe interactions, 

serving as the signal molecule for 

establishing the symbiotic relationship 

between plants and rhizobial bacteria that 

results in the formation of nitrogen-fixing 

root nodules. They are also the precursors 

to the major phytoalexins in legumes, 

indicating that the activation of their 

synthesis during the interaction of 

resistant plants with the pathogen 

provides a battery of defense compounds. 

Isoflavones and ptericarpans are the two 

largest of the about twelve classes 

constituting isoflavonoids. The four 

commonest isoflavones are daidzein 

(1,7,4’-trihydroxyisoflavone), 

formononetin (2,7-hydroxy-4’- 

methoxyisoflavone) (Fig. 1), genistein 

(3,5,7,4’-tridydroxyisoflavone) and 

biochanin A (4,5,7-dihydroxy-4’- 

methoxyisoflavone) (Fig. 1). 

Isoflavanones are less frequent than 

isoflavones and most of the products so 

far reported in the literature have 

antifungal activity, and have been 

characterized from phytoalexin 

investigations. Simple isoflavanones 

include 

dehydrodeidzein, 

dihydroformononetin 

and 

dihydrobiochanin A. Most of ptericarpans 

have been also isolated as phytoalexins 

and exhibit both antifungal and optical 

activity. They are conveniently devided 

into the ptericarpans, the 6ahydroxyptericarpans, 

and the 

ptericarpenes (73). Medicarpin (Fig. 1), a 

phytoalexin in many legume species, is 

undoubtedly the most widespread 

pterocarpan. Among the 27 members of 

the 6a-hydroxyptericarpans, pisatin was 

the first phytoalexin of this group isolated 

from pods of Pisum sativum (76). Over 

400 legumes have been studied for 

phytoalexins synthesis and most 

responded positively, with the production 

of one or more isoflavonoids. 

Induction of phenolic compounds 

and phytoalexins in chickpea. As 

indicated previously, different studies 

showed that induced resistance, through 

the accumulation of various phenolic 

compounds and phytoalexins, as well as 

the activation of oxidative and key 

enzymes in phenylpropanoid and 

isoflavonoid pathways, may play a crucial 

role in the biological control and 

resistance of chickpea to pathogenic 

attacks (2, 4, 13, 14). Plant protection by 

the biocontrol agents was generally 

associated with the accumulation of 

mRNA of defense genes, including the 

phenylpropanoid pathway gene encoding 

phenylalanine ammonia lyase (PAL), and 

secondary metabolites of phenolic nature 

(70). In the same context, Singh et al. 

(69), reported that treatment of chickpea 

seeds with Pseudomonas spp. increased 

the synthesis of cinnamic, ferulic and 

chlorogenic acids, which showed 

antifungal effects against Sclerotium 

rolfsii. Investigations, conducted recently 

in our laboratory, revealed that the pretreatment 

of chickpea seedlings with 

selected Rhizobium isolates before 

challenge with Foc, increased 

significantly the levels of peroxidases 

(POX), polyphenoloxidases (PPO), total 

phenolics and the constitutive 

isoflavonoids, formononetin and 

biochanin A (1, 2). These increases were 

particularly observed after pre-treatment 

with Rhizobium isolate PchDMS, which 

was reported to be the most effective in 


Vol. 2, No. 1, 2007

educing Fusarium wilt development (3). 

While the highest levels of POX were 

generally observed after 24 h of challenge 

with Foc, PPO and phenolics reached 

their highest levels 48 h later. Induced 

enzymatic activities and phenolic 

accumulation were usually higher in the 

moderately resistant cultivar INRAT87/1 

as compared to the susceptible cultivar 

ILC482. POX and PPO are known for 

their ability to oxidize several compounds 

particularly phenolics increasing their 

toxicity (17, 45, 71). They are also known 

to be important in symptom expression. A 

close relationship between increased 

activity of POX and PPO and appearance 

of symptoms in infected plant tissues was 

reported by several studies (12, 31, 51). 

POXs are usually associated with induced 

resistance (34, 61), and they are also 

implicated in several plant defense 

mechanisms such as lignin synthesis, 

oxidative cross linking of different plant 

cell wall components or generation of 

reactive oxygen species (53). 

Biochanin A 

Formononetin 

Medicarpin 

Maackiain 

Fig. 1. Chemical structure of the isoflavones biochanin A and formononetin and the phytoalexins medicarpin and 

maackiain produced in chickpea. 

In our experiments with Rhizobium 

antagonists and Foc, the maximum levels 

of formononetin and biochanin A were 

recorded in chickpea roots after 

respectively 10 days and 20 days of 

challenge with Foc. High performance 

liquid chromatography (HPLC) profiles 

revealed the presence of these 

isoflavones, both under free forms and 

glycosidically bound forms. 

Formononetin and biochanin A are 

synthesized constitutively in chickpea 

cells, stored as glycoside conjugates in 

the vacuoles, and upon elicitation with the 

antagonists and challenge with Foc, the 

amounts of these compounds show an 

important increase, through the 

conversion of glycoside conjugates to 

aglycons, which are themselves converted 

later to ptericarpans, such as the well 

documented compounds medicarpin and 

maackiain (Fig. 1) (2, 25, 46). In our 

experiments, the addition of phenolic 

extracts, obtained from roots of chickpea 


Vol. 2, No. 1, 2007

pretreated with Rhizobia and inoculated 

with Foc, to culture medium, inhibited the 

mycelial growth of the pathogen and 

induced marked changes in Foc 

morphology accompanied with the 

formation of numerous vesicles and large 

vacuoles within hyphal cells. These 

observed fungitoxic effects were 

presumably due to compounds such as 

medicarpin and maackiain, which were 

previously reported to be fungitoxic to 

Foc, causing the inhibition of spore 

germination and germ tube growth (70). 

In their studies, Stevenson et al. (70), 

demonstrated that medicarpin and 

maackiain have ED 50 values for spore 

germination of respectively about 80 and 

160 g/ml and that both phytoalexins 

caused 50% inhibition of germ tube 

growth at concentrations as low as 15 

g/ml. More importantly, these authors 

showed that the concentration of the two 

phytoalexins medicarpin and maachiain 

increased in roots of four chickpea 

cultivars inoculated with Foc races 1 and 

2. Concentrations of these phytoalexins 

were significantly higher in wilt resistant 

cultivars as compared to susceptible 

cultivars, both before and after challenge 

with the pathogen, indicating that they 

may be potential components of the 

resistance mechanism of chickpea to 

Fusarium wilt. The studies of Cachinero 

et al. (14) have also focused mainly on 

the role that phytoalexin synthesis and 

accumulation might have in the 

suppression of Fusarium wilt in chickpea 

plants induced by incompatible race 0 of 

Foc and nonhost isolates of F. 

oxysporum. In these experiments, prior 

inoculation (three days before challenge 

with Foc) with inducers delayed the onset 

of symptoms and significantly reduced 

Fusarium wilt caused by the highly 

virulent race 5 of the pathogen. 

Inoculation with the inducers gave rise to 

synthesis of the phytoalexins medicarpin 

and maachiain and related isoflavones 

formononetin and biochanin A. These and 

previous studies (4), showed that 

phytoalexins produced in response to 

induction and infection of chickpea roots 

were released into the liquid treatment 

carrier rather than accumulated in the 

roots. Therefore, these authors have 

analysed the levels of phytoalexins in 

inducer and challenger inoculum 

suspensions at the end of the inoculation 

periods and suggested that phytoalexin 

production is associated with the plant 

resistance response to the various 

inducers they have studied, and especially 

with nonhost resistance to nonhost F. 

oxysporum isolates. Moreover, Cachinero 

et al. (14), indicated that the mechanistic 

role of the phytoalexin response in 

induced resistance to Fusarium wilt in 

chickpea does not appear to relate to a 

plant sensitization process provoked by 

the inducing agents that enhances 

phytoalexin production after plantchallenger 

interaction, but it seems to be a 

consequence of the response developed in 

the plant by the prior interaction with the 

inducing agent. According to this 

assumption, biocontrol agents induce the 

expression of plant defense responses, but 

do not increase the plant’s potential for 

responding to subsequent challenge 

inoculation. Accordingly, the expressed 

defenses before challenge inoculation 

seem to interfere with the inoculum, and 

thus to contribute to induced resistance 

involved in Fusarium wilt suppression in 

chickpea. 

Phytoalexins (medicarpin and 

maackiain) and constitutive isoflavones 

(formononetin and biochanin A) and 

isoflavanones (homoferreirin and cicerin) 

were also induced in chickpea seedlings 

and cell cultures challenged with elicitors, 

such as yeast extracts, ATPase inhibitors 

(orthovanadate, 

N,N’- 

dicychlohexylcarbodiimide, and 

ionophores (carbonyl cyanide 3- 

chlorophenylhydrazone and nigericin). 

Barz and Mackenbrock (10) showed that 

elicitation of cell cultures leads to 

pronounced increases in the activities of 

biosynthetic enzymes with differential 

effects on the enzymes involved in 

conjugate metabolism. They indicated 


Vol. 2, No. 1, 2007

that low elicitor doses favour pterocarpan 

conjugate formation whereas high doses 

lead to pterocarpan aglycon accumulation 

accompanied by vacuolar efflux of 

formononetin and pterocarpan 

malonylglucosides. Armero and Tena (5) 

showed that the inhibition of the plasma 

membrane H + -ATPase, and particularly 

the proton efflux, may constitute a key 

step in the signalling pathway leading to 

the activation of phytoalexin and 

isoflavone production in chickpea 

seedlings. These authors assumed that 

external medium alkalinization, as a 

result of plasma membrane depolarization 

triggered by elicitors, is the main cause of 

the elicitation response, as has been 

concluded in different studies conducted 

previously with a significant number of 

elicitors (41, 50, 51). By investigating the 

signal transduction pathways in these 

systems, the mechanisms that control the 

production of these important 

phytoalexins and phenolic compounds 

can be discovered. 

Studies on phytoalexin tolerance in 

pathogenic fungi have also shown a 

relationship between virulence and the 

ability of fungi to detoxify phytoalexins. 

For instance, Miao and Vanetten (54) 

showed that Nectria haematococca 

mating type VI (MP VI), a fungus 

pathogenic on chickpea, can metabolise 

maackiain and medicarpin to less toxic 

products. These detoxification reactions 

are thought to be required for 

pathogenesis by this fungus on chickpea, 

which was tested by examining the 

phenotypes of progeny from crosses of 

the fungus that segregated for Mak genes 

controlling phytoalexin metabolism. In 

these studies, Mak1 and Mak2, two genes 

that individually confer the ability to 

convert maakiain to its 1ahydroxydienone 

derivative, were linked 

to higher tolerance of the phytoalexins 

and high virulence on chickpea. Mak1 

was also shown to be closely linked to 

Pda6, a member in a family of genes in N. 

heamatococca that encode enzymes for 

detoxification of pisatin. The gene Mak3, 

conferring the ability to convert maakiain 

to its 6a-hydroxypterocarpan derivative, 

was also shown to increase tolerance to 

the phytoalexin. Nevertheless, the 

contribution of this gene to the overall 

level of pathogenesis was not evaluated 

because of the low virulence of most of 

the progeny obtained from the cross 

segregating for Mak3. From these studies, 

the authors concluded that metabolic 

detoxification of phytoalexins seems to be 

necessary, as demonstrated in the Mak1 

and Mak2 crosses, but not sufficient by 

itself, as in the Mak3 cross, for high 

virulence of N. haematococca MP VI on 

chichpea. Use of mutants deficient in 

phytoalexin synthesis and elucidating 

biosynthetic pathways provide other 

approaches to evaluating the role of 

phytoalexins. Nevertheless, to our 

knowledge, these approaches have been 

studied using the Arabidopsis-camalexin 

system and other plant-phytoalexin 

systems rather than chickpea as a model. 

The accumulation of phenolics and 

phytoalexins, such as medicarpin and 

maackiain, is considered as a major 

defense mechanism frequently observed 

and well characterized in chickpea. These 

compounds were shown to accumulate 

both in roots and shoots in response to 

various fungal infections and elicitors, 

and their levels significantly increase in 

plants pre-inoculated with antagonistic 

microorganisms. These induced 

compounds seem to exhibit a rather 

unspecific antifungal character at 

physiological concentrations, enhancing 

the resistance of chickpea to various 

phytopathogenic fungi, including Foc, 

Nectria haematococca, Sclerotium rolfsii, 

Botrytis cinerea… Moreover, maackiain 

and medicarpin revealed a broad 

spectrum of activity against bacteria, 

phytopathogenic fungi and even 

zoopathogenic fungi (32). There is great 

potential for the use of these natural 

antifungal compounds and selected 

beneficial biocontrol agents as 

biofungicides and alternatives to 


Vol. 2, No. 1, 2007

fungicides in chickpea disease 

management. Despite the growing wealth 

of information indicating the importance 

of phenolic compounds and phytoalexins 

in resistance of chickpea to pathogenic 

fungi, the specific role of phytoalexins in 

disease resistance still remains to be 

demonstrated. In fact, much of the 

research in this domain has relied on the 

identification of induced antifungal 

compounds and correlating their presence 

with resistance. More studies aiming to 

provide good evidence that these 

compounds accumulate at the right time, 

concentration, and location to be effective 

in resistance are needed. Use of mutants 

deficient in their synthesis may provide 

also direct evidence for their importance 

as key mechanisms of resistance. 

Elucidating biosynthetic pathways, the 

enzymatic interactions between the key 

enzymes in the phenylpropanoid and 

isoflavonoid pathways and the 

transcriptional regulation of isoflavonoid 

synthesis provide other approaches to 

evaluating the role of phytoalexins. 

Cloning of genes of these key enzymes 

from chickpea and other legumes and 

their expression in other plants (legumes 

and non-legume plants) as well as the 

study of the mode of action of these 

enzymes may be also very useful in the 

elucidation of their role in resistance. 

Although most of the enzymatic steps 

involved in the biosynthesis of the major 

classes of phenylpropanoid compounds 

are now well established, and many of the 

corresponding genes have been cloned, 

less is understood about the regulatory 

genes involved in rapid, coordinated 

induction of phenylpropanoid defenses in 

response to fungal attack. Genetic 

engineering of legumes and non-legume 

plants can alter the production of these 

secondary metabolites and lead to the 

synthesis of novel isoflavonoids with 

significant benefits for disease resistance 

and human health. Transcriptional 

regulation of these pathways has to be 

also studied, with a particular focus on 

the transcription factors that activate gene 

expression during plant defense and 

plant-biocontrol agents interactions. Gene 

expression array analysis and metabolic 

profiling approaches constitute actually 

powerful tools to make comparative 

parallel analyses of global changes at the 

genome and metabolism levels, which 

will certainly facilitate the understanding 

of the relationships between changes in 

specific transcripts and subsequent 

alterations in chickpea metabolism in 

response to inoculation with biocontrol 

agents and infection with pathogenic 

fungi. 

__________________________________________________________________________ 

RESUME 

Chérif M., Arfaoui A. et Rhaiem A. 2007. Les composés phénoliques et leur rôle dans la lutte 

biologique et la résistance du pois chiche aux attaques des champignons pathogènes Tunisian 

Journal of Plant Protection 2: 7-21. 

Le pois chiche est une source majeure pour la nutrition humaine et animale, particulièrement dans les 

pays en voie de développement. Le pois chiche peut être attaqué par différentes maladies fongiques 

telles que l’anthracnose causée par Ascochyta rabiei, le flétrissement fusarien causé par Fusarium 

oxysporum f. sp. ciceris (Foc), la pourriture grise causée par Botrytis cinerea, la rouille causée par 

Uromyces ciceris-arietini, la pourriture du collet causée par Sclerotium rolfsii… Ces agents pathogènes 

sont difficiles à combattre par les pratiques culturales et la lutte chimique reste la méthode de lutte la 

plus utilisée. La lutte biologique et la résistance variétale offrent, toutefois, des moyens de lutte très 

appropriés sur les plans économique et environnemental et peuvent être inclus facilement dans le cadre 

d’une stratégie de lutte intégrée. En effet, l’usage de la résistance naturelle pour limiter les dégâts des 

maladies fongiques du pois chiche peut être amélioré par la lutte biologique faisant appel à des 

bactéries ou des champignons antagonistes. Différents agents de lutte biologique, tels que les bactéries 


Vol. 2, No. 1, 2007

ىعل 

appartenant aux genres Bacillus, Pseudomonas et Rhizobium et les champignons non pathogènes et 

non-hôtes du genre Fusarium, ont été utilisés avec succès et ont entraîné une réduction significative de 

la croissance de l’agent pathogène in vitro et du développement de la maladie in planta. Plusieurs 

études ont révélé que la résistance induite, à travers l’accumulation de composés phénoliques et de 

phytoalexines, ainsi que l’activation des peroxydases, des polyphénoloxydases et des enzymes clés des 

voies des phénylpropanoïdes et des isoflavonoïdes, peut jouer un rôle crucial dans la lutte biologique et 

la résistance du pois chiche vis-à-vis des attaques pathogéniques. A titre d’exemple, des études récentes 

ont révélé que le pré-traitement des plantules de pois chiche avec des isolats sélectionnés de Rhizobium 

avant l’inoculation par le pathogène Foc a conduit à une augmentation significative des niveaux des 

composés phénoliques totaux et des isoflavonoïdes constitutifs, formononetine et biochanine A. La 

protection du pois chiche contre le flétrissement fusarien au moyen des espèces non-pathogènes et nonhôtes 

de Fusarium a été démontrée être associée à une induction de la synthèse des phytoalexines 

medicarpine et maachiaine et des isoflavones apparentés formononetine et biochanine A. Les 

phytoalexines, maakiaine et medicarpine, ont révélé une très grande activité antifongique vis-à-vis des 

spores de Fusarium, et ce par l’inhibition de leur germination et croissance hyphale. Les études menées 

sur la tolérance des champignons pathogènes du pois chiche à l’égard des phytoalexines ont également 

montré une corrélation entre la virulence et la capacité de ces champignons à détoxifier les 

phytoalexines. Ceci a été illustré par le fait que le champignon Nectria heamatococca peut métaboliser 

et détoxifier le maakiain et la medicarpine et que ces réactions sont requises pour la pathogénie de ce 

champignon sur le pois chiche. Parmi les autres composés phénoliques étudiés, les acides gallique, 

cinnamique, férulique et chlorogénique ont été aussi associés à la protection du pois chiche des attaques 

fongiques à travers la résistance induite. Des mécanismes de défense induits chez le pois chiche, la 

production de composés phénoliques et l’accumulation de phytoalexines ont reçu une attention 

particulière. Cependant, des efforts supplémentaires sont nécessaires pour fournir plus de preuves quant 

à l’accumulation de ses composés au bon moment, à la bonne concentration et au bon emplacement et 

pour élucider les gènes de régulation impliqués dans leur induction rapide et coordonnée en réponse à 

une agression fongique. 

Mots clés: Pois chiche, composes phénoliques, phytoalexines, lutte biologique, résistance, maladies 

fongiques 

__________________________________________________________________________ 

ملخص 

.2007 

ومقاومة الحمص للأمراض الفطريّة.‏ 7-21 .Tunisian Journal of Plant Protection 2: 

الشريف،‏ محمد وعربية العرفاوي وعزّة رحيّم.‏ 

المرآبات الفينوليةّ‏ ودورها في المكافحة البيولوجية/الأحيائية 

يعتبر الحمص أحد المصادر الرئيسية لتغذية الإنسان والحيوان،‏ بشكل خاصّ‏ في الدول النامية.‏ يمكن للحمص أن تصيبه 

العديد من الأمراض الفطريّة بما في ذلك اللفحة الناجمة عن 

ومرض الصدأ الناجم 

، والتص ‏ّوف الرماديّ‏ الناجم عن 

عن ،Uromyces ciceris-iarietin وتعفن التاج الناجم عن ...Sclerotium rolfsii تصعب مكافحة هذه الأمراض 

بالاعتماد على المكافحة الزراعية وتمثل المكافحة الكيميائيةّ‏ الطريقة الأآثر استعمالا.‏ تمثل المكافحة البيولوجية/الأحيائية 

واستعمال الأصناف النباتية المقاومة للأمراض الطرق المناسبة من النّواحي الاقتصادية والبيئيّة ويمكن إدراجهما ضمن 

إستراتيجية مكافحة متكاملة.‏ إن استعمال المقاومة الطبيعيّة عند نبات الحمص للحد من الإصابات بالأمراض الفطريّة يمكن 

استحثاثها بواسطة المكافحة البيولوجية التي تعتمد على استعمال مضادات بكتيريّة أو فطريّة.‏ لقد وقع استعمال العديد من 

و Rhizobium والفطرية غير الممرضة من نوع 

الكائنات المضادة منها البكتيرية مثل و 

والتمكن من الحد بصفة حاسمة من نمو الفطر الممرض في المخبر ومن تطور المرض في الحقل.‏ لقد 

أظهرت العديد من الدراسات أنه يمكن للمقاومة المستحثّة من خلال تراآم المرآبات الفينولية والفيتوألكسينات وآذلك 

تنشيط الأنزيمات من نوع بيروإآسيداز وبولي فينولوإآسيداز والأنزيمات الأساسية لدروب الفينيلبروبانويد 

والإيسوفلفونويد أن تسهم بدور مهم في المكافحة البيولوجية و نسبة مقاومة الحمص للأمراض الفطرية.‏ سبيل المثال،‏ 

أظهرت البحوث مؤخرا أن معالجة نباتات الحمص مسبقا بعزلات منتقاة من الجنس البكتيري Rhizobium قبل إلقاحه 

بالفطر الممرض قاد إلي زيادة هامة في مستويات المرآبات الفينوليّة الإجمالية والإيسوفلفونويد الأساسية،‏ 

الفورمونونتين والبيوآنين أ.‏ آما بينت النتائج أن حماية الحمص من مرض الذبول الناتج عن بواسطة أنواع 

غير الممرضة تتم بتنشيط إفراز مادتي الفيتوألكسين،‏ المديكربين والمكيان والمرآبات ذات الصلة 

Fusarium والذبول الناجم عن ،Ascochyta rabiei 

،Botrytis cinerea 

Foc 

Pseudomonas 

Bacillus 

oxysporum f. sp. ciceris (Foc) 

،Foc 

Fusarium 

Fusarium 


Vol. 2, No. 1, 2007

بالإيسوفلفونويد،‏ الفورمونونتين والبيوآنين أ.‏ وأظهرت مادتي الفيتوألكسين،‏ المديكربين والمكيان،‏ فاعلية عالية ضد 

وذلك بالحد من نسبة إنبات الأبواغ ونمو الغزل الفطري.‏ لقد بينت دراسة طاقة التحمل عند الفطريات 

الممرضة للحمص للفيتوألكسين علاقة وثيقة بين نسبة الإمراض وقدرة الفطر على إزالة سمية الفيتوألكسين.‏ وتم توضيح 

قادر على إزالة السمية وتفكيك المديكربين 

هذه الظاهرة بالدراسة التي بينت أن الفطر 

والمكيان،‏ وأن هذه العملية ضرورية حتى يستطيع هذا الفطر إصابة الحمص.‏ من بين المرآبات الفينوليّة الأخرى التي 

وقعت دراستها واعتبارها ضمن المواد الحامية للحمص ضد الأمراض الفطرية وجود الحامض الغال ‏ّي والحامض القرفوي 

والحامض الفيرول ‏ّي والحامض مولّد الكلور.‏ ومن بين آليات المقاومة التي يقع استحثاثها لدى الحمص والتي وقع الاهتمام 

بها آثيرا نجد إنتاج المرآبات الفينوليّة وتراآم مواد الفيتوألكسين.‏ ولكن لابد من مجهودات إضافية لتقديم المزيد من 

المعلومات والبينات على أن تراآم هذه المواد يقع في الوقت المناسب وفي المكان المناسب وبالكميات المناسبة وآذلك 

للكشف وتشخيص المورثات الجينيّة المعدلة والمتسببة في التنشيط السريع والمنسق للرد على الإصابة بالفطر الممرض.‏ 

Nectria heamatococca 

،Fusarium 

آلمات مفتاحية:‏ الحمص،‏ مرآبات فينوليّة،‏ فيتوألكسين،‏ المكافحة البيولوجية/الأحيائية ، أصناف مقاومة،‏ أمراض فطرية 

__________________________________________________________________________ 

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