Physiological and Molecular Plant Pathology


Oct 23, 2013 (5 years and 2 months ago)


Mechanisms of date palm resistance to Bayoud disease:Current
state of knowledge and research prospects
Cherkaoui El Modafar
Laboratory of Biotechnology Valorisation and Protection of Agro-Resources,Agro Biotech L02B005,University of Cadi Ayyad,Faculty of Science and Technology Gueliz,P.O.Box 549,
Marrakech 40 000,Morocco
a r t i c l e i n f o
Article history:
Accepted 30 June 2010
Date palm
Fusarium oxysporum f.sp.albedinis
Host defense mechanisms
a b s t r a c t
The Bayoud disease,caused by Fusarium oxysporum f.sp.albedinis (Foa),represents a major limiting
factor of date palm culture in Morocco and constitutes a serious threat to the date palm plantations in
Algeria and all other countries.Efficient disease prevention requires the development of resistant
cultivars.In Morocco,among the cultivars listed,only six appear to be resistant to Bayoud disease,but
they produce poor quality fruit.Thus,the Moroccan programof date palmgenetic improvement is based
on directed crossing between resistant cultivars and susceptible cultivars with good date quality traits to
select resistant genotypes producing high quality fruits.In addition to the separation of the resistance to
Bayoud disease and quality of the fruits characters,this breeding program is really complex due to the
sex separation in the date palm,the duration of juvenile phase which is very long,and the lifespan of the
date palmwhich requires a durable polygenic resistance.Then,the selected genotypes must be of female
sex,of good date quality,and possess effective defense mechanisms against the pathogen.Moreover,the
selection of the date palm resistance must necessarily take into account the mechanisms of pathogen
aggressiveness.In this review,we will present and discuss studies developed on the Bayoud disease of
the date palm,particularly on the disease control,the biochemical and molecular markers of resistance,
the program of date palm genetic improvement of resistance,the Foa pathogenicity factors,and host
defense mechanisms.It will also highlight the recent studies that showed that differential behaviour of
the resistant and susceptible cultivars was not related to a difference of induction of the defense
mechanisms,but to the suppression of their elicitation in the susceptible cultivars.
￿ 2010 Elsevier Ltd.All rights reserved.
Bayoud disease,caused by Fusarium oxysporum f.sp.albedinis
(Foa),appeared for the first time in 1870 in the Draa valley in the
south of Morocco [1].It was described as the most important
disease of date palm [2].The pathogen invades the plant through
the roots [3] producing foliar withering,and leading to the death of
the date palm tree [4].Foa produces typical micro- and macro-
conidia,as well as chlamydospores,allowing the pathogen to
survive under adverse environmental conditions [4].During this
century,Foa has been responsible for the destruction of two-thirds
of Moroccan palmplantations (more than 10 million trees) causing
considerable economic,ecological and social damage [2,5].Indeed,
the incidence Bayoud causes not only reduction in the production
of dates,the principal foodof humans and animals inthe desert,but
also an imbalance of the oases ecosystem (desertification,disap-
pearance of the subjacent cultures:cereal,fodder and vegetables
cultures and fruit trees).Consequently,the dense Moroccan palm
plantations were transformed in one century into clearings.
Morocco which was previously a date exporter has now to import
dates to satisfy its own internal consumption.Similarly,the Bayoud
disease destroyed more than 3 million trees in Algeria [6].The
Tunisian palmplantations,56% of which are made up of the Deglet-
Nour cultivar,are currently only protected by prophylactic methods
[7,8].This disease was also found in Argentina [9] and constitutes
a serious threat to the palmplantations of other countries.
Among the 223 cultivars listed in Morocco,only six appear to be
resistant to the Bayoud disease,but they produce poor quality fruit
[10].Genetic resistance represents currently the only effective
means to control this disease.The Moroccan programof date palm
genetic improvement is based on directed crossing between Foa
resistant and susceptible cultivars of good date quality,in order to
select genotypes combining the two characteristics [2].This review
represents a critical synthesis of the major researchapproaches and
Contents lists available at ScienceDirect
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0885-5765/$ e see front matter ￿ 2010 Elsevier Ltd.All rights reserved.
Physiological and Molecular Plant Pathology 74 (2010) 287e294
achievements on date palm resistance to Bayoud disease and
discussions will be developed and future prospects will be
considered so that research could progress successfully.
2.Pathogenicity and genetic diversity of Foa
In addition to the date palm (Phoenix dactylifera),Foa also
attacks the Canary Island palm (Phoenix canariensis) and other
species of palmaceae [11].Other plant-hosts may serve as symp-
tomless carriers of Foa such as Henna (Lawsonia inermis),alfalfa
(Medicago spp.),and clover (Trifolium ssp.) [11,12].Various aggres-
siveness levels were observed among the isolates obtained from
the date palm and those isolated fromsymptomless carriers,such
as the soil and the Canary Island palm [13e15].In addition,the
strains isolated from the rachis were found to be generally more
aggressive than those isolated from the roots [2,16].However,the
precise evaluation of pathogen aggressiveness encounters meth-
odological difficulties,particularly in the determination of the plant
growth stage susceptible to the pathogen and the great heteroge-
neity of the seedlings,because they have been obtained fromseeds
and not from identical in vitro clones.Moreover,the reduced
number of date palm cultivars presenting differential behaviours
does not allow completed studies on virulence to determine the
occurrence of physiological races.In order to overcome several of
these difficulties,studies were developed using molecular markers
to identify the isolates and to analyse their genetic polymorphism.
Thus,several molecular approaches (RAPD,RFLP,AFLP,SSR,etc.)
were developed and the first analysis distinguished the special
form“albedinis” fromnon-pathogenic (saprophytes in the soil) and
pathogenic forms of F.oxysporum fromother plants [17e19].
The restriction profiles of mitochondrial DNA showed that Foa
isolates from Morocco and Algeria constitute one RFLP group and
one RAPD group [17,20,21] although they present different
phenotypic characters [22].In addition,it was shown that the
genome of F.oxysporumcontains several copies of the transposable
element Fot1.The activity of these transposable elements can
explain part of the genetic variation observed in F.oxysporum
species [23].The study of Foa genetic diversity was deepened by the
use of the transposable element Fot1 like repeated and dispersed
genomic probe [21].This molecular marker allowed the distinction
of various profiles of Foa populations,but without any relationship
with their pathogenicity or geographic origin [5,21,24].Molecular
fingerprinting results were exploited to develop a specific test for
detection of Foa isolates amplified by polymerase chain reaction
(PCR).The presence of the transposable element Fot1 in F.oxy-
sporum species and the conservation of some copies in the special
forms suggested that Fot1 could play a role in the pathogenicity of
Foa [23,25].The transposable element Fot1 exists in several copies
in Foa,whereas it is either rare or absent in non-pathogenic and
other pathogenic special forms of Fusarium[5,18,21].The analysis of
all the genetic fingerprinting of the Moroccan and Algerian Foa
isolates allowed the identification of four DNA bands which remain
preserved and can thus have a role in the determination of the
special form“albedinis” [25].The insertion sites of two DNA bands
were cloned and sequenced to determine the oligonucleotide
sequences to be used as PCR primers in order to develop a sensitive
diagnostic tool for Foa detection.Two couples of primer pairs were
defined:BIO3-FOA1 and FOA28-TL3 [25].The primer pair BIO3-
FOA1 led to the identification of 95% of Foa isolates and the second
primer pair FOA28-TL3 identified 99% of the isolates.However,no
amplification was obtained by the two sets of primers in the
isolates of others pathogenic and non-pathogenic Fusarim species
(Fernandez et al.,1998).Similar results were obtained with Foa
isolates of Algerian origin [15,24,26].
3.Control of Bayoud disease
3.1.Prophylactic control
Prophylactic treatments don’t present a viable mitigation option
in Morocco since all the palmplantations have been contaminated
by Foa [2].Similarly,the palm plantations of the Western and the
central regions of Algeria are infected by Foa [27].However,the
Tunisian palmplantations are not infected by Foa and are currently
protected almost exclusively by prophylactic methods [8].
3.2.Chemical control
Since Foa is a soil-borne fungus and a vascular pathogen,chem-
ical treatments using fungicides appeared constraining,expensive,
and ineffective [28].Foa produces chlamydospores that allow the
pathogen to survive under adverse environmental conditions [4],
can survive in the plant vessels and at great soil depths [29,30].
Although chemical control was considered through the global
approach taking account of the plantesoilepathogen complex,
soil-borne and vascular pathogens are difficult to control even
with systemic fungicides [28].Moreover,these chemical products
constitute a potential source of pollution for the fragile oases
ecosystemand can exert a selective pressure on the Foa populations
leading tothe possible selectionof pathogenpopulations resistant to
the fungicides.
3.3.Biological control
In order to exploit the good date quality traits of some suscep-
tible cultivars (particularly Mejhoul and Boufeggous cultivars)
which are threatened with disappearance,research on soils
suppressive to Bayoud disease constitutes an alternative which was
the subject of many studies [31,32].The suppressive nature of some
soils was related to a microbial antagonismagainst Foa by bacteria,
particularly various species of Pseudomonas [33] and Bacillus [34],
actinomycetes [35,36],and fungal species in particular Aspergillus,
Penicillium[34] and saprophytic species of Fusarium[32].Thus,the
amendment of palm plantation soils by these antagonistic micro-
organisms to Foa was suggested as a biological control [37].The
use of mycorrhizal fungi represents another approach of biological
control.Thus,the mycorrhization of date palm seedlings by
arbuscular mycorrhizal fungi,in particular by species of Glomus,
reduced disease severity [38,39].By checking the receptivity of the
palmplantation soils to the mycorrhizal fungi,this approach could
constitute an effective alternative not only to protect the palm
tree against Bayoud disease,but also for the improvement of
mineral nutrition and tolerance to drought.However,these bio-
logical approaches to control by antagonistic micro-organisms and
mycorrhizal fungi remain far from practical application in this
particular ecosystem,where the introduction of these micro-
organisms could lead to their ecological rejection.
3.4.Selection of resistant genotypes of date palm
The selection and/or creation of genetically resistant clones
would constitute the most effective solution to safeguard palm
plantations against Bayoud disease.Basic work lasting 25 years
characterized the behaviour of the various cultivars of the date
palm to Foa [10].The use of vitroplants led to the control of the
inoculation technique and use of appropriate inoculum concen-
trations [40,41],two fundamental variables whose optimization
plays a significant role in determining the level of resistance of
a specific cultivar.However,one of the major problems in the
selection of resistant genotypes to Bayoud disease resides in the
C.El Modafar/Physiological and Molecular Plant Pathology 74 (2010) 287e294288
fact that the resistant cultivars do not produce good date quality
[10].So,the Moroccan programof date palmgenetic improvement
relies mainly on directed crossing,between resistant cultivars and
susceptible cultivars of good date quality,in order to select geno-
types combining the two characteristics [2].The selection of the
date palm trees resistant to Foa has been based on experimental
inoculation of seedlings and the observation of foliar withering
symptoms [2,41].Although this method made it possible to char-
acterize resistant clones [2,42],it remains time-consuming and
arbitrary and cannot guarantee that the plant will be resistant at
the adult stage.Indeed,this selection test is generallycarried out on
young seedlings and the inoculum concentration represents an
arbitrary variable in the discrimination of the behaviour of the
seedlings.Consequently,a genotype not expressing the foliar
withering symptoms,with a determined inoculum concentration
and at a specific developmental stage,can still develop themwith
a higher concentration and/or a more advanced stage of the
development of the date palm.Moreover,this selection test does
not make it possible to guarantee the durability of the selected
resistance.It may be that exploited resistance is monogenic and
thus easily surmountable by the appearance of new virulent races
of Foa.
4.Biochemical markers of date palm resistance
Many studies sought markers able to distinguish the resistant
and susceptible cultivars to Bayoud disease.Enzymatic poly-
morphism was used for the study of several enzymatic systems
particularly of peroxidases [43e45],esterases,oxidases [46],
hydrolases [47],and transferases [47,48] which have beenproposed
as biochemical markers for the selection of resistant genotypes.
However,these studies were mainly carried out in the leaves which
are not the target organ of Foa and not located in the sites of
penetration and colonization of pathogen,in particular the roots
and the rachis.Moreover,the studied enzymes are involved in
various physiological processes and could present quantitative and
qualitative variations depending on plant developmental stage [49]
and in response to various nutritional and environmental factors
[50] generally not controlled in these studies.In addition,these
biochemical markers could also be used for varietal identification
[45,51],response to somatic embryogenesis [52,53],sex identifi-
cation [54,55],date fruit quality [56] (Booij et al.,1995) and char-
acterization of resistance to Bayoud disease [43,44].However,the
required genotypes must possess effective defense mechanisms
directly involved in resistance expression,and not only enzymatic
markers which could be correlated positively or negatively with
several other physiological processes.Moreover,the concept of
markers is difficult to associate with a very complex physiological
phenomenon such as resistance,which depends not only on the
defense mechanisms of the host-plant,but also on the pathoge-
nicity factors of the parasite,and the environment.
5.Molecular markers of date palm resistance
Several works sought to identify cytoplasmic and nuclear
molecular markers of date palm resistance to Bayoud disease.
Various mitochondrial plasmid-like DNAs were identified and
characterized in the date palm[57].A study undertaken on six date
palm cultivars showed that the size of these plasmids was associ-
ated with resistance/susceptibility to Foa.In particular,a plasmid R
346 Pb) was shown to exist only in the resistant cultivars and
a plasmid S (1454 Pb) appeared to exist only in susceptible cultivars
[58,59].However,the widening of these studies to include several
other cultivars did not showa correlation between the presence of
mitochondrial plasmid-like DNAs and date palm resistance to
Bayoud disease [60e62].
Several studies were undertaken on the use of nuclear molec-
ular markers,in particular RAPD,SSR and ISSR markers,for the
identification of resistant cultivars [63e67],the analysis of genetic
diversity of date palm [68e71] and the relationship with the
resistance to Foa [66,72,73].However,these molecular markers did
not allow workers to distinguish between the resistant and
susceptible cultivars [66,72,73].
Although molecular markers generally reflect the structure of
the nuclear and mitochondrial genome and can assist the genetic
improvement program for the selection of resistant genotypes
to Bayoud disease,the guarantee of effective resistance resides in
a solid knowledge of the defense mechanisms directly involved in
the resistance of the host and the pathogenicity factors responsible
for pathogen aggressiveness.
6.Defense mechanisms and date palm resistance
6.1.Induction of tyloses in vessel cells
The induction of tyloses in plant vessel cells infected by vascular
pathogens,representing one of the typical mechanisms of defense
to vascular diseases [74],was identified in the date palm [75].
Tyloses are vesicular expansions of the adjacent parenchyma cells
and play an important role in the mechanical resistance of the
plants infected by vascular pathogens [74,76].In the date palm
infected by Foa,the accumulation of polymerized flavans in the root
vessels was highlighted by both histological [38] and biochemical
[77] approaches.The accumulation of these phenolic compounds in
the date palm vessels could be the result of tylose disintegration.
Indeed,tyloses can contain antifungal substances,in particular
phenolic compounds [78].While disintegrating,the tyloses pour
their phenolic contents in side the vessels directly in contact with
the pathogen [76].A positive relationship was established between
the restriction of the pathogen development in the plant vessels,
the increase in the flavan-3-ols contents,their polymerization to
proanthocyanidins and their mobilization in the tyloses towards
the vessel cells [76,78].
6.2.Induction of pathogenesis-related proteins
Pathogenesis-related proteins (PR-proteins) are monomeric
proteins of low molecular weight having a great stability under
very acidic pHand a strong resistance to proteolysis [79].These PR-
proteins are defense molecules synthesized by the plants in
response to pathogen infection [80].Chitinases and poly-
galacturonases were identified in date palm roots in response to
Foa [81].Although the involvement of PR-proteins in resistance is
not yet established in the date palmeFo
a interaction,these proteins
have a serologic homology with those of corn whose role in
chemical defense has been clearly established [82].
6.3.Accumulation of polyamines and phenolamides
Investigating the potential role of polyamines in the chemical
defense of date palmto Foa,it is reported that in vitro fungitoxicity
tests showed that these molecules did not have a fungitoxic effect
[83] and could even stimulate fungal growth [84].Inhibitors of
polyamine biosynthesis were found to inhibit the growth of Foa
[84].Although these results suggested that polyamines were
required for Foa development,it was suggested that these mole-
cules might affect defense mechanisms of date palm to Bayoud
disease [83].On the other hand,the accumulation of molecules
associated with phenolamides was identified in the rachis naturally
C.El Modafar/Physiological and Molecular Plant Pathology 74 (2010) 287e294 289
infected by Foa [85].The treatment of date palm seedlings with
exogenic polyamines resulted in an increase in phenolamide
content and mortality in infected and non-infected seedlings [83].
It appears that phenolamide accumulation could be a consequence
of stress related to the toxicity of polyamines.The accumulation of
phenolamides in the rachis [85] would be rather a consequence of
stress associated with drying and death of the palms (leaves and
rachis),rather than mechanisms of host defense.The accumulation
of phenolamides in the necrosed callus of date palm[86] confirms
this hypothesis.Indeed,the rachis used in these studies came from
date palm trees at the drying stage,whereas it is known that
defense reactions must be active at earlier stages in pathogenesis
and particularly before symptoms development.
6.4.Accumulation of caffeoylshikimic acid and post-inhibitins
Resistant cultivars were characterized by a rhizospheric activity
of Foa weaker than that of susceptible cultivars [87,88].This
difference was related to a differential effect of the root exudates of
the two types of cultivars [89,90].Root exudates of resistant culti-
vars inhibited conidial germination of the various isolates of Foa
whereas those of susceptible cultivars led rather to a stimulation of
germination [90,91].Thorough biochemical analysis carried out in
date palm roots showed that caffeoylshikimic acid is the major
phenolic compound in the roots [92,93] and represents the main
fungitoxic compound against Foa [94].The binding of caffeoyl-
shikimic acid by polyvinylpyrrolidone (PVP) [95] greatly decreases
the fungitoxicity of the root extract [94].In addition,caffeoyl-
shikimic acid contents increase after infection in resistant cultivars
while those of susceptible cultivars do not differ significantly from
those obtained fromnon-infected plants [77].The caffeoylshikimic
acid accumulating in the resistant cultivars are suggested to inhibit
growth and conidiogenesis of Foa,whereas the much lower
concentrations in susceptible cultivars have no effect [94].Simi-
larly,caffeoylshikimic acid inhibits both directly and indirectly the
activity and production of cell-wall degrading enzymes of Foa [96].
It generates hydrolysis products (particularly caffeic acid) and
oxidation products (quinones) which inhibit the activity and
production of polygalacturonases,pectinemethylesterases,poly-
galacturaonate trans-eliminases,cellulases and proteases [96].The
caffeoylshikimic acid was then associated with an inhibitin,and
caffeic acid and the quinones were associated with post-inhibitins.
These results suggest that Foa produces esterases hydrolysing the
caffeoylshikimic into caffeic acid and shikimic acid and tyrosinases
oxidizing the caffeoylshikimic acid and the caffeic acid in quinones
[96].These oxidation products of phenolic compounds are very
toxic against micro-organisms and play an important role in the
inactivation of pathogen enzymes [97e99].However,the caf-
feoylshikimic acid contents accumulated in resistant cultivars do
not completely inhibit conidial germination,myceliumgrowth[94],
and the activity and production of the cell-wall degrading enzymes
by Foa [96].The role played by the caffeoylshikimic acid in date
palmdefense against Bayoud disease is not sufficient to explain the
level of resistance observed on plants suggesting the involvement
of other constitutive or induced defense mechanisms.
6.5.Induction of phytoalexin biosynthesis
The inoculation of date palm roots with Foa induces the accu-
mulation of phytoalexins identified as coumarin derivatives,
propyl-7-aesculetin and hydroxy-5-propyl-7-aesculetin [100,101].
The time course of phytoalexin accumulation clearly distinguishes
resistant and susceptible cultivars [101].Thus,during the first
infectionphase (5e30 days),phytoalexin accumulation is rapid and
reaches much higher contents in the resistant cultivars,with
maximumaccumulation on the 15th day (2.36
mol g
FW).In the
second phase (30e60 days),a reversal occurs and susceptible
cultivars accumulate higher contents reaching a maximum on the
40th day,(2.96
mol g
FW) coinciding with generalized root
necrosis and foliar withering on the 15th day after inoculation
mol g
FW) [101].The phytoalexin concentrations accu-
mulated in resistant cultivars at the 15th day after inoculation
mol g
FW) strongly reduced conidial germination by
17e86%,germtube growth,conidiogenesis,and myceliumgrowth
of Foa.However,the concentrations accumulated in susceptible
cultivars (0.55
mol g
FW) had only a weak inhibitory effect
(16e27%).The role of phytoalexins in date palm resistance to
Bayoud disease is then related to the rapidity and intensity of their
accumulation at the fungitoxic concentrations during the initial
infection stage.The phytoalexins do not seem to be efficacious in
date palmwhen they are induced at more advanced stages,even if
they are produced at larges quantities.Although the phytoalexins
appear to support the defense of the resistant cultivars,they do not
play the major role in date palmresistance to Bayoud disease [101].
Indeed,the phytoalexins concentrations accumulated in resistant
cultivars only have a biostatic effect and they do not completely
suppress Foa growth.
6.6.Cell-wall reinforcement by cell wall-bound
phenols and lignification
The studies undertaken on the interaction between the cell-wall
degrading enzymes produced by Foa (polygalacturonases,poly-
galacturonate trans-eliminases,pectinemethylesterases,and
cellulases) and date palm cell walls show a relationship between
the susceptibility of root cell walls and the susceptibility of cultivars
to Bayoud disease [102].The cell walls of resistant cultivars are
more resistant than those of susceptible cultivars to the action of
pathogen’s hydrolytic enzymes.This differential susceptibility of
cell walls in resistant and susceptible cultivars to Foa is related to
the involvement of two constitutive defense mechanisms in cell
walls of the resistant cultivars [102,103].The first,a mechanical
mechanism involving lignin and cell wall-bound phenolic acid,
intervenes in the initial cell-wall degradation stages to limit the
action of the pectinolytic and cellulolytic enzymes of the pathogen
on the cell wall of resistant cultivars.Asecond chemical mechanism
intervenes at a more advanced stage to inhibit the production of
cell-wall degrading enzymes by Foa.This inhibition is related,at
least in part,to the intervention of cell wall-bound phenolic acid
[103].These cell wall-bound phenolics,identified as p-hydrox-
ybenzoic,p-coumaric,ferulic and sinapic acids [104],inhibit
mycelium growth and cell-wall degrading enzyme production by
Foa [103].The degree of inhibition of these cell wall-bound phenols
depends on the concentration and structure of the phenolic
compounds particularly methoxylation and hydroxylation.
Methoxylation increases inhibition,whereas hydroxylation
decreases it [103].The cell wall-bound phenol concentrations
accumulated in roots of resistant cultivars greatly reduce Foa
growth and production of hydrolytic enzymes,whereas the
concentrations found in susceptible cultivars have no significant
effect.The resistance of date palmcell walls to Foa pectinolytic and
cellulolytic enzymes is related to the intervention of constitutive
cell wall-bound phenols and lignin,which constitute a component
of a mechanical defense and to the inhibiting effects of cell wall-
bound phenols on the mycelium growth and the production of
pathogen hydrolytic enzymes constituting a second component of
a chemical defense.In addition,the inoculation of date palmroots
with Foa results in important modifications in cell wall-bound
phenols and lignin contents,which allow distinction of the
different cultivars according to their resistance/susceptibility to
C.El Modafar/Physiological and Molecular Plant Pathology 74 (2010) 287e294290
Bayoud disease [104].Thus,the post-infectional response of
metabolismof parietal phenols and lignin occurs early and is strong
in the resistant cultivars,whereas it is late and weak in the
susceptible cultivars.The cell wall-bound phenols accumulate in
resistant cultivars at fungitoxic concentrations during the first
infection stages.The rapidity and intensity of cell wall-bound
phenol accumulation and the lignification process in the roots in
response to Foa infection are also determinants of the resistance of
the date palmto Bayoud disease.
6.7.Elicitation and suppression of defense mechanism induction
The principal mechanisms of defense induced in the date palm
(caffeoylshikimic acid,cell wall-bound phenols,phytoalexins,post-
inhibitins,flavanes,lignin) depend on the phenylalanine ammo-
niaelyase activity (PAL) [105,106],the key enzyme of phenyl-
propanoid metabolism [97].It was shown that the differential
induction of the defense mechanisms in the resistant and suscep-
tible cultivars in response to infection by Foa was related to
a difference in PAL activity [107].Post-infectional PAL activity in
roots the resistant cultivars was faster and higher than in suscep-
tible cultivars.The induction of these defense mechanisms occurs
early and intensely in resistant cultivars,whereas it occurs late and
weakly in susceptible cultivars.A slow response would give the
pathogen time to grow abundantly and produce toxins [108e111]
interfering with the regulation of different physiological functions
in the plant,thus causing the typical symptoms of the disease.
The post-infectional induction of PAL activity was related to
a carbohydrate elicitor localized in the mycelial wall of Foa [107].
However,the culture filtrate was not a significant elicitor activity of
PAL,contrary to studies which reported an increase in the total
contents of soluble phenols in the date palm callus in response to
culture filtrate from Foa [112,113].Although simplified models
(callus and cell culture) have been used to study plantepathogen
interactions [114e118],it is difficult to extrapolate the response of
cells cultivated in vitro on artificial mediumto that of the date palm
placed in its real environment.Indeed,in the case of a vascular
disease such as Bayoud disease,Foa preferentially colonizes the
vessels and the true hostepathogeninteraction is established when
the fungus reaches the vascular system of the host-plant [74].On
the other hand,phenolic metabolism is very sensitive to various
mechanical [119,120],nutritional [121,122],drought [123],and
environmental [124,125] types of stress.Moreover,the phenolic
composition of the callus is very different from that of the date
palm tree.The increase in the phenol content of the date palm
callus in response to the treatment by the culture filtrate of Foa
[112] could be the consequence of a stress rather than a defense
reaction since the culture filtrate does not elicitor defense mecha-
nisms in the plant [107].However,particularly in the case of the
vascular diseases,the cell remains better adapted for the in vitro
creation and selection of the resistant genotypes to pathogen,but
not to the study of the defense mechanisms of the host-plant
Furthermore,although infection induced differential responses
in resistant and susceptible cultivars,the carbohydrate elicitor from
the mycelial wall induced an identical PAL response in all date palm
cultivars [107].The differences in PAL induction in response to
Bayoud disease and to a carbohydrate elicitor of Foa is related to
suppression of the PAL induction in the susceptible cultivars by
a soluble proteinaceous suppressor,produced constitutively by the
pathogen [129].Thus,the differential induction of defense mech-
anisms in resistant and susceptible cultivars does not relate to the
degree of PAL elicitation [107],but seems to be related to the
suppression of PAL gene expression by the pathogen suppressor.In
susceptible cultivars,PAL gene expression would be suppressed by
Foa,whereas in the resistant cultivars,the suppression would be
absent or substantially reduced [129].PAL suppression by Foa
seems to constitute a primary factor determining date palm
susceptibility to Bayoud disease.These results suggest that speci-
ficity in the date palmeFoa interaction was not explained by
a difference in defense mechanismelicitation,but by a difference in
the degree of suppression of the mechanisms.Early suppressor
production by the pathogen,in particular by germinating conidia,
may predispose plants to pathogen colonization before penetration
[105,129].The characterization of the PAL induction suppressor
represents an important focus for future work.
7.Conclusion and research prospects
Date palm resistance to Bayoud disease is related to multifac-
torial defense mechanisms,some of which are constitutive (e.g.,
caffeoylshikimic acid,post-inhibitins,lignin,cell wall-bound
phenols,flavans),and others are induced de novo (e.g.,phyto-
alexins,PR-proteins,tyloses).Depending on their role in the host-
plant defense strategy,these mechanisms can be categorized in to
two types:
￿ Mechanical mechanisms (lignin,cell wall-bound phenols,
tyloses) which limit the action of the cell-wall degrading
enzymes of Foa on the cell wall of date palmroot cells;
￿ Chemical mechanisms (phytoalexins,caffeoylshikimic acid,
post-inhibitins,flavans,cell wall-bound phenols,PR-proteins,)
which have been shown to inhibit Foa growth as well as the
activity and production of its pectinolytic,cellulolytic,and
proteolytic enzymes.
Date palm resistance to Bayoud disease also depends on path-
ogenicity factors of Foa which can be distinguished as follows:
￿ Cell-wall degrading enzymes which allowpenetration and host
tissue colonization by Foa;
￿ Carboh
ydrate elicitor which induces identical defense mecha-
nisms in resistant and susceptible cultivars;
￿ A proteinaceous suppressor that suppresses the elicitation of
defense mechanisms in susceptible cultivars;
￿ Toxins involved in the development of disease symptoms.
Furthermore,in the absence of direct studies on the complex of
genes involved in the expression of the Foa pathogenic capacity,
genomic analysis by molecular markers shows that the Moroccan
and Algerian isolates of Foa are genetically very similar and seemto
have the same clonal origin.
Overall,these results (selection of resistant genotypes,molec-
ular characterization of the determinism of sex and date quality,
host defense mechanisms and fungal pathogenicity factors) would
certainly contribute to the development of a more effective resis-
tance of date palmto Bayoud disease.However,any improvement
due to only one component of defense could be surmounted by
new pathogen populations likely to appear by selective pressure.
Indeed,the principal defense mechanisms of the date palm are
under the control of a key enzyme,PAL.It was demonstrated that
the Foa can suppress PAL induction,and lead consequently,to the
suppression of defense mechanisms in the host-plant.Any
improvement in PAL induction is likely to exert a selective pressure
during the coevolution of the plantepathogen interaction leading
to the appearance of new Foa isolates able to suppress the
expression of genes coding for PAL.Bayoud disease symptoms were
thus observed in some cultivars (IKL,SLY and BFGM) which are
known for their resistance to Foa [10,17].Consequently,although
resistant genotypes were obtained by directed crossings and mass
C.El Modafar/Physiological and Molecular Plant Pathology 74 (2010) 287e294 291
selection,the improvement program for Bayoud resistance must
necessarily take into account the mechanisms of pathogen
aggressiveness determined by its aptitude to produce pathoge-
nicity factors,which could overcome the selected resistance.These
findings demonstrate the urgent need to acquire complementary
elements in order to better manage the genetic strategy for
improving durable resistance in date palm.The continuation of
studies of molecular markers related to the sex determinism and
date quality [130,131] and the thorough knowledge of the defense
mechanisms involved in date palm resistance and the pathoge-
nicity factors of Foa,would make it possible to assist the selection
program.The association of a multitude of defense components
must be taken into account to reinforce the resistance level of the
host-plant and to avoid thus their suppression by the pathogen.
Integrated genetic and biotechnological approaches can be
considered for the improvement of date palmgenetic resistance to
Bayoud disease.The use of callus and cell culture could be
combined with an in vitro selection approach.Foa produces toxins
involved in the expression of disease symptoms [111],and these
toxins were tested for the selection of seedlings resistant to Foa
[72].It is then conceivable to seek a resistance against pathogen
toxins by exposing the callus or the cell suspensions to the action of
these toxins.This approach would make mass selection possible
very quickly.However,in addition to the difficulties encountered in
date palm for the regeneration of the plants from cells and callus
[27,132,133],these approaches would have a practical interest only
if the toxins produced by Foa are the primary determinants of the
symptoms of the Bayoud disease.The characterization of Foa toxins
and their biological activity will undoubtedly have a fundamental
and applied interest.If the toxins proved to be major determinants
of the symptoms of Bayoud disease,the creation of transgenic
plants with detoxification genes of toxins can be realized.Indeed,
the genetic transformation of plants in order to detoxify toxins
strongly involved in pathogenesis has been successful
[128,134,135].Therefore,it is probable that this approach would
useful,particularly if combined with the techniques of genetic
transformation and regeneration of date palm vitroplants
This manuscript was revised by Dr.Albert Sasson (International
Adviser in agriculture and biotechnology,senior consultant of
United Nations and UNESCO,member of the Hassan II Academy for
Science and Technology and the Royal Institute of Strategic Studies-
Morocco,author of several books in biotechnology),Dr.Abdellah
Oihabi (Director of FOA Program,KSA),Dr.Rachid Serraj (IRRI,
Philippines),Pr.Josiane Courtois (University of Picardie Jules Verne,
France),Pr.Abdelkarim Filali (Director of National pole of
Biotechnology,Morocco),Pr.Lahcen Hassani (Director of Doctoral
Centre of the Cadi Ayyad University,Morocco) and Dr.Jean-Pierre
Péros (Montpellier SupAgro,France).
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