SUPPRESSION OF PLANT DISEASES BY COMPOSTS

H. A. J. Hoitink, A. G. Stone and D. Y. HanProfessor and Graduate Research Associates, Department of Plant Pathology, Ohio AgricultResearch and Development Center, The Ohio State University, Wooster, OH 44691

1. ABSTRACT 2. INTRODUCTION

Composts offer unique opportunities to examine fun- During the 1960's, nurserymen across the United Statesdam ental interactions between plant pathogens, biocontrol explored the possibility of using composted tree bark asagents, soil organic matter, and plant roots. These organic peat substitutes to reduce potting mix costs. Early duringamendments have the potential to provide consistent bio- the utilization of bark composts, improved plant growthlogical control of many plant diseases. Foliar, vascular as and decreased losses caused by Phytophthora root rots werewell as root pathogens may be affected by composts. Many observed as side benefits in the nursery industry. Today itfactors influence these beneficial effects. For example, the is recognized that control of such root rots with compostscomposition of the feedstock used in the preparation of can be as effective as that obtained with fungicides (Hardycomposts affects the potential for biological control as well and Sivasithamparam, 1991; Hoitink et al., 1991; Ownleyas the microflora active in control. Heat generated during and Benson, 1991). Therefore, the ornamental plant in-composting kills or inactivates pathogens if the process is dustry relies heavily on compost products for control ofmonitored properly. Unfortunately, biocontrol agents with diseases caused by these soilborne plant pathogens. Com-the exception of Bacillus spp. are also killed. Therefore posts have replaced methyl bromide in this industrythis beneficial microflora must largely recolonize composts (Quarles and Grossman, 1995). In field applications ofafter peak heating. The composting environment and con- composts similar results have been obtained (Hoitink andditions during curing and utilization also affect the poten- Fahy, 1986; Lumsden et al., 1983, SchUler et al., 1993).tial for recolonization of composts by biocontrol agents Examples of diseases controlled by composts are reviewedand the induction of disease suppression. In practice, con- in Hoitink and Fahy, 1986.trolled inoculation of compost with biocontrol agents has .proved necessary to induce consistent levels of disease Composts must be of consistent quality to be used suc-

. cessfully in biological control of diseases of horticulturalsuppression. . . .

crops, particularly If used m container media (Inbar et al.,Stability of composts must be considered in biological 1993). The rate of respiration is one of several procedures

control. Immature composts serve as food for pathogens. that can be used to monitor stability of composts (IannottiTheir populations increase in fresh organic matter and cause et al., 1994). Variability in compost stability is one of thedisease even if colonized by biocontrol agents. On the other principal factors limiting its widespread utilization. Matu-hand, biocontrol agents inhibit or kill pathogens in mature rity is less important in ground bed or field agriculture ascomposts and thereby induce disease suppression. long as the compost is applied sufficiently ahead of plant-Biocontrol agents in composts may induce systemic ac- ing to allow for additional stabilization; however, lack ofquired resistance to foliar plant pathogens. Finally, exces- maturity frequently causes problems here as well.

,i-' sively stabilized organic matter does not support the activ- .ity ofbiocontrol agents. Microorganisms incapable of pro- . Effects of.chemlcal properties of comp~sts on. soilb~~eviding biological control predominate here. Disease de- disease seventy o.ften are ~verlooked (reviewed m Holtlnkvelops on plants produced in such highly mineralized or- et al., 1991). Highly salIne composts enhance Pythiumganic matter and Phytophthora diseases unless they are applied months. ahead of planting to allow for leaching. Compost prepared

Physical and chemical properties of composts affect from municipal sewage sludge have a low carbon to nitro-biol~gical con.trol. Salinity and the rat~ of release of plant gen ratio. They release considerable amounts of nitrogen

Inutnents, particularly the amount of mtrogen released, af- and enhance Fusarium wilt (Hoitink et al., 1987). On thefect suppressiveness. Compost pH and timing of compost other hand, composts from high C/N materials, such as tree ;

application relative to planting of crops are other factors to barks, immobilize nitrogen and suppress Fusarium diseasesbe considered. In summary, the field is very complex. if colonized by an appropriate microflora (Trillas-Gay et

al., 1986). High amonium and low nitrate nutrition in-creases

I-.. ... X Congreso Nacional Agronomico 1111 Congreso de Fitopatologia 1996 47 '

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, Suppression of plant diseases by...

F . 'It (S hnei'der 1985) Perhaps the low in C/ tonia diseases than the same compost produced in a par-' usarlum Wi s c , , " ,

h fi ' b ' I ' N redominantly ammonium-nitrogen-releasing sludge tially enclosed faciltty were ew micro ia species sur-P st enhances Fusarium diseases for this reason, vive heat treatment (Kuter et al., 1983), Compost pr~-

compo duced in the open near a forest (field compost), an enVi-

3. FATE OF BIOCONTROL AGENTS ronmentthatishigh in microbial species diversity, iscolo-

DURING COMPO STING nized by a greater variety of biocontrol agents than the. .,. same produced in an in-vessel system (Kuter et al., 1983),

The composting process is ofte? divided mto three Frequently, however, Rhizoctonia and other diseases arephases, The initial phase occurs durmg the fiTst 24-48 hr observed for some time after composts are fiTst appliedas temperatures gradually rise to 40-50 C, and sugars and (Kuter et al., 1988; Lumsden et al., 1983). Three ap-other easily biodegradable su~stances are destroyed, Dur- proaches can be used to solve this problem: Curing of com-ing the second phase, when high tem~eratures of 55- 70 C posts for four months or more renders composts more con-prevail, less biodegradable cellulosIc substanc~s are de- sistently suppressive (Kuter et al., 1988). The second ap-stroyed. Thermophilic microorgansims predommate dur- proach is to incorporate composts ino field soils for sev-ing this part of the process. Plant pathogens and seeds are eral months before planting (Lumsden et ai" 1983), Thekilled by the heat generated during this high phase (Bollen third approach is to inoculate composts with specific1993; Farrell 1993), Compost piles must be turned fre- biocontrol agents (K wok et ai" 1987),quently to expose all parts to high temperature to produce. .a homogeneous product free of pathogens and weed seeds, A specific strain of Flavobacterium balust~num, andUnfortunately, most beneficial microorganisms also are an is~late of Tric~oderma hamatum have ~een ide,ntifiedkilled durin the high temperature phase of composting. that mduce consistent levels of suppression to ,di~easesg '" caused by a broad spectrum of plant pathogens, If mocu-

Curing begins as the concentration of readily blode- lated into compost after peak heating, but before signifi-gradable components in wastes declines, As a result, rates cant levels of recolonization have occurred, Patents haveof decomposition, heat output and temperatures decrease, been issued to The Ohio State University for this processAt this time, mesophilic microorganisms that grow at tem- (Hoitink, 1990). In Japan, Phae et al. (1990), isolated aperatures <40 C recolonize the compost from the outer low Bacillus strain that induces predictable biological controltemperature layer into the compost windro~ or pil,e, There- in composts, It has been recognized for decades that singlefore, suppression of pathogens and/or disease IS largely strains are not as effective in biological control in fieldinduced during curing, because m~st biocontrol agents re- applications as mixtures of microorganisms, (Garrett,colonize composts after peak heating also. 1955). The same applies to container media (Kwok et ai"

Bacillus spp" Enterobacter spp" Flavobacterium 1987),balustinum, Pseudomonas spp" other bacterial genera an~ 4. MECHANISMS OF SUPPRESSION INStreptomyces spp" as well as Penicillium spp" sever~l Trl- COMPOSTSchoderma spp" Gliocladium virens and other fungi havebeen identified as biocontrol agents in compost-amended Two classes of biological control mechanisms knownsustrates(ChungandHoitink 1990; HadarandGorodecki, as "general" and "specific" suppression have been de-1991; Hardy and Sivasithamparam 1991; Hoitink and,Fahy scribed for compost-amended substrates, The mechanisms1986; Nelson etal., 1983; Phae et al., 1990), The moisture involved are based on competition, antibiosis, hyperpara-content of compost critically affects the potential for bac- sitism and the induction of systemic acquired resistanceterial mesophiles to colonize the substrate after peak heat- in the host plant. Propagules of plant pathogens such asing, Dry composts «34% moisture, w/w) be~ome colo- Pythium and Phytophthora spp., are suppressed throughnized by fungi and are conducive to Pythium diseases, In the "general suppression" phenomenon (Boehm et ai"order to induce -suppression, the moisture content must be 1993; Chen et ai" 1988a; Chen et al., 1988b; Cook andhigh enough (at least 40-50%, w/w) so that bacteria as well Baker 1983; Hardy and Sivasithamparam 1991;as fungi colonize the substrate after peak heating. Water Mandelbaum and Hadar 1990), Many types of microor-must often be added to composts during composting and ganisms present in compost-amended container mediacuring to avoid the dry condition. Compost pH also af- function as biocontrol agents against diseases caused byfects the potential for beneficial bacteria to colonize com- Phytophthora and Pythium spp, (Boehm et ai" 1993; Hardyposts, A pH <5.0 inhibits bacterial biocontrol agents and Sivasithamparam 1991), Propagules of these patho.,(Hoitink et ai" 1991). gens, if inadvertently introduced into compost-~ended

, fRh ' t ' dampi'ng off substrates do not germinate in response to nutrients re- Variability in suppression 0 IZOC oma -, , ,

' d 'th leased in the form of seed or root exudates. The high ml-and Fusarium wilt encountered m substrates amende Wi " , ,

d b th " I 'I ' . art to random recolonization crobial activity and biomass cause y e genera SOtmature ~~~~os~~~c~~: ~~o~ontrol agents after peak heat- microflora" in such substrate~ pre~ents germination of

~g~O~~ld co~post more consistently suppresses Rhizoc- spores of these pathogens and mfection of the host, (Chen

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

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

et al., 1988a; Mandelbaum and Hadar 1990). Propagules matter due to high glucose concentrations in such wasteof these pathogens remain dormant and are typically not (de la Cruz et al., 1993). The same processes may occur inkilled if introduced in compost-amended soil (Chen et al., antibiotic production, which also plays an important role1988a; Mandelbaum and Hadar, 1990). An enzyme assay, in biocontrol.that determines microbial activity based on the rate ofhy- I h . ffr .. . . . n mature compost, were concentrations 0 ee nutrl-drolysls offluorescem dlacetate (FDA), predicts suppres- I (Ch I 1988 ) I . fR I .. .. .. ents are owen et a . a sc erotla 0 . so am are

slveness ofpottmg mixes to Pythlum diseases (Boehm and. :'.. .Hoitink 1992; Chen et al., 1988a; Mandelbaum and Hadar kIlled by the hyperparasite, and b~ologlcal control prevaIls1990.Y d S. .th 1994) S. .1 . fi (Nelson et al., 1983). The foregomg reveals that composts

, ouan Ivasl amparam, . Iml arm orma- b d I b.l . d h . .t. h b d I dfi .1 " . &: " h must e a equate y sta I Ize to reac that decomposItionIon as een eve ope or SOl s on organic larms were ..

.Ib d. I I t (W kn h t I 1993) level where biological control IS feasible. In practice, thisSOl orne Iseases are ess preva en or e ea. ,. .Th I th f t . th t th . ffi t I t I occurs m composts (tree barks, yard wastes, etc.) that have

e eng 0 Ime a e suppressive e ec as s a so . , " ,b d t . d 'th FDA t . .ty (B hm dH 't ' k been (I) stabIlized far enough to avoid phytotoxIcity and

may e e ermme WI ac IVI oe an 01 m , . ".1992) Th. . kn th ". 'ty " f th (2) colornzed by the approprIate specific mlcroflora.

, IS IS own as e carrymg capaci 0 e Pr . I 'd I ' th d fi h. ,.I fdb tr t I t ' t b. I ' I tr I actlca gul e IDes at e me t IS cntlca stage 0 ecom-

su s a e re a Ive 0 10 oglca con o. , ., f . I .pOSItion m terms 0 blo oglcal control are not yetThe mechanism of biological control for Rhizoctonia available. Industry presently controls decomposition level

solani in compost-amended substrates is different from that by maintaining constant conditions during the entire pro-of Pythium and Phytophthora spp, because only a narrow cess and adhering to a given time schedule, Compostedgroup of microorganisms is capable of eradicating R. solani. pine bark produced by such a process has been utilizedThis type of suppression is referred to as "specific sup- with great success in floriculture indicating that thispression" (Hoitink et aI" 1991), Trichoderma spp, includ- approach to quality control is quite acceptable (Hoitink eting T hamatum and T harzianum, are the predominant al,,1991).hyperparasites recovered from composts prepared ofligno- ,. .. ,

II I ' t (K t t I 1983. N I t I 1983) Excessively stabIlized organic matter, the opposite endce u OSIC was es u er ea., , e son ea., . f h d . .H 't . . bl f I ., 0 t e ecompOSltion scale, does not support adequate

yperparasl es are microorganisms capa e 0 co ornzmg , , . . .I t th It .' I ' d th Th fu ' activity of blocontrol agents. As a result, suppression IS

p anpa ogens resu mg m YSlS or ea. ese ngl . . .. t t .th . b t ' I tr . ' th b. I . I lackmg and soIlborne diseases are severe, as in highlym erac WI various ac ena s aIDS m e 10 oglca con- . ,. ,tr I f Rh ' t . d . ff (K k t I 1987) It . mmerahzed soIls where humic substances are the predomi-

0 0 lZOC oma ampmg-o wo e a" . IS ,f ' t t th t P . 'II . th d . t h nant forms of organic matter (Workneh et aI" 1993). The

0 meres a emCI lum spp. are e pre omman y- I h f. h 'I 'perparasites recovered from sclerotia of Sclerotium rolfsii edngt 0 I tImle tf abt .SOI -mco l rpo~a~edh composts support. . a equate eve s 0 locontro activity as notYet been de-m composted grape pomace a high sugar and low cellu-I t t t (H d 'd G d k ' 1991 ) '7'. h termined. Presumably, it varies with soil temperature, soilose con en was e a ar an oro ec I, , 1 rlC 0- , . .J t d fr th' t d characterIstIcs and the type of orgarnc matter from whichuerma spp. were no recovere om IS compos an were th d d' .

.. . . e compost wasPrepare. Loa mg rates and farmmgPrac-not effective when mtroduced, The composItion of the .. tIces of course also playa role.feed stock, as expected, appears to have an Impact on themicroflora in composts active in biological control. We have studied the "carrying capacity" of soil or-

ganic matter in potting mixes prepared with sphagnum peat5. BIOLOGICAL ENERGY AVAILABILITY to bring a partial solution to this problem (Boehm and

VERSUS SUPPRESSIVENESS Hoitink 1992; Boehm et al., 1993). Sphagnum peat typi-- cally competes with compost as a source of organic matter

The decomposition level of organic matter in compost- in horticulture, Both the microflora and the organic matteramended substrates has a major impact on disease suppres- in peat itself can affect suppression of soilborne diseases.sion. For example, R. solani is highly competitive as a The literature on that effect is reviewed briefly here.saprophyte (Garrett, 1962), It can utilize cellulose andcolonize fresh wastes but not low cellulose mature com- Dark, more decomposed sphagnum peat, harvestedpost (Chung et aI" 1988). Trichoderma, an effective from a four foot or greater depth in most peat bogs, is lowbiocontrol agent of R.solani, is capable of colonizing fresh in microbial activity and consistently conducive to Pythiumas well as mature compost but it grows better in fresh com- and Phytophthora root rots (Hoitink et al., 1991; Boehmpost (Chung et al., 1988; Nelson et al., 1983). In fresh, and Hoitink, 1992). On the other hand, light, less decom-undecomposed organic matter, biological control does not posed sources of sphagnum peat, harvested from near theoccur because both the pathogen and the biocontrol agent surface of peat bogs, have a higher microbial activity (FDAgrow as saprophytes. Therefore, R. solani (the pathogen) activity) and suppress root rot. Unfortunately, the suppres-remains capable of causing disease here. Prfsumably, syn- sive effect of light peat to Pythium root rots is of shortthesis of lytic enzymes involved in hyperparasitism of duration. (Boehm and Hoitink, 1992; Tahvonen, 1982;pathogens by Trichoderma is repressed in fresh organic Wolffltechel 1988). Light peats are used most effectively

X Congreso Nacional Agronomico / III Congreso de Fitopatologia 1996 49

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~ -

-~-Suppression alp/ant diseases by...

for short prod~ction cyc..es (6-10 week cr~ps), such as in Unfortunately, efficacy varies with the compost, batchesplug and flat mIxes u~ed m the ornamentals mdu.s~. Com- of steepages produced, crops and the disease under ques-posts have longer l~tmg effec~ (B~ehm and HoItmk, 1992; tion. Sackenheim (1993), utilizing plate counting proce-Boehm et aI, 1993, You and Sivasithamparam, 1994). dures, has reported that aerobic microorganisms predomi-

As mentioned above, the rate of hydrolysis of FDA pre- nate in steepages. The microflora includes strains of bac-dicts suppressiveness of peat mixes and of compost- teria and isolates of fungi already known as biocontrolamended substrates to Pythium root rot (Boehm and agents. He developed a number of enrichment strategies,Hoitink, 1992). As FDA activity in suppressive substrates that include nutrients as well as microorganisms, to im-declines to < 3.2 =B5g FDA hydrolyzed min-l g-1 dry prove efficacy of the steepages.weight mix, the population of Pythium ultimum increases,infection takes place and root rot develops. During this Control induced by compost steepages has also beencollapse in suppressiveness, the composition of bacterial attributed to systemic acquired resistance (SAR) inducedspecies also changes (Boehm et al., 1993). A microflora in plants by microbes present in the extracts (Weltzhien,typical of suppressive soils, which includes Pseudomonas 1992). The recent work by Sackenheim (1993) on grape,spp. and other rod-shaped Gram negative bacteria as the however, does not support this assumption. A factor thatpredominant rhizosphere colonizers, is replaced by pleo- has not been evaluated but could playa role in efficacy ofmorphic Gram-positive bacteria (e.g., Arthrobacter) and steepages is the condition of soil organic matter and theputative oligotrophs (Wu et al., 1993). The microflora of associated microflora in the soil in which treated plants arethe conducive substrate resembles that of highly miner- produced. Soils naturally suppressive to soilborne plantalized niches in soil (Kanazawa and Filip, 1986). pathogens (e.g., compost-amended soils) harbor active

. . .. . . populations of biocontrol agents (Boehm et al., 1993).. Non-.destructlve analysIs of soil organic matter, utIlIZ- Several of these rhizobacteria and fungi can induce pro-mg FounerTransform Infra Red spectroscopy (FT-IR) and tection to foliar pathogens in the leaves of plants (Ma h tiCross Polariza~ion Magic Angle Spinning -13Carbon et al., 1994; Wei et al., 1991). Zhang et al., (19~)or:~Nuclear MagnetIc Reson~c~ Spectro.scopy (CPMAS - 13C ported that pathogenesis - related proteins were activated

NMR), allows charactenzation of biodegradable compo- in roots and shoots of cucumberPlantsProd d . -f .1 . fr . ( b uce m com

nents 0 SOl organic actions In ar et al., 1989; Ch~n ~d post. Further work may reveal that composts affect resis-Inbar, 1993). CPMAS - 13CNMR allows quantitative tance of the roots and foliage to diseases. Presentl -analysis of concentrations of readily. biodegradable sub- trol of foliar diseases with composts or steepages iS~i;~ystances such as "carbohydrates" (hemicellulose, cellulose, variable.etc.) versus lignins and humic substances in soil organicmatter [reviewed in Chen and Inbar, 1993]. In a prelimi- 7. DISEASE SUPPRESSION - FUTUREnary report, Wu et al. (1993) reported that the "carbohy- OUTLOOKdrates" decline as suppressiveness is lost. During the same . .. '.time period, bacterial genera capable of causing biological . Suc.cess m bl~loglcal contr~l of dlse~es With comp~stscontrol are replaced by those that cannot provide control. IS pos~I~le ~nly If all factors Involved m the productionBiocontrol agents inoculated into the more decomposed and utilization of composts are defined and kept consis-substrate are not able to induce sustained biological con- tent. Most composts are variable in quality. Therefore,trol of Pythium root rot. The same phenomenon has been composted pine bark remains the principal compost usedobserved for Phytophthora root rot in the field (You and for th.e prepar:ation of potting mixes or soils naturally sup-Sivasithamparam, 1994). Therefore, biocontrol of these presslve to soilborne plant pathogens. Composted manures,diseases is determined by the "carrying capacity" of the yard and food wastes ar~ steadily gai~ing in popularity,substrate which.regulates species composition and activity and offer the same potential (Gorodeckl and Hadar, 1990;and, in turn, the potential for sustenance of biological con- Grebus etal., 1994; Inbar et al., 1993; Marugg et al., 1993;trol. SchUler et al., 1993).

6. COMPOST FOR CONTROL OF FOLIAR Controlled inoculation of composts with biocontrolDISEASES agents is a procedure that must be developed on a com-

. .. mercial scale to induce consistent levels of suppression toDurmg the past decade, a senes of projects have been pathogens such as R. solani (Hoitink et al., 1991; Phae et

publishedon~hecontrolofplantdiseasesofaboveground al., 1990; Grebus et al., 1993). Recently, tree bark wasplant parts With water extracts, als.o known as steepages, proposed as a food base for the culture ofbiocontrol agentsprepared from composts (Weltzhlen, 1992; Yoh.alem et and as a carrier of such agents for use in agricultural appli-al., 1994). Ste~pages ofte~ are prepared by soaking ma- cations (Steinmetz and Schl>nbeck, 1994). However, thisture composts m w~ter (still culture; 1:1, w/w) for 7-10 new field of biotechnology, is still in its infancy. Majordays. The steepage IS filtered and then sprayed on plants. research and development efforts will need to be directed

50 X Congreso Nacional Agronomico / III Congreso de Fitopatologia 1996

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

toward this approach for disease control. Recycling through Farrell, J. B. 1993. Fecal pathogen control during composting, p. 282-composting is being chosen as the preferred strategy for 300. In: Science and Engineering of Composting: Design,

. . Environmental, Microbiological and Utilization Aspects. H.waste treatment. ThIs also applIes to farm manures. Fqr A. J. Hoitink and H. M. Keener, eds. Renaissance Publications,

this reason, composts are becoming available in greater Worthington, OH. 728 p. Garrett, S. D. 1955. A century ofquantities. Peat, on the other hand, is a limited resource root-dise~e investigation. Ann. Appl. Bioi. 42:211-219.

that cannot be recycled. Future opportunities for both natu-I d tr II d . d d . f .lb I t Garrett., S. D. 1962. Decomposition of cellulose in soil by Rhizoctonia

ra an con 0 e -In uce suppressIon 0 SOl orne p an solani Kuhn. Trans. Br. Mycol. Soc. 45:114-120.

pathogens appear bright.Grebus, M. E., K. A. Feldman, C. A. Musselman, and H. A. J. Hoitink.

8. ACKNOWLEDGEMENT 1993. Production of biocontrol agent-fortified compost-amended potting mixes for predictable disease suppression.

Salaries and research support provided by State and Phytopathology 83:1406 (Abstr.).

federal funds appropriated to the Ohio Agricultural Re-search and Development Center The Ohio State Univer- Grebus, M. E., M. E. Watson, and H. A. J. Hoitink. 1994. Biological,

. db G t US2 I 96-22 from BARD the United ch~mi.cal and physic~1 properties o~ composted y~d trimmingsSlty, an y ran no. , as Indicators ofmatunty and plant disease suppression. Compost

States-Israel Binational Research and Development Fund. Sci. Util. 1:57-71.

9. REFERENCES Gorodecki, B. and Y. Hadar. 1990. Suppression of Rhizoctonia solaniand Sclerotium rolfsii in container media containing composted

Boehm, M. J. and H. A. J. Hoitink. 1992. Sustenance of microbial separat.ed cattle manure and composted grape marc. Cropactivity and severity of Pythium root rot of poinsettia. ProtectIon 9:271-274.

Phytopathology 82:259-264. . .. .Hadar, Y. and B. Gorodeckl. 1991. Suppression of germ mati on of

Boehm, M. J., L. V. Madden, and H. A. J. Hoitink. 1993. Effect of sclerotia of Sclerotium rolfsii in compost. Soil. Bioi. Biochem.organic matter decomposition level on bacterial species diversity 23:303-306.

and composition in relationship to Pythium damping-off . . .severity. A lied Environ. Microbiol. 59:4171-4179. Hardy, G. E. St. J. and K. Sivasithamparam. 1991. Suppresslon.of'

pp Phytophthora Root Rot by a Composted Eucalyptus Bark MIx.

Bollen, G. J. 1993. Factors involved in inactivation of plant pathogens Aust. J. Bot. 39:153-159.

during composting of crop residues, p. 301-318. In: Science.. ...and Engineering of Composting: Design, Environmental, Holtlnk, H. A}. 1990: Produc~lon of dls.ease suppressIve comp~st andMicrobiological and Utilization Aspects. H. A. J. Hoitink and contaIner media, and microorganism culture for use thereIn. USH. M. Keener, eds. Renaissance Publications, Worthington, Patent 4960348. Feb. 13, 1990.

OH. 728 p. H . . k J h doltln ,H. A. ., M. Daug tery, an H. K. Tayama. 1987. Control ofChen, W., H. A. J. Hoitink, A. F. Schmitthenner, and O. H. Tuovinen. cyclamen Fusarium wilt - A preliminary report. Ohio Florist't

1988a. The role of microbial activity in suppression of damping- Assoc. Bull. 693:1-3.off caused by Pythium ultimum. Phytopathology 78:314-322.

Chen, W., H. A. J. Hoitink, andL. V. Madden. 1988b. Microbial activity Hoitink, H. A. J. and P. C. ~ahy. 1986. Basis for the control of soilborneand biomass in container media predicting suppressiveness to plant pathogens With composts. Ann. Rev. Phytopathol. 24:93-damping-off caused by Pythium ultimum. Phytopathology 114.

78:1447-1450. . .k bHoltln H. A. J., Y. In ar, and M. J. Boehm. 1991. Status of com post ed-

Chen, Y. and Y. Inbar. 1993. Chemical and spectroscopical analyses of amended potting mixes naturally suppressive to soilborneorganic matter transformations during composting in relation diseases oftloricultural crops. Plant Dis. 75:869-873.to compost maturity, p. 551-600. In: Science and Engineeringof Composting: Design, Environmental, Microbiological and Iannotti, D. A., Grebus, M. E., Toth, B. L., Madden L. V. and Hoitink,Utilization Aspects. H. A. J. Hoitink and H. M. Keener, eds. H. A. J. 1994. Oxygen respirometry to assess stability andRenaissance Publications, Worthington, OH. 728 p. maturity of composted municipal solid waste. J. Env. Qual.

Chung, Y. R., H. A. J. Hoitink, and P. E. Lipps. 1988. Interactions 23:1177-1183.

between organic-matter decomposition level and soilborne .disease severity. Agric., Ecosys. Environ. 24:183-193. Inbar, Y., Y. Ch~n, and Y. Hadar. .1989. SolId-state carbon-13 nuclear

magnetic resonance and Infrared spectroscopy of compostedChung, Y. R. and H. A. J. Hoitink. 1990. Interactions between organic matter. Soil Sci. Soc. Am. J. 53:1695-1701.

thermophilicfungi and Trichoderma hamatum in suppressionof Rhizoctonia damping-off in a bark compost- amended Inbar, Y., Y. Hadar, and Y. Chen. 1993. Recycling of cattle manure:container medium. Phytopathology 80:73-77. The composting process and characterization of maturity: J.

Cook, R. J. and K. F. Baker. 1983. The Nature and Practice of Biological Environ. Qual. 22:857-863.

Control of Plant Pathogens. Am. Phytopathol. Soc., St. Paul,MN. 539 p. Kanazawa, S. and Z. Filip. 1986. Distribution of microorganisms, total

biomass, and enzyme activities in different particles of brownde la Cruz, J., M. Rey, J. M. Lora, A. Hidalgo-Gallego, F. Dominguez, soils. Microb. Ecol. 12:205-215.

J. A. Pintor-Toro, A. Llobell, and T. Benitez. 1993. Carbonsource control on -glucanases, chitobiase and chitinase from Kuter, G. A., H. A. J. Hoitink, and W. Chen. 1988. Effects ofmunicipalTrichoderma harzianum. Microbiol. 159:316-322. sludge compost curing time on suppression of Pythium and

Rhizoctonia diseases of ornamental plants. Plant Dis. 72:751-756.

X Cangreso Nacional Agronomico 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. Schneider, R. W. 1985. Suppression of Fusarium yellows of celeryFungal populations in container media amended with composted with potassium chloride and nitrate. Phytopathology 75:40-hardwood bark suppressive and conducive to Rhizoctonia 48.

damping-off. Phytopathology 73:1450-1456.SchUler, C., J. Pikny, M. Nasir, and H. Vogtrnann. 1993. Effects of

~wok, O. C. H., P. C, Fahy, H. A. J. Hoitink, G. A. and Kuter. 1987. composted organic kitchen and garden waste on MycosphaerellaInteractions between bacteria and Trichoderma hamatum in pinodes (Berk, et Blox) Vestergr., Causal organism of foot rotsuppression of Rhizoctonia damping-offin bark compost media. on peas (Pisum sativurn L.) Biolog. Agric. Hort. 9:353-360.

Phytopathology= 77:1206-1212.Steinmetz, J. and F. Sch(jnbeck. 1994. Conifer bark as growth medium

Lumsden, R. D., J. A. Lewis, and P. D. Millner. 1983. Effect of and carrier for Trichoderma harzianum and Gliodadiumroseumcornposted sewage sludge on several soilborne pathogens and to control Pythium ultimum on pea. J. Plant Dis. Proto ;diseases. Phytopathology 73:1543-1548. 101:200-211.

Mandelbaum, R. andY. Hadar. 1990. Effects of available carbon source Tahvonen, R. 1982. The suppressiveness of Finnish light coloredon microbial activity and suppression of Pythium Sphagnum peat. J. Sci. Agric. Soc. Finl. 54:345-356.

aphanidermatum in compost and peat container media. .Phytopathology 80:794-804. Tnllas -Gay, M. I., H. A. J. Hoitink, and L. V. Madden. 1986. Nature of

suppression of Fusarium wilt of radish in a container mediumMarugg, C., M. E. Grebus, R. C. Hansen, H. M. Keener, and H. A. J. amended with composted hardwood bark. Plant Disease:

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process. Compost Sci. & Util. 1:38-51.Wei, G., J. W. Kloepper, and Tuzun, S. 1991. Induction of systemic

Maurhofer, M., C. Hase, P. Meuwly, J-P. Metraux, and G. Defago. 1994. resistance of cucumber to Colletotrichum orbiculare by selectInduction of systemic resistance of tobacco to tobacco necrosis strains of plant growth-promoting rhizobacteria.virus by the root-colonizing Pseudomonasfluorescens strain Phytopathology 81:1508-1512.

CHAO: Influence of the gac, a gene and of pyoverdine .production. Phytopathology 84: 139-146. Weltzhlen, H. C. 1992. Biocontrol offoliar fungal diseases with compost

extracts, p. 430-450. In: Microbial Ecology of Leaves, J HNelson, E. B., Kuter, G. A. and Hoitink, H. A. J. 1983. Effects offungal Andrews and S Hirano (eds), Brock Springer Series in

antagonists and compost age on suppression of Rhizoctonia Contemporary Bioscience. BSBN 0387-97579-9,

damping-off in container media amended with compostedhardwood bark. Phytopathology 3:1457-1462. Woltlhechel, H. 1988. The suppressiveness of Sphagnum peat to

Pythium spp. Acta Hort. 221 :217-222.

Ownley, B. H. and D. M. Benson. 1991. Relationship ofmatric waterpotential and air-filled porosity of container media to Workneh, F., A. H. C. Van Bruggen, L. E. Drinkwater, and C. Sherman.development of Phytophthora root rot of rhododendron. 1993. Variables associated with a reduction in corky root andPhytopathology 81:936-941. Phytophthora root rot of tomatoes in organic compared to

conventional farms. Phytopathology 83:581-589.

Phae, C. G., M. Saski, M. Shoda, and H. Kubota. 1990. Characteristicsof Bacillus subtilis isolated from' composts suppressing Wu, T., M. J. Boehm, L. V. Madden, and H. A. J. Hoitink. 1993.phytopathogenic microorganisms, Soil Sci. PlantNutr. 36:575- Sustained suppression of Pythium root rot: A funtion of586. microbial carrying capacity and bacterial species composition.

Phytopathology 83: 1406 (Abstr.).

Quarles, W. and J. Grossmam. 1995. Alternatives to methyl bromide innurseries - Disease suppressive media. The IPM Practitioner Yohalem, D. S" R. F. Harris, and J. H. Andrews. 1994. Aqueousextracts17(8):1-13. of spent mushrooms substrate for foliar disease control.

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Sackenheim, R. 1993. Untersuchungen Uber Wirkungen vonWasserigen, mikrobiologisch aktiven Extracten aus You, M. P. and Sivasithamparam. 1994, Hydrolysis of fluoresceinkompostierten Substraten auf den Befall der Weinrebe (Vitis diacetate in an avocado plantation mulch suppressive tovinifera) mit Plasmopora viticola, Uncinula necator, Botrytis Phytophtora cinnamoni and its relationship with certain bioticcenerea und Pseudopezicula tracheiphila. Ph.D. thesis. and abiotic factors. Soil BioI. Biochem. 26:1355-1361.

Rheinische Friedrich-Wilhelms Universitat, Bonn, Germany.157 p. Zhang, W., W. A, Dick, and H. A. J. Hoitink. 1994. Compost induced

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