Bioefficacy and Characterization Effect of Arbuscular ...4)14/14.pdf · Recent advances in...

American-Eurasian J. Agric. & Environ. Sci., 14 (4): 363-378, 2014ISSN 1818-6769© IDOSI Publications, 2014DOI: 10.5829/idosi.aejaes.2014.14.04.12321

Corresponding Author: Masoud Zadehbagheri, Department of Horticultural Shiraz Branch, Islamic Azad University, Shiraz, Iran.

363

Bioefficacy and Characterization Effect of Arbuscular mycorrhizae Fungi onDefence Response Diseases and Soil Sickness In Crop Plants (Review)

Masoud Zadehbagheri, Shourangiz Javanmardi and Arash Azarpanah1 1 2

Department of Horticultural Shiraz Branch, Islamic Azad University, Shiraz, Iran1

Young Researchers and Elite Club, Arsanjan Branch, Islamic Azad University Arsanjan, Iran2

Abstract: Arbuscular mycorrhizal fungi (AMF) are multipurpose organisms with complex ecologicalramifications in the soil system that has been difficult to study and understand. The most common group ofmycorrhizal fungi are the arbuscular mycorrhizal fungi (AMF) which colonise the roots of over 80% of landplant families but they cannot be cultured, as yet, away from the host plant. AMF are primarily responsible fornutrient transfer from soil to plant but have other roles such as soil aggregation, protection of plant againstdrought stress and soil pathogens and increasing plant diversity. This is achieved by the growth of their fungalmycelium within a host root and out into the soil beyond. There is an urgent need to study the below-groundmicrobiology of soils in agro- and natural ecosystems as AMF are pivotal in closing nutrient cycles and havea proven multi-functional role in soil-plant interactions. More information is also needed on the biodiversityand functional diversity of these microbes and their interactions with crops and plants. The phytocentricconcept of AMF that has prevailed since the naming of these organisms is being replaced by a holistic visionrecognizing that AMF are a key element of soil functioning and health rather than a plant root component.Recent advances in knowledge brought about by new techniques for soil microbiology research open the wayto AMF management in crop production. Arbuscular mycorrhizal fungi may influence crop development, evenin phosphorus-rich soils. However, growing crops in soil with lower fertility would optimize the expression ofthe multiple beneficial effects of AMF in agro-ecosystem and reduce nutrient seepage to the environment.The consideration of the soil mycorrhizal potential within the framework of soil testing and fertilizationrecommendations, the development of improved inoculants and signal molecules to manipulate AMF and thedevelopment of cultivars with improved symbiotic qualities would insure the production of good crop yieldswhile improving agroecosystems’ sustainability.

Key words: Arbuscular mycorrhizal Fungi Bio-Control Field Crop Production Agriculture Soil Health Beneficial Effect

INTRODUCTION Avaid and Riaz, 2008). These fungi form essential

The crop is being affected by various diseases improve crop growth and productivity (Van Der Heijdencaused by bacteria, fungi and viruses. Among these, et al., 1998; Schreiner et al., 2003; Kapoor et al., 2004;fungal diseases contribute heavy loss in yield and Cavagnaro et al., 2006).diseases such as blight, stalk and ear rot and smut have Arbuscular mycorrhizal fungi play a key role inbeen reported with localized yield losses of about 11-50% natural ecosystems and influence plant productivity, plant(Nankam 1991; Ngoko 1994; Cardwell et al. 1997). nutrition and plant resistance (Demir and Akkopru 2007).

Arbuscular mycorrhiza (AM) is a group of obligate Biological control preserves environmental qualityfungi that lives in a symbiotic relationship with the roots by a reduction in applying chemical inputs and isof most agricultural crops (Smith and Read, 1997; characteristic of sustainable management practicesGiovannetti et al., 2006; Javaid, 2007; Javaid et al., 2007; (Altieri 1994, Barea and Jeffries 1995). AMF have potential

components of sustainable soil-plant systems and

Am-Euras. J. Agric. & Environ. Sci., 14 (4): 363-378, 2014

364

to reduce disease caused by fungal pathogens i.e., of VAM improved the plant growth by its direct effect onPhytopthora, Sclerotinia, Rhizoctonia, Pythium, improving the internal status of the crop or indirectly byVerticillium and Aphanomyces (Azcon-Aguilar and Barea reducing the harmful effect of the pathogen.1996, Demir and Akkopru 2007 and Aysan and Demir Inoculation with arbuscular mycorrhizal (AM) fungi2009). decreases disease incidence caused by Fusarium sp. In

Effective management strategies have not been asparagus (Wacker et al., 1990), tomato (Lycopersicondeveloped so far as the disease is considered to be more esculentum Mill.) (Caron et al., 1986; Datnoff et al., 1995)complex in nature. Biological control could be the best and potato (Solanum tuberosum L.) (Niemira et al., 1996).alternative and may be helpful, especially against soil Datnoff et al. (1995) found that both T. harzianumborne pathogens (Hajieghrari et al. 2008). It is evident and AM fungal inoculums reduced crown and root rotfrom several studies that arbuscular mycorrhizal (AM) disease (determined by percent of plants having necrosisfungi associations have been shown to reduce damage of the stem and root) caused by F. oxysporum f. sp.caused by soil-borne plant pathogens (Aguilar and Barea radicis-lycopersici in tomatoes.1996). Sivan and Chet (1986) found that application of

Glomus fasiculatum and Gigaspora margarita T. Harzianum with AM fungi reduced disease caused bydecrease root rot diseases caused by Fusarium Fusarium sp. in cotton, wheat and muskmelon.oxysporum in Asparagus (Matsubara et al. 2001), Glomus Nowadays, their application as a biofertilizer in cropclarum was able to reduce the root necrosis caused by production is recommended with the aim of increasingRhizoctonia solani in cow pea (Abdel-Fattah and productivity and reducing fertilizer use (Schwartz et al.,Shabana 2002) and Glomus mossae was shown to 2006). Benefits, however, are not guaranteed and thesystemically reduce disease infection caused by factors that determine the efficiency of this fungalGaeumannomyesgraminis in Barley (Khaosaad et al. association are still unclear. Some of these factors were2007). Therefore, in the present study an effort was made suggested to be AM and plant species, competition withto evaluate the effect of three AM fungi (Glomus other soil micro-organisms as well as, the nutrient statusfasiculatum (GF), Glomus mossae (GM) and Acaulispora of the soil (Sylvia et al., 2005).laevis (AL) on the management of black bundle However, research is needed to develop cultural anddisease caused by C. acremonium in poly house biological control methods to induce resistance of hostcondition. plant. The use of AMF to protect crops from soilborne

Establishing of the same crops in long term at the disease eventually inducing healthy growth of plants withsame site can cause a problem known as replant disease high yields at lower cost and minimum risk to humans and(Utkhede 2006). Soilborne plant pathogen control by environment is a promising strategy.fumigation, chemical pesticide and soil solarization isintensively investigated. The Function of AMF: There are four broad groups of soil

They benefit their host plants by improving nutrient microorganisms: soil animals, prokaryotes, fungaluptake like phosphorus (P), nitrogen (N) and saprotrophs and endophytes. Animals are involved inmicronutrients (Barea et al., 1991; Clark and Zeto, 2000; predation and comminution of soil organic matter.Ward et al., 2001; Javaid, 2009). AM fungi also provide Prokaryotes are a very diverse and versatile group.their host plants with protection against environmental They are responsible for much of the oxido-reductionabiotic stresses (Augé, 2001; Javaid, 2007; Azcón et al., reactions taking place in the soil and are also largely2009) as well as, biotic stress (Khaosaad et al., 2007). involved in soil organic matter mineralization, along withThe benefits of artificially inoculating a wide variety of fungal saprotrophs. In contrast to these later groups,agronomic plant species with AM fungi have been AMF are biotrophic endophytes that do not use soildocumented in numerous studies. organic matter as a source of carbon and energy but,

According to Artursson et al. (2006), VAM can rather, depend on a host plant for their supply. In return,increase growth and phosphorus content of many crops. AMF stimulate plant growth, improve the physicalOn the other hand, VAM significantly decreased disease quality of their soil environment and protect them againstincidence and severity compared to Rhizoctonia-infected soil-borne pathogens. Arbuscular mycorrhizal fungi formplants. This could be due to the direct antagonistic effect extensive hyphal networks in the top soil layer onto whichof VAM on the pathogen and/or the improvement of the most plants of an ecosystem are connected (Read andgrowth conditions of the host plant. Generally, application Birch 1988).


365

As much as 30 m of AMF hyphae can be found per Arbuscular mycorrhizal fungi are associated with,gram of soil (Leake et al. 2004). In nature, AMF networks but clearly distinct from plants and appear as theare involved in the distribution of nutrients in the top backbone of soil ecosystems rather than as a plant part oflayer of the soil and among plants within a community foreign origin. Evidence for the key role of AMF in soil(Marschner and Dell 1994; George et al. 1995; He et al. systems comes from the revelation of the very ancient2003; Neumann and George 2004; Simard and Durall 2004) origin of AMF. Fossil records indicate that the Glomites,and influence plant community structure (Hartnett and which existed 400 million years ago, were very similar toWilson 1999; Stampe and Daehler 2003; Urcelay and Diaz modern AMF and experts believe that the association of2003). plant and AMF may have helped land colonization by

The nature of AMF networks has been well plants (Pirozinsky and Dalpé 1992; Taylor et al. 1995;described recently (Giovannetti et al. 2004; de la Schussler et al. 2001).Providencia et al.2005). These networks are involved in The fact that AMF have remained largely unchangedthe distribution of photosynthesis-derived carbon in soil throughout the co-evolution of plants and soil, testifies to(Staddon et al. 2003a; Zhu and Miller 2003). Arbuscular their importance to soil functioning and quality. The soilmycorrhizal hyphae, which may account for 3-20% of root is an integrated and complex evolutive system withweight (Smith and Read 1997). physical and biological components (Crawford et al.

Thus, considerable amounts of carbon are distributed 2005). Since evolution proceeds through the replacementin the soil via AMF networks, potentially influencing soil of less performant systems with performant ones, AMF,microorganisms (Marschner et al. 2001; Soderberg et al. which have persisted through time, appear as a2002; Marschner and Baumann 2003) and the performant multipurpose component in soil ecosystems.accumulation of soil carbon (Rillig et al. 2001; Lovelock As exposed by Barea et al. (2002), AMF help plantset al. 2004). Our understanding of the soil systems has produce more biomass with lower levels of soil availableimproved and it has become clear that AMF are nutrients and at the same time are photosynthesis-drivenmultipurpose key components of soil functioning and soil quality builders.sustainability (Leake et al. 2004). AMF are involved in the maintenance of soil quality

Plants, AMF and the soil matrix are essential parts of (Barea et al. 2002). The physical soil entrapping effect andthe soil system and all these components must be contribution to soil organic matter of AMF hyphaeconsidered to understand the soil systems. Harris and directly influence soil aggregation and structural stabilityPaul (1987) estimated that 40-50% of photosynthesis- (Jastrow et al. 1998; Wright and Anderson 2000).derived carbon is channelled to AMF; more conservative Arbuscular mycorrhizal mycelium and spores produce avalues of 10-20% were reported by Jakobsen et al.(2002). cell surface glycoprotein, glomalin, which improves soilAlthough the carbon cost of AMF to plants varies with physical quality (Rillig 2004). Glomalin was found to bethe organisms involved and the environmental conditions, closely related to stable soil aggregate formation (Wrightit is certainly an appreciable drain on a host plant. and Upadhyaya 1998), except in high carbonate soilsThe carbon cost related to AMF maintenance is offset by where soil aggregate stability depends on carbonatesthe positive effects AMF have on plant growth and soil rather than on soil organic materials (Franzluebbers et al.quality. This beneficial impact of AMF is well documented 2000).(Smith and Read 1997). Glomalin and its degradation products appear to be

The AMF effect on plant growth promotion is most recalcitrant to decomposition in soil, where theyoften attributed to improved uptake of water and accumulate, as determined by their long-lasting detectionnutrients, in particular P, which has low mobility in soil with a monoclonal antibody. Glomalin is often(Bieleski 1973) and which is required in large amount by (Franzluebbers et al. 2000) but not always related to soilplants. Better nutrition, improved water relations and organic matter (Rillig et al. 2001). It appears, however, thatincreased carbon sink size have been proposed to explain glomalin is an important source of organic matter in soil.the high photosynthetic activity of AMF colonized These fungi form abundant mycelial networks, have aplants, of which the symbiotic condition would oscillate fast turnover rate and the glomalin they produce seems tobetween mutualistic and parasitic, depending on nutrient by-pass the microbial processing imposed on freshavailability (Bethlenfalvay et al. 1987). Although they are organic matter, thus contributing directly to the stable soilmost often beneficial, AMF have reduced plant organic matter pool. The Bradford-reactive- soil-proteinproductivity in nutrient- rich agricultural soils (Ryan and (BRSP) pool extracted from tropical soils was shown toGraham 2002; Stewart et al. 2005). have a minimum residence time of 6 to 42 yr, according to


366

carbon dating and the abundance of immunoreactive techniques that now allow us to track these fungi inglomalin has seemingly reached 3-10 mg cm in their A plants and soils. AMF ecology has recently become an-3

and O horizons (Rillig et al. 2001). active field of research, which should provide importantAll this suggests that glomalin-related soil proteins’ knowledge for the management of AMF in agricultural

contribution to the stable soil organic matter pool is fields.important. Thus, AMF hyphal networks possess theability to modify the physical quality of plant habitats The “Mycorrhizal Effects”: AMF influence cropthrough their important contribution to soil organic matter production in commercial farms although it is not alwaysbuild-up and stabilization of soil aggregates. Extra radical recognized, this influence being confounded with that ofAMF hyphae also influence the soil biological other soil factors. The creation of non-mycorrhizalenvironment and, hence, may influence soil biochemical controls through the chemical destruction of native AMFprocesses and the incidence of disease outbreaks. (Gazey et al. 2004) or their repression using non-hostArbuscular mycorrhizal fungi-soil microbial interactions crops (Vestberg et al. 2005), fallow (Abu-Zeyad et al.are complex and cannot be generalized. The zone of soil 1999) in rotation, or deep tillage (Drijber et al. 2000;immediately surrounding AMF hyphae, the hyphosphere, Miller 2000) have revealed that AMF influence crophosts selected rhizosphere bacteria (Vancura et al. 1990). development. Considering the profound influence of

These bacteria may require amino acid and growth AMF on many aspects of plant physiology and thefactors provided by AMF and their populations may complexity of the soil system, it is virtually impossible tofluctuate as AMF hyphae turnover throughout the soil pinpoint the mechanisms responsible for the AMF effectvolume. The AMF impact on the overall microbial in any particular case. However, we know that thecommunity has varied. AMF were also shown to have expression of this AMF effect in crop growth depends onlittle effect (Olsson et al. 1996) or negative impact three factors: environmental conditions including soil(Christensen and Jakobsen 1993) on the number and type and plant and fungal genotypes.activity of total soil bacteria. Marschner and Baumann AMF were considered as a monolithic group of(2003) observed a significant effect of AMF on the non-specific fungi. We now recognize that considerablestructure of the soil bacterial community. variation in plant growth response can be triggered

Numerous researchers report AMF-related changes by different AMF isolates (Stewart et al. 2005).in the quality of the soil microbial community (Marschner The symbiosis is more complex than it was first thoughtand Baumann 2003) and variation in the size of specific and there is no such thing as an all purpose AMF isolate;microbial populations (Green et al. 1999), but no general the effect of an AMF is plant (Hart and Klironomos 2002)trend for an AMF effect on soil microorganisms emerges, and soil (Rivera et al. 2007) dependant.most likely due to the complexity and wide biodiversity of Considerable interaction between the AMF and plantthe soil environment. species isolated from a woodland site illustrated well the

The AMF cytoplasm may also host bacterial ability of different AMF to enhance P uptake and growthendophytes, in particular plant growth promoting in different plant species and to colonize their rootsrhizobacteria (PGPR) (Ruiz-Lozano and Bonfante 2000; (Helgason et al. 2002). Inoculants contain one of a fewMinerdi et al. 2002; Bianciotto et al. 2004). The role of the AMF strains identified as effective, in monospecificendophytes living within AMF spores and hyphae still AMF inoculants. The different strains formulated areneeds to be clarified, but some evidence suggests that recommended for use in different soil types (Rivera et al.they could be involved in nutrient exchange between the 2007). Thus, the mycorrhizal effects depend on the plantpartners of this consequently tri-partite symbiosis and AMF genotypes interaction, as well as on soil(Minerdi et al. 2002) and stimulate AMF spore conditions.germination (Bianciotto et al. 2004). Plant genotype is a determinant of the AMF effect in

Important advances are being made in the field of two ways. First, plant species have a specific influence onAMF ecology with molecular tools such as polymerase AMF development and it appears that plant specieschain reaction (PCR) (Kowalchuk et al. 2002; determine, to a large extent, the composition of AMFVandenkoornhuyse et al. 2003; Gollotte et al. 2004; Hunt populations flourishing in a soil (Eom et al. 2000).et al. 2004;) and fatty acid methyl ester (FAME) (Olsson Some AMF are even denied access in some plant species,et al. 1999; Balser et al. 2005; Nilsson et al. 2005) based even if they are good colonizers on other species


367

(Helgason et al. 2002; Sanders 2003) and cannot genotypes presumably less fit in intensively managed soilreproduce. This specificity suggests that crop species in were found at greater depths (50-70 cm) in a soil zonerotations may influence the quality of the AMF unaffected by cultural practices (Oehl et al. 2005). population in the soil of a following crop. Second, the Arbuscular mycorrhizal fungi at greater depths can begenotype of a plant can also influence the response of seen as a bank of biodiversity that can feed the top soilthis plant to specific AMF. For example, Liu et al. (2000) inhabiting population when the conditions change indemonstrated the differential response of three maize surface soil, improving the adaptability of the AMFhybrids to inoculation with one AMF. population of cultivated soils. Furthermore, poor

Stewart et al. (2005), working with different taxonomic AMF diversity in intensively cropped systemsstrawberry cultivars in a P-rich field, also found large may not be indicative of poor AMF functionalintraspecific variation in plant response to mycorrhizal biodiversity, as pointed out by Munkvold et al. (2004)inoculation, with the growth of some cultivars being who found a large intraspecific functional diversity inlargely decreased by inoculation with a given AMF AMF. Thus, the management of AMF native toinoculant, while the growth of another was largely agricultural soils appears possible even in soil modifiedincreased. It makes no doubt that plant and AMF by a history of intensive crop management.genotypes influence the effect of AMF on cropdevelopment in agricultural fields. Enhancing Mycorrhizal Effects in Field Crops: It is clear

Most often, AMF effects were sought and found that AMF effects are less prominent in soil with high orin plant development. It has been overlooked, but excessive P fertility. The buildup of excessive soil Pmycorrhizal effects are also related to soil quality. fertility levels is not desirable as P loss to the environmentPlant genotype could indirectly modify soil physical may reduce water quality in rural areas (Beauchemin andquality or the risk of disease outbreak, through its effects Simard 1999) and excessively rich soils do not produceon AMF development or population composition. higher yields than well-managed P poor, sufficient or richPlants, AMF and soil are three interacting components of soils. The best scenario for both farmers and society isa system. In this system, plant genotype could have an the one where the efficiency of P fertilizer applied at lowerimportant effect on soil quality both through direct rates is enhanced by AMF. and indirect modifications of the soil environment. In this way, soil P fertility would not diminishVegetation is an important soil-forming factor (Brady and potential beneficial AMF effects other than plant PWeil 2001). nutrition and yields would be optimized. In soils

Plants directly influence soils in their quality as the excessively rich in P, following repeated application ofmain source of metabolically active and soil organic high rates of P fertilizers, manure or compost,matter C, as well as through their influence on soil water. manufactured signal molecules may be able to stimulatePlants indirectly modify the soil environment, as they are AMF development and optimize AMF contribution tothe determinant of the AMF networks development and, crop production and soil quality. Different molecules werethus, of their influence in soil. found to stimulate AMF development (Cruz et al. 2004;

It is well known that high soil P decreases AMF Dong and Zhao 2004).development (Linderman and Davis 2004a). This Manufactured signal molecules stimulating AMFsometimes led to the conclusion that AMF cannot are currently being tested and will soon enter theenhance plant growth in high P soils. However, soil market. These new biotechnological products couldfertility is not the only determinant of AMF development be advantageously integrated with known practicesand effectiveness. The AMF effect depends also on the optimizing AMF contribution to crop productivity, suchplant and AMF genotypes and AMF-related growth as cover cropping (Sorensen et al. 2005), crop rotationenhancement at high soil P levels has occurred (Singh (Johnson et al. 1992) reduced tillage (Miller et al. 1995)et al. 2002). and moderate fertilization (Miller 2000). Such tools could

Arbuscular mycorrhizal fungi are present in be also useful to enhance AMF effects in crop speciesagricultural fields, even in soils under intensive less receptive to AMF and allow the expression ofmanagement. Intensive management decreases AMF AMF-related benefits on soil quality and on thebiodiversity and selects for slow colonizing-fast development of a possibly mycorrhizae-dependentsporulating species,but the examination of AMF subsequent crop. Current P fertilization recommendationsbiodiversity throughout the soil profile revealed that are very imprecise.


368

Most soil test P used only estimate the available P in brings AMF-related benefits in the form of reducedthe mineral fraction of the soil and ignore P potentially disease incidence, improved crop tolerance to droughtavailable in the organic fraction of soils and the and other stresses and improved soil physical quality,mycorrhizal potential of soils. In order to implement which translate into reduced soil erosion and improvedstrategies of reduced fertilization and AMF management aeration and water infiltration, providing a betterin agricultural soils with no undue risk of yield loss, environment for plant growth.P fertilization recommendations could be based on a soil Crop production relies heavily on agrochemicalstest estimating both the amount of soil P potentially because these products are reliable and easy to use onavailable to a crop and the soil mycorrhizal potential, large highly mechanized farms although they may havewhich represents the potential contribution of indigenous negative impacts on the environment. Concerns relatedAMF populations to the recovery of this P. A few to the environmental impacts of crop productionmethods have been proposed to evaluate the status of effluents are now an incentive for the development ofAMF populations of soils; the most probable number or AMF technologies also in these countries. At theMPN (Porter 1979), the mycorrhizal soil infectivity (MSI) same time, scientific and technological progresses are(Plenchette et al. 1989) and the undisturbed core coming to a point where it may be possible to integrate(Brundrett et al. 1994) methods were the most favourably AMF management into intensive cropping systems.considered by the scientific community. The adoption of crop production practices considering

These methods all generate estimations of the extent the management of AMF would lead the improvement ofof the soil ability to produce mycorrhizal root colonization, the quality of agricultural soil and crop resistance tobut provide no information on the quality of the AMF stresses. Experts predict that global climate changepopulations. Furthermore, all these methods are bioassays will increase the frequency of extreme climatic eventsinvolving growing trap plants for weeks, which cannot (Patz et al. 2005), thus increasing risks of crop failure.be used for routine soil testing. It may be possible to The temperate latitudes, which are projected to warmdevelop a convenient soil test to estimate the potential disproportionately, are among the potentially vulnerablecontribution of AMF to crop nutrition based on molecular regions. Stress-resistant crop plants growing in high-methods. Theoretically, DNA analysis could produce quality soils will certainly be an asset in the future.estimates of the quality (Kowalchuk et al. 2002; de Souza Arbuscular mycorrhizal fungi have a place amongst theet al. 2004) and amounts of AMF in a soil. Real-time PCR biotechnologies of tomorrow’s agriculture.was used to quantify AMF (Filion et al. 2003) and PCRprobes were used to enumerate AMF isolates in Effect of Soil Sterilization and Fungicide Treatments onecosystems (Gollotte et al. 2004). Although the analysis Mycorrhizal Infection: Although large number ofof phospholipids FAME extracted from soil gives no experiments studied the effect of different sterilizationinformation on AMF biodiversity, it can estimate AMF methods on soil pathogenic fungi, little information wereabundance in soil (Nilsson et al. 2005). These analytical reported about their effect on useful soil fungi.techniques could be used in soil-testing laboratories toimprove the accuracy of soil P supply power estimates Fungicide Treatment: The effects of biocide use on nonand fertilization recommendations. The results of the test target organisms, such as VA-fungi, are of interest towould be entered into models specific to the crop to be agriculture, since inhibition of beneficial organisms maygrown, after calibration. counteract benefits derived from pest and disease control.

Fertilization using such an approach would maximize Most of the fungicides which have been used to studythe expression of AMF benefits to soils and crops, reduce their effect on VA mycorrhizal fungi were found to beagricultural reliance on fertilizers and reduce the risk of deleterious, but some were quite compatible with VAnutrient loss to the environment. Attempts are currently mycorrhizal fungi. Sreenivasa and Bagyaraj (1989) werebeing made to develop such analytical techniques. studied the effect of nine fungicides on root colonizationSoil mycorrhizal potential may well end up being with VA mycorrhizal fungi and indicated that reductionmodelled if we finally achieve development of a practical from 10 to 20% of root infection percentages weremethodology to measure it and develop models; this recorded when the recommended level of fungicides werewould considerably reduce the cost of AMF used. While some fungicides were significantly increasedmonitoring. A DNA-based analysis production of crops the percentage root colonization at half the recommendedwith fertilizer levels favouring AMF development also level.


369

In an experiment studied the effect of different Protection Against Toxic Methals and Pathogen: Fewfungicides on VA-fungi infection and population, it was investigations were made about the importance ofconcluded that application of fungicide to soil reduced endomycorrhizal and ectomycorrhizal fungi in protectingsporulation and the root length colonized by VA-fungus, host plants from phytopathogens and mineral elementsalthough interaction of VA-fungi and fungicide were toxicity. Still it was indicated that ectomycorrhizal fungiobserved to be highly variable depending on fungus protect trees from high concentrations of toxic heavyfungicide combination and on environmental conditions. metals, because these tend to be accumulated and

Solarization Treatment: Soil solarization was shown to 1984).be cost reducing, compatible with other pest managementtactics, readily integrated into standard production Effect of Soil Fertility on Mycorrhizal Infection: Mostsystems and a valid alternative to preplant fumigation authors report extensive colonization to occur mainly inwith methyl bromide (Chellami et al., 1997). It also plants growing in soils of low fertility (Khalil et al., 1991).reported that soil solarization induced better growth Field and greenhouse studies demonstrated that cropsresponse in plants even when no pathogen is present in growing in nutrient-poor soils had higher levels ofthe soil (Stapleton et al., 1986). In field experiment, it was mycorrhizal colonization than crops growing in betterreported that solarization of soil by covering it with soils (Gehring et al., 1994). Vesicular-arbusculartransparent plastic sheets resulted in reduction or mycorrhiza inoculation in combination with phosphoruscomplete elimination of soil pathogens between 0 and 25 increased dry and fresh shoot weight, leaf area and leafcm depth in soil covered for 30-60 days (Mansoori et al., number of strawberry compared to application of1996). phosphorus alone (Khanizadeh et al., 1995).

In other experiment it was observed that coveringthe soil with a clear plastic sheet resulted in complete Effect of Soil Amendment with Organic Wastes onelimination of endomycorrhizal fungi at 10 and 20 cm soil Mycorrhizal Colonization: The materials we refer asdepths (Al-Mommi et al., 1988). It was also reported that organic wastes are merely those which are not put to useroot nodulation, infection by mycorrhizal fungi and yield in our existing technological system. Once we begin toof cowpea were higher in plants grown in solarized soil use them, they will no longer be called wastes and if theywhen compared to control treatment without solarization are in demand, we may even seek to increase their(Alloush et al., 2000). Stapleton and DeVay (1986) production. Organic wastes are really resources out ofindicated that the beneficial response of plant growth to place. Farmers historically have applied animal manuresoil solarization might have resulted from the effects of and human wastes to the land, both treated and untreated,better root nodulation, enhanced VA mycorrhizal for crop production.association and the increased availability of some of the Animal and crop plant wastes are different in theirmacro and micro nutrients in soil solution due to chemical and biological composition depending on thesolarization. source of the material. Kale et al., (1992) found that

Methyl Bromide Treatment: Although there was a grave previously received chemical fertilizers compared to 10%environmental concern about the application of methyl in the soil with half the recommended dosage of chemicalbromide and it’s toxicity to mammals, it is still fertilizers and organic matter (OM) amendment.recommended for soil disinfection. Great reduction or Inoculation with VA-fungus did not significantly affectcomplete elimination of all living organisms in the soil seed yield of pea (Pisum sativum L.) plants in soil whichafter methyl bromide gas fumigation of soil is well is rich in OM and phosphorus. On the contrary, seed yielddocumented (Chllami et al., 1997). Soil disinfection by was significantly enhanced with VA-fungi inoculation inmethyl bromide fumigation or steam is often used to soil which is poor in OM and phosphorus (Bethlenfalvayeliminate soil-borne plant pathogens, but such treatments et al., 1994).can reduce VA mycorrhizal fungi as well (Mange, 1983).Several studies have indicated that plant stunting Exudates and Mycorrhiza Bio-Soil Against Soil-Bornefollowing soil fumigation treatments may be due to Disease: Symbiotic interaction between plant root andelimination of VA mycorrhizae (Alten et al., 1993; microbes depends on secondary metabolites in the rootAggangan et al., 1996). exudates for beneficial association initiation and

immobilized in the mycorrhizal sheath (Jackson et al.,

mycorrhizae in roots of a summer crop was 2.85% in soil


370

development (Vigo et al., 2000). The pathogenic P. parasitica development decreased in G. mosseae andinteraction depends on understanding the chemical non G. mosseae parts of tomato mycorrhizal root systemswarfare mediated by plant secretion of phytoalexins, in association with plant cell defense responses anddefense protein and other unknown chemical compounds accumulation of phenolics. Cortical cells containing(Flores et al., 1999; Bais et al., 2004, 2003). The protective G. mosseae are immune to the pathogen and exhibit aeffect of mycorrhizal symbioses against root pathogenic localized resistance response (Cordier et al., 1998).fungi has been tested by many researchers (Caron, 1989; Exudates from fungal mycelium were also shown to impactSt-Arnaud and Vujanovic, 2007; Oger et al., 2004). germination of other pathogens and soil microbes

Disease decrease within plants colonized by (Steinkellner et al., 2008). Extracts from G. intraradicesmycorrhizal species is the result of the complex mycelium stimulated the growth of Ps. chlororaphis andinteractions between pathogens, AMF and plant T. harzianum, had no effect on C. michiganens and(Harrier and Watson, 2004). Mycorrhizal symbiosis has reduced conidial germination of F. oxysporum f. sp.been shown to lessen the damage caused by soil-borne chrysanthemi (Filion et al., 1999). The use of naturalpathogens (Azcon-Aguilar and Barea, 1996). products for the control of fungal diseases in plants isPhytophthora parasitica proliferation was greatly considered an interesting alternative to syntheticminimized when tomato root were colonized by Glomus fungicide due to their less negative impact on themosseae and P. parasitica compared with non- environment (Brunelli, 1995).mycorrhizal tomato roots (Cordier et al., 1996). Root exudates are considered as one of the

Several biotic and a biotic factors are very important mechanisms that explain the ability of AMF to suppressfor the determination of efficiency of AMF as a disease or increase the soil-borne diseases (Mukerji et al., 2002).control agent such as soil moisture, soil contents, host Root exudates vary between different hosts and thegenotype, mycorrhizal level inoculums, inoculation time of composition of the exudates changes in the same plant atmycorrhiza, mycorrhizal fungi species virulence, different conditions (Marschner, 1995; Tahat et al., 2011).inoculums potential of pathogen and soil microflora The current knowledge about the importance of exudates(Singh et al., 2000). The increasing nutrient uptake in AM fungus-host interactions was recently developedresulted in more vigorous plants; thus, the plant itself may in in vitro culture technique and in situ compartmentalbe more resistant or tolerant to pathogen attack systems. Although it is believed that root exudates play(Linderman, 1994). Improvements in plant growth followed a major role in the infection and colonization of hosts byby root colonization by AMF occur as a result of AMF, the actual role or mode of action of exudates wasenhancement of the mineral nutrient status of plants elucidated only recently (Nagahashi, 2000; Smith and(Akhtar and Siddiqui, 2008). Phosphorus tolerant AMF Read, 2008).reduced nematode effect under high-P conditions; The germination of F. oxysporum f. sp Lycopersicitherefore, non-P-mediated mechanisms are involved, was inhibited in the presence of root exudates from theprobably physiological changes in the roots (Sharma tomato plant (Scheffknecht et al., 2006). Root exudateset al., 2007). can have direct defensive qualities. Pathogen-activated

Root exudates from mycorrhizal strawberry plants plant defenses can result in root secretion of antimicrobialsuppressed the sporulation of P. fragariae in in vitro compounds. It was shown that root-derived anti-microbialstudy (Norman and Hooker, 2000). Differential growth of metabolites from Arabidopsis confer resistance to aFusarium oxysporum f. sp chrysanthemi, Trichoderma variety of P. syringae pathovars (Bais et al., 2005).harzianum, Clavibactor michiganesis and Pseudomonas In another study, it was also predicted that transgenicchlororaphis was explained by substances released from plants that produce antimicrobial proteins can influenceG. intraradices under in vitro culture conditions (Filion rhizosphere microbial communities (Glandorf et al., 1997).et al., 1999). Grandmaison et al. (1993) suggested that Sugars and amino acids in the root exudates stimulatephenolic compounds bound to cell wall could be the germination of chlamydospores and other fungiindirectly responsible for the resistance of AMF roots to resting spores. The hyphal length of G. mosseae waspathogenic fungi since they increased the resistance of greatly affected by the exudates of mycorrhizal tomatocell wall to the action of digestive enzymes. root exudates and mycorrhizal corn root exudates.

Phytoalexins toxic components are not detected The growth of Ralstonia solanacearum wasduring the first stages of AMF formation but can be suppressed due to G. mosseae spores germinationdetected in the later stages of symbiosis (Morandi, 1996). (Tahat et al., 2010b).


371

The effect of parasitic nematode in the rhizosphere selective enrichment of specific functional groups ofroot exudates was studied (Foster, 1986; Griffiths, 1989; microbes from that medium is due to root and arbuscularHoriuch et al., 2005). Root feeding nematode could mycorrhizal fungus, hyphal exudates.participate in the interaction with root and soil ‘S’ The real nature of AMF and the importantmicroorganisms (Bais et al., 2006). Most information of contribution of these fungi to soil quality maintenancemicrobe-nematode interaction in mycorrhizosphere and and proper function are just being realized. Research onrhizosphere has been derived from rhizobi, mycorrhyza AMF has progressed slowly due largely to the biotrophicand plant pathogen researches (Khan, 1993). Horiuch et nature of AMF, which limited our ability to study andal. (2005) found that Caenorbabditis elegans may arrange understand these fungi. However, technologies are nowinteraction between plant roots and rhizobia in a positive in place for the development of the tools required for theway luminary to nodulation. In the same study, Horiuch management of AMF in crop production as well as toet al. (2005) reported that C. elegan can transfer the increase knowledge on the ecology of these fungi. WithSinorbizobium meliloti (rhizobium species) to the root of better understanding of AMF in agricultural soil and withMedicago truncatula in response to volatiles that tools to monitor and manage AMF, we will be able toreleased from plant root that attract nematode. optimize the contribution of AMF to agricultural

The hairy root exudates of sweet basil (Ocimum production and finally move toward the management ofbasilicum) cultures of elicited by fungal cell wall were more sustainable cropping systems, for the benefit ofextracted from P. cinnamoni. Basil roots were induced to societies and agro-industries.exude rosmarinic acid (RA) by fungal in situ challenge by Mycorrhizal inoculation tended to increasePythium ultimum and RA demonstrated strong macro-and micronutrient and increased growth of cropantimicrobial activity against soil-borne microorganisms plants, which was comparable to NP fertilizer application.such as P. aeruginosa (Bais et al., 2002b). Hairy roots of Here, the benefits obtained from indigenous AM fungiLithospermum erythrorhizon cell specifically produced surpassed those of commercial types. Thus, use of AMnaphthoquinones pigment upon elicitation and other fungi economizes on fertilizer use in plant productionbiological activity against soil-borne bacteria and providing a sustainable and environmentally saferfungi. The observed antimicrobial activity of RA and substitute. Further research is imperative for fieldnaphthoquinones suggest the importance of root appraisal of these fungi.exudates in defending the rhizosphere against pathogenicmicroorganisms (Brigham et al., 1999). REFERENCES

CONCLUSION Abu-Zeyad, R., A.G. Khan and C. Khoo, 1999.

Mycorrhizal fungi associated with plant roots have Castanospermum australe A. Cunn. and C. Fraserexisted for hundreds of millions of years. The role of and effects on growth and production ofmycorrhizal fungi in improving plant nutrition and their castanospermine. Mycorrhiza, 9: 111-117.interactions with other soil biota have been investigated Aggangan, N.S., B. Dell, N. Malajczuk andwith reference to the host plant growth, but little is R.E. DelaCruz, 1996. Oil fumigation and phosphorusknown about how these interactions affect soil structure. supply affect the formation of Pisolithus EucalyptusThe combination of these organisms in natural, urophylla ectomycorrhizas in two acid Philippineundisturbed ecosystems would seem to contribute to the soils. Plant and Soil, 180: 259-266.successful growth and health of plants. Several factors Akhtar, M.S. and Z.A. Siddiqui, 2008. Arbuscularinfluenced the production of root exudates such as mycorrhizal fungi as potential bioprotectants againstplant type, age, light, soil microflora, soil fertilizer and plant pathogens: In Mycorrhizae: Sustainablesoil pH. This view has attempted to characterize Agriculture and Forestry. (Eds): M.S. Akhtar and ZA.qualitative changes in populations of rhizobacteria Siddiqui and Futai K pp: 61-97. Springer Netherlands.associated with plants with mycorrhizae in what is called Alloush, G.A.Z., S.K. Zeto and R.B. Clark, 2000.the “mycorrhizosphere”. Microbial populations in the Phosphorus source, organic matter and arbuscularmycorrhizosphere can change dynamically over time and mycorrhiza effects on growth and mineral acquisitionare influenced by what microbes are present in the of chickpea grown in acidic soil. Journal Plant Nutr.,background soil or growth medium. The process of 23: 1351-1369.

Occurrence of arbuscular mycorrhiza in


372

Al-Momani, A., W. Abugarbiah and H. Saleh, 1988. Barea, J.M., F. El-Atrach and R. Azcon, 1991. TheThe effect of soil solarization on endomycorrhizal Role of VA Mycorrhizas in Improving Plant Nfungi (Glomus mosseae) and Fusaruim fungi. Dirasat, Acquisition from Soil as Assessed with 15N. In:15: 85-95. Fitton, C. (ed.), The Use of Stable Isotopes in PlantAltieria MA. 1994. Sustainable agriculture. Encyl. Nutrition, Soil Fertility and Environmental Studies,Agric. Sci.4:239-247. pp: 677- 808. Joint IAEA, FAO Division, ViennaAlten, H.V., A. Lindemann and F. Schönbeck, 1993. Barea, J.M., R. Azcon and C. Azcon-Aguilar, 2002.Stimulation of vesicular-arbuscular autochthone Mycorrhizosphere interactions to improve plantmycorrhiza by fungicides or rhizosphere bacteria. fitness and soil quality. Antonie Van LeeuwenhoekMycorrhiza., 2: 167-173. Int. J. Gen. Mol. Microbiol, 81: 343-351.Artursson, V., R.D. Finlay and J.K. Jansson, 2006 . Bianciotto, V., A. Genre, P. Jargeat, E. Lumini,Interactions between arbuscular mycorrhizal fungi G. Bécard and P. Bonfante, 2004. Verticaland bacteria and their potential for stimulating plant transmission of endobacteria in the arbusculargrowth. Environmental Microbiology,8, 1-10. mycorrhizal fungus Gigaspora margarita throughAugé, R.M., 2001. Water relations, drought and VA generation of vegetative spores. Appl. Environ.mycorrhizal symbiosis. Mycorrhiza, 11: 3-42 Microbiol, 70: 3600-3608.Azcón, R., M.C. Perálvarez, B. Biró, A. Roldán and Borea, J.M. and P. Jefferies, 1995. ArbuscularJ.M. Ruíz-Lozano, 2009. Antioxidant activities and mycorrhizas in sustainable soil plant systems. In:metal acquisition in mycorrhizal plants growing in a Hock B. Varma A (Eds) mycorrhizal structureheavy-metal multicontaminated soil amended with function, Molecular biology and biotechnology.treated lignocellulosic agrowaste. Appl. Soil Ecol., Springer, Heidelberg. pp: 521-559.41: 168-177 Beauchemin, S. and R. Simard, 1999. Soil phosphorusAzcon-Aguilar, C. and J.M. Barea, 1996. Arbuscular saturation degree: Review of some indices and theirmycorrhizas and biological control of soilborne plant suitability for P management in Québec, Canada. Can.pathogens-an overview of the mechanisms involved. J. Soil Sci., 79: 615-625.Mycorrhiza, 6: 457-464. Bethlenfalvay, G.J. and J.M. Barea, 1994. MycorrhizaeBais, H.P., F.R. Walker, R.A. Stermitz, in sustainable agriculture. I. Effects on seed yield andV.J.M. Hufbauer, 2002b. Enantiomeric-dependent soil aggregation. Am. J. Altern. Agric., 9: 157-161.phytotoxic and antimicrobial activity of (+/-)- Bethlenfalvay, G.J., M.S. Brown and W.E. Newton,catechin. A rhizosecreted racemic mixture from 1987. Photosynthetic, water and nutrient-usespotted knapweed. Plant Physiol, 128: 1173-1179. efficiency in a mycorrhizal legume. pp: 231-233 inBais, H.P., R. Vepachedu, S. Gilroy, R.M. Callaway, D.M. Sylvia, L.L. Hung and J.H. Graham, eds.J.M. Vivanco, 2003. Allelopathy and exotic plant Mycorrhizae in the next decade: Practical applicationsinvasion: from molecules and genes to species and research priorities. Proceedings of the 7th Northinteractions. Science, 301: 1377-1380. American Conference on Mycorrhizae. Gainesville,Bais, H.P., S.W. Park, T.L. Weir, R.M. Callaway, FL.J.M. Vivanco, 2004. How plants communicate using Bieleski, R.L., 1973. Phosphate pools, phosphatethe underground information super high way. Trends transport and phosphate availability. Ann. Rev. PlantPlant Sci., 9: 26-32. Physiol, 24: 225-252.Bais, H.P., B Prithiviraj, A.K. Jha, F.M. Ausubel, Brady, N.C. and R.R. Weil, 2001. The Nature andJ.M. Vivanco, 2005. Mediation of pathogen Properties of Soils. Prentice Hall, Upper Saddle River,resistance by exudation of antimicrobials from roots. NJ., pp: 960Nature, 434: 217. Brigham, L.A., PJ Michaels and H.E. Flores, 1999.Bais, H.P., T.L. Weir, G.L. Perry, S. Gilroy, Cell-specific production and antimicrobial activity ofJ.M. Vivanco, 2006. The role of root exudates in naphthoquinones in roots of Lithospermumrhizosphere interactions with plants and other erythrorhizon. Plant Physiol, 119:417-428.organisms. Annu. Rev. Plant Biol., 57: 233-266. Brunelli, A, 1995. I prodotti naturali nella lotta alleBalser, T.C., K.K. Treseder and M. Ekenler, 2005. malattie fungine. La Difesa delle Piante, 18(2): 57-69.Using lipid analysis and hyphal length to quantify Brundrett, M.C., L. Melville and L. Peterson, 1994.AM and saprotrophic fungal abundance along a soil Practical Methods in Mycorrhiza Research.chronosequence. Soil Biol. Biochem, 37: 601-604. Mycologue Publications, Sydney, BC., pp: 161


373

Cardwell, K.F., F. Schuthless and Z. Ndemah Rand Datnoff, L.E., S. Nemec and K. Pernezny, 1995.Ngoko, 1997. A systems approach to assess crop Biological control of Fusarium crown and roothealth and maize yield losses due to pests and rot of tomato in Florida using Trichodermadiseases in Cameroon. Agriculture, Ecosystems and harzianum and Glomus intraradices. Biol. Control,Environment. 65: 33-47. 5: 427-431.Caron, M., 1989. Potential use of mycorrhizae in De la Providencia, I.E., F.A. de Souza, F. Fernandez,control of soil-borne diseases. Can. J. Plant Pathol, N.S. Delmas and S. Declerck, 2005. Arbuscular11: 177-179. mycorrhizal fungi reveal distinct patterns ofCaron, M., J.A. Fortin and C. Richard, 1986. Effect of anastomosis formation and hyphal healingGlomus intraradices on infection by Fusarium mechanisms between different phylogenic groups.oxysporum f. sp.radicis-lycopersici in tomatoes over New Phytol, 165: 261-271.a 12-week period. Can. J. Bot. 64: 552-556. Demir, S. and Akkopru, 2007. Using of ArbuscularCavagnaro, T.R., L.E. Jackson, J. Six, H. Ferris, mycorrhizal Fungi (AMF) for Biocontrol of SoilborneS. Goyal, D. Asami and K.M. Scow, 2006. Arbuscular Fungal Plant Pathogens. In: Biological Control ofmycorrhizas, microbial communities, nutrient Plant Diseases, Chincholkar SB and Mukerji KGavailability and soil aggregates in organic tomato (Eds). Haworth press, USA. pp: 17-37.production. Plant Soil, 282: 209-225 De Souza, F.A., G.A. Kowalchuk, P. Leeflang, J. vanChellami, D.O., S.M. Olson, D.J. Mitchell, I. Secker Veen and E. Smit, 2004. PCR-denaturing gradient geland R. McSorley, 1997. Adaptation of soil electrophoresis electrophoresis profiling of inter- andsolarization to the integrated management of intraspecies 18S rRNA gene sequence heterogeneitysoilborne pests of tomato under humid conditions. is an accurate and sensitive method to assessAmer. Phyto. Soc., 87: 250-258. species diversity of arbuscular mycorrhizal fungi ofChristensen, H. and I. Jakobsen, 1993. Reduction of the genus Gigaspora Appl. Environ. Microbiol.bacterial growth by a vesicular-arbuscular 70: 1413-1424.mycorrhizal fungus in the rhizosphere of cucumber Dong, C.J. and B. Zhao, 2004. Arbuscular mycorrhizal(Cucumis sativus L.). Biol. Fertil. Soils, 15: 253-258. formation of crucifer leaf mustard induced byClark, R.B. and S.K. Zeto, 2000. Mineral acquisition flavonoids apigenin and daidzein. Chin. Sci. Bull,by arbuscular mycorrhizal plants. J. Plant Nut., 49: 1254-1261.23: 867-902. Drijber, R.A., J.W. Doran, A.M. Parkhurst andCordier, C., S. Gianinazzi and V. Gianinnazzi-Pearson, D.J. Lyon, 2000. Changes in soil microbial community1996. Colonization patterns of root tissues by structure with tillage under long-term wheat-fallowPhytophthora nicotianae var.parasitica related to management. Soil Biol. Biochem, 32: 1419-1430.reduced disease in mycorrhizal tomato. Plant Soil Eom, A.H., D.C. Hartnett and G.W.T. Wilson, 2000.185: 223-232. Host plant species effects on arbuscular mycorrhizalCordier, C., M.J. Pozo, J.M. Barea, S. Gianinazzi fungal communities in tallgrass prairie. Oecologia,and V. Gianinazzi-Pearson, 1998. Cell defense 122: 435-444.responses associated with localized and systemic Filion, M., M. St-Arnaud and J.A. Fortin, 1999.resistance to Phytophthora parasitica induced in Direct interaction between the arbusculartomato by an arbuscular mycorrhizal fungus. MPMI. mycorrhizal fungus Glomus intraradices and11: 1017-1028. different rhizosphere microorganisms. New Phytol,Crawford, J.W., J.A. Harris, K. Ritz and I.M. Young, 141: 525-533.2005. Towards an evolutionary ecology of life in soil. Filion, M., M. St-Arnaud and S.H. Jabaji-Hare, 2003.Tr. Ecol. Evo., 20: 81-87. Direct quantification of fungal DNA from soilCruz, A.F., T. Ishii, I. Matsumoto and K. Kadoya, substrate using real-time PCR. J. Microbiol. Meth.2004. Relationship between arbuscular mycorrhizal 53: 67-76.fungal development and eupalitin content in Flores, H.E., J.M. Vivanco and V.M. Loyola-Vargas,bahiagrass roots grown in a satsuma mandarin 1999. Radical biochemistry: the biology of root-orchard. J. Jpn. Soc. Hortic. Sci., 73:529-533. specific metabolism. Trends Plant Sci., 4: 220-26.


374

Foster, R.C., 1986. The ultrastructure of the Harrier, L.A. and C.A. Watson, 2004. The potentialrhizoplane and rhizosphere. Annu. Rev. Phytopathol, role of arbuscular mycorrhizal (AM) fungi in the24: 211-34. bio-protection of plants against soil-borne pathogensFranzluebbers, A.J., S.F. Wright and in organic and/or other sustainable farming systems.J.A. Stuedemann, 2000. Soil aggregation and glomalin Pest Manag. Sci., 60(2): 149-157.under pastures in the Southern Piedmont USA. Soil Harris, K.K. and E.A. Paul, 1987. CarbonSci. Soc. Am. J., 64: 1018-1026. Requirements of Vesicular Arbuscular mycorrhizae.Gazey, C., L.K. Abbott and A.D. Robson, 2004. Pages 93-105 in G. R. Safir, Ed.Ecophysiology of VAIndigenous and introduced arbuscular mycorrhizal Mycorrhizal Plants. CRC Press, Boca Raton, FL.fungi contribute to plant growth in two agricultural Hart, M.M. and J.N. Klironomos, 2002. Diversity ofsoils from south-western Australia. Mycorrhiza Arbuscular mycorrhizal Fungi and Ecosystem14: 355-362. Functioning. pp: 225-242 in M.G.A. van der HeijdenGehring, C.A. and T.G. Whitham, 1994. Comparisons and I. Sanders, eds. Mycorrhizal Ecology. Vol. 157.of ectomycorrhizae on pinyon pines (Pinus edulis: Ecological Studies. Springer-Verlag, BerlinPinaceae) across extremes of soil type and herbivory. Heidelberg, Germany.Amer. J. Bot., 81: 1509-1516. Hartnett, D.C. and G.W. T. Wilson, 1999. MycorrhizaeGeorge, E., H. Marschner and I. Jakobsen, 1995. Role influence plant community structure and diversity inof arbuscular mycorrhizal fungi in uptake of tallgrass prairie. Ecology, 80: 1187-1195.phosphorus and nitrogen from soil. Crit. Rev. He, X.H., C. Critchley and C. Bledsoe, 2003. NitrogenBiotechnol, 15: 257-270. transfer within and between plants through commonGiovannetti, M., L. Avio, P. Fortuna, E. Pellegrino, mycorrhizal networks (CMNs). Crit. Rev. Plant Sci.C. Sbrana and P. Strani, 2006. At the root of the wood 22: 531-567.wide web. Plant Signaling Behavior,1: 1-5 Helgason, T., J.W. Merryweather, J. Denison,Giovannetti, M., C. Sbrana, L. Avio and P. Strani, P. Wilson, J.P.W. Young and A.H. Fitter, 2002.2004. Patterns of below-ground plant Selectivity and functional diversity in arbuscularinterconnections established by means of arbuscular mycorrhizas of co-occurring fungi and plants from amycorrhizal networks. New Phytol, 164: 175-181. temperate deciduous woodland. J. Ecol. 90: 371-384.Glandorf, D.C., P.A. Bakker and L.C .Van Loon, 1997. Horiuchi, J.I., B. Prithiviraj, H.P. Bais, B.A. Kimball,Influence of the production of antibacterial and and J.M. Vivanco, 2005. Soil nematodes mediateantifungal proteins by transgenic plants on the positive interactions between legume plants andsaprophytic soil microflora. Acta Bot Neerl, 46:85-104. rhizobium bacteria. Planta, 15: 1-10.Grandmaison, J., G.M. Olah, M.R. Van Calsteren, Hunt, J., L. Boddy, P.F. Randerson and H. J. Rogers,V. Furlan, 1993. Characterization and localization of 2004. An evaluation of 18S rDNA approaches for theplant phenolics likely involved in the pathogen study of fungal diversity in grassland soils. Microb.resistance Mycorrhiza, 3(4): 155-164. Ecol., 47: 385-395.Green, H., J. Larsen, P.A. Olsson, D.F. Jensen and I. Jakobsen, I., S.E. Smith and F.A. Smith, 2002.Jakobsen, 1999. Suppression of the biocontrol agent Function and Diversity of Arbuscular mycorrhizae inTrichoderma harzianum by mycelium of the Carbon and Mineral Nutrition. pp: 75-92 in M.G. A.arbuscular mycorrhizal fungus Glomus intraradices in van der Heijden and I. Sanders, eds. Mycorrhizalroot-free soil. Appl Environ. Microbiol, 65: 1428-1434. ecology. Vol. 157. Ecological Studies. Springer-Gollotte, A., D. van Tuinen and D. Atkinson, 2004. Verlag, Berlin, Heidelberg, Germany.Diversity of arbuscular mycorrhizal fungi colonising Jackson, R.M. and P.A. Mason, 1984. Mycorrhiza.roots of the grass species Agrostis capillaris and Edward Arnold, Ltd., London, pp: 60. ISBN 0-7131-Lolium perenne in a field experiment. Mycorrhiza 2876-3.14: 111-117. Jastrow, J.D., R.M. Miller and J. Lussenhop, 1998.Griffiths, B.S., 1989. The role of bacterial feeding Contributions of interacting biological mechanisms tonematodes and protozoa in rhizosphere nutrient soil aggregate stabilization in restored prairie. Soilcycling. Asp. Appl. Biol, 22:141-45. Biol. Biochem, 30: 905-916.


375

Javaid, A., 2007. Allelopathic interactions in Linderman, R.G. and E.A. Davis, 2004a. Evaluation ofmycorrhizal associations. Allelopathy J., 20: 29-42. commercial inorganic and organic fertilizer effects onJavaid, A., T. Riaz and S.N. Khan, 2007. Mycorrhizal arbuscular mycorrhizae formed by Glomusstatus of Narcissus papyraceus Ker-Gawl. Co- intraradices. Hortic. Technol., 14: 196-202.cultivated with Cynodon dactylon Pers. Int. J. Agric. Liu, A., C. Hamel, R.I. Hamilton and D.L. Smith, 2000.Biol., 9: 901-904. Mycorrhizae formation and nutrient uptake of newJavaid, A. and T. Riaz, 2008. Mycorrhizal colonization corn (Zea mays L.) hybrids with extreme canopy andin different varieties of Gladiolus and its relation with leaf architecture as influenced by soil N and P levels.plant vegetative and reproductive growth. Int. J. Plant Soil, 221: 157-166.Agric. Biol., 10: 278-282. Mansoori, B. and N.K.H. Jaliani, 1996. Control ofJavaid, A., 2009. Mycorrhizal mediated nutrition in soilborne pathogens of watermelon by solar heating.plants. J. Plant Nut., (in press). Elsevier Sci., 15: 423-424.Johnson, N.C., P.J. Copeland, R.K. Crookston and Marschner, H., 1995. Mineral Nutrition ofF.L. Pfleger, 1992. Mycorrhizae: possible explanation Higher Plants. 2 Edn. Academic Press, London,for yield decline with continuous corn and soybean. pp: 889.Agron. J., 84: 387-390. Marschner, H. and B. Dell, 1994. Nutrient uptake inKapoor, R., B. Giri and K.G. Mukerji, 2004. Improved mycorrhizal symbiosis. Physiol. Planta, 159: 89-102.growth and essential oil yield and quality in Marschner, P. and K. Baumann, 2003. ChangesFoeniculum vulgare Mill. on mycorrhizal inoculation in bacterial community structure induced bysupplemented with P-fertilizer. Biores. Technol, mycorrhizal colonisation in splitroot maize. Plant Soil,93: 307-311 251: 279-289.Kale, R.D., B.C. Mallesh, K. Bano and D.J. Bagyaraj, Marschner, P., D.E. Crowley and R. Lieberei, 2001.1992. Influence of vermicompost application on the Arbuscular mycorrhizal infection changes theavailable macronutrients and selected microbial bacterial 16 S rDNA community composition in thepopulations in a paddy field. Soil Biol. and Biochem, rhizosphere of maize. Mycorrhiza, 11: 297-302.24: 1317-1320. Menge, J.A., 1983. Utilization of vesicular-arbuscularKhalil, S., T.E. Loynachan and H.S. McNabb, 1992. mycorrhizal fungi in agriculture. Can. Journal Bot.,Colonization of soybean by mycorrhizal fungi and 61: 1015-1024.spore populations in Iowa soils. Agron. Journal, Miller, M.H., 2000. Arbuscular mycorrhizae and the84: 832-836. phosphorus nutrition of maize: A review of GuelphKhaosaad, T., J.M.García-Garrido, S. Steinkellner and studies. Can. J. Plant Sci. 80: 47-52.H. Vierheilig, 2007. Take-all disease is systemically Miller, M.H., T. P. McGonigle and H.D. Addy, 1995.reduced in roots of mycorrhizal barley plants. Soil Functional ecology of vesicular arbuscularBiol. Biochem, 39: 727-734 mycorrhizas as influenced by phosphate fertilizationKowalchuk, G.A., F.A. De Souza and J.A. Van Veen, and tillage in an agricultural ecosystem. Crit. Rev.2002. Community analysis of arbuscular mycorrhizal Biotechnol, 15: 241-255.fungi associated with Ammophila arenaria in Dutch Minerdi, D., V. Bianciotto and P. Bonfante, 2002.coastal sand dunes. Mol. Ecol., 11: 571-581. Endosymbiotic bacteria in mycorrhizal fungi: fromLeake, J.R., D. Johnson, D.P. Donnelly, G.E. Muckle, their morphology to genomic sequences. Plant Soil,L. Boddy and D.J. Read, 2004. Networks of 244: 211-219.power and influence: the role of mycorrhizal Morandi, D., 1996. Occurrence of phytoalexins andmycelium in controlling plant communities and phenolic compounds in endomycorrhizal interactionagroecosystem functioning. Can. Journal Bot. and their potential role in biology control. Plant Soil,82: 1016-1045. 185: 241-251.Linderman, R.G., 1994. Role of VAM Fungi in Mukerji, K.G., C Manoharachary and B. ChamolaBiocontrol. In: Pfleger F.L. and Linderman R.G. 2002. Techniques in Mycorrhizal Studies. KluwerMycorrhizae and Plant Health. pp: 1-27. American Academic Publishers. London-Netherlands,Phytological Society, St. Paul.M.N. pp: 285-296.

nd


376

Munkvold, L., R. Kjoller, M. Vestberg, S. Rosendahl, Oger, P.M., H. Mansouri, X. Nesme and Y. Dessaux,and I. Jakobsen, 2004. High functional diversity 2004. Engineering root exudation of Lotus toward thewithin species of arbuscular mycorrhizal fungi. New production of two novel carbon compounds leads toPhytol., 164: 357-364. the selection of distinct microbial populations in theNagahashi, G., 2000. In vitro and In situ Techniques rhizosphere. Microb. Ecol., 47: 96-103.to Examination the Role of Roots and Root Patz, J.A., D. Campbell-Lendrum, T. Holloway andExudates during AM Fungus-host Interactions. In: J.A. Foley, 2005. Impact of regional climate change onKapulink, Y and. Douds. Jr., D. Arbuscular human health. Nature, 438: 310-317.Mycorrhizas: Physiology and Function: eds, Pirozinsky, K.A. and Y. Dalpé, 1992. The geologicalKluwer Academic Publishers. Netherlands, history of the Glomaceae with particular reference topp: 278-300. mycorrhizal symbiosis.Symbiosis, 7: 1-36.Nankam, J.C., 1991. Incidence of blight and race of Plenchette, C., R. Perrin and P. Duvert, 1989. TheExserohilumturcicumin Cameroon. Proceedings of concept of soil infectivity and a method for itsthe SAFGRAD Inter-Network Conference in Niamey, determination as applied to endomycorrhizas. Can. J.7-14 March 1991, Niger, pp: 257-261. Bot., 67: 112-115.Neumann, E. and E. George, 2004. Colonisation with Porter, W.M., 1979. The “Most Probable Number” forthe arbuscular mycorrhizal fungus Glomus mosseae enumerating infective propagules of vesicular(Nicol. and Gerd.) enhanced phosphorus uptake arbuscular mycorrhizal fungi. Aust. Journal Soil Res.,from dry soil in Sorghum bicolor (L.). Plant Soil 17: 515-519.261: 245-255. Read, D.J. and C.P.D. Birch, 1988. The effect andNgoko, Z., 1994. Maize Diseases in the Highlands of implication of disturbance of mycorrhizal mycelialCameroon. Technical Bulletin, Institute of systems. Proc. R. Soc.Edin., 948: 13-24.Agricultural Research, pp: 22. Rillig, M.C., 2004. Arbuscular mycorrhizae, glomalinNiemira, B., R. Hammerschmidt and G. Safir, 1996. and soil aggregation. Can. J. Soil Sci., 84: 355-363.Postharvest suppression of potato dry rot Rivera, R.A., F. Fernández and K. Fernández, 2007.(Fusarium sambucinum) in prenuclear minitubers by Advances in the management of effective arbusculararbuscular mycorrhizal fungal inoculum. Amer. Potato mycorrhizal symbioses in tropical ecosystems. InJournal, 73: 509-515. C. Hamel and C. Plenchette, eds. Mycorrhizae in cropNilsson, L.O., R. Giesler, E. Baath and H. Wallander, production. Haworth Press Inc., Binghamton NY.2005. Growth and biomass of mycorrhizal mycelia in (in press).coniferous forests along short natural nutrient Ruiz-Lozano, J.M. and P. Bonfante, 2000. Agradients. New Phytol, 165: 613-622. Burkholderia strain living inside the arbuscularNilsson, L.O., R. Giesler, E. Baath and H. Wallander, mycorrhizal fungus Gigaspora margarita possesses2005. Growth and biomass of mycorrhizal mycelia in the vacB gene, which is involved in host cellconiferous forests along short natural nutrient colonization by bacteria. Microb. Ecol., 39: 137-144.gradients. New Phytol, 165: 613-622. Ryan, M.H. and J.H. Graham, 2002. Is there a role forNorman, J.R. and J.E. Hooker, 2000. Sporulation arbuscular mycorrhizal fungi in productionof Phytophthora fragariae shows greater agriculture? Plant Soil, 244: 263-271.stimulation by exudates of non-mycorrhizal than Sanders, I.R., 2003. Preference, specificity andby mycorrhizal strawberry roots. Mycol. Res., cheating in the arbuscular mycorrhizal symbiosis.104: 1069-1073. Trends Plant Sci., 8: 143-145.Oehl, F., E. Sieverding, K. Ineichen, E.A. Ris, Schussler, A., D. Schwarzott and C. Walker, 2001. AT. Boller and A. Wiemken, 2005. Community structure new fungal phylum, the Glomeromycota: phylogenyof arbuscular mycorrhizal fungi at different soil and evolution. Mycol. Res., 105: 1413-1421.depths in extensively and intensively managed Scheffknecht, S., R. Mammerler, S. Steinkellner andagroecosystems. New Phytol, 165: 273-283. H. Vierheilig, 2006. Root exudates of mycorrhizalOlsson, P.A., E. Bååth, I. Jakobsen and B.Söderström, tomato plants exhibit a different effect on1996. Soil bacteria respond to presence of roots but microconidia germination of Fusarium oxysporum f.not to mycelium of arbuscular mycorrhizal fungi. Soil sp.lycopesici than root exudates from nonmycorrhizalBiol. Biochem, 28: 463-470. tomato plants. Mycorrhiza, 16(5): 365-370.


377

Schreiner, R.P., K.L. Mihara, K.L. Mc Daniel and Sreenivasa, M.N. and D.J. Bagyaraj, 1989. Use ofG.J. Benthlenfalvay, 2003. Mycorrhizal fungi pesticide for mass production of vesicular-arbuscularinfluence plant and soil functions and interactions. mycorrhizal inoculum. Plant and Soil, 119: 127-132.Plant Soil, 188: 199-209. St-Arnaud M. and V. Vujanovic, 2007. Effect of theSchussler, A., D. Schwarzott and C. Walker, 2001. A Arbuscular mycorrhizal Symbiosis on Plant Diseasesnew fungal phylum, the Glomeromycota: phylogeny and Pests. In: Hamel C, Plenchette C (eds)and evolution. Mycol. Res., 105: 1413-1421. Mycorrhizae in crop production. Haworth Press,Schwartz, M.W., J.D. Hoeksema, C.A. Gehring, Binghampton, New York, pp: 67-122.N.C. Johnson, J.N. Klironomos, L.K. Abbott and Staddon, P.L., N. Ostle, L.A. Dawson and A.H. Fitter,A. Pringle, 2006. The promise and the potential 2003a. The speed of soil carbon throughput in anconsequences of the global transport of mycorrhizal upland grassland is increased by liming. J. Exp. Bot.fungal inoculum. Ecol. Lett., 9: 501-515 54: 1461-1469.Simard, S.W. and D.M. Durall, 2004. Mycorrhizal Stampe, E.D. and C.C. Daehler, 2003. Mycorrhizalnetworks: a review of their extent, function and species identity affects plant community structureimportance. Can. J. Bot., 82: 1140-1165. and invasion: a microcosm study. Oikos, 100: 362-372.Singh, C., A.K. Sharma and B.N. Johri, 2002. Hostgenotype determines the impact of soil phosphorus Stapleton, J.J. and J.E. DeVay, 1986. Soil solarization:on arbuscular mycorrhizal symbiosis in maize A non-chemical approach for management of plant(Zea mays L.). Symbiosis, 33: 145-164. pathogens and pests. Crop Protection, 5: 190-198.Singh, R., A. Adholega and K.G. Mukerji, 2000. Steinkellner, S., R. Mammerler and H. Vierheilig, 2008.Mycorrhiza in Control of Soilborne Pathogens. In: Effects of membrane filtering of tomato root exudatesMukerji KG, Chamola BP, Singh,J (eds)., Mycorrhizal on conidial germination of Fusarium oxysporum f. sp.Biology, Kluwer Academic/Plenum Publishers, New lycopersici. J. Phytopathol. 156:489-492.York, USA, pp: 173-196. Stewart, L.I., C. Hamel, R. Hogue and P. Moutoglis,Sivan, A. and I. Chet, 1986. Biological control of 2005. Arbuscular mycorrhizal inoculated strawberryFusarium spp. in cotton, wheat and muskmelon by plant responses in a high soil phosphorus rotationTrichoderma harzianum. Phytopathology, 116: 39-47. crop system. Mycorrhiza, 15: 612-619.Sharma, M.P., A. Gaur and K.G. Mukerji, 2007. Sylvia, D.M., P. Hartel, J. Fuhrmann and D. Zuberer,Arbuscular mycorrhiza Mediated Plant Pathogen 2005. Principles and Applications of SoilInteractions and the Mechanisms Involved. In: Microbiology, 2 Edition. Prentice Hall, New Jersey,Sharma MP, Gaur A, Mukerji. KG Biological Control USA.of Plant Diseases. pp: 47-63. Haworth Press. Taylor, T.N., W. Remy, H. Hass and H. Kerp, 1995.Smith, S.E. and D.J. Read, 1997. Mycorrhizal Fossil arbuscular mycorrhizae from the EarlySymbiosis, 2 edition. Academic Press, London, UK. Devonian. Mycologia, 87: 560-573.nd

Smith, S.E. and D.J. Read, 2008. Mineral Nutrition, Tahat, M.M., K. Sijam and R. Othman, 2010b. The roleToxic Element Accumulation and Water Relations of of tomato and corn root exudates on Glomus mosseaeArbuscular mycorrhizal Plants. In: Smith, S.E. and spores germination and Ralstonia solanacearumRead. D.J. Mycorrhizal Symbiosis. 3 . pp: 145-18. growth in vitro. Int. J. Plant Pathol, 1:1-12rd

Academic Press, London. Tahat, M.M., K Sijam and R. Othman, 2011.Soderberg, K.H., P.A. Olsson and E. Bååth, 2002. Bio-compartmental in vitro system for GlomusStructure and activity of the bacterial community in mosseae and Ralstonia solanacraum interaction. Int.the rhizosphere of different plant species and the J. Bot., 7: 295-299.effect of arbuscular mycorrhizal colonisation. FEMS Urcelay, C. and S. Diaz, 2003. The mycorrhizalMicrobiol. Ecol., 40: 223-231. dependence of subordinates determines the effect ofSorensen, J.N., J. Larsen and I. Jakobsen, 2005. arbuscular mycorrhizal fungi on plant diversity. Ecol.Mycorrhiza formation and nutrient concentration in Lett, 6: 388-391.leeks (Allium porrum) in relation to previous crop Utkhede, R.S., 2006. Soil sickness, replant problem orand cover crop management on high P soils. Plant replant disease and its integrated control.Soil, 273: 101-114. Allelophaty Journal, 18: 23-28.

nd


378

Vancura, V., M.O. Orozco, O. Grauová and Z. Prikryl, Wacker, T., G. Safir and C. Stephens. 1990. Effect of1990. Properties of bacteria in the hyphosphere of Glomus fasciculatum on the growth of asparagusa vesicular-arbuscular mycorrhizal fungus. Agric. and the incidence of fusarium root rot. J. Amer. Soc.Ecosyst. Environ, 29: 421-427. Hort. Sci., 115(4): 550-554.Vandenkoornhuyse, P., K.P. Ridgway, I.J. Watson, Ward, N.I., K. Stead and J. Reeves, 2001. Impact ofA.H. Fitter and J.P.W. Young, 2003. Co-existing grass endomycorrhizal fungi on plant trace element uptakespecies have distinctive arbuscular mycorrhizal and nutrition. Nut. Pract., 32: 30-31communities. Mol. Ecol., 12: 3085-3095. Wright, S.F. and R.L. Anderson, 2000. AggregateVan Der Heijden, M.G.A., J.N. Klironomos, M. Ursic, stability and glomalin in alternative crop rotationsP. Moutoglis, R. Streitwolf-Engel, T. Boller, for the central Great Plains. Biol. Fertil. Soils,A. Wiemken and I.R. Sanders, 1998. Mycorrhizal 31: 249-253.fungal diversity determines plant biodiversity, Wright, S.F. and A. Upadhyaya, 1998. A survey ofecosystem variability and productivity. Nature, soils for aggregate stability and glomalin, a396: 72-75. glycoprotein produced by hyphae of arbuscularVestberg, M., K. Saari, S. Kukkonen and T. Hurme, mycorrhizal fungi. Plant Soil, 198: 97-107.2005. Mycotrophy of crops in rotation and soil Zhu, Y.G. and R.M. Miller, 2003. Carbon cycling byamendment with peat influence the abundance and arbuscular mycorrhizal fungi in soil-plant systems.effectiveness of indigenous arbuscular mycorrhizal Trends Plant Sci., 8: 407-409.fungi in field soil. Mycorrhiza, 15: 447-458.Vigo, C., J.R. Norman and J.E. Hooker, 2000.Bio-control of the pathogen Phytophthoraparasitica by arbuscular mycorrhizal fungi is aconsequence of effects on infection loci. PlantPathol, 49: 509-514.

Bioefficacy and Characterization Effect of Arbuscular ...4)14/14.pdf · Recent advances in...

Documents

Transcript of Bioefficacy and Characterization Effect of Arbuscular ...4)14/14.pdf · Recent advances in...