MycorrhizaeAND PLANT HEALTH

Edited by F. L. Pfleger and R. G. Lindennan

SYMPOSIUM SERIES

ROLE OF VAM FUNGÍ IN BIOCONTROL

Robert G. LindermanUSDA-ARS Horticultural Crops Research Laboratory

Corvallis, Oregon

Most terrestrial plant species have in theirroots a symbiotic association with soil fungí calledmycorrhiza. There are several categories ofmycorrhizae, of which the largest group, vesicular-arbuscular mycorrhizae (VAM), form with mostagricultural crops. VAM fungi exist in soil as thick-wal-led chlamydospores, or as vegetativa propagules inroots, that germinate in the rhizosphere/rhizopiane.Their hyphae penétrate the root cortex, ramifyingintercellularly from the point of penetration. Thefungus forms special haustoria-1ike structures(arbuscules or coiled hyphae) within cortical cells,separated from the host cytoplasm by the host plasmamembrane and the fungal cell wall. Arbuscules provideincreased surface área for metabolic exchanges betweenthe host and fungal partners. VAM fungi also developextraradical hyphae that grow into the surroundingsoil, increasing the potential of the root system fornutrient and water absorption, and contributinggreatly to the improvement of soil structure forbetter aeration and water percolation. New survivalspores are usually borne on the extraradical hyphae,although spores of some fungal species are producedprimarily intraradically.

Generally, VAM cause few changes in rootmorphology, but the physiology of the host plantchanges significantly. For example, tissueconcentrations of growth regulating compounds andother chemical constituents change, photosyntheticrates increase, and the partitioning of photosynthateto shoots and roots changes (16). The improved

2 CHAPTER ONE

potential for mineral uptake from the soil accountsfor changes in the nutritional status of the hosttissues, in turn changing structural and biochemicalaspects of root cells. This can alter membranepermeability and thus the quality and quantity of rootexudation. Altered exudation induces changes in thecomposition of microorganisms in the rhizosphere soil,now appropriately called the "mycorrhizosphere"(51,67,82). The net effect of these changes is ahealthier plant, better able to withstandenvironmental stresses (52) and tolérate or reduce theeffects of plant diseases.

The purposes of this review are (a) to discussthe role of VAM in the expression of plant disease andthe mechanisms involved therein, and (b) to discussfactors that influence the role of VAM in biologicalcontrol of plant diseases.

VAM EFFECTS ON FUNGAL ROOT PATHOGENS

Since VAM fungi are major components of therhizosphere, it is logical that they could affect theincidence and severity of root diseases. Whether theydo or not has been the subject of numerous reviewsover the last 15 years (18,32,46,71,72,73), but thereis still controversy. Much of the 1Herature suggeststhat VAM fungi reduce soilborne disease or the effectsof disease caused by fungal pathogens. Dehne (32)reported that disease damage was reduced in 17 out ofthe 32 reports cited. However, the reports are stillmixed, with some indicating no effect of the VAMfungus on disease (6,7,28,84,85), and othersindicating increased disease severity (29,30,31).Drawing conclusions is difficult, partly because somany different pathogens and diseases have beeninvolved, and partly because of the experimentalconditions of each study. Clearly, one should expectvaried results, even if the VAM fungi used had beenthe same (71).

VAM EFFECTS ON PATHOGENIC ROOT NEMATODES

Root infections by pathogenic nematodes are

generally less severe on VAM pplants, but the responses mayinvolved are controversial (42nematode infection are generalbut not always, nematode populindicated by number of galls,unit root 1ength)(41). Atilaishowed an increase in nematodiplants. These differences ma;differences between nematodebe due to differences in VAMcolonization. Furthermore, awith fungal pathogens, timing:nportant.

A number of mechanisms ofand nematode pathogens have bevidence supporting each is rproposed mechanisms depend orhost physiology. Changes inplants may change the attrad'e^iatode pathogens. VAM mayand thus reduce yield lossesinfection, especially in lowestablished early in the groiinfection. This mechanism othe reduced nematode responslowever, by work that showed(55). Cooper and Grandisonvariable by using P-tolerant

:er high P conditions. Steffects, leading these workeincreased resistance to nemsto improved host nutrition,other physiological changesStrobel et al. (78) and 01 \\g split root techniques

-eT.atode infection on VAM ptwo were together on the saisuggested that competitioninvolved, a mechanism suppoand Sikora (69), Suresh etükora (75), and MacGuidwinstudies indicated that nema

>take from the soil accountslonal status of the host

«9 structural and biochemical5 can alter membrane

ity and quantity of rootion induces changes in thesms in the rhizosphere soil

mycorrhizosphere"p of these changes is a

>le to withstandi and tolérate or reduce the

review are (a) to discusssion of plant disease and

•erein, and (b) to discussí of VAM in biológica!

UNGAL ROOT PATHOGENS

components of thethey could affect theseases. Whether they

F numerous reviews71,72,73), but there

:he literature suggestsHsease or the effects

logens. Dehne (32)reduced in 17 out ofthe reports are stillFfect of the VAM

')» and othersíverity (29,30,31)

- Partly because soises have been

:he experimental•ly, one should expectfungí used had been

GENIC ROOT NEMATODES

ogenic nematodes are

LINDERMAN 3

generally less severe on VAM plants than on nonVAMplants, but the responses may vary, and the mechanismsinvolved are controversia! (42,44). Symptoms ofnematode infection are generally reduced, and often,but not always, nematode populations are reduced (asindicated by number of galls, juveniles or eggs perunit root length)(41). Atilano et al. (3), however,showed an increase in nematode populations on VAMplants. These differences may be due largely todifferences between nematode pathogens, but could al sobe due to differences in VAM fungi and their levéis ofcolonization. Furthermore, as with VAM interactionswith fungal pathogens, timing of VAM formation isimportant.

A number of mechanisms of interaction between VAMand nematode pathogens have been considered, and theevidence supporting each is reasonable. All theproposed mechanisms depend on VAM-mediated changes inhost physiology. Changes in root exudation by VAMplants may change the attractiveness of roots tonematode pathogens. VAM may improve host plant vigor,and thus reduce yield losses caused by nematodeinfection, especially in low P soils and if VAM areestablished early in the growth cycle, before nematodeinfection. This mechanism of enhanced P nutrition inthe reduced nematode response has been challenged,however, by work that showed no effect from adding P(55). Cooper and Grandison (24,25) eliminated P as avariable by using P-tolerant VAM fungi on plants grownunder high P conditions. Still, VAM reduced nematodeeffects, leading these workers to conclude thatincreased resistance to nematodes was not entirely dueto improved host nutrition, but must involve someother physiological changes in the roots. Studies byStrobel et al. (78) and Oliveira and Zambolim (61)using split root techniques indicated that reducednematode infection on VAM plants only occurred if thetwo were together on the same roots. These resultssuggested that competition for food or space wasinvolved, a mechanism supported by results of Salenand Sikora (69), Suresh et al. (79), Sitaramaiah andSikora (75), and MacGuidwin et al. (55). Thesestudies indicated that nematode size was reduced and

4 CHAPTERONE

rate of development of infection was slower 1n VAMroots than nonVAM roots. Physiological changes in VAMroots could also change resistance to nematodes byincreased production of ínhibitory substances (79), orby changes in root exudation which could altermycorrhizosphere populations and affect nematodepopulations and survival.

While the mechanisms are still controversial, theevidence strongly indicates that VAM suppress nematodeinfections of roots or reduce nematode effects onplant growth and yield. Undoubtedly, the effects andthe mechanisms involved depend on the conditions ofthe test, the host plant, edaphic conditions, and thespecies of VAM fungus involved. Nonetheless, it seemssafe to say that VAM do play a role in the biologicalcontrol of root nematode diseases.

VAM EFFECTS ON BACTERIAL DISEASES

The effects of VAM on bacterial diseases have notbeen explored to any great extent. However, Garcia-Garrido and Ocampo (36) showed that VAM tomato(Lycopersicon Miller) plants exhibited greater growththan nonVAM plants inoculated with Pseudomonassynngae pv. syringae van Hall when the pathogen wasadded to the foí i age three weeks after the VAM fungus.Populations of the pathogen were lower in VAM thannonVAM plants.

VAM EFFECTS ON VIRUS AND FOLIAGE DISEASES

While soilborne diseases caused by funga!,nematode, and bacterial pathogens most often arereduced by VAM, those caused by viral and otherfoliage pathogens are generally increased in VAMplants (32,46,73). Reports indicate that diseaseincidence, but not necessarily severity of effect onthe plant, is increased in VAM compared to nonVAMplants. Viruses apparently multiply faster in VAMthan nonVAM plants. One might suspect that VAM fungicould acquire and vector viruses from root to rootbetween plants, but that apparently does not happen(45). VAM effects on viruses occur throughout the

plant due to changes in the ho2) pointed out, foliage dise

oblígate and non-obligate leafincreased on VAM compared to nto enhanced development of theto increased incidence or freq>at effect was correlated witigher physiological activitie

plants (32,73).

MECHANISMS OF VAM EFFEC1

Since VAM have such a sig?plant physiology and on bioloc"izosphere soil, it follows ^

the incidence and severity ofrole played by VAM in the bio"seases has been the subject5.18,32,41,46,70,71,72,73),"terpretations have preclude;hat VAM always suppress plan-nconsistencies should be expcansidering the diverse experuse of different VAM fungi onsifferent soils (71). Part crevolves around the mechanisrriXM and plant pathogens. Incontrol of plant diseases, 013contribute to biological conlorimarily by means of stress(10,12,23,62,72). The liter;however, indicates that biol<:iseases may be strongly inf"•nore mechanisms, including:(b) competition for host phosites, (c) morphological cha:issues, (d) changes in chemtissues, (e) reduction of ab•icrobial changes in the myc

Enhanced NutritionThe most obvious VAM con

disease is to increase nutri

infection was slower in VAMPhysiological changes in VAM

resistance to nematodes byinhibitory substances (79), or

ation which could altertions and affect nematode1 .; are still controversia!, theites that VAM suppress nematode'educe nematode effects onUndoubtedly, the effects and

depend on the conditions of, edaphic conditions, and thevolved. Nonetheless, it seemsplay a role in the biologicaldiseases.

BACTERIAL DISEASES

1 bacterial diseases nave nott extent. However, García-howed that VAM tomatonts exhibited greater growthated with PseudomonasHall when the pathogen was2 weeks after the VAM fungus.5n were lower in VAM than

S AND FOLIAGE DISEASES

es caused by fungal,thogens »ost often areed by viral and otherrally increased in VAMs indícate that disease

r severity of effect onMU coapared to nonVAM

r Nltiply faster in VAM;ght suspect that VAM fungiruses from root to rootparently does not happenes occur throughout the

LJNDERMAN 5

plant due to changes in the host physiology. As Dehne(32) pointed out, foliage diseases caused by bothiDÜgate and non-obligate leaf pathogens can beincreased on VAM compared to nonVAM plants, likely dueto enhanced development of the pathogens rather thanto increased incidence or frequency of infections.That effect was correlated with improved nutrition and- :her physiological activities in VAM than nonVAMplants (32,73).

HECHANISHS OF VAM EFFECTS ON PLANT DISEASE

Since VAM have such a significant effect on hostplant physiology and on biological interactions in thertnzosphere soil, it follows that they could affectthe incidence and severity of plant diseases. Therole played by VAM in the biological control of plantdiseases has been the subject of several reviews(8,18,32,41,46,70,71,72,73), but mixed responses andinterpretations have precluded any clear conclusiónthat VAM always suppress plant diseases. Suchinconsistencies should be expected, however,considering the diverse experimental approaches anduse of different VAM fungi on different hosts indifferent soils (71). Part of the controversy alsorevolves around the mechanisms of interaction betweenVAM and plant pathogens. In reviews of biologicalcontrol of plant diseases, mycorrhizae are thought tocontribute to biological control of plant diseasesprimarily by means of stress reduction(10,12,23,62,72). The literature of recent years,however, indicates that biological control of plantdiseases may be strongly influenced by VAM by one ormore mechanisms, including: (a) enhanced nutrition,(b) competition for host photosynthate and infectionsites, (c) morphological changes in roots and roottissues, (d) changes in chetnical constituents of planttissues, (e) reduction of abiotic stresses, and (f)microbial changes in the mycorrhizosphere.

Enhanced NutritionThe most obvious VAM contribution to reduced root

disease is to increase nutrient uptake, particularly P

6 CHAPTERONE

and other minerals, resulting in more vigorous plantsbetter able to resist or tolérate root disease. Theevidence to support the enhanced nutrition idea comesfrom experiments where effects comparable to VAMeffects were observed when more fértil izer P wasadded. Davis (28) showed this type of response in hisstudies on Thielaviopsis root rot of citrus where VAMplants were larger than nonVAM plants unless thelatter were fertilized with additional P. Graham andMenge (38) suggested a similar effect, where VAM oradded P reduced wheat take-all disease (Gaeumannomycesgraminis var. tritici (Sacc.) Arx & 01 iv.), andspeculated that enhanced P status of the plants causeda decrease in root exudates used by the pathogen forspore germination and infection. They did not,however, demónstrate increased pathogen sporegermination with those treatments. In some cases,reports indicate that VAM or added P increased diseaseincidence, as in the case of(Verticilliuai dahliae Kleb.)n'rsutum L.) (31).

In an attempt to clarifyrole of enhanced P nutritionroot disease expression, Graham and Egel (37) found nodifferences between Phytophthora root rot levéis onVAM and nonVAM citrus seedlings fertilized to be ofequal size and P content. Carón et al. (20,21,22)compared responses between VAM and nonVAM tomatoplants with a relatively low P threshold requirementto root and crown rot disease caused by Fusariumoxysporum f. sp. radicis-lycopersici Jarvis &Shoemaker. Added P did not reduce disease responseand pathogen populations in rhizosphere soil of nonVAMplants, but did with VAM plants, even though plantgrowth and tissue P were not different in the twotreatments. This work suggests the involvement ofsome mechanism of disease suppression other thanenhanced P uptake. Whether or not enhanced P uptakeby VAM is involved either directly or indirectly indisease expression remains controversial. Thepossibility that improved uptake of other mineralelements from soil could be involved has not beenexplored.

Verticillium wiltof cotton (Gossypium

the confusión about theassociated with VAM and

Coapetition for Nutrients andEven though VAM fungi depf

--<• carbohydrates from photos;*¿ether they compete with roo!itrients. Dehne (32) indica'thogens could occupy root &>se colonized by VAM fungí,^etition. It has been sugthogens, on the other hand,• reproduction and developm

DBnetition with VAM fungí ha•echanism of their inhibitionliUle or no direct evidencerpothesis, however. On theiré than make up for theirDancing photosynthesis witliply to root pathogens.

. lógica! ChangesLocalized morphologicaloccur in VAM roots. For

íchonbeck (33) showed increaMato and cucumber (Cucuims

-- »ndodermis in VAM plantsponses accounted for redusporum f. sp. lycopersici

ícker (15) showed a similaron (Pyrenochaeta terrestrLarson). Wick and Moore 1nd-barrier formation thalick root rot (Thielaviops-.) of VAM holly {I7ex ci

T»ese few examples indicateihological changes in ro>

tudies, however, roots wer; - . - - :al changes, so it r

. —:- .ely such a mechanis

. in Chemical ConstitPhysiological changes a

Involved in localized efjne et al. (34) demonstra

Kientrations of anti-func

sulting in more vigorous plantsDT tolérate root disease. The2 enhanced nutrition idea comeseffects comparable to VAM<hen more fértilizer P wasfed this type of response in hiss root rot of citrus where VAMnonVAM plants unless the

with additional P. Graham andsimilar effect, where VAM orake-all disease (GaeumannomycesSacc.) Arx & Oliv.), andJ P status of the plants causedites used by the pathogen forifection. They did not,:reased pathogen sporereatments. In some cases,W or added P increased diseasee of Verticillium wilteb.) of cotton (Gossypium

rify the confusión about thetion associated with VAM andGraham and Egel (37) found nojphthora root rot levéis onrflíngs fertilized to be of

Carón et al. (20,21,22)i VAM and nonVAM tomato

' threshold requirementcase caused by Fusariumlycopersici Jarvis &: reduce disease responsei rhízosphere soil of nonVAM

)lants, even though plantlot different in the twoigests the involvement ofsuppression other thanr or not enhanced P uptakedirectly or indirectly incontroversial, The

uptake of other mineral5 involved has not been

LINDERMAN 7

Competítion for Nutrients and Infection SiteEven though VAM fungi depend on the host plant

for carbohydrates from photosynthesis, it is not clearntiether they compete with root pathogens forlutrients. Dehne (32) indicated that fungal root:athogens could occupy root cortical cells adjacent tothose colonized by VAM fungi, indicating a lack ofzDTipetition. It has been suggested that nematodepathogens, on the other hand, require host nutrientsfor reproduction and development, and direct:-Tipetition with VAM fungi has been hypothesized as a•echanism of their inhibition (32,76). There islittle or no direct evidence to support thathypothesis, however. On the contrary, VAM appear to•ore than make up for their nutrient needs byenhancing photosynthesis without limiting the nutrientíupply to root pathogens.

Morphological ChangesLocalized morphological effects nave been shown

to occur in VAM roots. For example, Dehne andSchonbeck (33) showed increased 1ignification oftomato and cucumber (Cucumis satvus L.) root cells ofthe endodermis in VAM plants, and speculated that suchresponses accounted for reduced Fusarium wilt (f.oxysporum f. sp. lycopersici (Sacc.) Snyder & Hans.)-Becker (15) showed a similar effect on pink root ofonion (Pyrenochaeta terrestris (Hansen) Goreng, Walker& Larson). Wick and Moore (83) al so showed increasedwound-barrier formation that inhibited Thielaviopsisblack root rot (Thielaviopsis basicola (Berk. & Br.)Ferr.) of VAM holly (Ilex crenata Thundb.) plants.These few examples indícate that VAM may induce-orphological changes in root tissues. In most otherstudies, however, roots were not examined foranatomical changes, so it retnains unknown just howextensively such a mechanism may be involved.

Changes in Chemical Constituents of Plant TissuesPhysiological changes also nave been reported to

be involved in localized effects on root pathogens.Dehne et al. (34) demonstrated increasedconcentrations of anti-fungal chitinase in VAM roots,

8 CHAPTER ONE

and they al so suggested that increased arginineaccumulation in VAM roots suppressed Thielaviopsissporulation, a mechanism previously suggested byBaltruschat and Schonbeck (13). Morandl et al. (58)found increased concentrations of phytoalexin-likeisoflavonoid compounds in VAM vs. nonVAM soybeans(Glycine max L.). They postulated that such materialscould account for increased resistance to fungal andnematode root pathogens, compared to nonVAM plants.More recently, however, Morris and Ward (59) reportedchemoattraction of pathogen zoospores by isoflavonoidsfrom soybeans. It would appear that such compounds,as well as other compounds, could have differenteffects on disease incidence and/or severity. Justwhat role VAM play in these processes remains unknown,lacking direct evidence.

Alleviation of Abiotic StressEnvironmental stresses influence the incidence

and severity of biotic plant diseases and cause someabiotic diseases. VAM increase plant tolerance tosuch stresses by various mechanisms. In this context,VAM can function to biologically reduce plant diseasesby virtue of their capacity to reduce effects ofpredisposing stress factors such as nutritional stress(deficiency or excess), soil drought, and soiltoxicities.

Because of the greater volume of soil explored byextraradical hyphae of VAM fungi compared to nonVAMroots, nutrient mineral elements that are relativelyunavailable because they are bound to soil particles(i.e. P, Cu, and Zn) are absorbed by VAM fungal hyphaeand translocated to the root from beyond the zone ofnutrient depletion around the root. VAM are able toacquire these and relatively mobile nutrients likenitrogen (N) from soils where deficiency levéis wouldotherwise créate plant nutrient stress. Nutrientstress may weaken the plant, making it moresusceptible to pathogen ingress, or more sensitive toother environmental stresses such as cold or heat.Thus, VAM contribute greatly to the general health ofplants by helping to avoid nutrient stress andassociated disease-predisposing effects.

Drought stress is another ¡^redisposes plants to attack typathogens. Extraradical hyphaiabsorb water under soil droughthus help plants to tolérate d"o*ever, controversy over whetwater from soil is the mechaniplants tolérate drought, or wh•ptake by VAM is responsible (iat VAM change the physiology•afee them more drought toleran(4,5.26,37).

VAM plants are less sensit» soil toxicities resulting f

I or mineral elements such asre is controversy about thí

i some work implicating imfsalt tolerance (66), but littl:í*e mechanisms of heavy metaluses, however, the toxic matt

:luded or are somehow alten-~ects on plant growth. As \s are more tolerant to si

«alntain a higher leve! of gninVAM plants, and thus may b>

élseases.

•icrobial Changes in the MycoWhile any of the above me

CHÉrinations thereof, could bsappression of root diseases,rsidered more carefully isnzosphere populations of an

the evidence is clear that mii the mycorrhizosphere (57,7

iidered those changes reíacontrol of diseases, so relat«railable to support such a n

The concept of the "mycot- L - -..icrrhizae significan^

•icroflora of the rhizosphenpÉjysiology and exudation. Iihyphae of VAM fungi provide

d that increased arginineots suppressed Thielaviopsissm previously suggested bysck (13). Morandi et al. (58)trations of phytoalexin-likein VAM vs. nonVAM soybeans' postulated that such materials;ased resistance to funga! and., compared to nonVAM plants.Morris and Ward (59) reported

ogen zoospores by isoflavonoidsd appear that such compounds,nds, could nave differentJence and/or severity. Justíese processes remains unknown,

¡tresses influence the incidencelant diseases and cause somencrease plant tolerance tomechanisms. In this context,

ogically reduce plant diseasesity to reduce effects ofjrs such as nutritional stress¡oil drought, and soil

ir volume of soil explored byH fungí compared to nonVAM1e»ents that are relativelyare bound to soil particlesabsorbed by VAM fungal hyphaeoot frow beyond the zone ofthe root. VAM are able to»ly «obile nutrients liketere deficiency levéis would:rient stress. Nutrientit, «aking it moreigress, or more sensitive toes such as cold or heat.1y to the general health ofnutrient stress and

osing effects.

LINDERMAN 9

Drought stress is another abiotic factor that:-edisposes plants to attack by some opportunisticpathogens. Extraradical hyphae of VAM fungi mayiDsorb water under soil drought conditions (39), andfus help plants to tolérate drought. There is,-owever, controversy over whether direct absorption ofwater from soil is the mechanism whereby VAM helpplants tolérate drought, or whether the increased P-ptake by VAM is responsible (60). Others suggest:hat VAM change the physiology of plants in ways thatmake them more drought tolerant than nonVAM plants(4,5,26,27).

VAM plants are less sensitive than nonVAM plants> soil toxicities resulting from excess salts (40,

I or mineral elements such as heavy metáis (16),"ere is controversy about the mechanisms involved,

•Tth some work implicating improved P nutrition in(66), but little evidence exists as toof heavy metal tolerance. In boththe toxic materials are selectivelysomehow altered to prevent toxic

salt tolerance:ne mechanismscases, however,excluded or areFfects on plant growth. As with other stresses, VAM

:"ants are more tolerant to soil toxicities and thus•aintain a higher level of growth and health than•onVAM plants, and thus may be less susceptible to:iseases.

Ricrobial Changes in the MycorrhizosphereWhile any of the above mechanisms, or

combinations thereof, could be involved in VAMsuppression of root diseases, one that should beconsidered more carefully is the VAM alteration ofrhizosphere populations of antagonists. Even thoughthe evidence is clear that microbial shifts do occurin the mycorrhizosphere (57,74), most studies have notconsidered those changes relative to biologicalcontrol of diseases, so relatively little data areavailable to support such a mechanism.

The concept of the "mycorrhizosphere" impliesthat mycorrhizae significantly influence the•icroflora of the rhizosphere by altering rootphysiology and exudation. In addition, extraradicalhyphae of VAM fungi provide a physical or nutritional

10 CHAPTER ONE

substrate for bacteria. Analysis of rhizosphere soilof VAM and nonVAM plants in several studies(2,9,57,74,82) indicated both qualitative andquantitative changes in the mycorrhizosphere soil ofVAM plants, compared to rhizosphere soil of nonVAMplants. These microbial shifts were clearly time-dependent and dynamic, changing as the plantsdeveloped. Meyer and Linderman (57) used selectivemedia to demónstrate differences in populations oftaxonomic and functional groups of bacteria in therhizosphere and rhizoplane of VAM and nonVAM plants.Similarly, populations of bacteria and actinomycetesin pot cultures of different VAM fungí werequantitatively and qualitatively analyzed by Seciliaand Bagyaraj (74). They showed that total populationsof bacteria in the mycorrhizosphere soil of VAM plantswere greater than in the rhizosphere soil of nonVAMplants. Effects of VAM on other microbial groups,including nitrogen fixing bacteria, actinomycetes, andmorphological and physiological groups of bacteria(Gram positive and negative bacteria, spore formers,urea hydrolyzers, and starch hydrolyzers) varied witheach VAM fungal species. Furthermore, ureahydrolyzers were present in pot-culture solí of allthe VAM plants, but were absent in soil from thenonVAM plants. Vancura et al. (82) documented theselective effects of VAM fungal extraradical hyphae onbacteria from within the mycorrhizosphere. They didnot, however, evalúate the antagonistic potential ofthe microbes associated with the hyphae. Thesestudies demónstrate that VAM influence the microbialpopulations in the mycorrhizosphere soil; many ofthose microbial shifts could influence the growth andhealth of plants.

VAM fungal symbionts produce extraradical hyphaethat may extend several centimeters out into the soiland exude organic materials that are substrates forother soil microbes. These hypha-associated microbesfrequently produce sticky materials that cause soilparticles to adhere, creating small aggregates thatimpart structure to soil, allowing for improvedaeration, water percolation, and stability (81).Forster and Nicolson (35) analyzed the microbial

co^osition of such aggregate•f fungí, bacteria, actinomyccyanobacteria. These microbifvigí may profoundly affectryphae in soil, and their met

>rbed by the hyphae and trbe specific functional compc

- :i-es, and the metabolúAerein, are virtually unknov

VAH formation alters thepopulations of soil microorg;rtagonize root pathogens.

I zoospore production by titytophthora cinnamomi Rand.isence of rhizosphere lead

•trie- compared to leachates frilarly, more actinomycete

tagal and bacterial pathogeculture plants than from:-€ :onditions (74); nú

waried among pot cultures ofspecies.

Other studies have indics^pression by VAM involved

^nizosphere microbial p- •-_- al. (19,20,21,22) i

f*s*riua populations in the•atoes and a correspondínc

•ot in VAM plants reí a1¡ibly due to increased ai

«Mrrhizosphere. Their stiÁíced disease incidence w<

nutrítion, but dependeLh substrate. Anotherindicated protection

jomi root rot when píaa «ixture of VAM pot c

__jrs concluded that a miFffective than single fungí*n« been due to buildup of

:_'=s. as demonstrated t'-

[hese results indícate

AnalysTs of rhizosphere soilin several studiesboth qualitative andne mycorrhizosphere soil ofzosphere soil Of nonVAM"ts were clearly time-

anging as the plantsrman {57} used selective?nces in populations ofoups of bacteria in the

VAM and nonVAM plants.

LINDERMAN 11

íly analyzed by Seciliathat total populations•ere soil of VAM plants

)sphere soil of nonVAMier microbial groups

ia, actinomycetes, andI groups of bacteria:teria, spore formers

>lyzers) varied withner^ore, urea

"Iture soil of allsoil from thedocumented the

:raradical hyphae on>sphere. They didtic potential of

hyphae. Theseluence the microbial•ere soil; many of

ice the growth and

¡xtraradical hyphaei out into the soil

are substrates forha-associated microbes

• that cause soilI aggregates that

n9 for improvedstability (81).

zed the microbial*

composition of such aggregates, and identified a rangeof fungi, bacteria, actinomycetes and algae, includingcyanobacteria. These microbial associates of VAMfungi may profoundly affect the further development ofhyphae in soil, and their metabolic products could beabsorbed by the hyphae and translocated to the host.fhe specific functional composition of theseaggregates, and the metabolic products produced~"e-'ein, are virtually unknown.

VAM formation alters the selective pressure onzopulations of soil microorganisms, some of which canantagonize root pathogens. For example, sporangium¿"'d zoospore production by the root pathogen-"ytophthora cinnamomi Rand. was reduced in the;resence of rhizosphere leachates from VAM plants,wtíen compared to leachates from nonVAM plants (57).similarly, more actinomycetes antagonistic to selectedfungal and bacterial pathogens were isolated from VAMpot culture plants than from nonVAM plants grown under:he same conditions (74); numbers of antagonists.aried among pot cultures of different VAM fungalspecies.

Other studies have indicated that diseasesjppression by VAM involved changes inn/corrhizosphere microbial populations. The work ofCarón et al. (19,20,21,22) indicated a reduction inFusarium populations in the mycorrhizosphere soil of::-atoes and a corresponding reduction inroot rot in VAM plants relative to nonVAM plants,possibly due to increased antagonism in the VAMirycorrhizosphere. Their studies also showed thatreduced disease incidence was independent of the levelof P nutrition, but dependent on the nature of thegrowth substrate. Another study, by Bartschi et al.(14), indicated protection of host roots against P.:innamomi root rot when plants were pre-inoculatedwith a mixture of VAM pot culture inocula. Theauthors concluded that a mixture of VAM fungi was moreeffective than single fungi, but effects could alsohave been due to buildup of antagonists in the potcultures, as demonstrated by Secilia and Bagyaraj(74).

These results indicate that VAM fungi are

12 CHAPTER ONE

relatively tolerant of antagonísts that inhibit fungalpathogens by one or more mechanisms. They furthersuggest that VAM fungí, which evolved with plants, arehighly rhizosphere-competent and are compatible withsuch antagonists and even function in concert withthem (51). The possibility that antagonisticrhizosphere bacteria or fungí might inhibitmycorrhizal fungí and thereby reduce theireffectiveness was tested by Krishna et al. (48), whoobserved that the pathogen antagonist Streptomycescinnamomeous reduced sporulation and colonization ofG. fasciculatum (Thaxter) Gerd. & Trappe emend. Walker& Koske on finger millet (Pam'cum 1.) if it was addedtwo weeks before the VAM fungus. In spite of thatresponse, however, the combination of the twoorganisms resulted in greater plant dry weights thanif either was used alone.

In extensive triáis evaluating interactionsbetween VAM fungi and many fungal or bacterialantagonists, Linderman et al. (54) found little or noadverse effects of bacterial and fungal biocontrolagents on establishment and function of VAM on onion(Allium cepa !_.}• Other studies (63,64) showed thelack of adverse effects or even stimulation of VAMfungi (17) by biocontrol agents, whether applied asseed treatments or added to the soil. Earlier, Meyerand Linderman (56) had shown a positive interactionbetween the antagonist and plant growth-promotingrhizobacterium Pseudomonas putida (Migula) and VAM onsubclover (Tn'folium subterraneum L.). Suchinteractions must also occur to varying degrees in therhizospheres of plants grown in pathogen-infestedsoil, although such evaluations are rarely conducted.

Changes in mycorrhizosphere populations ofantagonists to pathogens seems a likely explanationfor many of the reported effects of VAM on diseases.Yet, with the exception of those reports mentionedabove, few workers have considered that mechanism.Selective increases in numbers of antagonists in themycorrhizosphere are possible only if the antagonistsare present in the background soil or growth médium.Thus, if potentially effective antagonists are presentand are increased by VAM, then disease suppression

coald be expected, On the oth-•-.::'-;:s were not present i

cffect of VAM might result. P:.se (32,72) would indic

iar. i ras e, decrease, or have ncSack responses could indícate«•rrespond to VAM increases ir

; ' ivons of antagonists orfrat could enhance disease (81

ther complicated by the dirains or species of VAM fumPferent host genotypes, has

rer, such complex interac~isistencies between studi-ungi, and soils from var

FACTORS INFLUENCING MANAGEMI

-••: ¿id Extent of VAM Forrriftien VAM are reported to

my generally must be establ-e invasión by the pathocffstrated by Stewart and tRhizoctonia root rot of [;-err/?7'ma Willd. ex Klotz:

[14) on Phytophthora root ro'>»aecypar/s lawsoniana (A

fxiahl (68) with Aphanomyisatírua L.). That this woul'jc-cal considering both the

: fungal root pathogens,- - - -r needed for VAM effe

i occur. Furthermore, othe3Ut established root infectcaí reduce colonization by Vllential for positive effecwerity (1,6,68,84,85). Ser- :;ens and VAM fungi occiwts without apparent effec

32?73).If early VAM formation •

iscase suppression, then wlt cxie has demonstrated din

L1NDERMAN 13

antagonists that inhibít funga!'-e mechanisms. They further, which evolved with plants, are)etent and are compatible with'en function in concert withlity that antagonisticfungí might inhibit

hereby reduce theird by Krishna et al. (48), whogen antagonist Streptomycesorulation and colonization ofr) Gerd. & Trappe emend. Walkert (Panicum L.) if it was added1 fungus. In spite of that:ombination of the two•eater plant dry weights than.

evaluating interactionsny fungal or bacterialt al. (54) found little or norial and fungal biocontroland function of VAM on onionstudles (63,64) showed their even stímulation of VAMagents, whether applied asto the soil. Earlier, MeyerIOMI a positive interaction.d plant growth-promotings putida (Higula) and VAM onemneum L.). Such

to varying degrees in theDMI in pathogen-infested¡tions are rarely conducted.sphere populations ofi&esis a likely explanationfffects of VAM on diseases.: those reports mentioned«sidered that mechanism.bers of antagonists in the>le only if the antagonistsimd soil or growth médium.;ive antagonists are present:hen disease suppression

;jld be expected. On the other hand, if potentialirtagonists were not present in the soil, then noeffect of VAM might result. Reviews on effects of VAM

• disease (32,72) would indicate that VAM canincrease, decrease, or have no effect on disease.Such responses could indicate that effects on diseasecorrespond to VAM increases in mycorrhizospherepopulations of antagonists or deleterious microbesAat could enhance disease (80). This hypothesis,*-jrther complicated by the differential effects of:rains or species of VAM fungí associating with

;-fferent host genotypes, has not been tested.•onever, such complex interactions could explain theiconsistencies between studies using different hosts,

MM fungi, and soils from various parts of the world.

FACTORS INFLUENCING MANAGEMENT OF VAM IN BIOCONTROL

Tining and Extent of VAM FormationWhen VAM are reported to suppress root disease,

:rey generally must be established and functioningr-e-ore invasión by the pathogen. This has been:evonstrated by Stewart and Pfleger (77) on Pythiumand Rhizoctonia root rot of poinsettia (Euphorbiaz^lcherrhima Willd. ex Klotzsch), by Bartschi et al.14) on Phytophthora root rot of Lawson cypressChamaecyparis lawsoniana (A. Murr.JParl.)> and by

23sendahl (68) with Aphanomyces root rot of pea (Pisumsativum L.). That this would be the case seems";gical considering both the faster infection rate of•ost fungal root pathogens, compared to VAM fungi, andthe time needed for VAM effects on the host physiologyto occur. Furthermore, other reports have indicated:hat established root infections by various pathogenscan reduce colonization by VAM fungi and therefore the:atential for positive effects on disease incidence orseverity (1,6,68,84,85). Sometimes, however, rootzathogens and VAM fungi occupy adjacent tissues in'•oots without apparent effects on each other(21,32,73).

If early VAM formation is required for rootdisease suppression, then what processes are involved?No one has demonstrated direct interactions between

14 CHAPTER ONE

VAM fungí and pathogens, so indirect effects on hostmorphology and/or physiology or mycorrhizospheremicrobial shifts must be involved. However,physiological effects could be localized or systemic.Aphanomyces root rot of peas was only suppressed byVAM when the two organisms were present on the sameroots (68). A similar response occurred withPhytophthora root rot of citrus (Citrus sinensis L.)in a split root study by Davis and Menge (29), leadingthem to conclude that the effect was not systemic.However, Rosendahl (68) showed that oospore productionwas reduced on nonVAM pea roots split from VAM roots,compared to plants with no VAM on either root system.Similarly, Davis and Menge (29) showed that citrusroots opposite the split from VAM roots had lessPhytophthora root rot than if split from nonVAM roots.These two studies suggest that VAM effects could beboth localized and systemic, probably involving twosepárate mechanisms. The systemic effect could havebeen a P effect, while the localized effect was due tosome morphological or physiological change in the roottissues in the immediate vicinity.

It is itnportant to consider the time or frequencyof observations within a disease cycle in evaluatingeffects of VAM on diseases. Most studies haveevaluated the interaction only once, usually at theend of the experiment. Carón et al. (21) demonstratedthat the interaction of VAM and Fusarium root andcrown rot of tomato was constant throughout a 12-weekexperiment, but the percent root necrosis was onlysignificantly reduced at 3 of the 12 observations.Had measurements been made at other than those times,reported effects would have been different.

Inoculum Level of the PathogenThe potential for biological control to occur in

any production system is directly related to theinoculum potential of the pathogen. A high pathogeninoculum density can overwhelm biocontrol agents (11,23), and this has been shown in VAM studies as well(47,71). It is difficult to draw conclusions aboutthe potential for biocontrol to occur unless a rangeof pathogen inoculum densities is used.

teriation in VAM Fungí, Host iax Nicrobial Composition of :

It is biologically fundamFferent interactions to occ: "ost plants, and plant

fe» studies have compared a r: (43), and none has don

•la«t diseases. Some studiesgenotypes for VAM formatstudies have not include

- - - =:vons. Add to that ce•eraction the variation inTobial composition, and i1

retations and comparisíies are difficult if not

ertheless, it is conceivalon of factors does ifor exploiting VAM

cav be found.

IB Management Strategies: VAM contribute to dis

•tari tur al practices that=nd associated antagon

- . -: :isease incidence. -_ •- :~i need for and us

•ve that compatible combi.: . -: occur in the sa-, could inocúlate see(itee early establishmei

_., invasión (51,53).Ived and economic margiitices to favor effectiV'. . . •: •-ate. In those

: antagonists coulailtural crops, managelition of the rhizosph

cowbinations of VAM._ and inoculated as:íon cycle at a timeroot system is guaracan benefit from bot:**¡9 against invasior

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16 CHAPTER ONE

CONCLUSIONS

With few exceptions, crop plants have VAM, butthe degree of root colonizatlon by VAM fungí and theeffects of the symbiosis may vary, depending on thetotal interaction between host, symbiont, andenvironment. In most cases, VAM significantly changethe physiology and chemical constituents of the host,the pattern of root exudation, and the microbialcomposition of mycorrhizosphere soil. These changescan greatly influence the growth and health of plants,in part due to the biological suppression of plantdiseases. Disease suppression may be the result ofreduction of environmental stresses that may limitplant growth and predispose the plants to infection byopportunistic pathogens. More important, however, arethe specific morphological and physiological changesthat directly or indirectly result in reducedíncidence and/or severity of plantplants compared to nonVAM plants.differed in design, the VAM fungalpathogen types and inoculum levéis,growth system used. This variation

diseases in VAMExperiments havesymbiont used,and the plantprevents easy

conclusions about the predictability of VAM effects onplant diseases. Where disease reduction is reported,one or more mechanisms can be involved, although thetendency is to implicate only one. Because VAMeffects on plant nutrition, especially P uptake, areoften so striking, many reports implicate improved Pnutrition as a mechanism of disease control. Enoughreports on VAM suppression of disease where P effectswere excluded are now available to suggest theinvolvement of other mechanisms. Generally, moststudies have not investigated other mechanisms such asmorphological changes, changes in disease-suppressingchemical constituents in plant tissues, and changes inrhizosphere populations of antagonistic microbesinduced by VAM formation. The mechanisms involvedprobably are múltiple, and will depend on theconditions of the test. The major effect of VAM maybe improved nutrition, but secondary effects inducedthereafter may contribute significantly to observedeffects on disease. Mycorrhizosphere changes in

ilations of antagonists to son having those antagoni

, . :^ound soil. If antagonistételeterious microbes are presentutf>ers and enhanced by VAM, thseverity can be increased. In:.;:jlations to result in biolocAseases, compatible VAM fungíirtagonists should be deliverecsjstem to guarantee their domirmartagement strategy could resul:'trol of diseases and improvt

LITERATURE (

Afek, U., and Menge, J. A.Pythium ultimum and metala;length and mycorrhizal colionion, and pepper. Plant IA»es, R. N., Reid, C. P. P1984. Rhizosphere bacterito root colonization by auycorrhizal fungus. New PAtilano, R. A., Menge, J.D. 1981. Interaction betweand Glomus fasciculatus in13: 52-57.ijge, R. M., Schekel, K. A1986. Osmotic adjustment i

--rhizal and nonmycorrhresponse to drought stress82:765-770.i-ge, R. M., Schekel, K. P1986. Greater leaf conduct

:orrhizal rose plants ispbosphorus nutrition. NevBaath, E., and Hayman, D.responses to vesicular-art;. Interactions with toeato plants. New Phyto"taath, E., and Hayman, D.

- - ::rrhiza on red core'-ans. Br. Mycol. Soc. 82

L1NDERMAN 17

3NCLUSIONS

, crop plants have VAM, butnization by VAM fungí and thes may vary, depending on theen host, symbiont, andases, VAM significantly changeical constituents of the host,Catión, and the microbialíosphere soil. These changesle growth and health of plants,)gical suppression of plant-ession may be the result of;al stresses that may limittose the plants to infection by

More important, however, are:al and physiological changestly result in reducedy of plant diseases in VAMM plants. Experiments haveVAM funga! symbiont used,lum levéis, and the plants variation prevents easyedictabilíty of VAM effects onisease reduction is reported,an be involved, although theonly one. Because VAM3n, especially P uptake, aresports implicate improved Pof disease control. Enough)n of disease where P effectsnlable to suggest thelanisms. Generally, mostlated other mechanisms such as<anges in disease-suppressingplant tissues, and changes inif antagonistic microbes

The mechanisms involvedd will depend on theThe major effect of VAM mayt secondary effects inducedsignificantly to observed

rrhizosphere changes in

zrsulations of antagonists to specific pathogens:epend on having those antagonists present in therackground soil. If antagonists are absent andaeleterious microbes are present in significant--Tibers and enhanced by VAM, then disease incidence orseverity can be increased. In managing rhizospherercpulations to result in biológica! control of plantaseases, compatible VAM fungí and effective=~tagonists should be delivered to the productionsestero to guarantee their dominance. Such aTT=nagement strategy could result in stable biological::ntrol of diseases and improve overall plant health.

LITERATURE CITED

Afek, U., and Menge, J. A. 1990. Effect ofPythium ultimum and metalaxyl treatments on rootlength and mycorrhizal colonization of cotton,onion, and pepper. Plant Dis. 74:117-120.Ames, R. N., Reíd, C. P. P., and Ingham, E. R.1984. Rhizosphere bacterial population responsesto root colonization by a vesicular-arbuscularmycorrhizal fungus. New Phytol. 96: 555-563.Atilano, R. A., Menge, J. A., and Van Gundy, S.D. 1981. Interaction between Meloidogyne arenariaand Glomus fasciculatus in grape. J. Nematol.13: 52-57.Auge, R. M., Schekel, K. A., and wample, R. L.1986. Osmotic adjustment in leaves of VAmycorrhizal and nonmycorrhizal rose plants inresponse to drought stress. Plant Physiol.82:765-770.

5. Auge, R. M., Schekel, K. A., and Wample, R. L..1986. Greater leaf conductance of well-watered VAmycorrhizal rose plants is not related tophosphorus nutrition. New Phytol. 103:107-116.

6. Baath, E., and Hayman, D. S. 1983. Plant growthresponses to vesicular-arbuscular mycorrhiza.XIV. Interactions with Verticillium wilt ontomato plants. New Phytol. 95: 419-426.

T. Baath, E., and Hayman, D. S. 1984. No effect ofVA mycorrhiza on red core disease of strawberry.Trans. Br. Mycol. Soc. 82: 534-536.

18 CHAPTER ONE

8. Bagyaraj, D., J. 1984. Biológica! interactionswith VA mycorrhizal fungi. Pages 131-153 in: VAMycorrhiza, C.L.Powell and D.J. Bagyaraj, eds,,CRC Press, Inc. Boca Ratón, FL. 234 pp.

9. Bagyaraj, D. J., and Menge, J. A. 1978.Interactions between a VA mycorrhiza andAzotobacter and their effects on rhizospheremicroflora and plant growth. New Phytol. 80:567-573.

10. Baker, K. F. 1987. Evolving concepts ofbiological control of plant pathogens. Annu. Rev.Phytopathol. 25:67-85.

11. Baker, K. F., and Cook, R. J. 1974. Biologicalcontrol of plant pathogens. W. H. Freeman, SanFrancisco, CA.

12. Baker, R. 1986. Biological control: an overview.Can. J. Plant Pathol. 8:218-221.

13. Baltruschat, H., and Schoenbeck, F. 1975. Studieson the influence of endotrophic mycorrhiza on theinfection of tobáceo by Thielaviopsis basicola.Phytopath. Z. 84:172-188.

14. Bartschi, H., Gianinazzi-Pearson, V., and Vegh,I. 1981. Vesicular-arbuscular mycorrhizaformation and root rot disease (Phytophthoracinnamomi) development in Chamaecyparislawsoniana. Phytopath. Z. 102: 213-218.

15. Becker, W. N. 1976. Quantification of onionvesicular-arbuscular mycorrhizae and theirresistance to Pyrenochaeta terrestris. Ph.D.Diss., University of Illinois, Urbana. (Diss.Abstr. 76:24041)

16. Bethlenfalvay, G. J. 1992. Mycorrhizae and CropProductivity. Pages 1-27 in: Mycorrhizae inSustainable Agriculture, G. J. Bethlenfalvay andR. G. Linderman, eds., ASA Spec. Publ. No. 54.,Amer. Soc. Agronomy Press, Madison, WI.

17. Calvet, C., Pera, J., and Barea, J. M. 1989.Interactions of Tnchoderma spp. with Glomusmosseae and two wilt pathogenic fungi. Agrie.,Ecosystems Environ. 29:59-65.

18. Carón, M. 1989. Potential use of mycorrhizaecontrol of soilborne diseases. Can. J. PlantPathol. 11:177-179.

.

Carón, M., Fortín, J, A., aInfluence of substrate on tGlomus intraradices and Fusradicis-lycopersici on toma233-239.

'. i-on, M. , Fortin, J, A. , ciffect of phosphorus concerintraradices on Fusarium crtonatoes. Phytopathol ogy iCarón, M., Fortin, J. A., ;Effect of Glomus intraradii:*sarium oxysporum f. sp. )tyiatoes over a 12-week peíÍEI-556.Carón, M., Richard, C., an<Effect of preinfestation ovesicular-arbuscular mycorintraradices, on Fusarium >toiíatoes, Phytoprotectionlook, R. J., and Baker, K.and practice of biologicalzathogens, APS Press, St.looper, K. M., and GrandisInteraction of vesicular-afungi and root-knot nematotcmato and white clover su*eloidogyne hapla. Ann. A

in

:3oper, K. M., and Grandisof vesicular-arbuscular m>ifection of tamarillo (C>

*eloidogyne incógnita in f:is. 71: 1101-1106.Gavies, F. T., Or., Potter: 5. 1992. Mycorrhiza ancexposure affect drought reextraradical hyphae devele-ndependent of plant sizeJ. Plant Physiol. 139:289-Davies, F. T., Jr., Pottei. G. 1993. Drought resisl

pepper plants independent- response in gas exchangí

LINDERMAN 19

Biológica! interactionsI fungí. Pages 131-153 1 n- VA

!ca L V ' Ba9yaraj> e¿s'ca Ratón, FL. 234 pp.Menge, J. A. 1978.

en a VA mycorrhiza andf effects on rhizosphere

- growth. New Phytol . 80:

•volving concepts ofF Plant pathogens. Annu. Rev•ao .

• R- J- 1974. Biologicallogens. W. H. Freeman, San

^nbeck, F. 1975. Studiesiic mycorrhiza on the

rtavJopsis basicola.

«n, V . , and Vegh,cular mycorrhiza

»se (Phytophthora~hatnaecyparis102: 213-218.¡catión of onionlizae and theirterrestris. Ph Ds, Urbana. (Diss!

Hycorrhizae and CropMycorrhizae in• Bethlenfalvay and

Spec. Publ. No. 54Madison, WI.

Barea, J. M. 1989spp. with Glomuslie fungi. Agrie..

-*9-65.use of mycorrhizae in

«ses. Can. J. Piant

9. Carón, M., Fortin, J. A., and Richard, C. 1985.Influence of substrate on the interaction ofGlomus intraradices and Fusarium oxysporum f. sp.radicis-lycopersici on tomatoes. Plant Soil 87:233-239.

::. Carón, M., Fortin, J. A., and Richard, C. 1986.Effect of phosphorus concentration and Glomusintraradices on Fusarium crown and root rot oftomatoes. Phytopathology 76: 942-946.

•. Carón, M., Fortin, J. A., and Richard, C. 1986.Effect of Glomus intraradices on infection byFusarium oxysporum f. sp. radicis-lycopersici intomatoes over a 12-week period. Can. J. Bot. 64:552-556.

:¿. Carón, M., Richard, C., and Fortin, J. A. 1986.Effect of preinfestation of the soil by avesicular-arbuscular mycorrhizal fungus, Glomusintraradices, on Fusarium crown and root rot oftomatoes. Phytoprotection 67: 15-19.

23. Cook, R. J., and Baker, K. F. 1983. The natureand practice of biológica! control of plantpathogens, APS Press, St. Paul, MN.

24. Cooper, K. M., and Grandison, G. S. 1986.Interaction of vesicular-arbuscular mycorrhizalfungi and root-knot nematode on cultivars oftomato and white clover susceptible toMeloidogyne hapla. Ann. Appl. Biol. 108: 555-565.

25. Cooper, K. M., and Grandison, G. S. 1987. Effectsof vesicular-arbuscular mycorrhiza] fungi oninfection of tamarillo (Cyphomandra betacea) byMeloidogyne incógnita in fumigated soil. PlantDis. 71: 1101-1106.

26. Davies, F. T., Jr., Potter, J. R., and Linderman,R. G. 1992. Mycorrhiza and repeated droughtexposure affect drought resistance andextraradical hyphae development of pepper plantsindependent of plant size and nutrient content.J. Plant Physiol. 139:289-294.

27. Davies, F. T., Jr., Potter, J. R., and Linderman,R. G. 1993. Drought resistance of mycorrhizalpepper plants independent of leaf P concentration- response in gas exchange and water relations.

20 CHAPTER ONE

Physiol, Plant. 87:45-53.28. Davis, R. M. 1980. Influence of Glomus

fasciculatus on Thielaviopsis basicola root rotof citrus. Plant Oís. 64: 839-840.

29. Davis, R. M., and Menge, J. A. 1980. Influence ofGlomus fasciculatus and soil phosphorus onPhytophthora root rot of citrus. Phytopathology70: 447-452.

30. Davis, R. M., and Menge, J. A. 1981. Phytophthoraparasítica inoculation and intensity ofvesicular-arbuscular mycorrhizae in citrus. NewPhytol. 87: 705-715.

31. Davis, R. M., Menge, J. A., and Erwin, D. C.1979. Influence of Glomus fasciculatus and soilphosphorus on Verticillium wilt of cotton.Phytopathology 69: 453-456.

32. Dehne, H. W. 1982. Interactions betweenvesicular-arbuscular mycorrhizal fungí and plantpathogens. Phytopathology 72: 1115-1119.

33. Dehne, H. W., and Schonbeck, F. 1979.Untersuchungen zum Einfluss der endotrophenMykorrhiza auf Pflanzenkrankheiten. II.Phenolstoffwechsel und Lignifizierung. (Theinfluence of endotrophic mycorrhiza on plantdiseases. II. Phenolmetabolism andlignification.) Phytopath. Z. 95: 210-216.

34. Dehne, H. W., Schonbeck, F., and Baltruschat, H.1978. Untersuchungen zum Einfluss der endotrophenMycorrhiza auf Pflanzenkrankheiten. 3.Chitinase-aktivitat und Ornithinzyklus. (Theinfluence of endotrophic mycorrhiza on plantdiseases. 3. Chitinase-activity and ornithine-cycle). Z. Pflkrankh. 85: 666-678.

35. Forster, S. M., and Nicolson, T. H. 1981.Aggregation of sand from a maritime embryo sanddune by microorganisms and higher plants. SoilBiol. Biochem. 13:199-203.

36. García-Garrido, J. M., and Ocampo, J. A. 1989.Effect of VA mycorrhizal infection of tomato ondamage caused by Pseudomonas syringae. Soil Biol.Biochem. 21:165-167.

37. Graham, J. H., and Egel, D. S. 1988. Phytophthoraroot rot development on mycorrhizal and

phosphorus-fertilized nonmyT T : " - n g s . Plant Dis . 7 2 :

iraham, J, H., and Menge, Jof vesicular-arbuscular mycpfcosphorus on take-all dise

- :::athology 72: 95-98.Hardie, K. 1985. The effectextraradical hyphae on watearbuscular mycorrhiza] piar101:677-684.lirrel, M. C., and GerdemarI^jroved growth of onion arsaline soils by two vesicul•fcorrhizal fungi. Soil Sd:::t^issey, R. S., and Roncadoi[nteraction of Pratylenchu;tigaspora margarita on cot'18-20.**issey, R. S., and Roncado1

fesicular-arbuscular mycor•eaatode activity and imppHs. 66:9-14.lanson, D. C., and Lindermfariation in VA mycorrhiza

~.n Rhizobium on pigeon pílie Rhizosphere and Plant-: D. B. Cregan, eds., Kl

^ublishers, Dordrecht, TheIngham, R. E. 1988. Inte•matodes and VA mycorrhizEnviron. 24:169-182.Jabaji-Hare, S. H., and StElectron microscopic examicoinfected with Glomus sp.

¡rus. Phytopathology 74:2Jalali, B. L., andJalal i ,plant disease control. Pac

: applied mycology. SoilArora, B. Rai, K. G. Mi

Rnudsen, eds., Marcel Dek^lye, J. W., Pfleger, F. í984. Interaction of Glomí

7:45-53.Influence of GJomus

toelavj'opsis basicoJa root rotOís. 64: 839-840ifSS' J:/\- Influence of

and soil phosphorus onF citrus. Phytopathology

Menge, J A. 1981. Phytophthoraition and intensity ofar mycorrhizae in citrus. New3 *

e, J. A., and Erwin, D. C./offlí/s fasciculatus and soil

Hura wilt of cotton.453-456.

Interactions betweenmycorrhizal fungi and plant

ithology 72: 1115-1119:honbeck, F. 1979,ünfluss der endotrophenenkrankheiten. II.

Lignifizierung. (Themycorrhiza on plant

tabolism and95: 210-216.

. and Baltruschat, Hinfluss der endotrophen

írankheiten. 3.Ornithinzyklus. (Themycorrhiza on plant

-activity and ornithine-85: 666-678.'son, T. H. 1981.

' maritime embryo sandligher plants. Soil

and Ocampo, J. A. 1989infection of tomato onwas synngae. Soil Biol.

• D. S. 1988. Phytophthoraon mycorrhizal and

LINDERMAN 21

r

phosphorus-fertilized nonmycorrhizal sweet orangeseedlings. Plant Dis. 72: 611-614.Graham, J. H., and Menge, J. A. 1982. Influenceof vesicular-arbuscular mycorrhizae and soilphosphorus on take-all disease of wheat.Phytopathology 72: 95-98.Hardie, K. 1985. The effect of removal ofextraradical hyphae on water uptake by vesicular-arbuscular mycorrhizal plants. New Phytol.101:677-684.Hirrel, M. C., and Gerdemann, J. W. 1980.Improved growth of onion and bell pepper insaline soils by two vesicular-arbuscularmycorrhizal fungi. Soil Sci. Soc. Am. J. 44:654-655.Hussey, R. S., and Roncadori, R. W. 1978.Interaction of Pratylenchus brachyurus andSigaspora margarita on cotton. J. Nematol. 10:18-20.Hussey, R. S., and Roncadori, R. W. 1982.Vesicular-arbuscular mycorrhizae may limitnematode activity and improve plant growth. PlantDis. 66:9-14.lanson, D. C., and Linderman, R. G. 1991.Variation in VA mycorrhizal strain interactionswith Rhizobium on pigeon pea. Pages 371-372 in:The Rhizosphere and Plant Growth, D. L. Keisterand P. B. Cregan, eds., Kluwer AcademicPublishers, Dordrecht, The Netherlands.Ingharn, R. E. 1988. Interactions betweeennematodes and VA mycorrhizae. Agrie., EcosystemsEnviron. 24:169-182.Jabaji-Hare, S. H., and Stobbs, L. W. 1984.Electron microscopic examination of tomato rootcoinfected with Glomus sp. and tobáceo mosaicvirus. Phytopathology 74:277-279.Jalali, B. L., and Jalali, I. 1991. Mycorrhiza inplant disease control. Pages 131-154 in: Handbookof applied mycology. Soil and Plants. Vol. 1, D.K. Arora, B. Raí, K. G. Mukerji, and G. R.Knudsen, eds., Maree! Dekker, New York, NY.Kaye, J. W., Pfleger, F. L., and Stewart, E. L.1984. Interaction of Glomus fasciculatum and

22

48

49

50

51

52

53

54

55

56

CHAPTER ONE

Pythium ultimum on greenhouse grown poinsettia.Can. J. Bot. 62:1575-1579.Krishna, K. R., Balakrishna, A. N., and BagyarajD. J. 1982. Interactions between a vesicular-arbuscular mycorrhizal fungus and Streptomycescinnamomeous and their effects on finger millet.New Phytol. 92Krishna, K. R.Andrews, 0. J.in mycorrhizalinoculation of125.Linderman, R. G. 1986microorganisms in thecrops. HortScience 21Linderman, R. G. 1988

401-405.Shetty, K. G., Dart, P. J., and1985. Genotype dependen! variationcolonization and response topearl millet. Plant Soil 86:113-

¿seuodmonas putida. Soil I190.Heyer, J. R., and LindermaiSelective influence on popíor rhizoplane bacteria and

•"rhizas formed by GlomJiol. Biochem. 18: 191-196Morandi, D., Bailey, J. A.Pearson, V. 1984. Isoflavosoybean roots infected witirvcorrhizal fungi. Physiol

Managing rhizosphereproduction of horticultural1299-1302.Mycorrhizal interactions

with the rhizosphere microflora: Themycorrhizosphere effect. Phytopathology 78:366-371.Linderman, R. G. 1988. VA (Vesicular-Arbuscular)mycorrhizal symbiosis. ISI Atlas of Science,Animal and Plant Sciences Section 1:183-188.Linderman, R. G. 1991. Mycorrhizal interactionsin the rhizosphere. Pages 343-348 in: TheRhizosphere and Plant Growth, D. L. Keister andP. B. Cregan, eds., Kluwer Academic Publishers,Dordrecht, The Netherlands.Linderman, R. G., Paulitz, T. C., Mosier, N. J.,Griffiths, R. P., Loper, J. E., Caldwell, B. A.,and Henkeís, M. E. 1991. Evaluation of theeffects of biocontrol agents on mycorrhizalfungi. Page 379 in: The Rhizosphere and PlantGrowth, D. L. Keister and P. B. Cregan, eds.,Kluwer Academic Publishers, Dordrecht, TheNetherlands.MacGuidwin, A. E., Bird, G. W., and Safir, G. R.1985. Influence of Glomus fasciculatum onMeloidogyne hapla infecting Allium cepa. J.Nematol. 17: 389-395.Meyer, J. R., and Linderman, R. G. 1986.Response of subterranean clover to dualinoculation with vesicular-arbuscular mycorrhizalfungi and a plant growth-promoting bacterium,

Morris, P. F., and Ward, E>emoattraction of zoosporpathogen, Phytophthora sojPnysiol. Mol. Plant Pathol•elson, C. E. 1987. The wa

;ular-arbuscular mycor"1 - 5 1 in: Ecophysiology of. R. Safir, ed., CRC Pres

liveira, A. A. R., and Z¡interacao entro o fungo er~:.-icatum e o nematoide (javanica em feijoeiro com::íopatol. Bras. 12: 222-¡Papavizas, G. C., ed., 191i crop production. AÍlanl

Totowa, NJ.Paulitz, T. C., and LindeInteractions between fluo¥A mycorrhizal fungi. Ne1Paulitz, T. C., and Linde: antagonism between the

Gliocladium virens and vewycorrhizal fungi. New Phrsnd, E. C., and Menge, Jgrowth of tomato in salínarbuscular mycorrhizal fusaline soils. Mycologia 7^tiss. J. A., Pond, E., MeV. M. 1985. Effect of salnon and tomato in soil

LINDERMAN 23

i greenhouse grown poinsettia.575-1579.ilakrishna, A. N., and Bagyaraj,ictions between a vesicular-n'zal fungus and Streptomyces,heir effects on finger millet.1-405.etty, K. G., Dart, P. J., and5. Genotype dependent variationonization and response torl millet. Plant Soil 86:113-

986. Managing rhizospherethe production of horticultural21:1299-1302.)88. Mycorrhizal interactions•e microflora: Therfect. Phytopathology 78:366-

88. VA (Vesicular-Arbuscular)is. ISI Atlas of Science,iences Section 1:183-188.91. Mycorrhizal interactionsPages 343-348 in: The

it Growth, D. L. Keister and, Kluwer Academic Publishers,;rlands.lulitz, T. C., Mosier, N. J.,iper, J. £., Caldwell, B. A.,991. Evaluation of the

agents on mycorrhizalThe Rhizosphere and Plant• and P, B. Cregan, eds.,ishers, Dordrecht, The

R.ird, G. W., and Safir, G.lomus fascicuJatum onFecting Allí uní cepa. J.

.- - •--". R. G. 1986.>ean clover to dualcular-arbuscular mycorrhizalwth-promoting bacteriurn,

Pseuodmonas putida. Soil Biol. Biochem. 18: 185-190.

. Heyer, J. R., and Linderman. R. G. 1986.Selective influence on populations of rhizosphereor rhizoplane bacteria and actinomycetes bymycorrhizas formed by Glomus fasciculatum. SoilBiol. Biochem. 18: 191-196.

. Morandi, D., Bailey, J. A., and Gianinazzi-Pearson, V. 1984. Isoflavonoid accumulation insoybean roots infected with vesicular-arbuscularmycorrhizal fungi. Physiol. Plant Pathol. 24:357-364.Morris, P. F., and ward, E. W. B. 1992.Chemoattraction of zoospores of the soybeanpathogen, Phytophthora sojae, by isoflavones.Physiol. Mol. Plant Pathol. 40:17-22.

. Nelson, C. E. 1987. The water relations ofvesicular-arbuscular mycorrhizal systems. Pages71-91 in: Ecophysiology of VA Mycorrhizal Plants.G. R. Safir, ed., CRC Press, Inc., Boca Ratón,FL.Oliveira, A. A. R., and Zambolim, L. 1987,Interacao entro o fungo endomicorrizico Glomusetunicatum e o nematoide de gal has Meloidogynejavam'ca em feijoeiro com raíz partida.Fitopatol. Bras. 12: 222-225.Papavizas, G. C., ed., 1981. Biological controlin crop production. Allanheld, Osmun Publishers,Totowa, NJ.

. Paulitz, T. C., and Linderman, R. G. 1989.Interactions between fluorescent pseudomonads andVA mycorrhizal fungi. New Phytol. 113:37-45.

- 3aulitz, T. C., and Linderman, R. G. 1991. Lackof antagonism between the biocontrol agentGliocladium virens and vesicular arbuscularmycorrhizal fungi. New Phytol. 117:303-308.Pond, E. C., and Menge, J. A. 1984. Improvedgrowth of tomato in salinized soil by vesicular-arbuscular mycorrhizal fungi collected fromsaline soils. Mycologia 76:74-84.Poss, J. A., Pond, E., Menge, J. A., and Jarrell,W. M. 1985. Effect of salinity on mycorrhizalonion and tomato in soil with and without

24 CHAPTER ONE

additional phosphate. Plant Soil 88:307-319.67. Rambelli, A. 1973. The rhizo.sphere of

mycorrhizae. Pages 299-343 in: Ectomycorrhizae.G. L. Marks and T. T. Kozlowski, eds., AcademicPress, New York, NY.

68. Rosendahl, S. 1985. Interactions between thevesicular-arbuscular mycorrhizal fungus Glomusfasciculatum and Aphanomyces euteiches root rotof peas. Phytopath. Z. 114: 31-40.

69. Saleh, H., and Sikora, R. A. 1984. Relationshipbetween Glomus fasciculatum root colonization ofcotton and Its effect on Meloidogyne incógnita.Nematologica 30: 230-237.

70. Schenck, N. C. 1983. Can mycorrhizae control rootdiseases? Plant Dis. 65:230-234.

71. Schenck, N. C. 1987. Vesicular-arbuscularmycorrhizal fungi and the control of fungal rootdiseases. Pages 179-191 in: Innovative Approachesto Plant Disease Control, I. Chet, ed., JohnWiley & Sons, Inc., New York, NY.

72. Schenck, N. C., and Kellam, M. K. 1978. Theinfluence of vesicular arbuscular mycorrhizae ondisease development. Fia. Agrie. Exp. Stn. Tech.JliOX ,7fl Jvúnpjv.i.i.lís .PJ.

73. Schonbeck, F. 1979. Endomycorrhiza in relation toplant diseases. Pages 271-280 in: Soil-borneplant pathogens. B. Schippers and W. Gams, eds.,Academic Press, New York, NY.

74. Secilia, J., and Bagyaraj, D. J. 1987. Bacteriaand actinomycetes associated with pot cultures ofvesicular-arbuscular mycorrhizas. Can. J.Microbiol. 33: 1069-1073.

75. Sitaramaiah, K., and Sikora, R. A. 1982. Effectof the mycorrhizal fungus Glomus fasciculatus onthe host-parasite relationship of Rotylenchulusreniformis in tomate. Nematologica 28: 412-419.

76. Smith, G. S. 1988. The role of phosphorusnutrition in interactions of vesicular-arbuscularmycorrhizal fungi with soilborne nematodes andfungi. Phytopathology 78:371-374.

77. Stewart, E. L., and Pfleger, F. L. 1977.Development of poinsettia as influenced byendomycorrhizae, fértilizer and root rot

Pythium ultimum at's Rev. 159:37, 79-8

i. E-, Hussey, R.Interactions of ve:sl fungi, Meloidogtilíty on peach. F

:. K., Bagyaraj, D.•5. Effect of vesiculc

;a on survival , per"icweflt of root-knot nt

, S«il 87:305-308.and Schroth

:«s rhizobacteria ¡CM9 crop growth. Phyti

, J. H. 1991. Funga. of soil . Aust. J, ?., Orozco, M. 0.Z. 1989. Properti

of a vesicularAgrie. , Ecosystems

. and Moore, L.and nonmycorrh

•Icri' chalí enged by JhJ. Plant Pathol. 6: 1

rtwlim, L. , and Schenck,the effects of pathoger

rwji on soybean by the miMUS mosseae. PhytopaUroolim, L., and Schenck,crophomina, Rhizoctonia.corrhizal fungus Glomus

non-nodulated soybean:lSileira 9: 129-138.

LINDERMAN 25

te. Plant Soil 88:307-319.The rhizo.sphere of299-343 in: Ectomycorrhizae.T. Kozlowski, eds., Academicr.Interactions between the

¡r mycorrhizal fungus Glomus¡hanomyces euteiches root roti. Z. 114: 31-40.Ta, R. A. 1984. Relationshipiculatum root colonization ofct on Meloidogyne incógnita.0-237.Can mycorrhizae control root

. 65:230-234.Vesicular-arbuscular

¡ the control of funga! root.91 in: Innovative Approaches

ntrol, I. Chet, ed., JohnNew York, NY,Kellam, M. K. 1978. Thelar arbuscular mycorrhizae on

:la. Agrie, Exp. Stn. Tech.He, FL.Endomycorrhiza in reíation to»s 271-280 in: Soil-borne

•ippers and W. Gams, eds.,York, NY.tyaraj, D. J. 1987. Bacteria

:1ated with pot cultures of• •ycorrhizas. Can. J.1073.¡Ikora, R. A. 1982. Effect•NJUS Glomus fasciculatus on"latlonship of Rotylenchulus

Me»atologica 28: 412-419.s role of phosphorus:ions of vesicular-arbuscular

i soilborne nematodes andf 78:371-374.Hleger, F. L. 1977.

;ia as influenced bytílizer and root rot

ofin

pathogens Pythium ultimum and Rhizoctonia solani.Torist's Rev. 159:37, 79-80.•trobel, N. E., Hussey, R. S., and Roncadori, R.M. 1982. Interactions of vesicular-arbuscularwycorrhizal fungí, Meloidogyne incógnita, andsoil fertility on peach. Phytopathology 72:690-:r-,Saresh, C. K., Bagyaraj, D. J., and Reddy, D. D.:. 1985. Effect of vesicular-arbuscularir/corrhiza on survival, penetration and:rvelopment of root-knot nematode in tomato.>lant Soil 87:305-308.Suslow, T. V., and Schroth, M. N. 1982. Role3eleterious rhizobacteria as minor pathogens-educing crop growth. Phytopathology 72:111-115."isdall, J. M. 1991. Fungal hyphae and structuralstability of soil. Aust. J. Soil Res. 29:729-743.Vancura, V., Orozco, M. 0., Grauova, 0., andPrikryl, Z. 1989. Properties of bacteria in the^yphosphere of a vesicular-arbuscular mycorrhizalfungus. Agrie., Ecosystems Environ. 29:421-427.Wick, R. L., and Moore, L. D. 1984. Histology of^ycorrhizal and nonmycorrhizal Ilex crenata'Mellen' challenged by Thielaviopsis basicola.Can. J. Plant Pathol. 6: 146-150.Zambolim, L., and Schenck, N. C. 1983. Reductionof the effects of pathogenic, root-infectingfungí on soybean by the mycorrhizal fungus,Glomus mosseae. Phytopathology 73: 1402-1405,Zambolim, L., and Schenck, N. C. 1984. Effect ofMacrophomina, Rhizoctonia, Fusarium and themycorrhizal fungus Glomus mosseae on nodulatedand non-nodulated soybeans. FitopatologíaBrasileira 9: 129-138.