lor nulr~enls and space. Growlh and sporulat~on. 1. '7-7I-m produclion. I . -. - -- --. Dispers~on. D~sease i Enzymes. , and ~nfecl~on --' development secrellon.
Chapter 12
The Nature of Fungal Mycoparasitic Biocontrol Agents C. Corks-Penagos V. Olmedo-Monfil A. Herrera-Estrella
INTRODUCTION h4otlcr11agriculture depends primarily on a small fraclion of the many thousmls 01' pl:rnl species grown globally. As plants have been redisrributed h o ~ ntheir centers of origin, pests have followed, resulting in devastating incidents of disexscs such as potato late blight (PAytoplltot~litlfi)sftrns) (Fry c~ al., 1993). Plant diseases, caused by various pathogens such as viruses, bacteria, and fungi can lead to severe yield losses in agricultural crops. Recent wo~.ldwitlcestimates, however, show that regardless of the control mettiods available, a high percentage of the potential yield is still lost through diseases, pests, and weeds, especially in developing countries (Oerke, 1904). The risk ot'global spread of disease is increased by the reduced genetic diversity of ~iioclerncrops, compared with that of the related wild spccies. Extreme exa~nplesare coffee (Monaco, 1977) and banana (Stover and Sirnnio~ids,I987), of which si~igleclones, propagated throughout h e tropics, are susceptible to leaf rust caused by the fungus Mrtnilricl ~ u s l a ~ t . iand x black leaf streak caused by the fungus Mjlco.sl)/ltret.ell~~ fijietr.ris, respectively. Long-distance dispersal (LDD) in the air of spores from pliytopathoge~iicfungi has also contributed to the spread of several important diseases on a continental or global scale and allows the regular establish~iwntof diseases in new awas (Brown and Hovmoller, 2002). Most of these involve rusts, wllich may be more likely than other diseases to be
0 2007
I~iologic~trl C . ' o ~ r / of'l'lir~rt t~~l I)iscwses TIK I l ; i w o ~ ~l'rcss, Ii Inc. A l l righrs rcscrvcd.
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21 l ' l l l j cllh~tL~l~cc1 ;lLlu>>,; l l l c l eve11 ocl~vccll.coll~lllclll.hl)ccil~l\elllcll. S ~ ) O I ~ C S 1.c most able to tlckar cnviron~ncntalc h n l l c ~ i ~ (Rotc111 es cr al.. IOXS). Many pl;~nrpatllogcns have ovcrcornc pesticides a ~ ~; t~lg r i c u l ~ u ~pr;~cxl ces thar once held rhcm under control. Ar rhe wine ~ i n ~sc o, ~ cl'l'cctive ~ ~ c hcmicals, such as IIK fungicitlc mc~hylbromide, arc hcing prohil)itcd bc~ u s ot~health c and cnvironmcntal concerns. During rhc pas1 Sew dccndcs, i t as bccn cstablishetl that disease control should nor depend rotally on Iicmical control. but that other resources available should be utilized more I'ficiently. Consistently, plant researchers are developing a series of new raregies of pest control, from high-tech genetic engineering to tccl~niques )at induce a plant to turn up its own defense n~echnnismsto relatively low>chstrategies designed to disrupt plant-pathogen interactions, including iological control. Biological control has been used as a rnanagemenL tool for the control of wp and foresr pests, and for the restoration of natural sysrenis affected by werging pests. The developnient of the concept of biological control oc.~rredwith the gradual accumulation of our biological and ecological 11owledgeof nature. Biological control based o n fi~ngalspecies car1 reduce le amount of inoculuni or disease-producing activity of a plant pathogen, sually another fungus. This chapter compiles the knowledge accumulated I this area, presenting the most recent nclvances o n the mechanisms indved i n the establislime~itof parasitic interfungal associations. whether ist:~nce-~netliatedprocesses (antibiotic production) or contact-dependent ~echanisrns(mycopnrasitism). The chapter also includes an overview of le developments achieved in their use as biocon~rolagents and their future )ssibilities. 'The ~nycoparasiticassociations are dcscribetl Srom early events ~ c has host recognition lo larc processes, including host death ;11i0h e ilse 1' its cellular components as a source of nutrients. Mosr niycopi~ri~sites are msidered i n this review, wirh emphasis on those with greatest impact as ocontrol agents.
.
Protection of crops from diseases can ultimately improve agricultural ,oduction. Tlic Sirst line of dcfcnsc against plant pn~hogcnsis natural rcsisncc, which can oftcn be ~n~nsfcrrctl bcrwccn spccics by crossb~wtling. csis~antculrivars wcrc almost the only stl-atcgy lo avoid disease losses in c early days of plant protection. Rut breeding fill. ~.csistanccis timemsurning, and microbial pathogens quickly evolve to overcome tlic new ~nllenge.In the past decatlc. the traditional nlcrhods of plant brccding crc irilproved l)y the usc o f ~ r ~ o l c c u~narkers l ; ~ ~ . ant1 l l i C i ~ ~ c o ~ - l ) oofgc~-a~io~~
ncric cngi~~ccring. 'I'llc I;t~lcrgcr~cl-arcdgenetically nlotiilietl (GM) crops. new loo1 1.01.plan1 proleelion I ~ I ; I I itllows slaying a slcp :~lic;~tl of ritpi(l c v o l v i n ~pcsls. l'llc 1i1oslprorninc~i~ clcvclop~llcnrinvolved lllc 11':1nsl?r.01 gene c ~ l c o ( l i ;~I I ~ I si~lscct-killing prorein (131) 1'1.onl tltc Iwclcria Ilcrc~ill~ / l ~ o r i ~ t g i c ~ ~ ~inlo . s i . vclup planrs. including tomato, tobacco, and cotto (Fischhol'l' el al.. 1987: Vricck el al., 1087; Perlak cr al., 1093). Totlay, 131 ptx)tcctctl corii, cotton, and pot:tto have been cornmcrcializetl in rhe Unite< Slates, and one or more ol'rhese ~wotluc~s are mnrkeled in Argentina, Ail5 tralia. Canada, France, Mexico. and Soi~tliAfrica (.lames, 1998, 1999) rcsulli~igi n I-cducctlapplication ot'chcmical insccticidcs I'or some crops. Dcspire rhe early succcss of GM crops. this technology srill hirs somc pracrical problcrns lo solvc. For example, onc source of undesirable vari ability i n rransgcnic planls is the rantlorn location o f t h e transgcnc. Also i~~ispecil'ietl rnl~rarionsyc~ieraredtluring rissuc culrul-c. which is rlecdetl tc grow r~mslhrrncdcells into wholc plants, can induce unprcclicted rrairs o~ loss of desirable qualirics. Furlherrnore, the anti-GM movcnicnt, i n c l u d i ~ l ~ ecologisrs and olher scicntisrs, has long eu?t-cssed conccrns abour rhc 130tential inlpacr ofrclcasing GI: planrs into thc cnvironnlcnt. l'hcy havc b a w l thcir opposition mostly on thc transplanting of genes fronl completely tliffcrent organis~ilsinto crcy planls. Idowcvcr. the complexity 01' ecological systems intcrti.res wit11 ~ h prctliction c of r s k , benel'its. and inevitable unccrtainties of CilJ plrtnrs. A co~nprehensivereview of rhe potential impacts 01' releasing genetically engitlecrcd organisms into the environment is not given here. as several excellent and recent papers are available (I3etz ct ;I].. 2000: Wollknhcrger anti I'liil~cr,2000). Currcnlly, an alkrnativc slr;tlc:y 10 crop p~-olccliol~ is lhc sli~nt~l:~lion 01' 1)1;1111s'n;t1~11.;11 ~ C I ' C I I S C I I I C C ~ I ; I I I ~ S I I I ~ , eitlicr- Il~rouglltllc i ~ s c01' clmnicals or lhc i~lsertio~l of' genes I'rom plan1 par hogcns (Goxzo. 2003).
I I L L ' X L~l,~lIl>. l>loLollilcll (11 ~ 1 l i l l l L d l h ~ i l 5 ~L i5l l l OL. ilclllc\c~l sing a hroad sl)cct~.umot' 01-ganisms,from insects to l'u~lgi2nd bactcriit. Two t y l m of biological control arc recognized: tlic cl;lssical antl the nuncl:~tivc.Clxssicnl hiologicnl control can he tlcl'inccl as rhc importation of ~aturalenemies thr the control of exotic, invasivc spccics. On the other land, inundativc control (or mass release) involves ~nnssivcnpplica~ionof' he biocontrol agent that can be mn~.ketetland c~nployedin much the sanic vay as a conventional chemical pesticide. This later strategy i s used when latural enemies are expected to be insufficient to supp~csspest population rrowth. The conceptual rnodel underlying biocontrol was derived from the )redator-prey theol-y (Smith and van dell Bosch, 1,967; van Driesche and 3ellows, 1996) and is based o n the notion that exotic species become inva.ive by evading the controlling influence of their natural enemies (Keane 111dCrawley. 2002). In this model. the introduction of any hioco~ltrolagent esults in a self-sustaining, balanced system in which tllc pest population is naintainetl below some economically or ecologically del'ined threshvlcl, as ts fitness or conlpetitive edge is weakened (Evans iind Ellison, 1990). During the past two decades. there has been a rre~nenclousincrease in inerest and research o n biocontrol, clriveu by a se;lrch for more environmenally benign niethocls of plant protection. 'The use of biological control is not I new idea. Its conception was estnblisl~edbetween the I;w nineteenth anel w l y twentieth centuries, as biological antl ecological knowledge of the ~aturalworld was gradually accumulatecl. I n successful biocontrol pro[rams, the reduction of pest densities and recovery of adversely affected lora or fauna 1e;ids toward a system with better ecological balmice and .o~nmunitystructure. Following its establishment. successful natural enenics can provide enduring pest c o n r ~ dant1 ; they can rcl>licatc ;~mltlispcrsc vitllout continuxi hu~nanmallagement. C ; w s ol'succcs~ft~l biological conrol programs ngai~istnoxious insects, mites, wccds (aquatic and tcrresrial), plant pathogens, and vcrtebratcs are extensive, and well-rlocu~ncntcd ,xaniplcs exist (Mukcrji and Garg. 1948; Syrno~ldsonct al., 2002; 13losscy ~ n dHunt-Soshi. 2003; Werner and Pont, 2003).
~ O > C I I L CL!l
'l'he ability of' antagonistic fungi to inhibit thc development of plmt lathogens has hccn cxl)loitctl in biocontrol of agricultural pests. including he no st problc~ll;~tic groups insects ;11ltl l.i~ngi.Altllo~~gh tllc~'care olhcr )iocontrol agents, sucli as bacteria and viruses, tllere arc scvcral clear dvant;~gcsin utilizing rungi: ( I ) most fungal spccics h a w the ability to diccrly inl'ect thc l l ! hy ~ pc~lctratingits O I I ~ C , I .s t ~ r l ' ;w11crc;is ~ ~ ~ . \;i~-i~s ;incl 1x1~-
01' insect c o n t r o l ) i r i o r d e r t o lw cll'cc and ( 3 ) the generic. d i c e r s i r y o f f u n g i a l l o w s a n u m b e r o f ' b i o c o n t r o l ;IF 10 h c riia(!c l ' 1 ~ ) 1 1si i ~ i g l cspccics 01' l'1111gi. S o l l i e insccr species, i n c l u t l i n f i I I ~ ; I~IC~ S I~ S , arc ~;III~cIII;II.I~ s u s c e p l o i n f ' c c t i o n h y natural ly o c c u r r i n g , insect- parhogenic l'ungi. M a n y ol gericra ol' the s o - c a l l e d entornopathogenic f u n g i [hat have hccri stu, eirlier h e l o r i g t o tllc E n t o ~ r l o p h t l i o r : ~ l e s( Z y g o m y c o ~ ; ~o) r t o tllc H y l rnycetes (Deuterornycota). Recent r e v i e w s by Rut[ et al. (2001) a n d 5 a n d P c l l (2003) p r o v i d e t'urrhcr i ~ i f o r n ~ n t i o ab n o ~ r rrlle p i n c i p l c s a n d slr s i c s o l ' i ~ ~ s c cb ri o l o g i c ; ~ cl o n t r o l rncdiaccd b y fungi. F i l a n i c n t o ~ ~Sungal s pathogens cnusc diseases on a l l a g r i c u l l u r n l cr nrmnd the w o r l d , rcwlling in r n i l l i o n s o f tons of c r o p losscs arid hillier d o l l a r s i n lost r c v c l i u e annually. D c s p i t e t h e rnariy achievements o f disc c o n t r o l . c e r t a i n c u l t u r a l practices have a c t u a l l y enlianccrl the tlcstruc p o t e n t i a l o f 1'1111gaI p ; ~ r I ~ o g c ~(Table is 12.1). 'l'hc m a j o r i t y ol' tllc l'u~ I ~I;II ~ r c c t tl o Ilc 111gcslctl( i n c;isc
TABLE 12.1. Ernerging fungal plant diseases.
Disease
Pathogen
Host
Geographic distribution
Blast
Magnaporthe gr~sea
Rice
Asia
Cultural, chemcal
Sorgum, sweet corn
S.E. Asia, Africa, Australia
Natural resistance, chemical
Downy m~ldew
manage me^
Early blight
Allernaria solani
Potato, tomato
Worldw~de
Chemical
Gray mold
Dot~ytiscil~clan
Greenhouse crops
Worldwide
Cult~rral, chemical
Karnal bunt
lillelia indica
Wheat
N. America, India
Cultural, chemical
Potalo, tomato
Worldwide
Nalural resistance, chemical
Late blight
Rust
Puccinia melanocephala
Sugarcane
Americas
Natural resistance, chem~cal
Rust
Phakopsora pnchyrhki Phnkopsora ineiboriiiae
Soybean
S.E. Asia. Russia, S. America
Chemical
Wilt
Fr lsari~mi oxysporum
Tomato
Worldwide
Cullural, chemical. natural resistance
I l l l l t l C ~ h . U ' I i t h , ; l l I d OI11CI C I O I ) 1)IlgtlI> susceptible to the antagonism ol'orhcr fungi. The lil'cstylc ol'rl~cscIalcr :ties is quite variable. ranging from species rhat arc obligate pamsircs to nsc thar attack only weakened Ilosts, l o some ~ t i u arc t ;lpparcn~lycotnlllcnlo symbiotic fungi. Most of the Cungal species rliat have been selected as cont~.olagents against phytopathogens establish parasitic rclationsllips. Biological c o ~ ~ t r through ol fungal species is a potent means of reducing damage caused by fungal plant pathogens. Co~nniercializcdsystems for biological control of plant diseases are few, although interisive activity ~ r r c u t l ybeing geared toward the introduction ol';in increasing ni~nibcr fung;il biocontrol agents into the market ('Table 12.2). L l c 3 l ~ ~ ~ & l I l .( 8 ~ 1 lI u ~b)l hl .c .\IIlLIth.
F U N G A L A N T A G O N I S M IN T H E HIOLOGICA I, COIVTHOI, O F I'lf Y7'OPA 7'IIOGftt.r1,qotlio11r~.c.r 111igitlo.srrsand irs host K/li:,octotlirr .so/rllli revealed the formation of n nlicro pore that Ilows a direct cytoplasmatic connection (13auer ant1 Oherwinklcr 1990). A pilrticulnr.ity of hiotropliic ~nycopwasitesis that they are obliga~m parasites, because they arc incapable of surviving without their hosts, am they have a limited host I-ange. Piptocepl~/lis~rliis/)otuis :I biotrophit mycoparsite rh;lt f'orrns haustoria as attack structures, antl irs host range i rcstrictctl to the suhgcnus A d i c t n ~ i(Cuthbert ~ ~ ~ r :~ntlJcf'f'r.ies, 1984). Sj~ointl P . Y I ~ I. ~~( .~/ (I, II~IO ~ ~ ~ ' O I . Ia11d I I I I T~,IYI.Y/O/)CI.III(I o l i g o ~ ~ / p.otlu~e r ~ d ~ ~tl;~ustol.il~nl ~~~ like inl'cctio~istructures to attack sclcrotia of'Sclc~nli~/t~z c.e/)ivonrtrl, I1ott-j ris CI'IW~CN, and S O I ~ Cspecies belonging to the genus Sclernli~lic~ (Avers an( Atlanis, 1981 ; Rullock et al., 1986). The species grouped in this class :u-I ~iotsuit;lldc f'or I>ioconrrol,hcci~l~sc their Ilost dcpcridcncc 111akcstllc~r~ tlil'li cult to manip~latc. The most successf'l~lspecies in biological conrrol are those th:u establisl nccrotropliic intcrl'ung;d associations. Fungi grouped i n this class arc f'u cultalive p i ~ i x i t c[hat ~ c:~ngrow by using organic conlpountls ol'tlcatl malt rial, throl~gha s;~protrophiclifestyle. Bur rhcy arc also able to pnrxiti/c living hosrs i n 01-tierto obti~intlic'necessary nl~trients.The ~najorityof th co~n~ilcrci:~l hiocon~rolp.otl~~c[s listed in Tahlc 12.2 are l'o~-~m~lnrcd hy 11s ing nccrotropllic rnycoparasites (At1ipelo171yc~.s r/~~i.sq/~(//i.s, tt/itlilr~tl.v,/ ' J ~ / / I ~ IO/~~(III(/I.IIIII, III~ 7i1/r/ro111y:~.s j7m~/1.s,jrj~i(~llo(lc~rtt~(~ spp.. a m C;lioc(1di~t7/spp). This fact reflects the relevance of this particular parasitic process as ;I s ~ ~ c c c s s tool f ~ ~ li n rhc tlcvclolmcnt of st~xlegiclito conlro
gal cl~sci~scs. N c c r o ~ . o / ) l ~I I~I ~c C. O ~ ; I I . ~ L ~I II; ILVCC Sw ~ d c11051 I C I I I ~aird C ~~ 1 1 5 y more general attack mechanis~iis,which involve host dci~thi m l the uti~rionof the host bio~iiassas a nutrient SOLII~CC. So~iie/11.tlrr.ol~otr:\~.~ q>ccics R. .soI~r~ii and other fungi hy liyphal interfcl-cncc without I'orn~ings p lizcd structures, but contact between hyphac ol'botli fungi is a ~iccess;~ry Idition (T7,ean and Estcy, 1978; Pcrsson ct al., 1985). In ollicr intcl-fungal ociations, the mycoparasite pcnctratcs the host hyphae iincl rcproductivc ~cturesthrough niechanical pressure carried out by specialized S I ~ L I C es i n conjunction witli bioLhen~ical degradation of physical barricrs ough the production of lytic enzymes. Mycoparsitcs witli this charactcrc are classified as invasive nccrotroplics (Jcfl'ries and Young, 1994). ctrio irllv~ltais an invasive species that attacks spores, vcgcti~tivc,and reductive structures of several fungi by secretion of adhesive substances I ajxessori~lmI'orrnation (Tsunetla and Skorop;~tl,1080). P h ~ ~ i r ~oli~rr 'rdr.urr1, a very aggressive parasite, pc~ictratc~ and grows inside the host pliac, such as Rotrytis c.i~le~.cw ancl S ' ( Y P I U ~ ~ I .scl~roiiorrr~)r I~(I (I~C;ICOII, 7 6 ) . Mycoparasitism by 7i-irS1otle1.11~i~r involves a positivc cllcmotrol>is~li Iiypliac toward its host, coiling around host Iiypliac, penetration of tlic st by appressoriuni-like structures, and the production of cell wallgrading cnzynlcs (Hcrrc~.a-Estrcllaand Clic~.2003). Ilircctccl T,-ic.110growth toward R. solwli hyphac has been obse~wcl(Clict ct ill., 198 I): wevcr, tlicre is no clear information about tlie nature of thc compounds d v e d in this behavior. Even when 7 ' r i d w t l o - I I Iattacks ~ a wide host Ige, a specific recognition event controlling coil formation sccrns to be cessary. Rarak et al. ( 1 985) proposed that lectins prcscrlt on tlie host sur.c p:~rticipatedin the molecular 1iicc1i;lnismsIcacling to the I'ormation of :cializetl structures tluring n 7i.iclrotli~1.1r1tr-l1ost intcrac~ion.'['cn years cr, Inbar and Chcr ( 1995) demonstrated that 7i.ic.lrocl0/-111tr WIS ahlc to )w with a sirnilar pattern to that shown i n an interfungill interaction, by ing a mimetic system. Nylon fibers simulated host hyphac and Icctins puicd from S d ~ r n t i r r ~~nv l j i i iwere the recognition molcculcs ~csponsiblc I. the induction of coiling and specialized S ~ ~ L I C I I Ifwnii1tion. I~C By using : same biomirnetic system, Onlero et al. (1999) found that cliitit~oligo:rs were also capable of activating those morphological cliangcs i n 7i.i0t1~r11iu. In an attempt to better understand the mcclianis~nscontrolling iling and stri~cti~rc forni;ltitxi as an i~~lportant aspcct i n niycoparasitism. vcral studies hilve been carriccl out at the hiocI1~11ii~;11 ancl genetic Icvcls. 'ncro et al. ( I 999) indicated that a signal transtluc~ionpatliw:~yinvolvill,~ \MP and Iletrotrimeric Gproteins participate i l l the regulation ol'coiling. oreovcr, transgenic 7: trt~aviridest~.ai~ls ovcrcxprcssing the tgtrl gene, cotl ling for the cx suhunit of a lictrotri~l~cric ioco~ltrol01' lrlcr
cl1ar;tctci-islics 01' spccics Iwlorlging to the genus 7i~i~.lrotlo1~11ro. tlowcvl t l l c ~is~ n o s t ~ . o ~cvitlc~~cc tp tlircu[ly linking ;I spccil'ic enzyme with IIO pcnctralion. Inhar ant1 Chet (1995) detected an increase in the ncriviry ol 102 kD:l inrriiccllula~-gl~rcosaniinidasei n mycelia growing under the 1 % ~ rl~imericsystem. Nevcr-rhclcss, the role of this chilinase (luring paras iris^ cspcci;llly in penetration, is srill unknown. The border line between pari~si ism and salmq,hytic behavior is unclear, because many of the cnzymcs :]I protlucctl i n a contacr-intlcl,e~lde~it manner, and a strong link exists bcrwcc nutritional limitation 2nd enzyme production. It is difficult to separate t l cnzym:~ticacrivirics from the parasitic process; i t is possible that rnnny lytl enzymes nl'l'cct the hosrs by simply rn;rking them Inore susceptible to pent rrariorl. P~~otluclin~l ol'lytic cn7.yrncs and its influcncc o n biocontrol cl'lic;\c is tliscusscd later in tllis chaptcr (hydrolytic cn7.y1ilcs).
Tile soil ant1 its microbial communities can form a very complex ancl tl! namic s r ~ ~ ~ c rNt~tric~tts ulc ;tml sp;~ccav;~ilahiliryarc ~ w ol'rt~c o ~ttainI i l r ~ i r ; tior~si n l l ~ ccoloni~aliono f a pu-ticular ecological niche. In this sense, tho.\ mic~.oorg:~~lis~its with a high growth rate and optimal nurrienr utilizario must have clear idvalrages for survival. Many of the fungi exploitctl a biocontrol systcn~sfulfill the characteristics mentioned above. If biologic: corltrol agents 21-ewell e.stablishetl in pl:~nts.ir will Ix dil'ficulr for phyrc palllogenic l'1111gilo twvc ;ICCCSS lo infcclion sites 111 the planl. l i t lltis scr~sc the ~ ~ ~ y c o ~ ~ irssociario~~s l ~ i / a l c;tn also provide bioconrrol by prevcnti~l: p;~tltogc~~ c1111.y~l~rougli roots (J.lookcr ct dl., 1994). Nitrogen. carbon. ~ I I I iron competition have been associated with Fri.so~~irrrii suppression by 7i.i clrotlrr~rrlnanel nonparhogcnic Fu.rcrr-irrr7~species (Sivan ant1 Chet, I989 Mantlccl ; ~ n t lI3;thcr, IO9I ; Coutcatlicr, 1902). There is no inli~rrnationwill regard lo n~cchanisn~s involved in competition for nitrogen and citrhor sources. Probably. the csrablislirnenr uf (his cornperition is derived from ; bcrtcr capacity ol' the biological control agents i n substrare colonizatio~ (R;tkcr. 1991). Iron competition is the best-understood mechanism. Iron i commonly prcscrtl i n a11insolublc~fhr~n. Sorrlc bacterial and fungal spccic II;IVC t I ~ \ ~ I o p c;It IS Y S I C I I I for iron uptake. This consists in rhc production o sitlcl-ol)llorcs,pcptidcs working as iron-binding ligantl, ancl ~ h 1rarlspol.t c 1'0 borh ~llolcculesinside the cell. l'.~c~rdor~~oric~s species consrirurc the bes pwkaryoric system slutlied i n relation to sitlerophore synthesis. The relc vancc o f sitlcl-opl~orrprotluction on plant cliscase suppression has b c c ~ t l c ~ t ~ ) ~ t s ~ Ily ~ - ; sing ~ r c t l/'.~t~ritlorr~o~rc~.~ rr~ularltIxking rllc ;iI,iliry to pl.otluc~
r
1 1 1 11111g1. lllclc I \ r l c r o l ~ l ~ (r 0~~ ~1 c1 ~ ~ 1C 1L d l . , IWJ; Lluyxcllx cl ill., I ' P N ) . ~ t l cinli)r~nationabout siclcrophore production and biocontrol. In 7: \~irc~~i.v. ~rccclasses of hydroxaniate sidcrophorcs have Ixcn idcnril'ictl (Jal;d cr ;\I., )X6); I n addition. tlic Psj-1 gene. encoding a l~eptitlc-sylllllc.~;~sc psol)al)ly ~volvcdi n siderophorc production, has bcc~icloncd fronl 7: virc>/l.\..Ncvcr~cless,elimination of P.sj~ldid not affccr the biocontsol capacity oftllc nunts toward R. .rol(liii and Pj~/hilrrilrlltiliill~r (Wiltlire et nl.. 3001). Thus, /en when the evidence suggests rhe participatio~lof fungal sidcropllorcs in on competition as a biocontrol mechanisn~,thcse is no strong evidence reting the two events. An important aspect to keep i n mind is that no dero~>hore-producing organisms call use siderophores previously liberated I soil, unless they have the right transport system (lina~jinlakerset al.. 995). This situation could be useful to the BCAs applied but co~rlclbe ex,nded to plant pathogens, making iron competition an unstahlq tool 1)rclis: Ise control.
Most fungi produce antimicrobial secondary metabolites. either as part t'tlieir normal growth and developmental program or in response to a bitic stress (parasitismj. T l ~ eprotluction of toxins and antibiorics l)y fungi is :ry sirnply delnonstrared in vitro. Numerous agar plate-based assays I~avc :en developed to detect volatile and nonvolatile antibioric producrion by i~tativebiocontrol agents and to quantify their effects on p l a ~ parhogens. ~t lowever, the relevance of antibiotic production during in vivo biological mtrol remains unclear. Species of Triclroder11ic7are well-known biological mrrol agents that produce ;I range of antibiotics thal arc ;~crivcagai~lsl athogens in vitro and, consequently, antibiotic production has conl~nonly een suggested as an advantageous trait for these fungi (Ghisalberti and ivnsithampamm, 199 1 ). The peptaibols are a fi1111ilyof anribiotic peptides isolated f s o r~i i~c ~ ~ ~ b c s s f the genus Trichode~nmand related genera, such as E ~ ~ ~ e ~ . i c ~ c l and lol~sis ;lioclcrdin~n,which exhibit antibacterial and antifungal properties. They lnge between 5 and 20 residues in length. Peptaibols are mphipathic in m r e , and this property allows many of [hem to I'orm voltage-dependent )n chaunnels in lipid bilaycr membr-anes(Sansom, 1991: RebulTat et ul., 1992). licsc channels arc I-csponsiblc for causing cyropl;~sn~aric Ic;lkagc, resulting I rhc loss of soluble proteins from the hypllac, Icarliny ro cell cicath. Ovcr 00 pepr;~ilbolsseqrlcnccs have bccn rcposrctl so IS, 111oslol' which arc olnpiled in the Peptaibol Lhtabasc at www.cryst.bbk.ac.r~k/~~cpti~ibol. A ccl'ul rcview about scqrlencc features and nlodcling srsucturcs o f tlil'fcrcnt ~.pl:~il)olx w:~s,secc~~lly p u l ~ l i s l ~( C~' IdI L I ~ I I;III(I W;~ll;~ci., 200 I ),
1'cl'l;iihol.; csllibit a r;lngc ol';~nlil)ioricSi~nctionsagainst tlill'crent 1 ; o r ~ ; r n i s ~ nalthough s, tllcre does nor appear to be :I clear cor-relation Iwtv ~ i ~ e ~ n hof'thc e r s S;IIW s ~ ~ l > I ' ; i(I>;ised ~ ~ ~ i l yon s e ( 1 i 1 c adi 1 n~rrin~adinrr~lysis)adinrr11~1;11iti1>1 adinrr~ctivily01. target. I t is pcrrinent lo nolicc ttw pcprnibolx ~)roduccc 7i-ic4otlr1-1rio spccics have shown lo act synergistically with hi' protluc 01' cell wall-rlegradinrr~linenzymes to inhibit the growth ol' fungal p;~tho; (1,orito et iil., 1006; l / o o et al., 2002). Pcptnibols, like nl;lny other pep1 roxiris i n bacteria and f'ungi, are prodwed nonribosom;illy by large 1111. fi~nclionalpcl>titlcsynlhascs. Recently, Wiest ct i l l . (2002) clonetl rhc ; respo~xihlclor the 131-oductionof pnptaibols i n 7: ~ ~ i r - o(~t ie. vs l ) . Consistel the clisruplion ofllie gcnc abolished the ~~roduction of all pcptaibol isofo by this species. Altliol~gh biocontrol capacily was not tested on tt,. strains, l~nravelingthe role of pcptaibols i n 7: virc.1l.s fungal anragon seems lo be closer. A large number of T ~ - i c h o t l e r ~spccics n ~ ~ arc capable of prcducing array of metalmlites orher than pcptaibols, which show antifungal a&\ Protluctio~lof glio(oxi11, a rnotlifictl cyclic phcnylalaninc-scrinc clip tide, is associated with 7: v i r c ~ ~suppression z.~ of daniping-off caused I ! ulii1111111r (Imvis et al.. I09 I : 1~i11i~sdcn ct al., 1092). 7j.ic,11o(1(,1.111(1 11(11.;i(it, and 7: kolli/i,qii both produce 6-11-pc1llyl-2H-1>yr:11i-2-011e (01'1') or reli~ arlalogl~cst I 1 ; i t ~ l ~ o w epolcnt rl inhihilory propcrtics agai~islsclcroria-fol ing palhogens. mtl considerably reduced the rate of damping-off i n lert~ seetllinp by R. soloili (Dickinsori et al., 1989). The previously ~ n e n t i o ~ 6PP has also been associated with the volatile compounds p~.oducetl 7: 1Grc~11.v(Moss ct al.. 1975). These antifungal cor~lpoundstogether H some other merabolires (e.g., antraql~inones:~ndsesqui~erpcries)may II;I\ signil'icanl ~.olc,cill~erin parxsitism or i n tlic competitive sapropl~ytic;\I iry OF 7i.i(.lio(l(~1.111o. ~ I i i c l is i critical for its survival in soil. Necrotrophic :~ssociationsbetween fungi may include hyphal interl' ence reactions. defined as the inhihitory effect of the mycelium of :I fun; that grows in close p r o x i ~ ~ ~ofi l unolhcr y species, reducing its rate ol'grov and causing cytopl:~sniicdisruption (Ikediugwu and Webqtcr, 1970). Lo molecular-weight ~iietabolitcshave been associated witli this plicnonienc which is witlcspreatl arnorig rnycoparasites used i n biocontrol. Some c tailed tlcscriprions of the cytological changes occurring during hyphal i tcrfercllce have hccn tlcscrihcd Tor several fungal intcracrions. Flowcver. I nali11.cof 111ctlil'l'usivc Il~ctorhas not been tlcrcrmincd in rnost ol'tlic cast R L I I I - ol'pinc I - ~ ~ trees, c;ii~sctlby the bracket fungus Hc,/c~mho.~itlio~i o171lo.\.it is p~~rve~llctl by I ' c ~ t i i o l ) l ~ o,ryt ~i g ( ~ ~ ~by f o oa comhirlarion of' Ilyplladinrr~lin1crl.c ence and direct conlpetition. The interference reaction involves a retluctic ill lllc I ~ I I I I IoI'~~~i~ocllo~l(Irin ~ C ~ i n file c y ~ o p l a sof ~ ~11. i (1111io.\.it111 (Ike(lii~g\
