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374
To successfully infect plants, pathogenic fungi must recognize andcommunicate with their host during different stages of the diseasecycle. In past years, techniques such as insertional mutagenesis,sensitive GFP-based reporter systems and microarray techniqueshave been developed to analyze these processes at the molecularlevel, and now novel insights into this fascinating aspect ofpathogen–plant communication are beginning to emerge. This isexemplified by a number of pathogenicity genes functioning indistinct stages of pathogenic development in
Magnaporthe grisea 
.
Addresses
Abteilung Organismische Interaktionen, Max-Planck-Institute fürterrestrische Mikrobiologie, Karl-von-Frisch-Straße, D-35043Marburg/Lahn, Germany
*
e-mail: kahmann@mailer.uni-marburg.de
e-mail: basse@mailer.uni-marburg.de
Current Opinion in Microbiology
2001,
4
:374–3801369-5274/01/$ see front matter © 2001 Elsevier Science Ltd. All rights reserved.
AbbreviationGFP
green fluorescent protein
Introduction
Approximately 10% of all fungal species known can causediseases in plants. Some of these fungi are obligate parasitesand remain associated with their host plant for their entirelife cycles, whereas the saprophytic fungi can proliferate onlive as well as dead plant material. Between these extremesare the nonobligate parasites that depend on the plant forcertain stages of their life cycles. These differences in lifestyle require specific adaptations to the host. Whereassaprophytic fungi presumably only need to overcome thehost defence system and may do so efficiently by killinghost cells through the production of specific toxins and/or bysecretion of lytic enzymes, the interplay between biotrophicfungi and plants must be finely tuned through signals fromboth partners. Obligate biotrophic pathogenic fungi, such asthe rusts and the mildews, live in intimate contact with theirhosts without eliciting cell death and defense responses,whereas necrotrophic pathogens may cause necrosis inadvance of penetration. Facultative biotrophic pathogenscan be cultured axenically but, as in
Ustilago maydis
,completion of the sexual life cycle may require intimatecontact with the host plant. Hemibiotrophs like
 Phytophthorainfestans
,
Cladosporium fulvum
,
 Magnaporthe grisea
and
Colletotrichum
species can complete their life cycles outsidethe plant, but develop specialized structures during infectionthat are not found during axenic growth.The life cycle of all these pathogens starts with sporegermination followed by hyphal growth on leaf or rootsurfaces. Chemical and physical signals can be involved ininduction of appressoria, specialised infection structuresthat penetrate through the plant cuticle and epidermallayer by generating high internal turgor pressure.Alternatively, natural openings such as stomata and woundsare used for entry. With the development of the haustorium,the intracellular absorbing organ of obligate or facultativeparasites, the host metabolism is successfully converted tothe requirements of the fungus [1]. The involvement of cAMP and mitogen-activated protein (MAP) kinase signalingin early communication with the plant has been emphasizedin several systems and is the subject of excellent recentreviews [2–4]. However, the distinct steps of the programsthat involve differentiation of the pathogen in the plantenvironment are largely uncharacterized. In particular, it isfor the most part unknown which plant compounds triggerfungal proliferation and development.In this review, we focus on genes expressed during fungalinfection and the knowledge about their role in pathogenicdevelopment, and describe strategies that serve to identifysignals and signaling pathways leading to their induction.
The identification of fungal genes that aredifferentially expressed during plant colonization
The interest in fungal genes specifically expressed duringcontact with the plant is nurtured by the idea that suchgenes will play a crucial role during pathogenic develop-ment. The identification of plant-induced genes canproceed through many different techniques: differentialdisplay, subtractive hybridization, protein purificationfollowed by reverse genetics, enhancer or promoter trappingapproaches, mutational screens, and
serial analysis of geneexpression
(SAGE) or array-techniques if the genomesequence or sufficient numbers of 
expressed sequence tags
(ESTs) are available.Several different methods have been established thatinduce developmental stages of various fungi that arenormally restricted to infected tissue. For example, in
Uromyces
species, early stages of development can beinduced on synthetic membranes; alternatively, intracellularinfection structures can be isolated directly from plants[5,6]. In other pathogens such as
C. fulvum
and
 P. infestans
,conditions of nitrogen and carbon deprivation induce genesthat are normally induced during infection ([7] and referencestherein; [8]). For
U. maydis
, evidence has been providedto show that embryonic maize cells produce diffusiblesubstances that allow the fungus to complete its sexualcycle without being in direct contact with the plantmaterial [9
]. In combination with reporter genes, such as
β
-glucuronidase
and
green fluorescent protein
(GFP), the
Fungal gene expression during pathogenesis-relateddevelopment and host plant colonization
Regine Kahmann
*
and Christoph Basse
 
Fungal gene expression
Kahmann and Basse 375
Table 1Fungal genes expressed during pathogenesis-related development.
Gene(s)PathogenPutative function/homologyExpression during infection Mutant phenotypeReferences(inducer)
Initial host contact
cap3,5,20,22C. gloeosporioide
Appressorial wall (CAP20,22)Host surface, invasionNonpathogenic (cap20)[5] —unknown (CAP3,5)(avocado surface wax)
CHIP1,2,3C. gloeosporioide
Ubiquitin-conjugation (CHIP1) Host surface (hard surfaceND (CHIP1), not essential – unknown (CHIP2, CHIP3)contact and ethylene)for pathogenicity (CHIP2,3)[18,19]
MPG1M. grise
HydrophobinAppressoria (nitrogen starvation)Appressoria formation [21]reduced on hydrophobicsurface, pathogenicity reduced
ipiOP. infestan
UnknownGerminating cysts, appressoria,ND[7]and invading hyphae (carbonstarvation)
PKS1, THR1,C. lagenariu
Melanin biosynthesisAppressoriaAppressoria lack[22]
SCD1
melanization,pathogenicity reduced
PCCUTINASPhytophthora capsici 
CutinaseUpon host contactND[25]
cutAB. cinere
CutinaseGerminated conidia andpenetration pegs (cutinmonomers)Not essential for pathogenicity[26]
clpg2Colletotrichu
EndopolygalacturonaseConidia, appressoria,ND[12
]
lindemuthianum 
penetrating hyphae
pelAF. solan
f.sp.
pisi 
Pectate lyaseOn pea epicotyl (pectin)Not essential for pathogenicity[29
]
pelDF. solan
f.sp.
pisi 
Pectate lyasePenetrationNot essential for pathogenicity[29
]
Response to plant defenses
CgDN3C. gloeosporioide
Suppressor of plant defenseEarly infection stageNonpathogenic[30
]
PDA1N. haematococc
Pisatin demethylase
*
Early infection stage (pisatin)Reduced lesion size[31,35]
PEP5N. haematococc
Efflux carrier
*
Early infection stageReduced lesion size[37
]
avenacinaseG. graminis 
AvenacinaseNDNonpathogenic on oat[32,34]gene
Avr4,9, Ecp2C. fulvum 
Avirulence proteinsBiotrophic growthPartially reduced in [8]pathogenicity
mig1U. maydi
UnknownBiotrophic growthNot essential for pathogenicity[14
]
ABC1M. grise
ABC transporter
*
Biotrophic growthNonpathogenic[38
••
]
FoTom1F. oxysporu
TomatinaseAll infection stages ND[33
]f.sp.
lycopersici 
(
α
-tomatine)
Tom1S. lycopersic
TomatinaseAdvanced infection stageNot essential for pathogenicity[36]
Acquiring nutrition
PIG1U. faba
Vitamin B1 biosynthesisHaustoria, infected leavesND[6]
PIG11,16,28U. faba
Metallothionein, cytochromeStrongly upregulated in ND[6]P-450 monooxygenase,haustoria and infected leavespeptidyl-prolyl cis-transisomerase
PIG2U. faba
Amino acid transporterHaustoriaND[41]
Necrotic phase
CHTG. sorgh
Cyanide hydratase
*
Infection stage (HCN)Not essential for pathogenicity[39]
ChtL. maculan
Cyanide hydrataseLate stage of infection (KCN)ND[40]
Cel1Claviceps purpure
CellobiohydrolaseInitial colonization phaseND[48]
pg1F. oxysporu
f.sp.EndopolygalacturonaseAll infection stages (pectin andNot essential for[43]
lycopersici 
galacturonic acid)pathogenicity
pgx4F. oxysporu
f.sp.ExopolygalacturonaseAll infection stages Not essential for pathogenicity[46]
lycopersici 
(pectin and PGA)
PGN1/PGX1C. carbonum 
Endo-exopolygalacturonaseAll infection stages (pectin)Not essential for pathogenicity[45]
Bcpg1B. cinere
EndopolygalacturonaseAll infection stagesReduced lesion size[44]
CLPG1C. lindemuthianu
EndopolygalacturonaseNecrotrophic stage (pectin)ND[27]
pl1F. oxysporu
f.sp.Pectate lyaseLate stage of infection (PGA)ND[47]
lycopersici cel2L. maculan
CellobiohydrolasesLate stage of infectionND[49]
HCf1-5C. fulvu
Hydrophobins Infection stage, upregulatedND[51]during sporulating (nitrogenand/or carbon starvation)
*
Expression during pathogenic development was not analyzed during the various stages of the disease cycle. ND, not determined; PGA,polygalacturonic acid.
 
376
Host–microbe interactions: fungi
activity of some of these genes that are differentially expressedduring plant colonization could be followed through thevarious stages of the infection cycle [7,10,11,12
,13
••
,14
].In the following paragraphs, we have divided the genesidentified into groups corresponding to events occurring onthe plant surface and during growth within the plant (Table 1).
The early phase: attachment, germination,appressorium development
Plant surface parameters determine initial developmentand can provide signaling cues, as exemplified by genesuniquely expressed at this stage in
Colletotrichum gloeosporioides
(Table 1) [5]. The function of these genes is unknown;however, they are selectively induced by waxes on thehost surface [5], and CAP20 is essential for appressoriumfunction [15]. For
Colletotrichum
species, it has also beendemonstrated that the plant hormone ethylene inducesboth germination and appressorium formation and, in doingso, probably links infection to the time of fruit ripening [5].The response to host wax and ethylene requires contact of conidia with a hard surface [16] and evidence exists, thathard surface contact induces Ca
2+
calmodulin signaling inthis fungus[17]. In extending these studies, a number of 
C.gloeosorioides
genes (
CHIP 
) that are expressed upon hardsurface contact were identified [18,19].
CHIP1
encodes afunctional ubiquitin-conjugating enzyme.
CHIP2
may be atranscription factor, and CHIP3 protein has been predictedto be membrane-localized.Hydrophobins are small, secreted fungal proteins thatassemble at hydrophobic/hydrophilic interfaces and thusmay be involved in adherence of fungi to the hydrophobicsurface of plants [20].Such a role may be fulfilled byMPG1, a hydrophobin of 
 M. grisea
that is expressed duringappressorium formation ([21] and references therein). Inthe same fungus,
 PTH11
was identified as a genuine path-ogenicity gene that is required for efficient appressoriumformation in response to cutin monomers as well as contactsurface hydrophobicity [13
••
].
 PTH11
encodes a noveltransmembrane protein, Pth11p, which is only weaklydetectable in the cell cortex and is redistributed to vacuolarmembranes upon appressorium induction, which mayindicate downregulation. Both appressorium formationand pathogenicity could be restored by cAMP treatment of two independent REM1 mutants lacking PTH11, suggestingthat Pth11p is an upstream activator of cAMP-mediatedsignaling or functions in an overlapping signaling pathway.On poorly inductive surfaces, Pth11p appears to repressappressorium differentiation and may thus direct thefungus to the appropriate site of entry [13
••
].Melanization of appressoria is necessary for their functionand key genes of melanin biosynthesis have been identifiedin
 M. grisea
and
Colletotrichum lagenarium
([22] and referencestherein; [23,24]). In
C. lagenarium
, the expression of threeof these genes is developmentally regulated [22].Successful penetration of the plant may not only dependon infection structure formation but may also be supportedby enzymes capable of degrading components of the plantcell wall. Cutinase genes that are induced during the earlyinteraction stage have been identified in several pathosys-tems (Table 1) [5,25,26]. In
Colletotrichum lindemuthianum
,an endopolygalacturonase encoding gene,
clpg2,
was tran-siently induced by pectin and showed expression ingerminating conidia, in appressoria, as well as in penetratinghyphae [12
,27]. In
Fusarium solani 
f. sp.
 pisi 
, the pectate
Figure 1
Strategies to identify regulatory componentsof plant-induced genes.
(a)
Identification ofa negative regulator (R). The promoter (P) ofa negatively regulated gene (
mig1
) is fusedto a selectable marker gene (
SM 
) and isectopically introduced into the fungalgenome. After UV-mutagenesis, strains areselected that express
SM 
. Candidates arethen analyzed for increased expression ofthe endogenous
mig1
gene to exclude cismutations.
(b)
Identification of positivelyacting cues. A strain is constructed thatcontains two reporter genes (for SM andGFP) each, fused to the regulated promoterof
mig1
. Three alternative methods foridentifying positive regulators of thepromoter are shown. (1) An expressionlibrary is introduced and strainsconstitutively expressing a positive regulator(Ac) are selected via SM. (2) Plantcompounds (PS) are screened for elevatedGFP expression levels. (3) AfterUV-mutagenesis, strains are isolated thatexpress
SM 
. In these mutants, componentsof the signaling cascade are constitutivelyactivated. The second reporter gene(forGFP) allows monitoring of the strengthof induction conferred.
AcAc
mig1mig1P SM mig1P 
GFP
mig1P SM mig1P 
PS
Current Opinion in Microbiology
UVExpressionlibraryUVR123
mig1mig1P SM mig1P 
R
(a)(b)
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