Mycorrhizae AND PLANT HEALTH Edited by F. L. Pfleger and R. G. Lindennan

SYMPOSIUM SERIES ROLE OF VAM FUNGÍ IN BIOCONTROL Robert G. Linderman USDA-ARS Horticultural Crops Research Laboratory Corvallis, Oregon Most terrestrial plant species have in their roots a symbiotic association with soil fungí called . There are several categories of mycorrhizae, of which the largest group, vesicular- arbuscular mycorrhizae (VAM), form with most agricultural crops. VAM fungi exist in soil as thick- wal-led chlamydospores, or as vegetativa propagules in roots, that germinate in the rhizosphere/rhizopiane. Their hyphae penétrate the root cortex, ramifying intercellularly from the point of penetration. The fungus forms special haustoria-1ike structures (arbuscules or coiled hyphae) within cortical cells, separated from the host cytoplasm by the host plasma membrane and the fungal cell wall. Arbuscules provide increased surface área for metabolic exchanges between the host and fungal partners. VAM fungi also develop extraradical hyphae that grow into the surrounding soil, increasing the potential of the root system for nutrient and water absorption, and contributing greatly to the improvement of soil structure for better aeration and water percolation. New survival spores are usually borne on the extraradical hyphae, although spores of some fungal species are produced primarily intraradically. Generally, VAM cause few changes in root morphology, but the physiology of the host plant changes significantly. For example, tissue concentrations of growth regulating compounds and other chemical constituents change, photosynthetic rates increase, and the partitioning of photosynthate to shoots and roots changes (16). The improved 2 CHAPTER ONE potential for mineral uptake from the soil accounts generally less severe on VAM p for changes in the nutritional status of the host plants, but the responses may tissues, in turn changing structural and biochemical involved are controversial (42 aspects of root cells. This can alter membrane infection are general permeability and thus the quality and quantity of root but not always, nematode popul exudation. Altered exudation induces changes in the indicated by number of galls, composition of microorganisms in the rhizosphere soil, unit root 1ength)(41). Atilai now appropriately called the "mycorrhizosphere" showed an increase in nematodi (51,67,82). The net effect of these changes is a plants. These differences ma; healthier plant, better able to withstand differences between nematode environmental stresses (52) and tolérate or reduce the be due to differences in VAM effects of plant diseases. colonization. Furthermore, a The purposes of this review are (a) to discuss with fungal pathogens, timing the role of VAM in the expression of plant disease and :nportant. the mechanisms involved therein, and (b) to discuss A number of mechanisms of factors that influence the role of VAM in biological and nematode pathogens have b control of plant diseases. evidence supporting each is r proposed mechanisms depend or host physiology. Changes in VAM EFFECTS ON FUNGAL ROOT PATHOGENS plants may change the attrad Since VAM fungi are major components of the 'e^iatode pathogens. VAM may rhizosphere, it is logical that they could affect the and thus reduce yield losses incidence and severity of root diseases. Whether they infection, especially in low do or not has been the subject of numerous reviews established early in the groi over the last 15 years (18,32,46,71,72,73), but there infection. This mechanism o is still controversy. Much of the 1Herature suggests the reduced nematode respons that VAM fungi reduce soilborne disease or the effects lowever, by work that showed of disease caused by fungal pathogens. Dehne (32) (55). Cooper and Grandison reported that disease damage was reduced in 17 out of variable by using P-tolerant the 32 reports cited. However, the reports are still :er high P conditions. St mixed, with some indicating no effect of the VAM effects, leading these worke fungus on disease (6,7,28,84,85), and others increased resistance to nems indicating increased disease severity (29,30,31). to improved host nutrition, Drawing conclusions is difficult, partly because so other physiological changes many different pathogens and diseases have been Strobel et al. (78) and 01 \\g split root techniques involved, and partly because of the experimental conditions of each study. Clearly, one should expect -eT.atode infection on VAM p varied results, even if the VAM fungi used had been two were together on the sai the same (71). suggested that competition involved, a mechanism suppo and Sikora (69), Suresh et VAM EFFECTS ON PATHOGENIC ROOT ükora (75), and MacGuidwin Root infections by pathogenic nematodes are studies indicated that nema LINDERMAN 3

>take from the soil accounts generally less severe on VAM plants than on nonVAM lonal status of the host plants, but the responses may vary, and the mechanisms «9 structural and biochemical involved are controversia! (42,44). Symptoms of 5 can alter membrane nematode infection are generally reduced, and often, ity and quantity of root but not always, nematode populations are reduced (as ion induces changes in the indicated by number of galls, juveniles or eggs per sms in the rhizosphere soil unit root length)(41). Atilano et al. (3), however, mycorrhizosphere" showed an increase in nematode populations on VAM p of these changes is a plants. These differences may be due largely to >le to withstand differences between nematode pathogens, but could al so i and tolérate or reduce the be due to differences in VAM fungi and their levéis of colonization. Furthermore, as with VAM interactions review are (a) to discuss with fungal pathogens, timing of VAM formation is sion of plant disease and important. •erein, and (b) to discuss A number of mechanisms of interaction between VAM í of VAM in biológica! and nematode pathogens have been considered, and the evidence supporting each is reasonable. All the proposed mechanisms depend on VAM-mediated changes in UNGAL ROOT PATHOGENS host physiology. Changes in root exudation by VAM plants may change the attractiveness of roots to components of the nematode pathogens. VAM may improve host plant vigor, they could affect the and thus reduce yield losses caused by nematode seases. Whether they infection, especially in low P soils and if VAM are F numerous reviews established early in the growth cycle, before nematode 71,72,73), but there infection. This mechanism of enhanced P nutrition in :he literature suggests the reduced nematode response has been challenged, Hsease or the effects however, by work that showed no effect from adding P logens. Dehne (32) (55). Cooper and Grandison (24,25) eliminated P as a reduced in 17 out of variable by using P-tolerant VAM fungi on plants grown the reports are still under high P conditions. Still, VAM reduced nematode Ffect of the VAM effects, leading these workers to conclude that ')» and others increased resistance to nematodes was not entirely due íverity (29,30,31) to improved host nutrition, but must involve some - Partly because so other physiological changes in the roots. Studies by ises have been Strobel et al. (78) and Oliveira and Zambolim (61) :he experimental using split root techniques indicated that reduced •ly, one should expect nematode infection on VAM plants only occurred if the fungí used had been two were together on the same roots. These results suggested that competition for food or space was involved, a mechanism supported by results of Salen GENIC ROOT NEMATODES and Sikora (69), Suresh et al. (79), Sitaramaiah and Sikora (75), and MacGuidwin et al. (55). These ogenic nematodes are studies indicated that nematode size was reduced and 4 CHAPTERONE

rate of development of infection was slower 1n VAM plant due to changes in the ho roots than nonVAM roots. Physiological changes in VAM 2) pointed out, foliage dise roots could also change resistance to nematodes by oblígate and non-obligate leaf increased production of ínhibitory substances (79), or increased on VAM compared to n by changes in root exudation which could alter to enhanced development of the mycorrhizosphere populations and affect nematode to increased incidence or freq populations and survival. >at effect was correlated wit While the mechanisms are still controversial, the igher physiological activitie evidence strongly indicates that VAM suppress nematode plants (32,73). infections of roots or reduce nematode effects on plant growth and yield. Undoubtedly, the effects and MECHANISMS OF VAM EFFEC1 the mechanisms involved depend on the conditions of the test, the host plant, edaphic conditions, and the Since VAM have such a sig? species of VAM fungus involved. Nonetheless, it seems plant physiology and on bioloc safe to say that VAM do play a role in the biological "izosphere soil, it follows ^ control of root nematode diseases. the incidence and severity of role played by VAM in the bio "seases has been the subject VAM EFFECTS ON BACTERIAL DISEASES 5.18,32,41,46,70,71,72,73), The effects of VAM on bacterial diseases have not "terpretations have preclude been explored to any great extent. However, Garcia- ;hat VAM always suppress plan Garrido and Ocampo (36) showed that VAM tomato -nconsistencies should be exp (Lycopersicon Miller) plants exhibited greater growth cansidering the diverse exper than nonVAM plants inoculated with Pseudomonas use of different VAM fungi on synngae pv. syringae van Hall when the pathogen was sifferent soils (71). Part c added to the foí i age three weeks after the VAM fungus. revolves around the mechanisrr Populations of the pathogen were lower in VAM than iXM and plant pathogens. In nonVAM plants. control of plant diseases, 013 contribute to biological conl orimarily by means of stress VAM EFFECTS ON VIRUS AND FOLIAGE DISEASES (10,12,23,62,72). The liter; While soilborne diseases caused by funga!, however, indicates that biol< nematode, and bacterial pathogens most often are :iseases may be strongly inf" reduced by VAM, those caused by viral and other •nore mechanisms, including: foliage pathogens are generally increased in VAM (b) competition for host pho plants (32,46,73). Reports indicate that disease sites, (c) morphological cha incidence, but not necessarily severity of effect on :issues, (d) changes in chem the plant, is increased in VAM compared to nonVAM tissues, (e) reduction of ab plants. Viruses apparently multiply faster in VAM •icrobial changes in the myc than nonVAM plants. One might suspect that VAM fungi could acquire and vector viruses from root to root Enhanced Nutrition between plants, but that apparently does not happen The most obvious VAM con (45). VAM effects on viruses occur throughout the disease is to increase nutri LJNDERMAN 5 infection was slower in VAM plant due to changes in the host physiology. As Dehne Physiological changes in VAM (32) pointed out, foliage diseases caused by both resistance to nematodes by iDÜgate and non-obligate leaf pathogens can be inhibitory substances (79), or increased on VAM compared to nonVAM plants, likely due ation which could alter to enhanced development of the pathogens rather than tions and affect nematode to increased incidence or frequency of infections. 1. That effect was correlated with improved nutrition and ; are still controversia!, the - :her physiological activities in VAM than nonVAM ites that VAM suppress nematode plants (32,73). 'educe nematode effects on Undoubtedly, the effects and HECHANISHS OF VAM EFFECTS ON PLANT DISEASE depend on the conditions of , edaphic conditions, and the Since VAM have such a significant effect on host volved. Nonetheless, it seems plant physiology and on biological interactions in the play a role in the biological rtnzosphere soil, it follows that they could affect diseases. the incidence and severity of plant diseases. The role played by VAM in the biological control of plant BACTERIAL DISEASES diseases has been the subject of several reviews (8,18,32,41,46,70,71,72,73), but mixed responses and 1 bacterial diseases nave not interpretations have precluded any clear conclusión t extent. However, García- that VAM always suppress plant diseases. Such howed that VAM tomato inconsistencies should be expected, however, nts exhibited greater growth considering the diverse experimental approaches and ated with Pseudomonas use of different VAM fungi on different hosts in Hall when the pathogen was different soils (71). Part of the controversy also 2 weeks after the VAM fungus. revolves around the mechanisms of interaction between 5n were lower in VAM than VAM and plant pathogens. In reviews of biological control of plant diseases, mycorrhizae are thought to contribute to biological control of plant diseases S AND FOLIAGE DISEASES primarily by means of stress reduction (10,12,23,62,72). The literature of recent years, es caused by fungal, however, indicates that biological control of plant thogens »ost often are diseases may be strongly influenced by VAM by one or ed by viral and other more mechanisms, including: (a) enhanced nutrition, rally increased in VAM (b) competition for host photosynthate and infection s indícate that disease sites, (c) morphological changes in roots and root r severity of effect on tissues, (d) changes in chetnical constituents of plant MU coapared to nonVAM tissues, (e) reduction of abiotic stresses, and (f) r Nltiply faster in VAM microbial changes in the mycorrhizosphere. ;ght suspect that VAM fungi ruses from root to root Enhanced Nutrition parently does not happen The most obvious VAM contribution to reduced root es occur throughout the disease is to increase nutrient uptake, particularly P 6 CHAPTERONE and other minerals, resulting in more vigorous plants Coapetition for Nutrients and better able to resist or tolérate root disease. The Even though VAM fungi depf evidence to support the enhanced nutrition idea comes --<• carbohydrates from photos; from experiments where effects comparable to VAM *¿ether they compete with roo! effects were observed when more fértil izer P was itrients. Dehne (32) indica' added. Davis (28) showed this type of response in his thogens could occupy root & studies on Thielaviopsis root rot of citrus where VAM >se colonized by VAM fungí, plants were larger than nonVAM plants unless the ^etition. It has been sug latter were fertilized with additional P. Graham and thogens, on the other hand, Menge (38) suggested a similar effect, where VAM or • reproduction and developm added P reduced wheat take-all disease (Gaeumannomyces DBnetition with VAM fungí ha graminis var. tritici (Sacc.) Arx & 01 iv.), and •echanism of their inhibition speculated that enhanced P status of the plants caused liUle or no direct evidence a decrease in root exudates used by the pathogen for rpothesis, however. On the spore and infection. They did not, iré than make up for their however, demónstrate increased pathogen spore Dancing witl germination with those treatments. In some cases, iply to root pathogens. reports indicate that VAM or added P increased disease incidence, as in the case of Verticillium wilt . lógica! Changes (Verticilliuai dahliae Kleb.) of cotton (Gossypium Localized morphological n'rsutum L.) (31). occur in VAM roots. For In an attempt to clarify the confusión about the íchonbeck (33) showed increa role of enhanced P nutrition associated with VAM and Mato and cucumber (Cucuims root disease expression, Graham and Egel (37) found no -- »ndodermis in VAM plants differences between Phytophthora root rot levéis on ponses accounted for redu VAM and nonVAM citrus seedlings fertilized to be of sporum f. sp. lycopersici equal size and P content. Carón et al. (20,21,22) ícker (15) showed a similar compared responses between VAM and nonVAM tomato on (Pyrenochaeta terrestr plants with a relatively low P threshold requirement Larson). Wick and Moore 1 to root and crown rot disease caused by Fusarium nd-barrier formation thal oxysporum f. sp. radicis-lycopersici Jarvis & ick root rot (Thielaviops Shoemaker. Added P did not reduce disease response -.) of VAM holly {I7ex ci and pathogen populations in rhizosphere soil of nonVAM T»ese few examples indicate plants, but did with VAM plants, even though plant ihological changes in ro> growth and tissue P were not different in the two tudies, however, roots wer treatments. This work suggests the involvement of ;-.-- :al changes, so it r some mechanism of disease suppression other than . —:- .ely such a mechanis enhanced P uptake. Whether or not enhanced P uptake by VAM is involved either directly or indirectly in ^. in Chemical Constit disease expression remains controversial. The Physiological changes a possibility that improved uptake of other mineral Involved in localized ef elements from soil could be involved has not been ^jne et al. (34) demonstra explored. Kientrations of anti-func LINDERMAN 7 sulting in more vigorous plants Competítion for Nutrients and Infection Site DT tolérate root disease. The Even though VAM fungi depend on the host plant 2 enhanced nutrition idea comes for carbohydrates from photosynthesis, it is not clear effects comparable to VAM ntiether they compete with root pathogens for

and they al so suggested that increased arginine Drought stress is another ¡ accumulation in VAM roots suppressed Thielaviopsis ^redisposes plants to attack ty sporulation, a mechanism previously suggested by pathogens. Extraradical hyphai Baltruschat and Schonbeck (13). Morandl et al. (58) absorb water under soil drough found increased concentrations of phytoalexin-like thus help plants to tolérate d isoflavonoid compounds in VAM vs. nonVAM soybeans "o*ever, controversy over whet (Glycine max L.). They postulated that such materials water from soil is the mechani could account for increased resistance to fungal and plants tolérate drought, or wh nematode root pathogens, compared to nonVAM plants. •ptake by VAM is responsible ( More recently, however, Morris and Ward (59) reported iat VAM change the physiology chemoattraction of pathogen zoospores by isoflavonoids •afee them more drought toleran from soybeans. It would appear that such compounds, (4,5.26,37). as well as other compounds, could have different VAM plants are less sensit effects on disease incidence and/or severity. Just » soil toxicities resulting f what role VAM play in these processes remains unknown, I or mineral elements such a lacking direct evidence. sre is controversy about thí i some work implicating imf Alleviation of Abiotic Stress salt tolerance (66), but littl Environmental stresses influence the incidence :í*e mechanisms of heavy metal and severity of biotic plant diseases and cause some uses, however, the toxic matt abiotic diseases. VAM increase plant tolerance to :luded or are somehow alten such stresses by various mechanisms. In this context, -~ects on plant growth. As \s are more tolerant to si VAM can function to biologically reduce plant diseases by virtue of their capacity to reduce effects of «alntain a higher leve! of gn predisposing stress factors such as nutritional stress inVAM plants, and thus may b> (deficiency or excess), soil drought, and soil élseases. toxicities. Because of the greater volume of soil explored by •icrobial Changes in the Myco extraradical hyphae of VAM fungi compared to nonVAM While any of the above me roots, nutrient mineral elements that are relatively CHÉrinations thereof, could b unavailable because they are bound to soil particles sappression of root diseases, (i.e. P, Cu, and Zn) are absorbed by VAM fungal hyphae rsidered more carefully is and translocated to the root from beyond the zone of nzosphere populations of an nutrient depletion around the root. VAM are able to the evidence is clear that mi acquire these and relatively mobile nutrients like i the mycorrhizosphere (57,7 nitrogen (N) from soils where deficiency levéis would iidered those changes reía otherwise créate plant nutrient stress. Nutrient control of diseases, so relat stress may weaken the plant, making it more «railable to support such a n susceptible to pathogen ingress, or more sensitive to The concept of the "mycot other environmental stresses such as cold or heat. - L- -..icrrhizae significan^ Thus, VAM contribute greatly to the general health of •icroflora of the rhizosphen plants by helping to avoid nutrient stress and pÉjysiology and exudation. Ii associated disease-predisposing effects. hyphae of VAM fungi provide LINDERMAN 9 d that increased arginine ots suppressed Thielaviopsis Drought stress is another abiotic factor that sm previously suggested by :-edisposes plants to attack by some opportunistic pathogens. Extraradical hyphae of VAM fungi may sck (13). Morandi et al. (58) iDsorb water under soil drought conditions (39), and trations of phytoalexin-like fus help plants to tolérate drought. There is, in VAM vs. nonVAM soybeans -owever, controversy over whether direct absorption of ' postulated that such materials water from soil is the mechanism whereby VAM help ;ased resistance to funga! and plants tolérate drought, or whether the increased P ., compared to nonVAM plants. -ptake by VAM is responsible (60). Others suggest Morris and Ward (59) reported :hat VAM change the physiology of plants in ways that ogen zoospores by isoflavonoids make them more drought tolerant than nonVAM plants d appear that such compounds, (4,5,26,27). nds, could nave different VAM plants are less sensitive than nonVAM plants Jence and/or severity. Just > soil toxicities resulting from excess salts (40, íese processes remains unknown, I or mineral elements such as heavy metáis (16), "ere is controversy about the mechanisms involved, ¡tress •Tth some work implicating improved P nutrition in salt tolerance (66), but little evidence exists as to es influence the incidence :ne mechanisms of heavy metal tolerance. In both lant diseases and cause some cases, however, the toxic materials are selectively ncrease plant tolerance to excluded or are mechanisms. In this context, somehow altered to prevent toxic ogically reduce plant diseases Ffects on plant growth. As with other stresses, VAM ity to reduce effects of :"ants are more tolerant to soil toxicities and thus jrs such as nutritional stress •aintain a higher level of growth and health than ¡oil drought, and soil •onVAM plants, and thus may be less susceptible to :iseases. ir volume of soil explored by H fungí compared to nonVAM Ricrobial Changes in the Mycorrhizosphere 1e»ents that are relatively While any of the above mechanisms, or are bound to soil particles combinations thereof, could be involved in VAM absorbed by VAM fungal hyphae suppression of root diseases, one that should be oot frow beyond the zone of considered more carefully is the VAM alteration of the root. VAM are able to rhizosphere populations of antagonists. Even though »ly «obile nutrients like the evidence is clear that microbial shifts do occur tere deficiency levéis would in the mycorrhizosphere (57,74), most studies have not :rient stress. Nutrient considered those changes relative to biological it, «aking it more control of diseases, so relatively little data are igress, or more sensitive to available to support such a mechanism. es such as cold or heat. The concept of the "mycorrhizosphere" implies 1y to the general health of that mycorrhizae significantly influence the nutrient stress and •icroflora of the rhizosphere by altering root osing effects. physiology and exudation. In addition, extraradical hyphae of VAM fungi provide a physical or nutritional 10 CHAPTER ONE co^osition of such aggregate substrate for . Analysis of rhizosphere soil •f fungí, bacteria, actinomyc of VAM and nonVAM plants in several studies cyanobacteria. These microbi (2,9,57,74,82) indicated both qualitative and fvigí may profoundly affect quantitative changes in the mycorrhizosphere soil of ryphae in soil, and their met VAM plants, compared to rhizosphere soil of nonVAM >rbed by the hyphae and tr plants. These microbial shifts were clearly time- be specific functional compc dependent and dynamic, changing as the plants - :i-es, and the metabolú developed. Meyer and Linderman (57) used selective Aerein, are virtually unknov media to demónstrate differences in populations of VAH formation alters the taxonomic and functional groups of bacteria in the populations of soil microorg; rhizosphere and rhizoplane of VAM and nonVAM plants. rtagonize root pathogens. Similarly, populations of bacteria and actinomycetes I zoospore production by ti in pot cultures of different VAM fungí were tytophthora cinnamomi Rand. quantitatively and qualitatively analyzed by Secilia isence of rhizosphere lead and Bagyaraj (74). They showed that total populations •trie- compared to leachates f of bacteria in the mycorrhizosphere soil of VAM plants rilarly, more actinomycete were greater than in the rhizosphere soil of nonVAM tagal and bacterial pathoge plants. Effects of VAM on other microbial groups, culture plants than from including nitrogen fixing bacteria, actinomycetes, and :-€ :onditions (74); nú morphological and physiological groups of bacteria (Gram positive and negative bacteria, spore formers, waried among pot cultures of species. urea hydrolyzers, and starch hydrolyzers) varied with Other studies have indic each VAM fungal species. Furthermore, urea s^pression by VAM involved hydrolyzers were present in pot-culture solí of all ^nizosphere microbial p the VAM plants, but were absent in soil from the - •-_- al. (19,20,21,22) i nonVAM plants. Vancura et al. (82) documented the f*s*riua populations in the selective effects of VAM fungal extraradical hyphae on •atoes and a correspondínc bacteria from within the mycorrhizosphere. They did •ot in VAM plants reí a1 not, however, evalúate the antagonistic potential of ¡ibly due to increased ai the microbes associated with the hyphae. These «Mrrhizosphere. Their sti studies demónstrate that VAM influence the microbial Áíced disease incidence w< populations in the mycorrhizosphere soil; many of nutrítion, but depende those microbial shifts could influence the growth and Lh substrate. Another health of plants. indicated protection VAM fungal symbionts produce extraradical hyphae jomi root rot when pía that may extend several centimeters out into the soil a «ixture of VAM pot c and exude organic materials that are substrates for __jrs concluded that a mi other soil microbes. These hypha-associated microbes Fffective than single fungí frequently produce sticky materials that cause soil *n« been due to buildup of particles to adhere, creating small aggregates that :_'=s. as demonstrated t impart structure to soil, allowing for improved '- aeration, water percolation, and stability (81). [hese results indícate Forster and Nicolson (35) analyzed the microbial LINDERMAN 11

AnalysTs of rhizosphere soil composition of such aggregates, and identified a range in several studies of fungi, bacteria, actinomycetes and algae, including both qualitative and cyanobacteria. These microbial associates of VAM ne mycorrhizosphere soil of fungi may profoundly affect the further development of zosphere soil Of nonVAM hyphae in soil, and their metabolic products could be "ts were clearly time- absorbed by the hyphae and translocated to the host. anging as the plants fhe specific functional composition of these rman {57} used selective aggregates, and the metabolic products produced ?nces in populations of ~"e-'ein, are virtually unknown. oups of bacteria in the VAM formation alters the selective pressure on VAM and nonVAM plants. zopulations of soil microorganisms, some of which can antagonize root pathogens. For example, sporangium ¿"'d zoospore production by the root pathogen íly analyzed by Secilia -"ytophthora cinnamomi Rand. was reduced in the that total populations ;resence of rhizosphere leachates from VAM plants, •ere soil of VAM plants wtíen compared to leachates from nonVAM plants (57). )sphere soil of nonVAM similarly, more actinomycetes antagonistic to selected ier microbial groups fungal and bacterial pathogens were isolated from VAM ia, actinomycetes, and pot culture plants than from nonVAM plants grown under I groups of bacteria :he same conditions (74); numbers of antagonists :teria, spore formers .aried among pot cultures of different VAM fungal >lyzers) varied with species. ner^ore, urea Other studies have indicated that disease "Iture soil of all sjppression by VAM involved changes in soil from the n/corrhizosphere microbial populations. The work of documented the Carón et al. (19,20,21,22) indicated a reduction in :raradical hyphae on Fusarium populations in the mycorrhizosphere soil of >sphere. They did ::-atoes and a corresponding reduction in tic potential of root rot in VAM plants relative to nonVAM plants, hyphae. These possibly due to increased antagonism in the VAM luence the microbial irycorrhizosphere. Their studies also showed that •ere soil; many of reduced disease incidence was independent of the level ice the growth and of P nutrition, but dependent on the nature of the growth substrate. Another study, by Bartschi et al. ¡xtraradical hyphae (14), indicated protection of host roots against P. i out into the soil :innamomi root rot when plants were pre-inoculated are substrates for with a mixture of VAM pot culture inocula. The ha-associated microbes authors concluded that a mixture of VAM fungi was more • that cause soil effective than single fungi, but effects could also I aggregates that have been due to buildup of antagonists in the pot n9 for improved cultures, as demonstrated by Secilia and Bagyaraj stability (81). (74). zed the microbial* These results indicate that VAM fungi are 12 CHAPTER ONE relatively tolerant of antagonísts that inhibit fungal coald be expected, On the oth pathogens by one or more mechanisms. They further -•-.::'-;:s were not present i suggest that VAM fungí, which evolved with plants, are cffect of VAM might result. P highly rhizosphere-competent and are compatible with :.se (32,72) would indic such antagonists and even function in concert with iar. i ras e, decrease, or have nc them (51). The possibility that antagonistic Sack responses could indícate rhizosphere bacteria or fungí might inhibit «•rrespond to VAM increases ir mycorrhizal fungí and thereby reduce their ; ' ivons of antagonists or effectiveness was tested by Krishna et al. (48), who frat could enhance disease (81 observed that the pathogen antagonist Streptomyces ther complicated by the di cinnamomeous reduced sporulation and colonization of rains or species of VAM fum G. fasciculatum (Thaxter) Gerd. & Trappe emend. Walker Pferent host genotypes, has & Koske on finger millet (Pam'cum 1.) if it was added rer, such complex interac two weeks before the VAM fungus. In spite of that ~isistencies between studi response, however, the combination of the two -ungi, and soils from var organisms resulted in greater plant dry weights than if either was used alone. FACTORS INFLUENCING MANAGEMI In extensive triáis evaluating interactions between VAM fungi and many fungal or bacterial -••: ¿id Extent of VAM Forrr antagonists, Linderman et al. (54) found little or no iftien VAM are reported to adverse effects of bacterial and fungal biocontrol my generally must be establ agents on establishment and function of VAM on onion -e invasión by the pathoc (Allium cepa !_.}• Other studies (63,64) showed the ffstrated by Stewart and t lack of adverse effects or even stimulation of VAM Rhizoctonia root rot of [ fungi (17) by biocontrol agents, whether applied as ;-err/?7'ma Willd. ex Klotz: seed treatments or added to the soil. Earlier, Meyer [14) on Phytophthora root ro' and Linderman (56) had shown a positive interaction >»aecypar/s lawsoniana (A between the antagonist and plant growth-promoting fxiahl (68) with Aphanomyi rhizobacterium Pseudomonas putida (Migula) and VAM on satírua L.). That this woul' subclover (Tn'folium subterraneum L.). Such jc-cal considering both the interactions must also occur to varying degrees in the : fungal root pathogens, rhizospheres of plants grown in pathogen-infested - - - -r needed for VAM effe soil, although such evaluations are rarely conducted. i occur. Furthermore, othe Changes in mycorrhizosphere populations of 3Ut established root infect antagonists to pathogens seems a likely explanation caí reduce colonization by V for many of the reported effects of VAM on diseases. llential for positive effec Yet, with the exception of those reports mentioned werity (1,6,68,84,85). Se above, few workers have considered that mechanism. r- :;ens and VAM fungi occi Selective increases in numbers of antagonists in the wts without apparent effec mycorrhizosphere are possible only if the antagonists 32?73). are present in the background soil or growth médium. If early VAM formation • Thus, if potentially effective antagonists are present iscase suppression, then wl and are increased by VAM, then disease suppression t cxie has demonstrated din L1NDERMAN 13 antagonists that inhibít funga! ;jld be expected. On the other hand, if potential '-e mechanisms. They further irtagonists were not present in the soil, then no , which evolved with plants, are effect of VAM might result. Reviews on effects of VAM )etent and are compatible with • disease (32,72) would indicate that VAM can 'en function in concert with increase, decrease, or have no effect on disease. lity that antagonistic Such responses could indicate that effects on disease fungí might inhibit correspond to VAM increases in mycorrhizosphere hereby reduce their populations of antagonists or deleterious microbes d by Krishna et al. (48), who Aat could enhance disease (80). This hypothesis, gen antagonist Streptomyces *-jrther complicated by the differential effects of orulation and colonization of :rains or species of VAM fungí associating with r) Gerd. & Trappe emend. Walker ;-fferent host genotypes, has not been tested. t (Panicum L.) if it was added •onever, such complex interactions could explain the 1 fungus. In spite of that iconsistencies between studies using different hosts, :ombination of the two MM fungi, and soils from various parts of the world. .•eater plant dry weights than evaluating interactions FACTORS INFLUENCING MANAGEMENT OF VAM IN BIOCONTROL ny fungal or bacterial Tining and Extent of VAM Formation t al. (54) found little or no When VAM are reported to suppress root disease, rial and fungal biocontrol :rey generally must be established and functioning and function of VAM on onion r-e-ore invasión by the pathogen. This has been studles (63,64) showed the :evonstrated by Stewart and Pfleger (77) on Pythium ir even stímulation of VAM and Rhizoctonia root rot of poinsettia (Euphorbia agents, whether applied as z^lcherrhima Willd. ex Klotzsch), by Bartschi et al. to the soil. Earlier, Meyer 14) on Phytophthora root rot of Lawson cypress IOMI a positive interaction. Chamaecyparis lawsoniana (A. Murr.JParl.)> and by d plant growth-promoting 23sendahl (68) with Aphanomyces root rot of pea (Pisum s putida (Higula) and VAM on sativum L.). That this would be the case seems emneum L.). Such ";gical considering both the faster infection rate of to varying degrees in the •ost fungal root pathogens, compared to VAM fungi, and DMI in pathogen-infested the time needed for VAM effects on the host physiology ¡tions are rarely conducted. to occur. Furthermore, other reports have indicated sphere populations of :hat established root infections by various pathogens i&esis a likely explanation can reduce colonization by VAM fungi and therefore the fffects of VAM on diseases. :atential for positive effects on disease incidence or : those reports mentioned severity (1,6,68,84,85). Sometimes, however, root «sidered that mechanism. zathogens and VAM fungi occupy adjacent tissues in bers of antagonists in the '•oots without apparent effects on each other >le only if the antagonists (21,32,73). imd soil or growth médium. If early VAM formation is required for root ;ive antagonists are present disease suppression, then what processes are involved? :hen disease suppression No one has demonstrated direct interactions between 14 CHAPTER ONE teriation in VAM Fungí, Host i VAM fungí and pathogens, so indirect effects on host ax Nicrobial Composition of : morphology and/or physiology or mycorrhizosphere It is biologically fundam microbial shifts must be involved. However, Fferent interactions to occ physiological effects could be localized or systemic. : "ost plants, and plant Aphanomyces root rot of peas was only suppressed by fe» studies have compared a r VAM when the two organisms were present on the same : (43), and none has don roots (68). A similar response occurred with •la«t diseases. Some studies Phytophthora root rot of citrus (Citrus sinensis L.) genotypes for VAM format in a split root study by Davis and Menge (29), leading studies have not include them to conclude that the effect was not systemic. - - - =:vons. Add to that ce However, Rosendahl (68) showed that oospore production •eraction the variation in was reduced on nonVAM pea roots split from VAM roots, Tobial composition, and i1 compared to plants with no VAM on either root system. retations and comparisí Similarly, Davis and Menge (29) showed that citrus ies are difficult if not roots opposite the split from VAM roots had less ertheless, it is conceival Phytophthora root rot than if split from nonVAM roots. on of factors does i These two studies suggest that VAM effects could be for exploiting VAM both localized and systemic, probably involving two cav be found. sepárate mechanisms. The systemic effect could have been a P effect, while the localized effect was due to IB Management Strategies some morphological or physiological change in the root : VAM contribute to dis tissues in the immediate vicinity. •tari tur al practices that It is itnportant to consider the time or frequency =nd associated antagon of observations within a disease cycle in evaluating - . -: :isease incidence effects of VAM on diseases. Most studies have . -_ •- :~i need for and us evaluated the interaction only once, usually at the •ve that compatible combi end of the experiment. Carón et al. (21) demonstrated .: . -: occur in the sa- that the interaction of VAM and Fusarium root and , could inocúlate see( crown rot of tomato was constant throughout a 12-week itee early establishmei experiment, but the percent root necrosis was only _., invasión (51,53). significantly reduced at 3 of the 12 observations. Ived and economic margii Had measurements been made at other than those times, tices to favor effectiV' reported effects would have been different. ... •: •-ate. In those : antagonists coul Inoculum Level of the Pathogen ailtural crops, manage The potential for biological control to occur in lition of the rhizosph any production system is directly related to the cowbinations of VAM inoculum potential of the pathogen. A high pathogen ._ and inoculated as inoculum density can overwhelm biocontrol agents (11, :íon cycle at a time 23), and this has been shown in VAM studies as well root system is guara (47,71). It is difficult to draw conclusions about can benefit from bot the potential for biocontrol to occur unless a range :**¡9 against invasior of pathogen inoculum densities is used. "O C CU S-S-3 CU cu -o i— O Q J3 00 3 re O EJ •r- Oí U QJ 4- "-i- QJ QJ -i- S- rO ••- "O -O •— E a.ajcnoEQJo-0 QJ s- E Q -=Jc +- >s- •> - ooi— oo U -i— Q-> rO O 1/1 -i-> -O • 4_> rC S~ oo i— -i- 3 oo ••- . o QJ o ) 3 E re •• —oo O QJ +-> i— S-U i— E 00 • s- oii— re QJ o QJ Q- o o S- re en_E E .E en o. QjrO C 3 •<-•*-» 00 QJ -r- E u o QJ re -t-»-Qjre c S -si E QJ oo >^ OQJ+JCC-MQJ-M "Oí— •f-^isoo >•) cus-rere C EQJOO-DEQJ QJ QJ -i- > i— QJ -E E E •oV'-QJircna.cCoo QJ !- O O _E ^-^ S--)-1 oo oreoo> re E re .a -r- oorOrOOOOEO •T- 3 00 ••-LnEcu-E reN4--D +-J en E re ,— * 4-4->t/>E-'-oaJ o > ^3 ^-i (_ )4- 4- > .C -M re oo s- E rüLf>-i-QJEOO ^S-oore 4-J- E •— <"i" 00 Ei— 00 OS- EO-QJO3 QJCCO * O O -C -r- (J OO > OJO>S-+J4-> O i— c/>Qj4-re-»-> 4-E-i-

E o c en Qj o o re c 4-> QJ o. re 3 -i- E QJ4J -t-> c en re -r- u oo 3 4->(J QJ 00 L) E o 4-> a.-.- QJ C-4-J cu oo s- E +->.— t7i n CJOO r8J^ UO oo CLQJ CLO.

" " 16 CHAPTER ONE CONCLUSIONS ilations of antagonists to s on having those antagoni With few exceptions, crop plants have VAM, but , . :^ound soil. If antagonist the degree of root colonizatlon by VAM fungí and the ételeterious microbes are presen effects of the may vary, depending on the tutf>ers and enhanced by VAM, th total interaction between host, symbiont, and severity can be increased. In environment. In most cases, VAM significantly change :.;:jlations to result in bioloc the physiology and chemical constituents of the host, Aseases, compatible VAM fungí the pattern of root exudation, and the microbial irtagonists should be deliverec composition of mycorrhizosphere soil. These changes sjstem to guarantee their domir can greatly influence the growth and health of plants, martagement strategy could resul in part due to the biological suppression of plant :'trol of diseases and improvt diseases. Disease suppression may be the result of reduction of environmental stresses that may limit LITERATURE ( plant growth and predispose the plants to infection by opportunistic pathogens. More important, however, are Afek, U., and Menge, J. A. the specific morphological and physiological changes Pythium ultimum and metala; that directly or indirectly result in reduced length and mycorrhizal coli íncidence and/or severity of plant diseases in VAM onion, and pepper. Plant I plants compared to nonVAM plants. Experiments have A»es, R. N., Reid, C. P. P differed in design, the VAM fungal symbiont used, 1984. Rhizosphere bacteri pathogen types and inoculum levéis, and the plant to root colonization by a growth system used. This variation prevents easy uycorrhizal fungus. New P conclusions about the predictability of VAM effects on Atilano, R. A., Menge, J. plant diseases. Where disease reduction is reported, D. 1981. Interaction betwe one or more mechanisms can be involved, although the and Glomus fasciculatus in tendency is to implicate only one. Because VAM 13: 52-57. effects on plant nutrition, especially P uptake, are ijge, R. M., Schekel, K. A often so striking, many reports implicate improved P 1986. Osmotic adjustment i nutrition as a mechanism of disease control. Enough --rhizal and nonmycorrh reports on VAM suppression of disease where P effects response to drought stress were excluded are now available to suggest the 82:765-770. involvement of other mechanisms. Generally, most i-ge, R. M., Schekel, K. P studies have not investigated other mechanisms such as 1986. Greater leaf conduct morphological changes, changes in disease-suppressing :orrhizal rose plants is chemical constituents in plant tissues, and changes in pbosphorus nutrition. Nev rhizosphere populations of antagonistic microbes Baath, E., and Hayman, D. induced by VAM formation. The mechanisms involved responses to vesicular-art probably are múltiple, and will depend on the ;. Interactions with ^ conditions of the test. The major effect of VAM may toeato plants. New Phyto" be improved nutrition, but secondary effects induced taath, E., and Hayman, D. thereafter may contribute significantly to observed - - ::rrhiza on red core effects on disease. Mycorrhizosphere changes in '-ans. Br. Mycol. Soc. 82 L1NDERMAN 17

3NCLUSIONS zrsulations of antagonists to specific pathogens :epend on having those antagonists present in the , crop plants have VAM, but rackground soil. If antagonists are absent and nization by VAM fungí and the aeleterious microbes are present in significant s may vary, depending on the --Tibers and enhanced by VAM, then disease incidence or en host, symbiont, and severity can be increased. In managing rhizosphere ases, VAM significantly change rcpulations to result in biológica! control of plant ical constituents of the host, aseases, compatible VAM fungí and effective Catión, and the microbial =~tagonists should be delivered to the production íosphere soil. These changes sestero to guarantee their dominance. Such a le growth and health of plants, TT=nagement strategy could result in stable biological )gical suppression of plant ::ntrol of diseases and improve overall plant health. -ession may be the result of ;al stresses that may limit LITERATURE CITED tose the plants to infection by More important, however, are Afek, U., and Menge, J. A. 1990. Effect of :al and physiological changes Pythium ultimum and metalaxyl treatments on root tly result in reduced length and mycorrhizal colonization of cotton, y of plant diseases in VAM onion, and pepper. Plant Dis. 74:117-120. M plants. Experiments have Ames, R. N., Reíd, C. P. P., and Ingham, E. R. VAM funga! symbiont used, 1984. Rhizosphere bacterial population responses lum levéis, and the plant to root colonization by a vesicular-arbuscular s variation prevents easy mycorrhizal fungus. New Phytol. 96: 555-563. edictabilíty of VAM effects on Atilano, R. A., Menge, J. A., and Van Gundy, S. isease reduction is reported, D. 1981. Interaction between Meloidogyne arenaria an be involved, although the and Glomus fasciculatus in grape. J. Nematol. only one. Because VAM 13: 52-57. 3n, especially P uptake, are Auge, R. M., Schekel, K. A., and wample, R. L. sports implicate improved P 1986. Osmotic adjustment in leaves of VA of disease control. Enough mycorrhizal and nonmycorrhizal rose plants in )n of disease where P effects response to drought stress. Plant Physiol. nlable to suggest the 82:765-770. lanisms. Generally, most 5. Auge, R. M., Schekel, K. A., and Wample, R. L.. lated other mechanisms such as 1986. Greater leaf conductance of well-watered VA

8. Bagyaraj, D., J. 1984. Biológica! interactions Carón, M., Fortín, J, A., a with VA mycorrhizal fungi. Pages 131-153 in: VA Influence of substrate on t Mycorrhiza, C.L.Powell and D.J. Bagyaraj, eds,, Glomus intraradices and Fus CRC Press, Inc. Boca Ratón, FL. 234 pp. radicis-lycopersici on toma 9. Bagyaraj, D. J., and Menge, J. A. 1978. 233-239. Interactions between a VA mycorrhiza and '. i-on, M. , Fortin, J, A. , c Azotobacter and their effects on rhizosphere iffect of phosphorus concer microflora and plant growth. New Phytol. 80: intraradices on Fusarium cr 567-573. tonatoes. Phytopathol ogy i 10. Baker, K. F. 1987. Evolving concepts of Carón, M., Fortin, J. A., ; biological control of plant pathogens. Annu. Rev. Effect of Glomus intraradii Phytopathol. 25:67-85. :*sarium oxysporum f. sp. ) 11. Baker, K. F., and Cook, R. J. 1974. Biological tyiatoes over a 12-week peí control of plant pathogens. W. H. Freeman, San ÍEI-556. Francisco, CA. Carón, M., Richard, C., an< 12. Baker, R. 1986. Biological control: an overview. Effect of preinfestation o Can. J. Plant Pathol. 8:218-221. vesicular-arbuscular mycor 13. Baltruschat, H., and Schoenbeck, F. 1975. Studies intraradices, on Fusarium > on the influence of endotrophic mycorrhiza on the toiíatoes, Phytoprotection infection of tobáceo by Thielaviopsis basicola. look, R. J., and Baker, K. Phytopath. Z. 84:172-188. and practice of biological 14. Bartschi, H., Gianinazzi-Pearson, V., and Vegh, zathogens, APS Press, St. I. 1981. Vesicular-arbuscular mycorrhiza . looper, K. M., and Grandis formation and root rot disease (Phytophthora Interaction of vesicular-a cinnamomi) development in Chamaecyparis fungi and root-knot nemato lawsoniana. Phytopath. Z. 102: 213-218. tcmato and white clover su 15. Becker, W. N. 1976. Quantification of onion *eloidogyne hapla. Ann. A vesicular-arbuscular mycorrhizae and their resistance to Pyrenochaeta terrestris. Ph.D. :3oper, K. M., and Grandis Diss., University of Illinois, Urbana. (Diss. of vesicular-arbuscular m> Abstr. 76:24041) ifection of tamarillo (C> 16. Bethlenfalvay, G. J. 1992. Mycorrhizae and Crop *eloidogyne incógnita in f Productivity. Pages 1-27 in: Mycorrhizae in :is. 71: 1101-1106. Sustainable Agriculture, G. J. Bethlenfalvay and Gavies, F. T., Or., Potter R. G. Linderman, eds., ASA Spec. Publ. No. 54., : 5. 1992. Mycorrhiza anc Amer. Soc. Agronomy Press, Madison, WI. exposure affect drought re 17. Calvet, C., Pera, J., and Barea, J. M. 1989. extraradical hyphae devele Interactions of Tnchoderma spp. with Glomus -ndependent of plant size mosseae and two wilt pathogenic fungi. Agrie., J. Plant Physiol. 139:289- Ecosystems Environ. 29:59-65. Davies, F. T., Jr., Pottei 18. Carón, M. 1989. Potential use of mycorrhizae in . G. 1993. Drought resisl control of soilborne diseases. Can. J. Plant pepper plants independent Pathol. 11:177-179. - response in gas exchangí LINDERMAN 19

Biológica! interactions 9. Carón, M., Fortin, J. A., and Richard, C. 1985. I fungí. Pages 131-153 1n- VA Influence of substrate on the interaction of Glomus intraradices and Fusarium oxysporum f. sp. 'c!ca LRatón^, VFL. ' Ba9yaraj 234 pp.> e¿s radicis-lycopersici on tomatoes. Plant Soil 87: Menge, J. A. 1978. 233-239. en a VA mycorrhiza and ::. Carón, M., Fortin, J. A., and Richard, C. 1986. f effects on rhizosphere Effect of phosphorus concentration and Glomus - growth. New Phytol . 80: intraradices on Fusarium crown and root rot of tomatoes. Phytopathology 76: 942-946. •volving concepts of •. Carón, M., Fortin, J. A., and Richard, C. 1986. F Plant pathogens. Annu. Rev Effect of Glomus intraradices on infection by •ao . Fusarium oxysporum f. sp. radicis-lycopersici in • R- J- 1974. Biological tomatoes over a 12-week period. Can. J. Bot. 64: logens. W. H. Freeman, San 552-556. :¿. Carón, M., Richard, C., and Fortin, J. A. 1986. Effect of preinfestation of the soil by a vesicular-arbuscular mycorrhizal fungus, Glomus ^nbeck, F. 1975. Studies intraradices, on Fusarium crown and root rot of iic mycorrhiza on the tomatoes. Phytoprotection 67: 15-19. rtavJopsis basicola. 23. Cook, R. J., and Baker, K. F. 1983. The nature and practice of biológica! control of plant «n, V., and Vegh, pathogens, APS Press, St. Paul, MN. cular mycorrhiza 24. Cooper, K. M., and Grandison, G. S. 1986. »se (Phytophthora Interaction of vesicular-arbuscular mycorrhizal ~hatnaecyparis fungi and root-knot nematode on cultivars of 102: 213-218. tomato and white clover susceptible to ¡catión of onion Meloidogyne hapla. Ann. Appl. Biol. 108: 555- lizae and their 565. terrestris. Ph D 25. Cooper, K. M., and Grandison, G. S. 1987. Effects s, Urbana. (Diss! of vesicular-arbuscular mycorrhiza] fungi on infection of tamarillo (Cyphomandra betacea) by Hycorrhizae and Crop Meloidogyne incógnita in fumigated soil. Plant Mycorrhizae in Dis. 71: 1101-1106. • Bethlenfalvay and 26. Davies, F. T., Jr., Potter, J. R., and Linderman, Spec. Publ. No. 54 R. G. 1992. Mycorrhiza and repeated drought Madison, WI. exposure affect drought resistance and Barea, J. M. 1989 extraradical hyphae development of pepper plants spp. with Glomus independent of plant size and nutrient content. lie fungi. Agrie.. J. Plant Physiol. 139:289-294. -*9-65. 27. Davies, F. T., Jr., Potter, J. R., and Linderman, use of mycorrhizae in R. G. 1993. Drought resistance of mycorrhizal «ses. Can. J. Piant pepper plants independent of leaf P concentration - response in gas exchange and water relations. 20 CHAPTER ONE

Physiol, Plant. 87:45-53. phosphorus-fertilized nonmy 28. Davis, R. M. 1980. Influence of Glomus TT:"-ngs. Plant Dis. 72: fasciculatus on Thielaviopsis basicola root rot iraham, J, H., and Menge, J of citrus. Plant Oís. 64: 839-840. of vesicular-arbuscular myc 29. Davis, R. M., and Menge, J. A. 1980. Influence of pfcosphorus on take-all dise Glomus fasciculatus and soil phosphorus on - :::athology 72: 95-98. Phytophthora root rot of citrus. Phytopathology Hardie, K. 1985. The effect 70: 447-452. extraradical hyphae on wate 30. Davis, R. M., and Menge, J. A. 1981. Phytophthora arbuscular mycorrhiza] piar parasítica inoculation and intensity of 101:677-684. vesicular-arbuscular mycorrhizae in citrus. New lirrel, M. C., and Gerdemar Phytol. 87: 705-715. I^jroved growth of onion ar 31. Davis, R. M., Menge, J. A., and Erwin, D. C. saline soils by two vesicul 1979. Influence of Glomus fasciculatus and soil •fcorrhizal fungi. Soil Sd phosphorus on Verticillium wilt of cotton. ::: Phytopathology 69: 453-456. t^issey, R. S., and Roncadoi 32. Dehne, H. W. 1982. Interactions between [nteraction of Pratylenchu; vesicular-arbuscular mycorrhizal fungí and plant tigaspora margarita on cot' pathogens. Phytopathology 72: 1115-1119. 18-20. 33. Dehne, H. W., and Schonbeck, F. 1979. **issey, R. S., and Roncado1 Untersuchungen zum Einfluss der endotrophen fesicular-arbuscular mycor Mykorrhiza auf Pflanzenkrankheiten. II. •eaatode activity and impp Phenolstoffwechsel und Lignifizierung. (The Hs. 66:9-14. influence of endotrophic mycorrhiza on plant lanson, D. C., and Linderm diseases. II. Phenolmetabolism and fariation in VA mycorrhiza lignification.) Phytopath. Z. 95: 210-216. ~.n Rhizobium on pigeon p 34. Dehne, H. W., Schonbeck, F., and Baltruschat, H. ílie Rhizosphere and Plant 1978. Untersuchungen zum Einfluss der endotrophen -: D. B. Cregan, eds., Kl Mycorrhiza auf Pflanzenkrankheiten. 3. ^ublishers, Dordrecht, The Chitinase-aktivitat und Ornithinzyklus. (The Ingham, R. E. 1988. Inte influence of endotrophic mycorrhiza on plant •matodes and VA mycorrhiz diseases. 3. Chitinase-activity and ornithine- Environ. 24:169-182. cycle). Z. Pflkrankh. 85: 666-678. Jabaji-Hare, S. H., and St 35. Forster, S. M., and Nicolson, T. H. 1981. Electron microscopic exami Aggregation of sand from a maritime embryo sand coinfected with Glomus sp. dune by microorganisms and higher plants. Soil ¡rus. Phytopathology 74:2 Biol. Biochem. 13:199-203. Jalali, B. L., andJalali, 36. García-Garrido, J. M., and Ocampo, J. A. 1989. plant disease control. Pac Effect of VA mycorrhizal infection of tomato on : applied mycology. Soil damage caused by Pseudomonas syringae. Soil Biol. Arora, B. Rai, K. G. Mi Biochem. 21:165-167. Rnudsen, eds., Marcel Dek^ 37. Graham, J. H., and Egel, D. S. 1988. Phytophthora lye, J. W., Pfleger, F. í root rot development on mycorrhizal and 984. Interaction of Glomí LINDERMAN 21

7:45-53. phosphorus-fertilized nonmycorrhizal sweet orange Influence of GJomus seedlings. Plant Dis. 72: 611-614. toelavj'opsis basicoJa root rot Graham, J. H., and Menge, J. A. 1982. Influence Oís. 64: 839-840 of vesicular-arbuscular mycorrhizae and soil ifSS' J:/\- Influence of phosphorus on take-all disease of wheat. and soil phosphorus on Phytopathology 72: 95-98. F citrus. Phytopathology Hardie, K. 1985. The effect of removal of extraradical hyphae on water uptake by vesicular- Menge, J A. 1981. Phytophthora arbuscular mycorrhizal plants. New Phytol. ition and intensity of 101:677-684. ar mycorrhizae in citrus. New Hirrel, M. C., and Gerdemann, J. W. 1980. 3 * Improved growth of onion and bell pepper in e, J. A., and Erwin, D. C saline soils by two vesicular-arbuscular ./offlí/s fasciculatus and soil mycorrhizal fungi. Soil Sci. Soc. Am. J. 44:654- Hura wilt of cotton. 655. 453-456. Hussey, R. S., and Roncadori, R. W. 1978. Interactions between Interaction of Pratylenchus brachyurus and mycorrhizal fungi and plant Sigaspora margarita on cotton. J. Nematol. 10: ithology 72: 1115-1119 18-20. :honbeck, F. 1979, Hussey, R. S., and Roncadori, R. W. 1982. ünfluss der endotrophen Vesicular-arbuscular mycorrhizae may limit enkrankheiten. II. nematode activity and improve plant growth. Plant Lignifizierung. (The Dis. 66:9-14. mycorrhiza on plant lanson, D. C., and Linderman, R. G. 1991. tabolism and Variation in VA mycorrhizal strain interactions 95: 210-216. with Rhizobium on pigeon pea. Pages 371-372 in: . and Baltruschat, H The Rhizosphere and Plant Growth, D. L. Keister influss der endotrophen and P. B. Cregan, eds., Kluwer Academic írankheiten. 3. Publishers, Dordrecht, The Netherlands. Ornithinzyklus. (The Ingharn, R. E. 1988. Interactions betweeen mycorrhiza on plant nematodes and VA mycorrhizae. Agrie., Ecosystems -activity and ornithine- Environ. 24:169-182. 85: 666-678. Jabaji-Hare, S. H., and Stobbs, L. W. 1984. 'son, T. H. 1981. Electron microscopic examination of tomato root ' maritime embryo sand coinfected with Glomus sp. and tobáceo mosaic ligher plants. Soil virus. Phytopathology 74:277-279. Jalali, B. L., and Jalali, I. 1991. Mycorrhiza in and Ocampo, J. A. 1989 plant disease control. Pages 131-154 in: Handbook infection of tomato on of applied mycology. Soil and Plants. Vol. 1, D. was synngae. Soil Biol. K. Arora, B. Raí, K. G. Mukerji, and G. R. Knudsen, eds., Maree! Dekker, New York, NY. • D. S. 1988. Phytophthora r Kaye, J. W., Pfleger, F. L., and Stewart, E. L. on mycorrhizal and 1984. Interaction of Glomus fasciculatum and 22 CHAPTER ONE

Pythium ultimum on greenhouse grown poinsettia. ¿seuodmonas putida. Soil I Can. J. Bot. 62:1575-1579. 190. 48 Krishna, K. R., Balakrishna, A. N., and Bagyaraj Heyer, J. R., and Lindermai D. J. 1982. Interactions between a vesicular- Selective influence on popí arbuscular mycorrhizal fungus and Streptomyces or rhizoplane bacteria and cinnamomeous and their effects on finger millet. •"rhizas formed by Glom New Phytol. 92 401-405. Jiol. Biochem. 18: 191-196 49 Krishna, K. R. Shetty, K. G., Dart, P. J., and Morandi, D., Bailey, J. A. Andrews, 0. J. 1985. Genotype dependen! variation Pearson, V. 1984. Isoflavo in mycorrhizal colonization and response to soybean roots infected wit inoculation of pearl millet. Plant Soil 86:113- irvcorrhizal fungi. Physiol 125. 50 Linderman, R. G. 1986 Managing rhizosphere Morris, P. F., and Ward, E microorganisms in the production of horticultural >emoattraction of zoospor crops. HortScience 21 1299-1302. pathogen, Phytophthora soj 51 Linderman, R. G. 1988 Mycorrhizal interactions Pnysiol. Mol. Plant Pathol with the rhizosphere microflora: The •elson, C. E. 1987. The wa mycorrhizosphere effect. Phytopathology 78:366- ;ular-arbuscular mycor 371. "1-51 in: Ecophysiology of 52 Linderman, R. G. 1988. VA (Vesicular-Arbuscular) . R. Safir, ed., CRC Pres mycorrhizal symbiosis. ISI Atlas of Science, Animal and Plant Sciences Section 1:183-188. liveira, A. A. R., and Z¡ 53 Linderman, R. G. 1991. Mycorrhizal interactions interacao entro o fungo er in the rhizosphere. Pages 343-348 in: The ~:.-icatum e o nematoide ( Rhizosphere and Plant Growth, D. L. Keister and javanica em feijoeiro com P. B. Cregan, eds., Kluwer Academic Publishers, ::íopatol. Bras. 12: 222-¡ Dordrecht, The Netherlands. Papavizas, G. C., ed., 191 54 Linderman, R. G., Paulitz, T. C., Mosier, N. J., i crop production. AÍlanl Griffiths, R. P., Loper, J. E., Caldwell, B. A., Totowa, NJ. and Henkeís, M. E. 1991. Evaluation of the Paulitz, T. C., and Linde effects of biocontrol agents on mycorrhizal Interactions between fluo fungi. Page 379 in: The Rhizosphere and Plant ¥A mycorrhizal fungi. Ne1 Growth, D. L. Keister and P. B. Cregan, eds., Paulitz, T. C., and Linde Kluwer Academic Publishers, Dordrecht, The : antagonism between the Netherlands. Gliocladium virens and ve 55 MacGuidwin, A. E., Bird, G. W., and Safir, G. R. wycorrhizal fungi. New Ph 1985. Influence of Glomus fasciculatum on rsnd, E. C., and Menge, J Meloidogyne hapla infecting Allium cepa. J. growth of tomato in salín Nematol. 17: 389-395. arbuscular mycorrhizal fu 56 Meyer, J. R., and Linderman, R. G. 1986. saline soils. Mycologia 7 Response of subterranean clover to dual ^tiss. J. A., Pond, E., Me inoculation with vesicular-arbuscular mycorrhizal V. M. 1985. Effect of sal fungi and a plant growth-promoting bacterium, non and tomato in soil LINDERMAN 23 i greenhouse grown poinsettia. Pseuodmonas putida. Soil Biol. Biochem. 18: 185- 575-1579. 190. ilakrishna, A. N., and Bagyaraj, . Heyer, J. R., and Linderman. R. G. 1986. ictions between a vesicular- Selective influence on populations of rhizosphere n'zal fungus and Streptomyces or rhizoplane bacteria and actinomycetes by ,heir effects on finger millet. formed by Glomus fasciculatum. Soil 1-405. Biol. Biochem. 18: 191-196. etty, K. G., Dart, P. J., and . Morandi, D., Bailey, J. A., and Gianinazzi- 5. Genotype dependent variation Pearson, V. 1984. Isoflavonoid accumulation in onization and response to soybean roots infected with vesicular-arbuscular rl millet. Plant Soil 86:113- mycorrhizal fungi. Physiol. Plant Pathol. 24:357- 364. 986. Managing rhizosphere Morris, P. F., and ward, E. W. B. 1992. the production of horticultural Chemoattraction of zoospores of the soybean 21:1299-1302. pathogen, Phytophthora sojae, by isoflavones. )88. Mycorrhizal interactions Physiol. Mol. Plant Pathol. 40:17-22. •e microflora: The . Nelson, C. E. 1987. The water relations of rfect. Phytopathology 78:366- vesicular-arbuscular mycorrhizal systems. Pages 71-91 in: Ecophysiology of VA Mycorrhizal Plants. 88. VA (Vesicular-Arbuscular) G. R. Safir, ed., CRC Press, Inc., Boca Ratón, is. ISI Atlas of Science, FL. iences Section 1:183-188. Oliveira, A. A. R., and Zambolim, L. 1987, 91. Mycorrhizal interactions Interacao entro o fungo endomicorrizico Glomus Pages 343-348 in: The etunicatum e o nematoide de gal has Meloidogyne it Growth, D. L. Keister and javam'ca em feijoeiro com raíz partida. , Kluwer Academic Publishers, Fitopatol. Bras. 12: 222-225. ;rlands. Papavizas, G. C., ed., 1981. Biological control lulitz, T. C., Mosier, N. J., in crop production. Allanheld, Osmun Publishers, iper, J. £., Caldwell, B. A., Totowa, NJ. 991. Evaluation of the . Paulitz, T. C., and Linderman, R. G. 1989. agents on mycorrhizal Interactions between fluorescent pseudomonads and The Rhizosphere and Plant VA mycorrhizal fungi. New Phytol. 113:37-45. • and P, B. Cregan, eds., - 3aulitz, T. C., and Linderman, R. G. 1991. Lack ishers, Dordrecht, The of antagonism between the biocontrol agent Gliocladium virens and vesicular arbuscular ird, G. W., and Safir, G. R. mycorrhizal fungi. New Phytol. 117:303-308. lomus fascicuJatum on Pond, E. C., and Menge, J. A. 1984. Improved Fecting Allí uní cepa. J. growth of tomato in salinized soil by vesicular- arbuscular mycorrhizal fungi collected from .- - •--". R. G. 1986. saline soils. Mycologia 76:74-84. >ean clover to dual Poss, J. A., Pond, E., Menge, J. A., and Jarrell, cular-arbuscular mycorrhizal W. M. 1985. Effect of salinity on mycorrhizal wth-promoting bacteriurn, onion and tomato in soil with and without 24 CHAPTER ONE

additional phosphate. Plant Soil 88:307-319. Pythium ultimum a 67. Rambelli, A. 1973. The rhizo.sphere of t's Rev. 159:37, 79-8 mycorrhizae. Pages 299-343 in: Ectomycorrhizae. i. E-, Hussey, R. G. L. Marks and T. T. Kozlowski, eds., Academic Interactions of ve Press, New York, NY. :sl fungi, Meloidog 68. Rosendahl, S. 1985. Interactions between the tilíty on peach. F vesicular-arbuscular mycorrhizal fungus Glomus fasciculatum and Aphanomyces euteiches root rot :. K., Bagyaraj, D. of peas. Phytopath. Z. 114: 31-40. •5. Effect of vesiculc 69. Saleh, H., and Sikora, R. A. 1984. Relationship ;a on survival , per between Glomus fasciculatum root colonization of "icweflt of root-knot nt cotton and Its effect on Meloidogyne incógnita. , S«il 87:305-308. Nematologica 30: 230-237. and Schroth 70. Schenck, N. C. 1983. Can mycorrhizae control root :«s rhizobacteria ¡ diseases? Plant Dis. 65:230-234. CM9 crop growth. Phyti 71. Schenck, N. C. 1987. Vesicular-arbuscular , J. H. 1991. Funga mycorrhizal fungi and the control of fungal root . of soil . Aust. J diseases. Pages 179-191 in: Innovative Approaches , ?., Orozco, M. 0. to Plant Disease Control, I. Chet, ed., John Z. 1989. Properti Wiley & Sons, Inc., New York, NY. of a vesicular 72. Schenck, N. C., and Kellam, M. K. 1978. The Agrie. , Ecosystems influence of vesicular arbuscular mycorrhizae on . and Moore, L. disease development. Fia. Agrie. Exp. Stn. Tech. and nonmycorrh JliOX ,7fl^ Jvúnpjv.i.i.lís .PJ. •Icri' chalí enged by Jh 73. Schonbeck, F. 1979. Endomycorrhiza in relation to J. Plant Pathol. 6: 1 plant diseases. Pages 271-280 in: Soil-borne rtwlim, L. , and Schenck, plant pathogens. B. Schippers and W. Gams, eds., the effects of pathoger Academic Press, New York, NY. rwji on soybean by the mi 74. Secilia, J., and Bagyaraj, D. J. 1987. Bacteria MUS mosseae. PhytopaU and actinomycetes associated with pot cultures of roolim, L., and Schenck, vesicular-arbuscular mycorrhizas. Can. J. crophomina, Rhizoctonia. Microbiol. 33: 1069-1073. corrhizal fungus Glomus 75. Sitaramaiah, K., and Sikora, R. A. 1982. Effect non-nodulated soybean: of the mycorrhizal fungus Glomus fasciculatus on lSileira 9: 129-138. the host-parasite relationship of Rotylenchulus reniformis in tomate. Nematologica 28: 412-419. 76. Smith, G. S. 1988. The role of phosphorus nutrition in interactions of vesicular-arbuscular mycorrhizal fungi with soilborne nematodes and fungi. Phytopathology 78:371-374. 77. Stewart, E. L., and Pfleger, F. L. 1977. Development of poinsettia as influenced by endomycorrhizae, fértilizer and root rot LINDERMAN 25 te. Plant Soil 88:307-319. pathogens Pythium ultimum and Rhizoctonia solani. The rhizo.sphere of Torist's Rev. 159:37, 79-80. 299-343 in: Ectomycorrhizae. •trobel, N. E., Hussey, R. S., and Roncadori, R. T. Kozlowski, eds., Academic M. 1982. Interactions of vesicular-arbuscular r. wycorrhizal fungí, Meloidogyne incógnita, and Interactions between the soil fertility on peach. Phytopathology 72:690- ¡r mycorrhizal fungus Glomus :r-, ¡hanomyces euteiches root rot Saresh, C. K., Bagyaraj, D. J., and Reddy, D. D. i. Z. 114: 31-40. :. 1985. Effect of vesicular-arbuscular Ta, R. A. 1984. Relationship ir/corrhiza on survival, penetration and iculatum root colonization of :rvelopment of root-knot nematode in tomato. ct on Meloidogyne incógnita. >lant Soil 87:305-308. 0-237. Suslow, T. V., and Schroth, M. N. 1982. Role of Can mycorrhizae control root 3eleterious rhizobacteria as minor pathogens in . 65:230-234. -educing crop growth. Phytopathology 72:111-115. Vesicular-arbuscular "isdall, J. M. 1991. Fungal hyphae and structural ¡ the control of funga! root stability of soil. Aust. J. Soil Res. 29:729-743. .91 in: Innovative Approaches Vancura, V., Orozco, M. 0., Grauova, 0., and ntrol, I. Chet, ed., John Prikryl, Z. 1989. Properties of bacteria in the New York, NY, ^yphosphere of a vesicular-arbuscular mycorrhizal Kellam, M. K. 1978. The fungus. Agrie., Ecosystems Environ. 29:421-427. lar arbuscular mycorrhizae on Wick, R. L., and Moore, L. D. 1984. Histology of :la. Agrie, Exp. Stn. Tech. ^ycorrhizal and nonmycorrhizal Ilex crenata He, FL. 'Mellen' challenged by Thielaviopsis basicola. Endomycorrhiza in reíation to Can. J. Plant Pathol. 6: 146-150. »s 271-280 in: Soil-borne Zambolim, L., and Schenck, N. C. 1983. Reduction •ippers and W. Gams, eds., of the effects of pathogenic, root-infecting York, NY. fungí on soybean by the mycorrhizal fungus, tyaraj, D. J. 1987. Bacteria Glomus mosseae. Phytopathology 73: 1402-1405, :1ated with pot cultures of Zambolim, L., and Schenck, N. C. 1984. Effect of • •ycorrhizas. Can. J. Macrophomina, Rhizoctonia, Fusarium and the 1073. mycorrhizal fungus Glomus mosseae on nodulated ¡Ikora, R. A. 1982. Effect and non-nodulated soybeans. Fitopatología •NJUS Glomus fasciculatus on Brasileira 9: 129-138. "latlonship of Rotylenchulus Me»atologica 28: 412-419. s role of phosphorus :ions of vesicular-arbuscular i soilborne nematodes and f 78:371-374. Hleger, F. L. 1977. ;ia as influenced by tílizer and root rot