SUPPRESSIONOF PLANT DISEASES BY COMPOSTS

H. A. J. Hoitink, A. G. Stone and D. Y. Han

Professor Graduate and Research Associates, Department Plant Pathology,Ohio Agricult of Research DevelopmentCenter,The Ohio StateUniversity, Wooster,OH 44691 and

1. ABSTRACT
Compostsoffer unique opportunitiesto examinefundamentalinteractions between plant pathogens, biocontrol agents, organicmatter,andplant roots. Theseorganic soil amendments havethe potentialto provide consistent biological control of manyplant diseases.Foliar, vascularas well asroot pathogens be affectedby composts.Many may factorsinfluencethesebeneficialeffects. For example, the compositionof the feedstockused in the preparationof composts affectsthepotentialfor biological control aswell asthe microflora active in control. Heatgenerated during compostingkills or inactivatespathogens the processis if monitoredproperly.Unfortunately,biocontrol agents with the exceptionof Bacillus spp. are also killed. Therefore this beneficialmicrofloramustlargelyrecolonizecomposts after peakheating. The compostingenvironmentandconditions during curing and utilization also affect the potential for recolonizationof compostsby biocontrol agents andthe inductionof disease suppression. practice,conIn trolled inoculationof compostwith biocontrol agentshas
proved necessary to induce consistent levels of disease .

2. INTRODUCTION
During the 1960's, nurserymen across United States the explored the possibility of using composted tree bark as peatsubstitutes reducepotting mix costs. Early during to the utilization of bark composts,improved plant growth anddecreased losses caused Phytophthora rotswere by root observed sidebenefitsin the nurseryindustry. Today it as is recognizedthat control of suchroot rots with composts canbe aseffectiveasthat obtainedwith fungicides (Hardy andSivasithamparam, 1991; Hoitink et al., 1991;Ownley and Benson, 1991). Therefore,the ornamentalplant industry relies heavily on compostproductsfor control of diseases caused thesesoilborneplant pathogens.Comby posts have replaced methyl bromide in this industry (Quarles and Grossman,1995). In field applicationsof compostssimilar resultshavebeenobtained(Hoitink and Fahy, 1986; Lumsdenet al., 1983, SchUleret al., 1993). Examplesof diseases controlledby composts reviewed are in Hoitink and Fahy, 1986. . . . . crops,particularly If usedm containermedia(Inbar et al., 1993). The rateof respirationis oneof severalprocedures that can be usedto monitor stability of composts (Iannotti et al., 1994). Variability in compoststability is one of the principal factorslimiting its widespread utilization. Maturity is lessimportant in ground bed or field agricultureas long asthe compostis appliedsufficiently ahead plantof ing to allow for additional stabilization;however, lack of maturity frequentlycauses problemshereaswell. . . Effectsof.chemlcal properties comp~sts soilb~~e of on. disease seventyo.ften ~verlooked(reviewedm Holtlnk are et al., 1991). Highly salIne compostsenhance Pythium andPhytophthoradiseases unlessthey areappliedmonths
ahead of planting to allow for leaching. Compost prepared Composts must be of consistent quality to be used successfully in biological control of diseases of horticultural

suppression.

,i-'

Stability of composts mustbe consideredin biological control. Immaturecompostsserveas food for pathogens. Their populations increase freshorganicmatterandcause in disease evenif colonizedby biocontrolagents.On the other hand,biocontrol agents inhibit or kill pathogens mature in composts and thereby induce disease suppression. Biocontrol agentsin compostsmay induce systemicacquired resistance foliar plant pathogens. to Finally, excessively stabilizedorganicmatterdoesnot supportthe activity ofbiocontrol agents.Microorganisms incapable proof viding biological control predominatehere. Diseasedevelopson plantsproducedin suchhighly mineralizedorganicmatter

.. I-

Physicaland chemical propertiesof compostsaffect biol~gical con.trol.Salinity and the rat~ of releaseof plant nutnents,particularlythe amountof mtrogenreleased, affect suppressiveness. CompostpH andtiming of compost applicationrelativeto plantingof cropsareother factorsto be considered.In summary,the field is very complex.

from municipal sewage sludgehavea low carbonto nitrogen ratio. They release considerable amountsof nitrogen and enhance Fusarium wilt (Hoitink et al., 1987). On the otherhand,composts from high C/N materials, suchastree barks,immobilizenitrogenandsuppress Fusariumdiseases if colonizedby an appropriatemicroflora (Trillas-Gay et al., 1986). High amonium and low nitrate nutrition increases
47 '

I
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...

X CongresoNacional Agronomico 1111 Congresode Fitopatologia 1996

Suppression plant diseasesby... of

'

Fusarlum .

' Wi' Its (Sc hneider, 1985) Perha the low in C/ , ps N redominantly ammonium-nitrogen-releasing sludge P st enhances Fusarium diseases this reason, for compo

" , tonia diseases than the samecompostproducedin a partially enclosedfaciltty were fiew microb iaI speciessurh ' ' ' vive heat treatment(Kuter et al., 1983), Compostpr~duced in the opennear a forest (field compost),an enVi-

3. FATE OF BIOCONTROL AGENTS

COMPO STING . .,. The composting process is ofte? divided mto three phases,The initial phaseoccursdurmg the fiTst24-48 hr astemperatures gradually rise to 40-50 C, and sugarsand other easily biodegradable su~stances destroyed, are During the secondphase,when high tem~eratures 55- 70 C of prevail, lessbiodegradablecellulosIc substanc~s deare stroyed. Thermophilic microorgansims predommate during this part of the process.Plantpathogens seeds and are killed by the heatgenerated during this high phase(Bollen 1993; Farrell 1993), Compostpiles must be turned frequently to exposeall partsto high temperature produce. to a homogeneous productfree of pathogens weedseeds, and Unfortunately, most beneficial microorganismsalso are killed during the high temperature '" of composting. phase
Curing begins as the concentration of readily blode-

DURING

ronmentthatishigh in microbial species diversity, iscolonized by a greatervariety of biocontrol agentsthan the sameproducedin an in-vesselsystem(Kuter et al., 1983), Frequently,however,Rhizoctoniaand other diseases are observedfor sometime after compostsare fiTst applied (Kuter et al., 1988; Lumsden et al., 1983). Three approaches beusedto solvethis problem:Curingof comcan postsfor four monthsor morerenders composts moreconsistentlysuppressive (Kuter et al., 1988). The second approach is to incorporatecompostsino field soils for several monthsbeforeplanting (Lumsdenet ai" 1983), The third approach is to inoculate composts with specific biocontrol agents(K wok et ai" 1987), . A specific strain of Flavobacterium balust~num, and an is~lateof Tric~odermahamatumhave ~eenide,ntified that mduce consistentlevels of suppression If mocuto caused by a broad spectrum of plant pathogens, ,di~eases
lated into compost after peak heating, but before signifi-

gradablecomponents wastesdeclines,As a result, rates in of decomposition, heatoutput and temperatures decrease, At this time, mesophilicmicroorganisms grow at temthat peratures C recolonizethe compostfrom the outer low <40 temperature layerinto the compost windro~ or pil,e,Therefore, suppression pathogensand/or diseaseIS largely of inducedduring curing, because m~stbiocontrol agents recolonizecompostsafter peakheatingalso. Bacillus spp" Enterobacter spp" Flavobacterium balustinum,Pseudomonas spp" otherbacterialgeneraan~ Streptomyces spp" aswell asPenicillium spp" sever~lTrlchodermaspp" Gliocladium virens and other fungi have beenidentified as biocontrol agentsin compost-amended sustrates(ChungandHoitink1990; HadarandGorodecki, 1991;Hardy andSivasithamparam 1991;Hoitink and,Fahy 1986;Nelsonetal., 1983;Phaeet al., 1990), The moisture contentof compostcritically affectsthe potential for bacterial mesophiles colonizethe substrate to after peakheating, Dry composts34% moisture,w/w) be~omecolonized by fungi and are conduciveto Pythium diseases,In order to induce-suppression, moisturecontentmust be the high enough(at least40-50%,w/w) sothat bacteriaaswell as fungi colonize the substrateafter peak heating. Water must often be addedto compostsduring compostingand curing to avoid the dry condition. CompostpH also affectsthe potential for beneficial bacteriato colonize composts, A pH <5.0 inhibits bacterial biocontrol agents (Hoitink et ai" 1991).
' t Variability in suppression 0fRh IZOC ' ng -,off oma ' d ' andFusariumwilt encountered substrates m amende With ' . art to randomrecolonization mature~~~~os~~~c~~: ~~o~ontrol agents after peakheat-

cant levelsof recolonizationhaveoccurred, Patents have beenissuedto The Ohio StateUniversity for this process (Hoitink, 1990). In Japan,Phaeet al. (1990), isolateda Bacillus strainthat inducespredictablebiological control in composts,It hasbeenrecognized decades single for that strainsare not as effective in biological control in field applications as mixtures of microorganisms, (Garrett, 1955). The sameappliesto containermedia(Kwok et ai" 1987),

4. MECHANISMS OF SUPPRESSION IN
COMPOSTS Two classes biological control mechanisms of known as "general" and "specific" suppressionhave been describedfor compost-amended substrates, mechanisms The involved arebased competition,antibiosis,hyperparaon sitism and the induction of systemicacquiredresistance in the host plant. Propagules plant pathogens of suchas Pythium and Phytophthoraspp., are suppressed through the "general suppression"phenomenon(Boehm et ai" 1993;Chen et ai" 1988a;Chen et al., 1988b;Cook and Baker 1983; Hardy and Sivasithamparam 1991; Mandelbaumand Hadar 1990), Many types of microorganisms present in compost-amended container media function as biocontrol agentsagainstdiseases causedby Phytophthora Pythiumspp,(Boehmet ai" 1993;Hardy and and Sivasithamparam 1991), Propagules thesepatho., of gens,if inadvertentlyintroducedinto compost-~ended substratesdo not germinatein response nutrients reto , , leased the form of seedor root exudates.The high mlin crobial activity and biomasscause by the " genera SOt d I 'I microflora" in such substrate~ pre~entsgermination of
" , ,

dampi'

~g~O~~ldco~post more consistentlysuppresses Rhizoc48 -;

spores thesepathogens mfection of the host,(Chen of and

X Congreso Naciona/Agronomico Congreso Fitopat%gia 1996 fIll de

H.A. .J. Hoitink, A. G. Stone and D. Y. Han

et al., 1988a;Mandelbaumand Hadar 1990). Propagules of thesepathogens remain dormant and are typically not killed if introducedin compost-amended (Chenet al., soil 1988a;Mandelbaum Hadar, 1990).An enzymeassay, and that determines microbial activity basedon the rate ofhy. . . .

drolysls offluorescem dlacetate (FDA),predicts suppres. .. ..

slveness ofpottmg mixesto Pythlumdiseases (Boehmand. Hoitink 1992;Chenet al., 1988a;Mandelbaum Hadar and 1990 Y . d S. .th 1994) S. .1 . fi , ouan Ivasl amparam, . .Iml arm" orma.1 h t Ion hasbeendeveIopedfior SOl on "organic&: . s larms were Ib d. I I t (W kn h t I 1993) . SOl orne Iseases essprevaen are or e ea. ,. Th I th f t . th t th . ffi t I t I e eng 0 Ime a e suppressive ec as s a so e 't ' be determme WI FDA ac IVI (Boehm and H01mk , . d ' th t . .ty may 1992) Th . . kn th ". 'ty " f th , IS IS own as e carrymg capaci 0 e b tr t I t ' t b. I ' I tr I su s a e re a Ive 0 10oglca con o.

matter due to high glucose concentrations such waste in (de la Cruz et al., 1993). The sameprocesses occurin may antibiotic production, which also plays an importantrole in biocontrol. ffr . I h . n mature compost, were concentrations eenutrl0 I (Ch I 1988 ) I . fR I . entsare owen et a . a sc erotla0 . so am are :'.. . kIlled by the hyperparasite, b~ologlcal and control prevaIls (Nelsonet al., 1983). The foregomgrevealsthat composts b d I b.l . d h .. must e a equatey sta I Ize to reac that decomposItion .. level wherebiological control ISfeasible. In practice,this .
occurs m composts (tree barks, yard wastes, etc.) that have
. , " ,

The mechanismof biological control for Rhizoctonia solani in compost-amended substrates differentfrom that is of Pythiumand Phytophthoraspp,because only a narrow groupof microorganisms capable eradicating solani. is of R. This type of suppressionis referred to as "specific suppression"(Hoitink et aI" 1991), Trichodermaspp,including T hamatumand T harzianum,are the predominant hyperparasites recovered from composts prepared oflignoII I ' t (K t t I 1983 N I . t I 1983) ce u OSIC es u er ea., was , e sonea., H 't . . bl f I ., . p anpa ogensresu mg m YSlS ea. or ese ngl b t ' I tr . ' th b. I . I t .th . . mt erac WI various ac ena s aIDS e 10oglca conm tr I f Rh ' t . d . ff (K k t I 1987) It . 0 0 lZOC oma ampmg-o wo e a" . IS . t f merest that PemCI lum spp. are the predomman hy' t . 'II . 0 perparasites recoveredfrom sclerotiaof Sclerotiumrolfsii m composted t (H d I t t grapepomace a highdsugar1991 low cellu'd G k ' and ) '7'. h osecon en was e a ar an oro ec I, , 1 rlC 0t d fr th' t d J uermaspp.wereno recovere om IScompos an were .. .. not effective when mtroduced, The composItionof the . feed stock,as expected, appears havean Impacton the to microflora in composts active in biological control.
. .
I yperparasl t th es are microorganisms It .' I ' capa d e 0 co th Th ornzmg fu '

been(I) stabIlizedfar enoughto avoid phytotoxIcity and . ". (2) colornzedby the approprIatespecific mlcroflora. Pr . I ' d I ' th d fi h. ,. actlca gul e IDes at e met IScntlcaI stage fd ecom0 f . I . , ., pOSItion m terms 0 blo oglcal control are not yet available.Industry presentlycontrolsdecomposition level by maintaining constantconditions during the entire processand adheringto a given time schedule,Composted pine bark produced by such a processhas beenutilized with great successin floriculture indicating that this approach quality control is quite acceptable to (Hoitink et al,,1991). ,. .. , ExcessivelystabIlizedorganicmatter,the oppositeend f h d ..
0 t e ecompOSltion scale, does not support adequate
, , activity of . blocontrol . agents. As a result, suppression . IS

. . . lackmg and soIlborne diseasesare severe,as in highly . ,. , mmerahzed soIlswherehumic substances thepredomiare , nant forms of organicmatter(Workneh et aI" 1993). The I h f. h 'I ' b engt 0 I tImle tf at .SOI -mco l rpo~a~ed composts support d h a equate eve s 0 locontro activity asnot Yet beendetermined. Presumably, varieswith soil temperature, it soil characterIstIcs the type of orgarncmatterfrom which and th d d' . e compostwasPrepare. Loa mg rates and farmm g Prac. tIcesof coursealso playa role. We have studied the "carrying capacity" of soil organicmatterin potting mixesprepared with sphagnum peat
to bring a partial solution to this problem (Boehm and
, . .

5. BIOLOGICAL ENERGY AVAILABILITY

VERSUS SUPPRESSIVENESS Thedecomposition level of organicmatterin compostamended substrates a major impacton disease has suppression. For example,R. solani is highly competitive as a saprophyte(Garrett, 1962), It can utilize cellulose and colonize fresh wastesbut not low cellulosematurecompost (Chung et aI" 1988). Trichoderma, an effective biocontrol agentof R.solani,is capable colonizingfresh of aswell asmaturecompostbut it growsbetterin freshcompost (Chung et al., 1988;Nelson et al., 1983). In fresh, undecomposed organicmatter,biological control doesnot occur because both the pathogenandthe biocontrol agent grow as saprophytes.Therefore,R. solani (the pathogen) remainscapable causing of disease here. Prfsumably,synthesis of lytic enzymesinvolved in hyperparasitismof pathogens Trichodermais repressed fresh organic by in

Hoitink 1992;Boehm et al., 1993). Sphagnum peattypically competes with compostasa sourceof organicmatter in horticulture, Both the microflora andthe organicmatter in peat itself can affect suppression soilbornediseases. of The literatureon that effect is reviewedbriefly here. Dark, more decomposedsphagnumpeat, harvested from a four foot or greaterdepthin mostpeatbogs,is low in microbial activity andconsistently conducive Pythium to and Phytophthoraroot rots (Hoitink et al., 1991;Boehm and Hoitink, 1992). On the otherhand,light, lessdecomposedsourcesof sphagnum peat,harvested from nearthe surface peatbogs,havea highermicrobialactivity (FDA of activity) andsuppress rot. Unfortunately,the suppresroot sive effect of light peat to Pythium root rots is of short duration. (Boehm and Hoitink, 1992; Tahvonen, 1982; Wolffltechel 1988). Light peatsareusedmost effectively 49

X Congreso Nacional Agronomico/ III Congreso Fitopatologia1996 de

l

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Suppression alp/ant diseasesby...

for short prod~ctioncyc..es (6-10 week cr~ps),suchas in plug andflat mIxesu~edm the ornamentals mdu.s~. Compostshavelongerl~tmg effec~ (B~ehmandHoItmk, 1992; Boehmet aI, 1993,You and Sivasithamparam, 1994). As mentioned above,therateof hydrolysisof FDA predicts suppressivenessof peat mixes and of compostamended substrates to Pythium root rot (Boehm and Hoitink, 1992). As FDA activity in suppressive substrates declinesto < 3.2 =B5g FDA hydrolyzed min-l g-1 dry weight mix, the populationof Pythium ultimumincreases, infection takes place and root rot develops. During this collapsein suppressiveness, compositionof bacterial the species also changes(Boehmet al., 1993). A microflora typical of suppressive soils, which includesPseudomonas spp. and other rod-shapedGram negativebacteriaas the predominantrhizospherecolonizers,is replacedby pleomorphic Gram-positivebacteria (e.g., Arthrobacter) and putativeoligotrophs(Wu et al., 1993). The microflora of the conducive substrateresemblesthat of highly mineralized nichesin soil (Kanazawaand Filip, 1986). . . .. .. . Non-.destructlve analysIsof soil organicmatter,utIlIZmg FounerTransformInfra Redspectroscopy (FT-IR) and Cross Polariza~ion Magic Angle Spinning -13Carbon NuclearMagnetIcReson~c~Spectro.scopy (CPMAS- 13C NMR), allows charactenzationb biodegradable of compof .1 . fr . ( nents0 SOlorganic actions In ar et al., 1989;Ch~n~d Inbar, 1993). CPMAS - 13CNMR allows quantitative analysisof concentrations readily.biodegradable of substances suchas "carbohydrates" (hemicellulose, cellulose, etc.) versuslignins and humic substances soil organic in matter [reviewed in Chenand Inbar, 1993]. In a preliminary report, Wu et al. (1993) reportedthat the "carbohydrates"declineassuppressiveness lost. During the same is time period,bacterialgeneracapableof causingbiological control are replacedby thosethat cannotprovide control. Biocontrol agentsinoculated into the more decomposed substrate not able to induce sustained are biological control of Pythiumroot rot. The samephenomenon been has observedfor Phytophthoraroot rot in the field (You and Sivasithamparam, 1994). Therefore,biocontrol of these diseases determinedby the "carrying capacity" of the is substrate which.regulates species compositionandactivity and,in turn, the potentialfor sustenance biological conof trol. 6. COMPOST FOR CONTROL OF FOLIAR DISEASES . .. Durmg the past decade,a senesof projectshavebeen publishedon~hecontrolofplantdiseasesofaboveground plant parts With water extracts,als.oknown as steepages, preparedfrom composts (Weltzhlen, 1992; Yoh.alemet al., 1994). Ste~pages ofte~ are preparedby soakingmature compostsm w~ter (still culture; 1:1, w/w) for 7-10 days. The steepage filtered and then sprayedon plants. IS

Unfortunately, efficacy varies with the compost,batches of steepages produced,cropsand the disease under question. Sackenheim(1993), utilizing plate counting procedures,hasreportedthat aerobicmicroorganisms predominate in steepages. The microflora includesstrainsof bacteria and isolates of fungi already known as biocontrol agents. He developeda numberof enrichmentstrategies, that include nutrients as well as microorganisms, imto prove efficacy of the steepages. Control induced by compoststeepages also been has attributed to systemicacquiredresistance (SAR) induced in plants by microbespresentin the extracts(Weltzhien, 1992). The recentwork by Sackenheim (1993) on grape, however,doesnot supportthis assumption.A factor that hasnot beenevaluatedbut could playa role in efficacy of steepages the condition of soil organic matter and the is associated microflora in the soil in which treatedplantsare produced. Soils naturally suppressive soilborneplant to pathogens(e.g., compost-amended soils) harbor active populations of biocontrol agents(Boehm et al., 1993). Severalof theserhizobacteriaand fungi can induce protectionto foliar pathogens the leaves plants(Ma h ti in of et al., 1994; Wei et al., 1991). Zhang et al., (19~)or:~ ported that pathogenesis related proteins were activated . in roots and shootsof cucumberPlantsProduced m compost. Further work may revealthat compostsaffect resistanceof the roots and foliage to diseases.Presentl trol of foliar diseases with composts steepages or iS~i;~y variable.

7. DISEASE SUPPRESSION - FUTURE

OUTLOOK . .. '. . Suc.cess bl~loglcal contr~lof dlse~esWithcomp~sts m IS pos~I~le~nly If all factors Involved m the production and utilization of compostsare defined and kept consistent. Most compostsare variable in quality. Therefore, composted pine bark remainsthe principal compost used for th.eprepar:ation potting mixes or soils naturally supof presslve soilborneplantpathogens. to Composted manures, yard and food wastesar~ steadily gai~ing in popularity, and offer the samepotential(Gorodeckland Hadar, 1990; Grebusetal., 1994;Inbar et al., 1993;Marugget al., 1993; SchUler al., 1993). et Controlled inoculation of compostswith biocontrol agentsis a procedurethat must be developedon a commercial scaleto induceconsistent levelsof suppression to pathogens such asR. solani (Hoitink et al., 1991;Phaeet al., 1990; Grebuset al., 1993). Recently,tree bark was proposed a food basefor the cultureofbiocontrol agents as andasa carrierof suchagents usein agriculturalapplifor cations(Steinmetzand Schl>nbeck, 1994).However,this new field of biotechnology,is still in its infancy. Major research and development efforts will needto be directed

50

X CongresoNacional Agronomico / III Congresode Fitopatologia 1996

H.A..J: Hoitink, A.G. Stoneand D.Y. Han

toward this approach for disease control. Recycling through composting is being chosen as the preferred strategy for
. waste treatment. ThIs also . applIes to farm manures. Fqr

Farrell, J. B. 1993. Fecalpathogencontrol during composting,p. 282300. In: Science and Engineering of Composting: Design,
Environmental, Microbiological A. J. Hoitink and H. M. Keener, and Utilization eds. Renaissance Aspects. H. Publications,

this reason, composts are becoming available in greater quantities. Peat, on the other hand, is a limited resource that cannot be recycled. Future opportunities ra an

Worthington, OH. 728 p. Garrett, S. D. 1955. A century of root-dise~e investigation. Ann. Appl. Bioi. 42:211-219. Garrett.,S. D. 1962. Decompositionof cellulosein soil by Rhizoctonia solani Kuhn. Trans. Br. Mycol. Soc. 45:114-120.
Grebus, M. E., K. A. Feldman, C. A. Musselman, and H. A. J. Hoitink.

con

tr II d . d

0 e -In uce

suppressIon 0 SOl orne p an

for both natu-

.lb

I t

pathogens appear bright. 8. ACKNOWLEDGEMENT Salaries and research support provided by State and federal funds appropriated to the Ohio Agricultural Research and Development Center The Ohio State Univer. db G t US2 I 96-22 from BARD the United Slty, an y ran no. , States-Israel Binational Research and Development Fund. 9. REFERENCES Boehm, M. J. and H. A. J. Hoitink. 1992. Sustenance microbial of activity and severity of Pythium root rot of poinsettia. Phytopathology82:259-264. Boehm, M. J., L. V. Madden, and H. A. J. Hoitink. 1993. Effect of organicmatterdecomposition level on bacterialspecies diversity and composition in relationship to Pythium damping-off severity. A lied Environ. Microbiol. 59:4171-4179. pp Bollen, G. J. 1993. Factorsinvolved in inactivation of plant pathogens during compostingof crop residues,p. 301-318. In: Science.. and Engineering of Composting: Design, Environmental, Microbiological and Utilization Aspects. H. A. J. Hoitink and H. M. Keener, eds. Renaissance Publications, Worthington, OH. 728 p. Chen, W., H. A. J. Hoitink, A. F. Schmitthenner, and O. H. Tuovinen. 1988a.The role of microbialactivity in suppression dampingof off causedby Pythium ultimum. Phytopathology78:314-322. Chen,W., H. A. J. Hoitink, andL. V. Madden. 1988b.Microbial activity and biomassin containermedia predicting suppressiveness to damping-off caused by Pythium ultimum. Phytopathology 78:1447-1450. Chen,Y. andY. Inbar. 1993. Chemicalandspectroscopical analyses of organic matter transformationsduring composting in relation to compostmaturity, p. 551-600. In: Scienceand Engineering of Composting: Design, Environmental,Microbiological and Utilization Aspects. H. A. J. Hoitink and H. M. Keener,eds. Renaissance Publications,Worthington, OH. 728 p. Chung, Y. R., H. A. J. Hoitink, and P. E. Lipps. 1988. Interactions between organic-matter decomposition level and soilborne disease severity.Agric., Ecosys.Environ. 24:183-193. Chung, Y. R. and H. A. J. Hoitink. 1990. Interactions between thermophilicfungi and Trichodermahamatum in suppression of Rhizoctonia damping-off in a bark compost- amended containermedium. Phytopathology80:73-77. Cook,R. J. andK. F. Baker. 1983.TheNatureandPracticeof Biological Control of Plant Pathogens.Am. Phytopathol.Soc., St. Paul, MN. 539 p. de la Cruz, J., M. Rey, J. M. Lora, A. Hidalgo-Gallego,F. Dominguez, J. A. Pintor-Toro, A. Llobell, and T. Benitez. 1993. Carbon source control on -glucanases, chitobiaseand chitinase from Trichodermaharzianum.Microbiol. 159:316-322. 1993. Production of biocontrol agent-fortified compostamendedpotting mixes for predictable diseasesuppression. Phytopathology83:1406 (Abstr.). Grebus,M. E., M. E. Watson,and H. A. J. Hoitink. 1994. Biological, ch~mi.cal physic~1 and propertieso~composted y~d trimmings asIndicators ofmatunty andplant disease suppression. Compost Sci. Util. 1:57-71. Gorodecki,B. and Y. Hadar. 1990. Suppression Rhizoctoniasolani of
and Sclerotium rolfsii in container media containing composted

separat.ed cattle manure and composted grape marc. Crop ProtectIon9:271-274. . .. . Hadar, Y. and B. Gorodeckl. 1991. Suppressionof germmation of sclerotiaof Sclerotiumrolfsii in compost. Soil. Bioi. Biochem. 23:303-306. . . . Hardy, G. E. St. J. and K. Sivasithamparam. 1991. Suppresslon.of' PhytophthoraRoot Rot by a CompostedEucalyptusBark MIx. Aust. J. Bot. 39:153-159. ... Holtlnk, H. A}. 1990: Produc~lon dls.ease of suppressIve comp~stand contaIner media,andmicroorganismculturefor usethereIn. US Patent4960348. Feb. 13, 1990. H .. oltln k,H. A. J., M. Daughtery, and H. K. Tayama. 1987. Control of cyclamenFusarium wilt - A preliminary report. Ohio Florist't Assoc.Bull. 693:1-3. Hoitink, H. A. J. andP. C. ~ahy. 1986. Basisfor the control of soilborne plant pathogens With composts.Ann. Rev. Phytopathol.24:93114. .. Holtlnk H. A. J., Y. Inbar, andM. J. Boehm. 1991. Statusof compost edamended potting mixes naturally suppressive to soilborne diseases oftloricultural crops. Plant Dis. 75:869-873. Iannotti, D. A., Grebus,M. E., Toth, B. L., Madden L. V. and Hoitink, H. A. J. 1994. Oxygen respirometryto assess stability and maturity of compostedmunicipal solid waste. J. Env. Qual. 23:1177-1183. Inbar, Y., Y. Ch~n,and Y. Hadar. .1989. SolId-statecarbon-13nuclear magnetic resonanceand Infrared spectroscopyof composted organic matter.Soil Sci. Soc. Am. J. 53:1695-1701. Inbar, Y., Y. Hadar, and Y. Chen. 1993. Recycling of cattle manure: The composting processand characterizationof maturity: J. Environ. Qual. 22:857-863. Kanazawa, andZ. Filip. 1986. Distribution of microorganisms, S. total biomass,and enzymeactivities in different particlesof brown soils. Microb. Ecol. 12:205-215. Kuter, G. A., H. A. J. Hoitink, andW. Chen. 1988. Effectsofmunicipal sludge compost curing time on suppressionof Pythium and Rhizoctoniadiseases ornamentalplants. Plant Dis. 72:751of 756. I III Congreso de Fitopatologia 1996 51

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Suppression olplant diseases by... Kuter, G. A., E. B. Nelson, H. A. J. Hoitink, and L. V. Madden. 1983. Fungalpopulations containermediaamended in with composted hardwood bark suppressive and conducive to Rhizoctonia damping-off. Phytopathology73:1450-1456. ~wok, O. C. H., P. C, Fahy, H. A. J. Hoitink, G. A. and Kuter. 1987. Interactions between bacteria and Trichoderma hamatum in suppression Rhizoctoniadamping-offin bark compostmedia. of Phytopathology= 77:1206-1212. Lumsden, R. D., J. A. Lewis, and P. D. Millner. 1983. Effect of cornposted sewagesludgeon severalsoilborne pathogensand diseases.Phytopathology73:1543-1548. Mandelbaum, andY. Hadar. 1990. Effectsof availablecarbonsource R. on microbial activity and suppression of Pythium aphanidermatum in compost and peat container media. Phytopathology80:794-804. Marugg, C., M. E. Grebus,R. C. Hansen,H. M. Keener,and H. A. J. Hoitink. 1993. A kinetic model of the yard waste composting process. CompostSci. & Util. 1:38-51. Maurhofer,M., C. Hase,P. Meuwly, J-P.Metraux,andG. Defago. 1994. Induction of systemicresistance tobaccoto tobacconecrosis of virus by the root-colonizing Pseudomonasfluorescens strain CHAO: Influence of the gac, a gene and of pyoverdine production. Phytopathology84:139-146. Nelson,E. B., Kuter, G. A. and Hoitink, H. A. J. 1983. Effects offungal antagonistsand compost age on suppressionof Rhizoctonia damping-off in container media amended with composted hardwoodbark. Phytopathology3:1457-1462. Ownley, B. H. and D. M. Benson. 1991. Relationshipofmatric water potential and air-filled porosity of container media to development of Phytophthora root rot of rhododendron. Phytopathology81:936-941. Phae,C. G., M. Saski,M. Shoda,andH. Kubota. 1990. Characteristics of Bacillus subtilis isolated from' composts suppressing phytopathogenic microorganisms,Soil Sci. PlantNutr. 36:575586. Quarles,W. andJ. Grossmam.1995. Alternativesto methyl bromidein nurseries Diseasesuppressivemedia. The IPM Practitioner 17(8):1-13. Schneider,R. W. 1985. Suppressionof Fusarium yellows of celery with potassiumchloride and nitrate. Phytopathology75:4048. SchUler,C., J. Pikny, M. Nasir, and H. Vogtrnann. 1993. Effects of composted organickitchenandgarden wasteon Mycosphaerella pinodes (Berk, et Blox) Vestergr.,Causalorganismof foot rot on peas(Pisum sativurnL.) Biolog. Agric. Hort. 9:353-360. Steinmetz,J. and F. Sch(jnbeck. 1994. Conifer bark asgrowth medium andcarrierfor TrichodermaharzianumandGliodadiumroseum to control Pythium ultimum on pea. J. Plant Dis. Proto 101:200-211. Tahvonen, R. 1982. The suppressiveness Finnish light colored of Sphagnumpeat. J. Sci. Agric. Soc. Finl. 54:345-356. . Tnllas -Gay, M. I., H. A. J. Hoitink, and L. V. Madden. 1986. Natureof suppression Fusarium wilt of radish in a containermedium of amended with composted hardwood bark. Plant Disease: 70:1023-1027. Wei, G., J. W. Kloepper, and Tuzun, S. 1991. Induction of systemic resistance cucumberto Colletotrichum orbiculare by select of strains of plant growth-promoting rhizobacteria. Phytopathology81:1508-1512. Weltzhlen,H. C. 1992. Biocontrol offoliar fungal diseases with compost extracts,p. 430-450. In: Microbial Ecology of Leaves,J H Andrews and S Hirano (eds), Brock Springer Series in ContemporaryBioscience. BSBN 0387-97579-9, Woltlhechel, H. 1988. The suppressiveness Sphagnumpeat to of Pythium spp.Acta Hort. 221:217-222. Workneh,F., A. H. C. Van Bruggen,L. E. Drinkwater, andC. Sherman. 1993.Variables associated with a reduction in corky root and Phytophthora root rot of tomatoes in organic compared to conventionalfarms. Phytopathology83:581-589. Wu, T., M. J. Boehm, L. V. Madden, and H. A. J. Hoitink. 1993. Sustained suppression of Pythium root rot: A funtion of microbial carrying capacity and bacterialspeciescomposition. Phytopathology83:1406 (Abstr.). Yohalem,D. S" R. F. Harris,and J. H. Andrews. 1994. Aqueousextracts of spent mushrooms substrate for foliar disease control. CompostSci. Util. 2:67-83. You, M. P. and Sivasithamparam. 1994, Hydrolysis of fluorescein diacetate in an avocado plantation mulch suppressive to Phytophtoracinnamoni and its relationshipwith certain biotic and abiotic factors. Soil BioI. Biochem. 26:1355-1361. Zhang, W., W. A, Dick, and H. A. J. Hoitink. 1994. Compostinduced systemicacquiredresistancein cucumberto Pythium root rot and anthracnose.Phytopathology84:1138.

Sackenheim, R. 1993. Untersuchungen Uber Wirkungen von Wasserigen, mikrobiologisch aktiven Extracten aus kompostiertenSubstratenauf den Befall der Weinrebe (Vitis vinifera) mit Plasmoporaviticola, Uncinula necator, Botrytis cenerea und Pseudopezicula tracheiphila. Ph.D. thesis. RheinischeFriedrich-Wilhelms Universitat, Bonn, Germany. 157 p.

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X Congreso Naciona/ Agronomico / III Congresode Fitopat%gia /996