ia

hri

, CM

plexiffeostshe

that may be involved in dynamics of patches. These potential mechanisms are discussed. It is essential toknow about the mechanisms involved to develop an effective control strategy. Although more work is

ed byinclud

i, Fusarvecto

(Schoeny et al., 2001; Smith et al., 2003). The efcient economicalcontrol of these diseases whether by chemical, biological, genetic orcultural means, depends upon understanding the ecology of these

physico-chemical properties of soil as well as the environmentalconditions; it has been well established that the patches of diseaseincrease in intensities for the rst few years and then decline inmonoculture due to rise of suppressive microorganisms (Cook,2003). Rhizomania, a well-known sugar beet (Beta vulgaris L.)soil-borne disease especially in U.K. and northern Europe which iscaused by the virus Beet necrotic yellow vein virus (BNYVV) andvectored by the plasmophorid soil-borne fungus Polymyxa betae

* Corresponding author. Tel.: 33 380 693 050; fax: 33 380 693 224.

Contents lists availab

Soil Biology &

.e ls

Soil Biology & Biochemistry 42 (2010) 1661e1672E-mail address: christian.steinberg@dijon.inra.fr (C. Steinberg).microorganisms. These microbial pathogens live in soil in thepresence or absence of their hosts, compete with microora andhave restricted means of spread over space and time, whichdepends on a number of biological and environmental factors(Foster, 1988). These facts grant an inherent epidemiological vari-ability to the diseases caused by soil-borne pathogens and uncer-tainty to the farmers about the severity of the disease in a givencropping season. Even though losses caused by these pathogens arehighly uncertain, soil-borne root diseases reduce yields consider-ably and the extent of disease attacks determines the yield losses

killed or stunted plants and vary in size. However, the symptomsvary with the type of disease and host species. Patches caused bysoil-borne pathogens are generally dynamic in the eld crops,changing their conguration from one season to another (Gilliganet al., 1996; MacNish, 1996; Schneider et al., 2001). Different soil-borne pathogens cause patches of disease with different charac-teristics and the dynamic nature of soil-borne diseases depends onthe species of microorganisms causing disease. For instance, take-all disease caused by G. graminis var. tritici (Ggt) occurs in patchesand the occurrence and spread of the disease is affected by variousSpatial dynamicsTemporal dynamicsPrimary infectionSecondary infectionPopulation dynamics of soil-borne plantpathogensEpidemiologyDisease suppressionPredictabilityBiological control

1. Introduction

Soil-borne root diseases are incitisms, mainly fungi and oomycetes,Gaeumannomyces graminis var. triticPhytophthora spp., and the viruses0038-0717/$ e see front matter 2010 Elsevier Ltd.doi:10.1016/j.soilbio.2010.05.013needed to investigate different mechanisms of parasitism deployed by different AGs in different hosts, itseems that many mechanisms external to the host are operating at the same time which necessitates anintegrative research approach to study and control the diseases caused by R. solani.

2010 Elsevier Ltd. All rights reserved.

soil-borne microorgan-ing Rhizoctonia solani,ium spp., Pythium spp.,red by the soil-borne

pathogens and the epidemiology of these diseases (Forster andGilligan, 2007; Gilligan, 2008).

One of the important epidemiological characteristics of soil-borne plant diseases is that they generally occur in patches (Belmaret al., 1987; MacNish, 1996; Pascual and Hyakumachi, 2000;Truscott and Gilligan, 2001). These disease patches compriseKeywords:

can be grouped into three main categories: host plant, pathogen and environment. However, each of thecategories in its detail may depend on or react with the other categories. There are a number of factorsAvailable online 27 May 2010 management strategy. The patchy appearance of the disease caused by this pathogen is well-known. Thepatches show within and between season dynamics. The factors which affect the spread of the diseaseReview

Build up of patches caused by Rhizocton

Muhammad Anees a, Vronique Edel-Hermann b, CaKohat University of Science and Technology, Kohat, Pakistanb INRA-Universit de Bourgogne, UMR 1229 Microbiologie du Sol et de lEnvironnement

a r t i c l e i n f o

Article history:Received 24 July 2009Received in revised form13 May 2010Accepted 13 May 2010

a b s t r a c t

Rhizoctonia solani is a comthese different AGs show dwith a wide spectrum of hbehaviour as a parasite. T

journal homepage: wwwAll rights reserved.solani

stian Steinberg b,*

SE, 17 rue Sully, BP 86510, 21065 Dijon, France

species that is composed of different anastomosis groups (AG). Althoughrences in their host ranges, generally R. solani is a phytopathogenic species. It has the ability to grow as a saprotroph, which further complicates itslosses caused by R. solani are very important and need a sustainable

le at ScienceDirect

Biochemistry

evier .com/locate/soi lb io

Biocalso occurs in patches (Tamada and Abe, 1989; Stacey et al., 2004).However, these patches only expand between the seasons (Tuitertand Hofmeester, 1992). In this review we will concentrate onR. solani which is a soil-borne phytopathogenic fungus that wasoriginally described by Julius Khn on potato (Solanum tuberosum)in 1858. It is frequently studied because of its ability to causedisease in diverse hosts resulting in considerable losses. R. solani isan imperfect, asexual form (anamorph) of Thanatephorus cucumeris(Frank) Donk (teleomorph). According to phylogeneticists(Gonzalez Garcia et al., 2006) the name T. cucumeris should now beused to designate R. solani, but for the sake of clarity, the termsR. solaniwill be maintained in this text. R. solani is a ubiquitous soilsaprotroph and facultative parasite (Ogoshi, 1996). It can growsaprotrophically in soil, on soil organic matter or plant debris(Papavizas, 1970). The history of R. solani is almost as long as thehistory of plant pathology. It is a diverse group of fungi and isdivided intra-specically mainly based on its hyphal anastomosisreactions (Ogoshi, 1996; Carling et al., 2002). Fourteen anastomosisgroups (AGs) have been dened to date. Complementary charac-teristics including morphology, virulence, host range, nutritionalrequirements, biochemical characteristics, molecular characteris-tics and DNA sequences have been used to further subdivide AG1eAG 4 and AG 6eAG 9 (Carling et al., 2002). R. solani causesdisease all over the world in all kinds of crops including forage,sugar, oilseed, ornamental crops and has a wide host spectrum(Bolkan and Ribeiro, 1985; MacNish, 1996; Wrather et al., 1997;Demirci, 1998; Ryder et al., 1998; Pascual and Hyakumachi, 2000;Hietala et al., 2005). The width of host range, however, varieswith the anastomosis groups. R. solani is a fungus that does notproduce asexual spores and therefore has no reliable means toensure its dispersal over long distances (Ogoshi, 1987). Sexualspores called basidiospores are rarely produced. Despite theabsence of spores, R. solani survives in unfavourable conditions byforming sclerotia containing a compact mass of mycelia or restingmycelia (Sumner, 1996). The inoculum density of R. solani is highlyvariable and is generally not correlated to the disease incidence(Kinsbursky and Weinhold, 1988) apart from specic situationsincluding AG 8 (Ophel-Keller et al., 2008). Most inoculum is presentin the top soil (MacNish and Dodman, 1987; Paula et al., 2008).

R. solani has been well documented in literature for productionof patches but it still remains to be demonstrated why thesepatches change their conguration from one season to another(Hyakumachi and Ui, 1982; MacNish, 1996; Schneider et al., 2001).It has been shown that such patches expand at different rates. Thesize of patches may vary from one to several tens of meters, andthey expand during the growing season according to the primaryinoculum density and the crop (MacNish et al., 1993). MacNish(1985a,b), for instance, showed that there could be dramaticchanges in area, size and shapes of patches in cereals caused byR. solani AG 8. Similar information was reported concerningR. solani AG 2-t in tulips (Schneider et al., 2001). Besides the natureof the crop, the expression of the disease varies according to thematurity of the plant (noticeable stunting of seedlings, temporarycryptic rotting of roots or crown of adult plants) making it difcultto estimate the actual size of the patches. Moreover, in many cases,many small patches may occur and merge (MacNish, 1996;MacNish et al., 1993). In the case of sugar beet crops, thesepatches are highly mobile and never occur in the same place wherethey were observed the previous year (Hyakumachi and Ui, 1982)while they are more stable in the case of wheat crops (Cook et al.,2002). Long-distance transmission is observed between seasonsand is generally attributed to water movement and mainly tomechanical dispersal of inoculum during harvest and cultivationprocedures (MacNish, 1996; Truscott and Gilligan, 2001; Gill et al.,

M. Anees et al. / Soil Biology &16622002). The production of patches with changing congurations isa phenomenon related to epidemics of soil-borne plant diseasesmainly caused by restricted dispersal of inoculum. Patches arisefrom the presence of natural primary inoculum carried over fromprevious crops in the eld. During the parasitic phase, this primaryinoculum infests the host plant, and then two types of strategy maybe used by the secondary inoculum of the pathogenic funguswithin the root system of the host plants. The rst one results inlocal increase of the inoculum through autoinfection of the hostplant i.e. multiple consecutive infections of the same host plantperformed by the pathogen developing itself in the close vicinity ofthe host plant, and the second corresponds to the short-distancetransmission through alloinfection between contiguous plants i.e.when the pathogen moves from one host plant to the next one.

For an efcient control of disease, it is important to know themechanisms underlying development and dynamics of thesepatches. Without such knowledge, we cannot restrict the pathogenfrom causing economic losses in all sorts of cultures. Themain focusshould be on understanding the factors that inuence the invasion,persistence and spread of the pathogenic strains, howandwhy theyoutcompete the microora, what controls the variability ofepidemics between one location to another as well as from oneseason to another and what makes the disease unpredictable(Gilligan and van den Bosch, 2008). These are the basic questionsthat need to be addressed for development of a durable control fora given soil-borne disease. The biggest obstacle in this direction isthe fact that R. solani is one of the most complex epidemiologicalsystems as described above. In the present review, we will explorethe literature for the mechanisms involved in spread of patchescaused by R. solani. Various factors involved in the spatial distri-bution of the pathogen and mechanisms proposed so far to explainthe dynamics of disease patches as well as its control strategies willbe reviewed.

2. Spatial distribution and spread of R. solani

Soil-borne pathogens have limited means of spread in the eldand it is usually the host plant that inadvertently grows towards thestationary pathogen (Gilligan, 1983). Therefore, spatial distributionof the inoculum in the eld is of crucial importance for soil-bornepathogens. This inoculum responsible for the start of the infectionis known as primary inoculum and the infection is known asprimary infection (Gilligan and Kleczkowski, 1997). Primary infec-tions may contribute to the patterns found in plant pathogeninteractions and is partially responsible for the dynamics of thedisease observed during the season (Burdon et al., 1989). Theprimary infection is of vital importance as small changes in initialconditions are later amplied during the course of epidemics(Kleczkowski et al., 1996). Once the infection process has begun,R. solanimaygrow fromone plant to another and spread the diseaseas well as the inoculum. This inoculum is known as secondaryinoculum and the infection incited by it is denoted as secondaryinfection (Gilligan, 2002). Secondary infection is responsible forthe distribution of the pathogen during the main growing season ofthe crop.

Thus the disease produced by R. solani depends upon balancebetween the primary and the secondary inoculum which areinterdependent (Bailey and Gilligan, 1999). Theoretically thequantity of primary inoculum is the sum of the disease producedand the saprotrophic growth until the end of the previous season aswell as the saprotrophic growth between the two seasons minusthe decay of the inoculum during intercrop period (Bailey et al.,2004). This principle is true for any soil-borne microorganismthat shows primary and secondary infection. The amount ofsecondary infection also depends on the biological and environ-

hemistry 42 (2010) 1661e1672mental conditions that can directly or indirectly inuence the rate

Biocof growth of the fungus. Because R. solani has the ability to grow inthe soil, secondary infection is of great importance. This differsfrom Rhizomania, where secondary infection is almost negligibleand the disease spreads mainly between the seasons. While in thecase of Ggt, being a poor saprotroph (Cook, 2003), growth in soil isnot that important, however, we cannot ignore the secondaryinfection caused by root to root contact of the host plants (Colbachet al., 1997).

The main question that needs to be addressed here is whatfactors affect the spatial distribution as well as growth and spreadof R. solani in the eld. These factors are very important to under-stand the disease epidemiology. For instance, in Rhizomania, theagricultural machinery plays the most important role in the spreadof disease while disease appearance is also dependant on thetemperature; hence disinfecting agricultural equipment andaltering sowing time have been reported to be benecial in controlof the disease (Blunt et al., 1992; Rush, 2003). On the contrary,R. solani is a facultative parasite (Ogoshi, 1996) and the fact that itcan grow both parasitically as well as saprotrophically has longbeen known (Garrett, 1970; Papavizas, 1970). It points towardsthree main factors responsible for patterns of the spatial distribu-tion and spread of the fungus: the host plant, the intrinsic char-acteristics of the pathogen and the environment.

2.1. Host plant

The presence of a susceptible host plant is necessary for thedisease to develop while the extent to which the disease spreadsdepends on the degree of susceptibility of the plant population.Here a few questions arise: Do all the plants in a given populationof hosts have the same degree of susceptibility? Does the suscep-tibility of a given plant towards R. solani changes with time? If thedegree of susceptibility varies among plants within a population,the ratio of the susceptible and resistant plants will explain theoutcome of the disease spread. There exists a threshold number ofsusceptible plants above which the pathogen may invade the eld.The presence of enough resistant plants (threshold density) maycompletely inhibit invasion by the pathogenic fungus (Bailey et al.,2000; Otten et al., 2004a). It is also important to know the factorsthat can alter the susceptibility of the plants including changes withthe age of the plant (Gibson et al., 1999), the genetic makeup of theplant (Fu et al., 2005), and the environmental factors (Shehata et al.,1984). Plants become more resistant with age and thus remainhealthy even in presence of the fungus. The most fatal is the earliestattack which causes damping-off leading to bare patches. Lateattack is in the form of root rot that may not kill the plant but atleast causes losses in yield. The genetic resistance/tolerance againstthe disease due to R. solani has been observed inmany crops such astobacco (Nicotiana tabacum), peanut (Arachis hypogaea), bean(Phaseolus vulgaris L.), rice (Oryza sativa L.), sorghum (Sorghumbicolour L.), and sugar beet (Montoya et al., 1997; Franke et al., 1999;Pan et al., 1999; Pascual et al., 2000; Scholten et al., 2001; Elliottet al., 2008). Recently, genetic resistance/tolerance has also beendeveloped in wheat (Triticum aestivum L.) against R. solani AG 8disease by using a chemical mutagenesis technique (Okubara et al.,2009). Such techniques could be helpful to create genetic resistancein different hosts against R. solani diseases. In the case of sugar beet,although the reduction of disease has been obtained using tolerantvarieties coupled with crop rotations (Buhre et al., 2009), completecontrol of the disease has not been accomplished so far. Some plantgenes are activated by pathogenic invasion resulting in an inducedresistance. In this case, the plants produce pathogenesis-relatedproteins (PR-proteins) that are involved in control of a wide rangeof pathogens including R. solani. These plant defence reactions have

M. Anees et al. / Soil Biology &been reported in rice, bent grass (Agrostis palustris Huds.) and inwheat (Datta et al., 1999; Fu et al., 2005; Kirubakaran et al., 2008).Environmental factors including temperature and moisture havebeen suggested to change the degree of susceptibility of the planttowards the disease (Shehata et al., 1984), however, the mecha-nisms have not been well demonstrated. From these facts it isapparent that the susceptibility of the plant is variable, changingwith time and environmental conditions as well as its interactionwith different microorganisms and therefore it can affect thedistribution of the disease in the eld (Bailey et al., 2000). It appearsthus that the host susceptibility is one single component of a morecomplex combination including on one side the climatic conditionsand the crop management and on the other side the soil inoculumpotential. The soil inoculum potential is certainly the component tofocus on. It will be detailed thereafter. It can be dened as anintegrative bio-indicator of the infectious activity the pathogenicpopulations may have in the soil according to their density, theirinnate saprotrophic and infectious capacity and the way the soilmicroora and the soil abiotic factors may regulate their develop-ment (Steinberg et al., 2007).

2.2. Intrinsic characteristics of the pathogen

It is quite important to know how R. solani survives in unfav-ourable environmental conditions. Unfavourable ecological condi-tions may comprise the absence of a susceptible host, lack ofnutrients, competition with microora, etc. These conditions areinterdependent and may not be separated from each other. Forinstance, presence or absence of the host may lead to quantitativeand qualitative changes in the availability of the nutrient resourcesfor the whole microora and may in turn be related to its compe-tition with the pathogen and dynamics of antagonistic microor-ganisms. For instance with Ggt the presence of susceptible host andvirulent pathogen is necessary to develop an antagonistic micro-ora (Raaijmakers and Weller, 1998; Walker et al., 2003). In somecases, such as in Rhizomania disease, survival of the pathogenicvirus is assured by the production of viruliferous spores by thefungal vector P. betae. These spores can survive up to 15 years in thesoil (Sayama et al., 2006). Conversely for Ggt, the survival phase isthe weakest part of the life cycle which offers good opportunitiesfor control (Cook, 2003). However in the case of R. solani, thesituation is more complex. R. solani may survive between consec-utive host crops as sclerotia in the organic matter or debris of theprevious years crop (Papavizas, 1968; Papavizas et al., 1975) andcan cause the disease in the following season. Because there arevarious AGs with overlapping host spectra, the soil inoculum ofR. solani is likely to nd a convenient host plant or related debris inwhich to survive without causing detectable damages. This is thecase for AG 2-2 which can cause small necroses on the roots ofmaize without affecting the yield but causing severe crown androot rotting of the subsequent sugar beet crop (Guillemaut, 2003).Thus, the broad host spectrum of R. solani helps it to survive forlonger periods of time. Briey, some AGs (AG 1, AG 2, and AG 4)have very wide host spectra (Ogoshi, 1996; Tewoldemedhin et al.,2006). On the other hand, host specicity has been reported forsome AGs (AG 3 and AG 8) at least in relation to the importantlosses they have caused in various crops (Ogoshi, 1996). R. solani AG3 can be considered as the anastomosis group having the narrowesthost range, causing disease in potato, tobacco and tomato (Solanumlycopersicum L.) (Kuninaga et al., 1997). R. solani AG 8 is known tocause important losses in cereals as well as in legumes (You et al.,2008), but it has been reported that the same AG can also infectthe broad leaf crops like mustard (Brassica hirta) and safower(Carthamus tinctorius L.) (Cook et al., 2002). Concerningwheat, bothAG 2-2 and AG 2-1 have been isolated from disease patches and are

hemistry 42 (2010) 1661e1672 1663highly pathogenic to wheat (Roberts and Sivasithamparam, 1986).

BiocSimilarly, the bulbous crops such as tulips can be infected by AG 2-t,AG 2-2, AG 4, AG 5 and AG BI (Schneider et al., 1997). On the otherhand, AG 2-t is also able to infect sugar beet, crucifers and lettuceseedlings (Lactuca sativa) in addition to bulbous crops. Despite thebroad and partially overlapping host spectra of the various AGs ofR. solani, no clear evidence about the ability of one AG or another todisplay patches at a greater extent than the others on similar hostplants has been determined so far. On the contrary the attentionwas brought to the environmental conditions that will allowa single population within a given AG to colonise the soil and newhost plants from a single infection focus (MacNish, 1996; Baileyet al., 2000).

Besides survival, the second important question regarding thepathogen is the rate of growth to produce secondary infection. Rateof growth of R. solani is variable on the surface of soil or through thesoil (Otten and Gilligan, 1998). On the soil surface it spreads aboutthree times faster than through the soil. The reason for decreasedrate of spread below the surface of soil is the limited supply of airand space. The infectivity of soil-borne fungi depends on theirability to grow on or through the soil (MacDonald, 1994) and tocompete for nutrient sources due to progressive changes in the hostplant resistance (Kleczkowski et al., 1996; Gilligan and Kleczkowski,1997; Gibson et al., 1999; Bailey et al., 2000). Hence, the dynamicsof epidemics are partially determined by the growth rate ofR. solani.

Another important factor is the competitiveness and virulenceof the pathogen in the given environment (Papavizas, 1970).However, although a continuum between virulent and avirulentstrains towards various hosts has been described among binucleateRhizoctonia (Herr, 1995; Sharon et al., 2007), less diversity in termsof hypovirulence has been depicted among the R. solani species(Cardinale et al., 2006). It has been shown for instance thata double-stranded (ds)RNA was associated with hypovirulencewithin AG 3 (Liu et al., 2003) but also that the occurrence, distri-bution, and genetic relatedness of dsRNA components were foundamong 36 isolates of R. solani belonging to nine anastomosis groups(AG) without any demonstration of a relationship between dsRNAand hypovirulence (Bharathan et al., 2005). Dark brown pigmen-tation of R. solani hyphae has been associated with melaninbiosynthesis that is considered important for its competitivenessand virulence (Hyakumachi et al., 1987; Kawamura et al., 1997; Kimet al., 2001). Melanin is also associated with the protection ofmicroorganisms against environment stresses such as UV light,temperature and solar irradiation (Durrell, 1964). It also providesresistance against microbial attacks (Lockwood, 1960). Furtherresearch is expected to better explain the role of melanin in viru-lence and the role of hypovirulence in the epidemiology of thedisease. More generally, although isolates of the binucleateRhizoctonia spp. and hypovirulent R. solani have been demonstratedto be effective in biocontrol of a range of hosteR. solani combina-tions (Sneh et al., 2004), neither mycoparasitism or antibiosis wereinvolved in biocontrol of R. solani byany of these isolatesmentionedin the literature. Moreover, their occurrence has rarely been asso-ciated to disease suppression in soil (Hyakumachi et al., 1990).

2.3. Environment

The biotic and abiotic components of the soil environmentconstitute a complex set of interacting factors which inuence thegrowth and spread of R. solani. Among biotic components, thewhole microora plays an important role in inuencing the growthof R. solani. The microorganisms are in fact regulating each other inthe microbiological environment. Increase in the pathogenicactivity of R. solani may lead to increase in activity of antagonistic

M. Anees et al. / Soil Biology &1664populations (Anees et al., 2010) that in turn may lead to reducedactivity of R. solani (Croteau and Zibilske, 1998). For example,pathogenic colonization may be restricted by competitive orantagonistic microorganisms that are present in the soil microora(Toyota et al., 1996). Microorganisms can limit the developmentand spread of R. solani either by the general microbial suppressionthrough exploitation of available global resources (Diab et al., 2003)or by specic suppression (Grosch et al., 2006). Specic microbialsuppression results from different antagonistic mechanisms suchas production of antibiotics (Arora et al., 2008), mycoparasitism(Rocha-Ramirez et al., 2002; Howell, 2003) or induced resistance(Harman et al., 2004; Shoresh et al., 2005). The most well-knownantagonists of R. solani reported so far are Trichoderma spp. andPseudomonas spp. (Scherwinski et al., 2008; Vinale et al., 2008;Scherm et al., 2009). Additionally Bacillus spp., Aspergillus spp.,Penicillium spp., binucleate Rhizoctonia spp., Gliocladium spp. andyeast spp. have also been reported (Mukherjee et al., 1995; El-Tarabily, 2004; Nicoletti et al., 2004; Jabaji-Hare and Neate, 2005;Mojica-Marn et al., 2008; Singh et al., 2008).

Because soil-borne pathogens live in soil, their activities arehighly affected by soil properties and the cultural practices thatdisturb the soil. Soil physical conditions play an important role inthe extent, rate and variability of mycelial growth of R. solani (Ottenand Gilligan, 1998; Otten et al., 1999). Texture, structure, moisture,nutrition of soil and tillage that dene soil physical conditions, haveprofound effects on the spatial distribution of R. solani. Concerningsoil texture, the disease spreads more in sandy soils than in soilswith heavy textures and the patches expand eight times faster insandy soils compared to heavy soils (de Beer, 1965; Gill et al., 2000).Indeed the rate of transmission of disease caused by R. solani ishigher in sand than in soil and even more in coarse sand comparedto ne sand (Otten et al., 2004b). Hence, the time required forgrowth and establishment of fungus in soil varies with different soiltypes (Gill et al., 2000). Of course soil structure has a major inu-ence on water and air movement, has a signicant role on rootdevelopment (Stewart et al., 1999), movement of nutrients(Shipitalo et al., 2000) and in turn on processes involving soilbacteria and fungi (Holden and Firestone, 1997).

The extent and rate of fungal growth may depend on the soilporosity because there is restricted space available which limits thespread of the hyphae of R. solani. R. solanimay preferentially followlarger pores and hyphal densities are higher in small holes incompact soils than in the bulk soil (Otten and Gilligan, 2006).Another feature of soil pores is known as tortuosity which is thenon-uniform nature of soil pores that depends on soil texture,structure and, for the air-lled pore volume, the degree of wetness.Tortuosity increases with increased degree of wetness by blockingthe air space. The geometry of the air-lled pore volume also limitsthe spread of the fungus. Connectivity and tortuosity of air-lledsoil pores may play important role in invasion of soil by R. solani(Otten et al., 1999). Primary infection is favoured by compacted,high-bulk density soils where fungi cannot spread easily andproduce locally higher biomasses while large pores permit moreexpansion and saprotrophic invasion that favours secondary infec-tion. Thus the air-lled pore volume is an important factor affectingthe strategies of fungal spread (Glenn and Sivasithamparam, 1990).Another important factor is soil moisture as growth and spread ofR. solani is favoured by drought (Smiley et al., 1996). High soilmoisture affects the development of disease caused by R. solani (Gillet al., 2001a) due to its inuence on growth and root colonization ofR. solaniwhichwill be discussed later (Shehata et al.,1984; Gill et al.,2001b).R. solani can growand infect the host plant at awide rangeofsoil temperatures andpH. Temperature ranging from20 to30 C andpH ranging from 4 to 8 may be considered optimum for growth ofR. solani in general (Dorrance et al., 2003; Grosch and Kofoet, 2003).

hemistry 42 (2010) 1661e1672However, the disease severity may vary at different temperatures

Biocwith different AGs (Kumar et al.,1999). For instance, AG8 is favouredby lower temperature ranging from 6 to 20 C while AG 11 isfavoured by temperature ranging from 20 to 25 C (Smiley andUddin, 1993; Kumar et al., 1999). Generally higher temperatures(>15 C) may expose the pathogen to microbial competition thatmay lead to general disease suppression (Smiley and Uddin, 1993;Gill et al., 2001b).

It will be worth mentioning the role of soil depth becauseactivity of R. solani is mostly conned to the top 10 cm and onlysmall amounts of the inoculum are found below 5 cm of depth ofsoil (Papavizas et al., 1975). In the Maryland soil where they didtheir experiments, Papavizas et al. (1975) were unable to detect anyRhizoctonia at 20e25 cm depth of soil. One of the possible expla-nations is accumulation of CO2 that has the capacity to inhibit thegrowth of R. solani in deeper fractions of soil (Papavizas and Davey,1962; Glenn and Sivasithamparam, 1990).

The distribution, size and quality of substrate present in the soilmay affect the activity of soil-borne fungal mycelia (Grifth andBardgett, 2000) and mycelial growth may be proportional tosubstrate availability. It is known that R. solani is able to translocatenutrients and spread them to some distance away from their source(Thornton and Gilligan, 1999; Jacobs et al., 2004). However, suf-cient nutrients lead to dense colonies while a lack of nutrientsmakes R. solani change its growth strategies to an explorative one(unpublished observations).

Cultural practices alter the soil structure and its physico-chemical properties, and thus have a considerable inuence on thefungal growth and spread. Minimum tillage increases somediseases as the crop residues left on the surface serve as a source ofnutrition for the soil-borne pathogens and provide favourableenvironments for their growth and nourishment (Rovira, 1986;Bockus and Shroyer, 1998; Cook, 2001) while tillage reduces thedisease both by fragmenting the mycelial network and by buryingthe residues (Pumphrey et al., 1987). However, tillage reduces thedisease but does not remove it completely and returning back to notillage, leads to revival of the disease (MacNish,1985b). On the otherside, a suppressive microora can also develop in the uppermostlayers of the soil where reduced tillage concentrated plant patho-gens. This microora may control the development of the pathogenthrough mycoparasitism, antibiosis or competition for space andenergy substrate in the root-zone and therefore prevent rootdiseases from developing (Alabouvette et al., 1996; Sturz et al.,1997). These contradicting statements highlight that the relation-ship between tillage and disease is not that straight forward.

Similarly, crop rotation has also been reported to have an effecton the disease. Disease intensity decreases with the increase inlength of crop rotation (Gilligan et al., 1996), but again the disease isnot completely controlled.

Application of herbicide and their time of application (Smileyet al., 1992), use of fertilizers (Srihuttagum and Sivasithamparam,1991) and manipulating the C/N ratio of the soil (Croteau andZibilske, 1998) have also been reported to reduce the growth andspread of R. solani; however, so far the mechanisms behind theseeffects are not clear. As far as use of fertilizers is concerned, the roleof nitrogen was considered important in disease control whichseems to be an indirect effect through improvement of plantgrowth (Papavizas et al., 1975). However, among nitrogen fertil-izers, there are contrasting reports of effect of form of nitrogenfertilization (nitrate or ammonium) on disease suppression (Elmer,1997; Rodrigues et al., 2002). Additionally, we can also nd an effectof sulphur and phosphorus fertilization (Srihuttagum andSivasithamparam, 1991; Klikocka et al., 2005). In general, theeffect of the fertilizers seems to be indirect through the host plant.

The ecological tness of the fungus is very important for disease

M. Anees et al. / Soil Biology &initiation and spread in the eld where a variety of biotic andabiotic environmental factors interact with each other as well aswith the inert growth and pathogenic capabilities of R. solani andthe plant hosts susceptibility. It seems that the multiple ecologicalrequirements of R. solani are able to compensate themselves whena few of them are not fullled by the environment, which mayexplain the large distribution of this fungus and the frequentoccurrence of Rhizoctonia patches. These observations suggest thatwe must consider how appropriate agricultural practices promoteconditions which may affect the soil inoculum potential towardsRhizoctonia disease.

3. Patchy nature of disease

The patterns of disease incited by R. solanimay be in the form ofpatches of either dead, chlorotic or stunted plants (Belmar et al.,1987; Gilligan et al., 1996; MacNish, 1996; Hyakumachi et al.,1998; Schneider et al., 2001). Patches usually have distinct edgesbetween the stunted plants and the normal sized plants in thesurrounding healthy area of the crops. Plants immediately outsidethe patch usually show no symptoms of the disease, but may haveconsiderable root rot that may be due to late infection (MacNishand Neate, 1996). A biochemical interaction of signals betweenroots and fungus has been suggested (Kirkegaard et al., 1995). Thepatch symptoms appear usually when the plants are young andsusceptible towards the disease (MacNish, 1996). Patch expressiondepends upon a combination of factors including the host suscep-tibility, the soil inoculum potential, the crop management and theenvironmental conditions along with the climatic conditions inrelation to the geographic location. This is the case for cereal rotcaused by R. solani AG 8. Disease prevalence is very high in thePacic Northwest USA and patches coalesce together (Smiley andWilkins, 1993) while in Australia there are distinct abrupt edgedpatches (Sweetingham, 1990). Patch size is highly variable anddynamic (MacNish, 1985a; Gilligan et al., 1996; Schneider et al.,2001; Cook et al., 2002). They are sometimes circular, but moreoften elongated in the direction of sowing which shows spread ofthe pathogen bymachines (Roberts and Sivasithamparam,1986). Ofcourse the machines used for soil cultivation also change the soilstructure which in turn affects disease. Certainly, the planteplantdistance in a given row is smaller than the rowerow distance in theeld, which may affect the patch shape or direction of diseasemovement. The patches caused by R. solani are dynamic in nature(Hyakumachi and Ui, 1982; MacNish, 1985a; Schneider et al., 2001).Thus the distribution, size, shape and number of patches varyconsiderably between seasons (Cook et al., 2002).

4. Mechanisms involved in dynamics of patches

Despite several decades of investigation, the mechanismsinvolved in the dynamics of disease patches caused by R. solani arestill unclear. R. solani presents a scenario in which the patchdynamics in various crops infected with various AGs have beenexplained (Table 1). An inherent complexity of this pathogen is thatit is a heterogeneous group of many different AGs. Additionally,the growth in soil, the broad host spectrum and the ability tosurvive in unfavourable conditions imparts further complications.Thus, a number of hypotheses have been proposed to explain themechanisms involved in dynamics of patches caused by R. solani.

One of the propositions to explain the patchy dynamics ofRhizoctonia diseases is based on the density of R. solani in the eld.de Beer (1965) demonstrated that there was more R. solani insidepatches than outside. He concluded that the pathogen is widelydistributed in the eld, but with higher concentration insidepatches, that may be due to some unknown stimulus. Higher

hemistry 42 (2010) 1661e1672 1665density inside patches being responsible for the disease is quite

rou

AG

AG

G 4,

Biocunderstandable and it has been recently reported that R. solani AG 8applied in higher densities in barley (Hordeum vulgare) causedmore disease (Schroeder and Paulitz, 2008). However, the basicquestion here is to know the reason for higher densities insidepatches that was denoted as unknown stimulus by De Beer.This unknown stimulus may be populations of antagonisticmicroorganisms involved in the dynamics of patches. In some casesthe expansion of patches may be due to receding antagonisticpopulations instead of advancement of the pathogen (Baker andCook, 1974).

Similarly, the disease suppression observed in a portion ofa sugar beet eld where there had been a major disease in theprevious year may indicate that an unknown type of biocontrol haddeveloped in that area (Hyakumachi, 1996). The host monoculturedecreased the disease pressure in the part of a wheat eld wherethere was higher disease the previous year. This observationsuggested that some components of the microora if not the whole

Table 1Factors involved in the dynamics of patches caused by Rhizoctonia solani.

Factors Host plant Anastomosis g

Stimulation of the growth of thepathogen inside the patch

Wheat, sugar beet AG 2-2, AG 8

Antagonistic microorganisms Wheat, sugar beet,potato

AG 2-2, AG 3,

Soil microbial diversity Potato AG 3Hypovirulence and accumulation

of double-stranded RNAPotato AG 3

Tillage Cereals, common bean AG 8, aAG e

Crop rotation Cereals, sugar beet, potato,common beans, carrot

AG 2-2, AG 3,

Soil moisture Wheat, potato, lupin, pea,rye grass

AG 1, AG 3, A

Soil texture Cereals, common beans AG 8, aAG e

Soil structure Barley AG 8Host susceptibility AG 2-1Temporal niche differentiation Bulbous crops AG 2-t

a Unknown AG.

M. Anees et al. / Soil Biology &1666reacted to the activity of the pathogen in relation with thesuccessive cultivation of the host plant and may have limitedfurther infectious activity of the pathogen (Lucas et al., 1993).Similarly in crops of ower bulbs, higher isolation of pathogen wasreported coupled with reduced disease pressures caused by AG 2-t(Schneider et al., 2001). Suppressiveness towards damping-offcaused by R. solani AG 4 in radish (Raphanus sativus) was articiallyestablished by successive weekly plantings of the host; the mech-anism involved was increased density of Trichoderma spp. insuppressive soils as compared to the conducive soils (Henis et al.,1978). When these Trichoderma spp. were added to conducivesoils in the same densities as observed in suppressive soils, thesuppression was achieved (Liu and Baker, 1980). Similarphenomenawere observed in a sugar beet eld where soil from thepatches of disease caused by R. solani AG 2-2, had higher density ofthe pathogen but was more suppressive towards the disease thansoil originating from healthy areas (Guillemaut, 2003; Anees et al.,2010). This higher suppressiveness was related to the increasedactivity of antagonistic populations especially Trichoderma spp. Theisolates originating from the disease patches showed relativelyhigher antagonistic potential than isolates in healthy areas (Aneeset al., 2010). The inuence of the antagonistic fungi, Trichodermaharzianumwas also reported on dynamics of R. solani in potatoes inthe initial stages; however, the effect could not be seen in the laterstages of plant growth and it was suggested that the pathogenicfungus had overcome the antagonist (Wilson et al., 2008). Apartfrom Trichoderma spp., the microbial diversity of Bacillus andPseudomonas communities was related to the suppression ofdisease caused by R. solani AG 3 in potato, although the suppressiontests were performed in vitro (Garbeva et al., 2006). The microbialdiversity in general is also related to the increased suppressivenessand disease control which itself is inuenced by the host species(Picard et al., 2004) as well as by the cultivation methods (van Elsaset al., 2002). Thus, cultivation of a specic crop affects the microbialdiversity and a specic suppression may be achieved. Hence, it isclear that increased antagonistic activity may be one of the reasonsfor the changing congurations of the patches. As the presence ofantagonists has been reported in different crops diseased withdifferent AGs, this phenomenon could be considered for diseasescaused by all AGs of R. solani.

The changes in patch conguration can also be attributed to thetillage effects that may cause changes to the inoculum potential as

ps (AG) References

(de Beer, 1965; Anees et al., 2010)

4, AG 8 (Baker and Cook, 1974; Liu and Baker, 1980; Hyakumachi, 1996;Cardinale et al., 2006; Wilson et al., 2008)(van Elsas et al., 2002; Garbeva et al., 2006)(Hyakumachi et al., 1990; Jian et al., 1997; Sneh et al., 2004;Lakshman et al., 2006)(MacNish, 1985b; de Toledo-Souza et al., 2008;Schroeder and Paulitz, 2008)

8, aAG e (Davis and Nunez, 1999; Larkin and Honeycutt, 2006;Schillinger and Paulitz, 2006; Larkin and Grifn, 2007;de Toledo-Souza et al., 2008; Buhre et al., 2009)

AG 8, AG 11 (Shehata et al., 1984; Lootsma and Scholte, 1997;Gross et al., 1998; Kumar et al., 1999; Gill et al., 2001a)(de Beer, 1965; MacNish and Neate, 1996; Gill et al., 2000;de Toledo-Souza et al., 2008)(Otten and Gilligan, 2006; Schroeder and Paulitz, 2008)(Bailey et al., 2000)(Schneider et al., 2001)

hemistry 42 (2010) 1661e1672in case of cereals (MacNish, 1996). Soil tillage may affect thepathogen directly but it could also have an effect on conducivenessor suppressiveness of soil because compaction increases diseaseand mixing reduces it (MacNish, 1984; Schroeder and Paulitz,2008). The effect can be explained by decomposition of thedebris and residues of crop that harbour the soil-borne pathogensbecause biomass decay is maximum with conventional tillage(Almeida et al., 2001). With no tillage, the percentage of organiccarbon increases in the top 0e5 cm (Schillinger et al., 2007) whichis the main part of soil where most of R. solani inoculum is found.That is why the soil-borne populations of Rhizoctonia spp. weremore abundant in the no tillage areas in Brazil (de Toledo-Souzaet al., 2008). Apart from this, a number of explanations about thedisease reduction by tillage are given in the literature such asbreaking the contacts between hyphae and nutrient sources andhence reducing the soil inoculum potential (McDonald and Rovira,1985), reducing macropores that are usually used by the fungus togrow (Otten et al., 1999) and increasing soil tortuosity (Rosebergand McCoy, 1992). In brief, there is an increased probability ofexposure of R. solani to microbial competition and antagonisticattacks. Tillage also plays an important role in the dispersal of theinoculum. Indeed, the patches of disease caused by R. solani AG 8 inwheat expand along the direction of cultivation or machinemovement that suggests the dispersal of the pathogen bymachines(MacNish, 1985a).

BiocNevertheless R. solani has a broad host spectrum; crop rotationhas also been reported to decrease intensity in some of the recentreports (Table 1). For instance, the disease intensity reduced whenwheat was grown in rotation with barley (Schillinger and Paulitz,2006) or by green manuring with mustard (Brassica sp.) in potatocropping (Larkin and Grifn, 2007) or by growing sugar beet afterwheat (Brantner and Windels, 2008). Of course, the duration ofrotation can also be an important factor (Peters et al., 2004).However, the increased suppressiveness by monoculture as abovehas been well described in literature. Which mechanisms can bebehind the reduction of disease by crop rotation or by monocultureare not well demonstrated. The characteristics of the soil microbialcommunity including microbial activity and diversity, and pop-ulation of benecial organisms may be improved by cropmanagement practices that include crop rotation and the choice ofhost as an important factor (Larkin, 2006).

The soil structure has a major inuence on the proliferation ofR. solani observed in barley infestedwith R. solani AG 8 inwhich thepathogen grew faster in the soil core containing untilled soil(Schroeder and Paulitz, 2008). This effect was specic to R. solani asR. oryzae had similar growth in both cases i.e. tilled and non-tilledsoil cores. Similarly the soil texture also affects the patchy nature ofdisease caused by R. solani AG 8 inwheat that was reduced in heavysoils as explained earlier (MacNish and Neate, 1996).

Changes in patch conguration in cereals between seasons mayalso be due to changes in environmental factors such as soilmoisture whichmay allow expression or suppression of the diseasecaused by R. solani present at different amounts of inoculum (Gillet al., 2001a). Decrease in disease over time has been reported insoil cropped with potato infected with AG 3 or with lupins (Lupinusangustifolius L.) infected with AG 11 when soil moisture increased(Lootsma and Scholte, 1997; Kumar et al., 1999). An increasedmicrobial activity at higher soil moisture contents or highertortuosity of soil or both can explain the reduction of diseasecaused by R. solani (Otten et al., 1999; Gill et al., 2001b). An inter-action of soil temperature and moisture has also been reportedwhere suppression towards the disease was higher at temperatureshigher than 15 C at higher moisture contents coupled with highermicrobial activity (Gill et al., 2001b). It means that the microbialactivity may be the principal effect of the higher moisture contentson the disease occurrence followed by soil tortuosity. However,there are reports where the disease intensities increase with highermoisture contents (Shehata et al., 1984; Gross et al., 1998). Hencethere are contrasting reports for the effect of soil moisture ondisease intensity, for instance in beans (Paula et al., 2007). Althoughthere is no agreement for the effect of soil moisture in the literature,it is obvious that the soil moisture plays an important role indening patch dynamics. The mechanisms involved in this direc-tion are to be demonstrated. From the above, it is clear that theenvironmental and the soil related factors as well as tillage and croprotation could have an inuence on the diseases caused by variousAGs in different host crops.

The competition and the temporal niche differentiation are themechanisms proposed to explain the dynamics of Rhizoctonia barepatches in ower bulbs caused by AG 2-t (Schneider et al., 2001).Microbial competition perhaps induces the replacement of AG 2-tisolates of R. solaniwith other AGs or other microorganisms that arenot virulent towards bulbous crops and there are series of nichesavailable for a succession of microorganisms to colonise one afteranother in the same location, depending on soil temperature andthe developmental stage of the host plant. However, this hypoth-esis needs further verication among other AGs also.

Accumulation of hypovirulent strains in the disease affectedareas can lead to disease suppressiveness followed by disease

M. Anees et al. / Soil Biology &dynamics. For instance, accumulation of hypovirulent strains hasbeen proposed in disease decline caused by AG 2-2 in sugar beetmonoculture (Hyakumachi et al., 1990). The virulence of fungi hasbeen shown to be diminished by nuclear or cytoplasmic factorssuch as viruses, virus-like particles carrying genetic materialknown as double-stranded RNA (dsRNA) (Elliston, 1982). There arecontradictory reports in literature about the role of dsRNA in thedecreased virulence in R. solani. For some specic strains of AG 3,a direct relationship was shown between virulence and the pres-ence or absence of dsRNA (Jian et al., 1997). Others have reportedthe presence of dsRNA as a common characteristic of R. solani in allAGs with no direct correlation with virulence in this pathogen(Kousik et al., 1994; Bharathan et al., 2005).

It is also possible that evolutionary changes in pathogens mayoccur along a time scale and selection favours non-virulent strainsof the pathogen in susceptible populations of host plants and viceversa (Thrall and Burdon, 2003).

While discussing the different probable mechanisms that maybe involved in the dynamics of a patch, it is important to know therole of primary and secondary infection in the development ofa patch. It is suggested that the patches of disease are predenedand are likely to be determined by saprotrophic growth of inoc-ulum from previous infections while primary infections dominatean epidemic development (Gilligan and Kleczkowski, 1997; Gillet al., 2002). The proposition is based on the assumption thatcontrary conditions may be required for the spreading of R. solani inthe eld and for its growth and increase of biomass which isconsidered essential for the host infection upon contact with roots(Gilligan and Bailey, 1997; Otten et al., 1999). For instance, highmoisture blocks the aeration channels and increases their tortu-osity thus prohibiting the further spreading of the fungus due to thereduction in the total volume of air-lled pores. As a result thefungus grows and increases its biomass without spreading toomuch (Otten et al., 1999). Hence, the patches may result fromoverwintered inoculum at the onset of favourable conditions andsymptoms rapidly develop giving an expression of expandingpatches (Aoyagi et al., 1998). But, it has been mentioned earlier thatthe higher moisture conditions also inhibit the disease infectionand secondly, it is also known that the disease occursmore in sandysoils than in heavier soils. Of course, the sandy soils have less waterholding capacity and hence decreased tortuosity which encouragesthe fungal spread. Another argument is the limited time availablefor the fungus during the season that may not be sufcient to grow,spread and attack the roots that necessitate a predened structureof mycelial network before the start of the season (Gill et al., 2002).This argument was based on experiments in which articiallydesigned pots with two compartments were used; one of the twocompartments was infested articially with R. solani AG 8 atdifferent times before and after sowing, and the other compartmentremained uninfested, although the fungus could approach it bygrowing across the walls of the compartments. In these experi-ments, less diseasewas observed in the non-infested compartmentswhen the fungus was inoculated at or after the time of sowing.

It seems that the patch development of R. solani in various cropsis the result of both primary and secondary infections. However, itis very difcult to quantify the primary and secondary infectionseparately. Of course, the higher primary inoculum should result inhigher primary and secondary infections. The rapid demarcationsof the patches are explained by the fact that the young roots aremore sensitive to pathogen attacks and the aggressiveness ofR. solani towards plants decreases with plant maturity or in otherwords, plants may become more resistant or the rhizosphere mayhave been occupied by another microbial community (Gill et al.,2002). There may exist a threshold distance between infectedplant and susceptible plant for fungal spread below which it may

hemistry 42 (2010) 1661e1672 1667invade and above which nite patches develop (Bailey et al., 2000).

BiocHence the fungus spreads and causes the disease up to the time thatthe plants are susceptible and this creates a border line betweenhealthy and disease plants, so that nite growth of fungus due tounavailability of more susceptible plants may prevent furtherexpansion of the patch. Although the fungus may continue to growin the soil it may not contribute to the development of bare patchesduring the season. Such growth, if it survives between the seasons,becomes the primary inoculum for the next season and it mayincrease the patch area in the following season. Here the questionwill be again about the presence or absence of R. solani as we knowthat the mere presence of the pathogen may be considered asa powerful indicator of the disease in the given area (Anees et al.,2010). The respective role of the primary and secondary growthof R. solani in situ in natural soil as well as the accurate identica-tion of the mechanisms involved in the spread and dynamics ofpatches remain to be determined. The problems then become howto record the growth and intensity of the fungus and how todifferentiate the primary infection from secondary infection.

Apparently, there is no single mechanism but rather a group ofmechanisms in operation dening the patch dynamics within andbetween seasons. The expression of these mechanisms dependson i) the host spectrum of susceptible plants, ii) the ecologicaltness of R. solani to the soil environment including the physico-chemical and the biotic factors which are in turn subdivided intogeneral and specic suppressive parameters, and iii) the agricul-tural practices including tillage system, rotation scheme andmanagement of the residues. These factors are interacting andfocusing on their individual effects on the disease expression leadsto the contradictory results that we have recorded so far. This iswhy an integrative strategy is the best way to approach andunderstand the environmental conditions which will determinethe behaviour of R. solani.

Of course, acquiring knowledge of the mechanisms involved isof utmost importance to control the disease. In Rhizomania diseaseof sugar beet, it has been reported that the patch expansion duringthe season is almost negligible because P. betae, the fungus carryingthe virus cannot grow saprotrophically in the eld (Rush, 2003).The patch dynamics are due tomovement of the viruliferous sporesof P. betae between seasons (Sayama et al., 2006). The diseaseappears as soon as the threshold limit of inoculum density is ach-ieved in the eld and hence, it may take many years for infection tobecome visible after invasion of the pathogenic viruliferous fungalvector (Gilligan and van den Bosch, 2008). So during this prepa-ratory period, there is the danger of the inoculum being dispersedby agricultural machinery to the surrounding healthy areas.Therefore, the control strategy for the Rhizomania disease shouldbe designed with all these factors in mind. Similarly, in the take-alldisease in cereals the disease intensity increases for the rst fewyears in monoculture and then declines due to an increase in thepopulation of antagonistic microorganisms e.g. 2,4-diacetylphlor-oglucinol producing Pseudomonas spp. that suppress the pathogenand control the disease in the coming seasons if present abovea threshold inoculum density (Raaijmakers and Weller, 1998). Thiscase study has been well documented in the literature and thedisease suppression by host monoculture is known as take-alldecline (TAD). However, TAD can only be established by mono-culture of the host crop but if the host crop is replaced by a differentcrop, the soil suppressive effects are reversed leading to increasedconduciveness. Additionally, the mechanisms that trigger theantagonistic bacterial secondary metabolism in the rhizosphere toproduce the antibiotic compounds are still obscure (Haas and Keel,2003). That is why their use as biocontrol agents against take-alldisease has not shown consistent results. Nevertheless, it ishypothesized that Pseudomonas spp. may be activated to produce

M. Anees et al. / Soil Biology &1668antibiotics by root exudates and the root exudates may beinuenced by the pathogenic activities (Walker et al., 2003).Acquiring the knowledge of such a mechanism in TAD seemsimportant to establish a consistent biocontrol of take-all disease.

5. Disease control

A variety of measures have been reported in the literature tocontrol the disease. As far as chemical control is concerned, con-trasting reports can be found. None of the available seed treatmentfungicides move systemically to roots (Paulitz et al., 2002). Severalfungicides that exhibited activity against R. solani AG 8 in thelaboratory were ineffective in eld trials (Smiley et al., 1990; Cooket al., 2002). No change or rather increase in root rot activity wasobserved with fungicide seed treatment in wheat (Smiley et al.,1990; MacNish and Neate, 1996). In plants cropped for owers,Rhizoctonia disease is mainly controlled by full eld application offungicides or by the soil disinfection that is not environment-friendly. In conclusion, there is no single method of chemicalcontrol of epidemics caused by R. solani that is effective, econom-ically practical and environmentally safe. Cultural practices that canbe used mainly include tillage (Roget et al., 1996; Smiley et al.,1996), disruption of soil in the seed zone during seeding andplacement of fertilizer below the seed in direct seeding crop (Rogetet al., 1996; Cook et al., 2000), paired rows of wheat in eld (Cooket al., 2000), starter fertilizer in wheat (Patterson et al., 1998) andapplication of N to reduce Rhizoctonia bare patch in some cases(MacNish and Neate, 1996). Crop rotation has also been reported todecrease the disease in various AGs as described earlier, however, itcannot be used alone to control the disease because the pathogenhas a wide host spectrum and can escape even the long rotations(Balali et al., 1995). Biological control is an important measure thatmay be exploited in future as it may control the disease withoutharming the environment. There are many reports of biocontrolusing various microorganisms, Trichoderma spp. and Pseudomonasspp. being the most important. Biocontrol comprises mechanismssuch as antibiosis, siderophore production, induced resistance, andcompetition (Kloepper et al., 1980; Cardoso and Echandi, 1987;Harris et al., 1997). However, no major successes with thesemechanisms have been reported in eld trials. Earthworms(Apporrectodea trapezoids) have also been reported to reducedisease on wheat and in pastures (Stephens and Davoren, 1997).No or partial host resistance is observed but that is not sufcientfor complete control of the disease. Finally, monoculture ofa susceptible host leads to Rhizoctonia disease decline presentinga natural way of disease control involving the accumulation ofantagonists (Hyakumachi, 1996; Wiseman et al., 1996) but obvi-ously, it is not perennial or reliable as it depends on too manyuncontrolled variables. Many mechanisms seem to operate hencewe need an integrative approach for this purpose. For instance,recently it has been shown that the combined use of crop rotation,cultivation and resistant cultivars of sugar beet reduced the severityof the disease caused by R. solani AG 2-2 (Buhre et al., 2009). Suchan integrative approach will be much more fruitful if we canunderstand the different mechanisms underlying the epidemic.

6. Conclusions

Wehave seen above that there are a number of mechanisms thatmay be involved in the disease expression and dynamics. They bothdepend on the plant susceptibility and the population dynamics ofR. solani, the latter being regulated by the biotic and abioticcomponents of the soil, which in turn are a result of agriculturalpractices. Modelling is probably the only approach that can inte-grate these variables and identify their respective role in given

hemistry 42 (2010) 1661e1672climatic and geographical conditions.

there are numerous factors that need further understanding.

Biochemistry 42 (2010) 1661e1672 1669Therefore, one nds very limited number of reports about model-ling of this pathogen and most of them come from the group ofCambridge University who introduced the concept of pathozone(Kleczkowski et al., 1996; Bailey and Gilligan, 1997; Gibson et al.,1999; Bailey et al., 2004). The concept of pathozone has beenintroduced as a theoretical area around the root where the path-ogen must be present to cause the disease (Gilligan and Bailey,1997). The pathozone is a convenient way to summarize thecomplicated growth dynamics through soil and soileplantepath-ogen interactions, including the variation that is characteristicallyassociated with these processes (Otten and Gilligan, 2006). Thisconcept was used to model the extent of the biological control ofR. solani attacking radish (R. sativus) seedlings by Trichoderma viridein microcosms (Bailey and Gilligan, 1997). The authors showed thatthe antagonistic fungus reduced the pathozone of radish seedlingsfor R. solani. They modelled the interaction of T. viride and R. solanibut did not take into account the microora, which needs to bedone. The models have not been validated in the eld so far. Theyneed to be included inmore global models, focusing on the plot, theeld or the landscape, taking into account the main mechanismswe underlined previously (i.e. the plant susceptibility, the ecolog-ical tness of R. solani and the agricultural practices) in the frame ofan integrative approach. An epidemiological study was conductedin a sugar beet eld andmodels were tted to plant data to describethe positive role of mustard as an intercrop on the disease severity(Motisi, 2009). Unfortunately, the soil microbial components werenot explicitly considered in this study, limiting thus the signicanceof the conclusions drawn concerning the mechanisms involved inthe control of the disease. On the other side, the populationdynamics of R. solani, the structure of soil microbial communitiesand the evolution of the soil inoculum potential to R. solani diseaseswere measured in situ without the measure of the disease severityin the crop above ground in a similar study (Friberg et al., 2009). Inthe latter case, the authors had to conclude in terms of risks aboutthe benets and putative negative impacts brought by the incor-poration of mustard in the wheat-sugar beet rotation.

The above example showed the point of combining eldobservations to take into account the epidemic behaviour asrevealed through the plant health and the epidemic processes asrevealed through primary and secondary infections resulting fromthe population dynamics of the pathogen. This example demon-strates even more the need for understanding the mechanismsdetermining the population dynamics in the soil environment toelaborate the appropriate epidemiological theory and to explainthe dynamics of the patches. The knowledge of these mechanismsis vital to develop a control strategy adapted to the ecology of thepathogen of interest because the epidemiological theory does notstand equally to TAD, Rhizomania or R. solani diseases. Data fromboth eld and meso- or microcosm experiments are required tomodel the whole process including soil microbial ecology and theprevailing fungal penetration in the plant to accurately predictthe fate of the disease, and ultimately to optimize the controlpractices.

Acknowledgements

The authors are grateful to the review editor and the twoanonymous reviewers for their helpful comments and suggestionsModelling represents a powerful tool to predict populationbehaviour based on the individual behaviour. However, thepredictability of a system depends on the extent to which knowl-edge have been acquired and integrated. In the case of R. solani,

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