American Journal of Plant Sciences, 2013, 4, 2240-2258
Published Online November 2013 (
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia
Gyula Oros1*, Zoltán Naár2, Donát Magyar3
1Plant Protection Institute, Hungarian Academy of Sciences, Budapest, Hungary; 2Department of Microbiology and Food Technol-
ogy, Eszterházy Károly College, Eger, Hungary; 3National Institute of Environmental Health, Budapest, Hungary.
Email: *
Received September 22nd, 2013; revised October 20th, 2013; accepted October 30th, 2013
Copyright © 2013 Gyula Oros et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Response of 19 wheat varieties cultivated in Hungary varied within large limits to soil borne Rhizoctonia infection. The
most frequent symptom, usually leading to damping off was the root neck necrosis. Four significant factors influencing
the susceptibility of wheat comprised 71% of total variation but none of them was dominant. The inhibition of devel-
opment of survivors in Rhizoctonia infested soil correlated with overall susceptibility of variety concerned. The varie-
ties Emese, Kikelet and Palotás are proved to be less susceptible, but none of the varieties could be certified as tolerant.
No relationships were revealed between pathogenicity of 26 Rhizoctoni a strains studied and their taxonomic position or
origin. The anamorph strains of Athelia, Ceratobasidium, Ceratorhiza and Waitea similar to Thanatephorus ana-
morphs selectively infected the wheat varieties, but the syndromatic pictures were undistinguishable with unarmed eye.
R. solani was proved to be more aggressive against germinating wheat than R. cerealis . Nine significant factors influ-
encing the virulence of Rhizoctonia strains comprised 82% of total variation, and six of them influenced exclusively
Thanatephorus anamorphs.
Keywords: Wheat; Rhizoctonia ; Tolerance; Brown Patch; Soil-Borne; Virulence
1. Introduction
In August 2002, brown patches were observed on turf
grasses in parks at four locations in Budapest. The symp-
toms observed were necrotic lesions on the roots and
stems, as well as brown lesions on the leaves. Two types
of sclerotia, nearly globose, pinkish to orange and ir-
regularly shaped, dark brown were found on roots. On
potato dextrose agar fast growing, colourless colonies with
small reddish/coloured scelrotia uprose of the first type.
This fungus was identified as Rhizo ctonia zeae Voor-
hees (teleomorph Waitea circinata Warcup and P.H.B.
Talbot) [1]. Buff-coloured, fast growing colonies of
Rhizoctonia solani Kühn (teleomorph Thanatephorus cu-
cumeris (A.B. Frank) Donk) arose of the second type.
The study of more than 150 plant species cultivated in
Hungary [2] revealed that R. zeae attacked monocotyle-
donous species more aggressively than dicotyledonous
ones, contrarily to R. solan i. This latter species was for-
merly reported as pathogen of winter wheat [3] and oat
[4] in Hungary.
Traditionally, farmers paid little attention to field dam-
age caused by soilborne Rhizoctonia infection in wheat,
because either seedborne or airborne fungi (rust, mildew,
smut etc.) infecting stem, leaves and spikelets had been
the main constrains of yield. Due to success in breading
and arousal of new synthetic fungicides, these fungi
presently do not cause catastrophic yield losses. However,
in the last two decades increasing number of papers was
published on yield losses (30% to 50%) caused by
Rhizoctonia species [2,5] in main wheat cultivating areas
[6-8]. In Europe and North America winter wheat suf-
fered mainly of R. solani AG-8 strains [7] with the R.
cerealis [6-8], while in Australia AG-1 and AG-8 and in
Turkey five different anastomosis groups of R. solan i
[9,10] were revealed. In South Eastern Hungary damage
by the R. cerealis and R. solani has been observed in
spring wheat [3].
Rhizoctonia species are well known soil borne patho-
gens frequently causing damping off prevalently in moist
and cool conditions that are the main stress factors re-
*Corresponding author.
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection 2241
quested to induce disposition to increased susceptibility
of potential host plants [11]. These species have no vege-
tative bodies for spreading, but infected seeds and propa-
gating material can distribute infecting propagula. The
disease is more severe in sandy soils, as the fungus can
grow more rapidly [12], and the hyphae tend to colonize
rhizoplane reducing the vitality of plant even without
penetrating into tissues. Infection cushions are formed on
the surface before individual hyphae penetrate with mi-
nor morphological modifications [13]. The ability to pro-
duce discrete appressoria is highly variable and regulated
seemingly by numerous factors. Hyphae may penetrate
without an appressorium through stomata or wounds [14-
16]. All Rhizoctonia species are obligate aerobic fungi,
which are habiting mainly in rhizosphere, however, they
may survive as saprobionts in the upper layer of the soil
forming a mycelial web, thus the undisturbed soil enhance
the risk of the infection of young roots [17]. Rhizoctonia
root rot is more frequent and severe under reduced or
conservation tillage [18,19] as the conventional tillage
disrupts the mycelial web [20]. This underlines the im-
portance of the elaboration of new root health manage-
ment practices, because formerly minor pest problems,
such as Rhizoctonia root rot of wheat became major
problems. In last two decades new research has been
started and several hundred scientific papers reported
data on etiology of root rot and sharp eyespot caused by
Rhizoctonia species, on genetic background of suscepti-
bility of wheat as well as on Rhizoctonia virulence. Ac-
tually, we can conclude that environment dependent
mechanisms regulate the progress of this disease with
complex etiology that is not under gene for gene control
[21], and further research is requested to understand the
multicomponent syndromatic picture.
The disease caused by R. zeae was described for the
first time in Florida, by Voorhees in 1934 [22], as scle-
rotial rot of corn. Since that this fungus distributed in
temperate regions, in Europe firstly reported in 2004 [1].
In a host-range study, the isolate proved to be highly
pathogenic to germlings of several ornamental and culti-
vated plants, including Beta vulgaris ssp. vulgaris , Cal-
listephus sinensis, Dahlia variabilis, Daucus carota, Lu-
pinus polyphyllus, Papaver somniferum, Pennisetum glau-
cum, Phaseolus vulgaris, Sesamum indicum, Solanum
melongena, S. tubero sum, Sorghum bicolor and Triticum
aestivum [1,2,23]. The estimation of risk on wheat pro-
duction caused by this pathogen was the aim of our work.
Actually, both seed and soil borne infections might be
well controlled in early stage of germination with seed
dressing [24], however, we have no effective methods
with reliable cost/benefit ratio for protection of wheat
against Rhizoctonia during the vegetation. Although min-
eral nutrients can manipulate the reaction of plants [25],
such treatments can not combat serious yield loss. Sev-
eral attempts were made to explore antifungal potential
of eubiotic preparations and to desing suppressive soil
[26-32], however, in order to prevent the harm, these de-
velopments have had not satisfactory results. In the case
of soil-borne infections correlative influences among
members of microbial consortia associated to potential
host plant may influence both the invading pathogen and
disposition of potential host to adverse factors of envi-
ronment thus change both the virulence of pathogen and
the susceptibility of host to pathogen at any time de-
pending on the genetic potential of these partners. Due to
complexity of interactions there is difficult to predict the
success of biocontrol measures. Currently the effective
protective method is the appropriate crop rotation, and
the breeding of wheat cultivars for improved tolerance to
factors inducing disposition to increased susceptibility to
the presence of Rhizoctonia in the soil can be considered.
Our objectives of this study were the comparative
evaluation of responses of germinating wheat seeds to
Rhizoctonia strains of various origin and taxonomic posi-
tion as well as to reveal patterns in factors influencing
the wheat/Rhizoctonia interaction.
2. Materials and Methods
Greenhouse experiment was undertaken to compare the
infective potential of R. zeae strain with 25 Rhizoctonia
strains of various taxonomic position. Susceptibility of
two sortiments of Triticum aestivum L., moreover, T.
monococcum L., T. turgidum L. and four small seed
grains were involved into the tests. No seed dressing or
any other manners to depress the microbiota of sper-
mosphere were applied. The potting medium was made
by mixing forest soil with peat before autoclaving (1.15
atm per 20 min), at the ratio of 3:1.
2.1. Test Plants
Seeds of wheat varieties (Table 1) were gifted by Elit-
mag Kft (Martonvásár, Hungary). Except Alkor (Triti-
cum monococcum L.) and Hegyes (T. turgidu m L.) all are
T. aestivum L. cultivars. Small seed grains Eleusine
coroacana Gaertn., Panicum milliaceum L., Phalaris
canadiensis L. and Setaria italica (L.) P. Beauvois were
purchased of the market (HERMES Ltd., Budapest, Hun-
2.2. Test Fungi
Rhizoctonia strains were originated of different locations
and various hosts:
Rhizoctonia solani strains of CBS collection: B-415
(AG-1, Pinus sylvestris L., Canada, CBS 522.96), B-432
(AG-2, Daucus carota L., Netherlands, CBS 326.84),
B-446 (AG-3, Solanum tuberosum L., Spain, CBS 117248),
B-417 (AG-4, Citrus sp., Argentina, CBS 341.35), B-430
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
Open Access AJPS
Border limits of the scale of evalutaion: 0 = all germlings killed, 5 = all seedlings survived. (1) Wheat varieties; T. monococcum cv Alkor, T. turgidum cv Hegyes and all others are T. aestivum. (2) Strains 1-13 refer to
anastomosis groups AG-1-AG-11 and AG-E of R. solani of CBS collection, respectively, strains 14-20 are Hungarian isolates of R. solani and R. stahlii (21); all are Thanatephorus anamorphs. Rhizoctonia strains
22-26 are anamorphs of Waitea (22), Cerathorrhiza (23, 24), Ceratobasidium (25) and Athelia (26), respectively. (3) Code; accession numbers of the Mycological Collection of Plant Protection Institute HAS
. The bold labelled strains had been isolated of wheat.
tomless = no visual s
toms observed at 8th da
= no one survived over 8th da
Table 1. Evaluation of the response of wheat varieties to soil borne Rhizoctonia infection.
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection 2243
(AG-4, Phaseo lus sp., England, CBS 340.51), B-418
(AG-5, Zeae mays L., Netherlands, CBS 339.84), B-419
(AG-6, Conyza canadensis (L.) Cronquist, CBS 137.82,
USA), B-420 (AG-7, soil, Japan, CBS 214.84), B-421
(AG-8, Triticum aestivum L., Australia, CBS 101782),
B-422 (AG-9, S. tuberosum, USA, CBS 970.96), B-423
(AG-10, T. aestivum, USA, CBS 971.96), B-424 (AG-11,
Lupinus angustifolus L., Australia, CBS 974.96), B-434
(AG-E, Malus sp., Netherlands, CBS 340.84).
R. solani strains isolated in Hungary: B-411 (S. tube-
rosum, cv Desirée) and B-410 (S. tuberosum cv Kis-
várdai rózsa), B-413 (Malu s domestica L.); B-409 (Hi-
biscus rosa-chinensis L., imported of Lybia, Tripoli);
B-245 (Allium cepa L., imported of China, Henan);
B-521 (Impatiens balsamina L.); B-433 (Festuca arun-
dinacea Schreb.).
R. stah lii Burgeff (teleomorph: Thanatephorus sp.): B-
441 (Platanthera chlorantha (Custer) Rchb.), Germany,
CBS 119.92).
R. fraga riae S. Husain & W.E. McKeen (teleomorph:
Ceratorhiza fragariae (S.S. Husain & W.E. McKeen)
R.T. Moore): B-438 (Fragaria × ananassa Duchense,
R. ramico la W.A. Weber & D.A. Roberts (teleomorph:
Ceratorhiza ramicola (W.A. Weber & D.A. Roberts) R.T.
Moore): B-427 (Pittospo rum tobira (Thunb.) W. T. Ai-
ton, Florida, USA, CBS 400.51).
R. cerealis E.P. Hoeven (teleomorph: Ceratobasidium
cereale D.I. Murray & Burpee): B-447 (T. aestivum L.,
Germany, CBS 559.77).
R. zeae: B-405 (mixed grass of Festuca and Lolium,
Athelia rolfsii (Curzi) C.C. Tu & Kimbr. (Syn:
Scelotium rolfsii Sacc.): B-442 (S. tuberosum, Italy, CBS
The strains were maintained on potato dextrose agar
(Merck, Darmstadt, Germany) amended with 2 g soya
peptone L44 (Oxoid, Basingstoke, UK).
2.3. Test for Pathogenicity
The potting medium was made by mixing forest soil with
peat before autoclaving (1.15 atm per 20 min), at the
ratio of 3:1.
The soil was inoculated with Rhizoctonia by the fol-
lowing manner: the sterile soil prepared as above was
admixed with chickpea seeds previously infected with
the pathogen (10 seeds per 250 g pot), than incubated 96
hours at 26˚C - 28˚C for evolving the mycelial net. The
seeds were put on the surface of infested soil (1 × 1 cm),
than covered with 5 mm layer of sterile soil. Sterile dis-
tilled water was used to moist the surface (15 mL per
pot), and covered with plastic wrap layer to avoid des-
siccation. Subsequently, the pots were evaluated each
day counting the emerged germlings, and observing the
occurrence of disease symptoms (damping off and leaf
spots). The height of seedlings was regularly measured to
nearest millimetre to follow the dinamics of growth. The
control plants were grown up in Rhizoctonia free soil.
The growth inhibition was calculated as a ratio between
control and treated plants.
When the coleptyles of control plants had been fully
developed (8 days after emergence of first germling) the
pathological status of all seedlings was evaluated, their
height and mass of measured to nearest millimetre and
milligramm, respectively. Inhibition rates were calcu-
lated as related to control. The percentages were trans-
formed into probit values, and this transformed data were
analyzed according to Sváb [33]. The state of roots was
assessed as well, and tissue sections were examined un-
der microscope in cases where no visual symptoms were
observed. The method was discussed in detail previously
[23]. The following six fold scale was used to assess the
tolerance of test plants at the 8th days: 0 = all seedlings
were destroyed; 1 = the majority of seedlings was dead,
but at least one survivor was presented either symptom-
less or bearing severe symptoms (the coleoptyle and the
roots damaged, the root neck scoring), 2 = less than half
of seedlings survived, the survivor were either symptom-
less or bearing severe symptoms (the coleoptyle and the
roots damaged, the root neck scoring), 3 = more than half
of seedlings survived, the symtoms of disease syndrome
largely varied, 4 = most of seedlings were similar to con-
trol, but as minimum as one diseased, 5 = none of seed-
lings had any symptoms visible to the naked eye. The
results of observations were compiled into data matrix
((19 wheat varieties + 4 small grains) × 26 Rhizoctonia
Surviving specimens were grown up to 21 days and
their development and evolution of disease syndrome
were observed.
2.4. Data Analysis
Box plot analysis was applied to demonstrate alterations
both in tolerance of test plants and and virulence of
Rhizoctonia strains as well as variations in growth pa-
rameters of wheat varieties as influenced by the presence
of Rhizoctonia in the soil. The relationships between host
(wheat varieties and small grains) and Rhizoctonia strains
(potential soil borne pathogens) have been analyzed by
multivariate methods: Non-linear Mapping (NLM) [34],
Cluster Analysis (CA), Principal Component Analysis
(PCA), Regression Analysis combined with Canonical
Correlation Analysis (CCA) and Potency Mapping (PM)
technique [35] following a previously described scheme
[36]. PCA was carried out on the correlation matrix [37]
and only the components having an eigenvalue greater
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
than one were included in the evaluation of data to dem-
onstrate potential number of factors influencing on host
parasite system, and the results were not delineated in
details. The protocol of experiments is shown in Figure
Statistical functions of Microsoft Office Excel 2003
(Microsoft, Redmondton, USA) and Statistica5 program
(StatSoft 5.0., Tusla, USA) were used for analysis of data.
The graphical presentation of result of data analysis was
edited uniformly in MS Office Power Point 2003.
3. Results
3.1. Dynamics of Germination
The dynamics of germination of wheat was altered by
Rhizoctonia strains in cultivar dependent manner (Figure
2). In majority of cases first germlings emerged within 2
days after sowing in Rhizoctonia free soil, moreover, the
process was finished rapidly. The seeds of Pannon Pre-
mium sortiment germinated more uniformly, than the
other varieties. In the presence of Rhizoctonia strains
emergence had been delayed with exception of most tol-
erant varieties (Petrence, Emese, Alkor, Hegyes). The
last day means the limit after that no further germlings
outcropped. Several seeds having been destroyed, seem-
ingly, the susceptible individual were killed either before
emergence or suffered damping off within 2 - 3 days
after outcropping. This ratio strongly varied, and it was
not possible to carry out the statistical analysis within
frames of the experimental model applied.
3.2. Syndromatic Picture of Disease
The growth of infected or diseased seedlings of wheat
was conspiciously retarded than the control, however, not
all symptoms of disease syndrome turned up. Even seed-
lings without any visible symptoms suffered damping off
before full development of coleoptyle, the roots of such
individuals were symptomless in many cases, although
brown spots could be frequently observed on roots and
root neck, even in the cases of robust survivors too. In
some cases small black spots (<1 mm) were found on
root necks, but these were not spread later. Leaf spots with
dark brown edge were randomly observed after 6 days.
The development of seedlings which survived the infec-
1 New disease
2 Survay of host range
3 Survay of data bases
Zer o hypothesis
Design of experiments
Collection of test
-Wheat varieties
-Smal l gr ains
Germinating seeds in
Rhizoctoniainfested soil
8th day
Mass Length
Box plot
Survivors Obser va tion
until 21 days
Map Potency
Box plotBox plot
Dynamics of
Evaluation of
disease syndrome
Data Matrix
(T olerance) of
wh eat cultivar s
Virulence of
Map Nonlinear
Response of
test plants
Analyisis Potency
Map Cluster
Box plot
Figure 1. Flow diagram of the experimental protocol. The labels F and T in ellipses mark figures and tables in the body text
where the results of computations were used for demonstration, while V means verbal interpretation of result. The zero hy-
pothesis was: on the base of screening large number of varieties there is possible to select candidates for breeding wheat cul-
tivar tolerant to soil borne Rhizoctonia infection.
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection 2245
Emergence (days)
* Hegyes
** Alkor
Palo tás
Other varieties Pannon Standard
Pannon Premium
Figure 2. Susceptibility of wheat varieties to soil borne Rhizoctonia infection. The gray and black stri ps mark varieties grow n
up in Rhizoctonia infected (+R) and non-inculated (control) pots, respectively. Wheat varieties are listed on the x-axis,
grouped as: other wheat varieties, Pannon Premium group of varieties, Pannon Standard group of varie ties. F and L are up-
per and lover values of the limits of emergence of first and last seeds, respectively.
tion without root neck symptoms was retarded at various
degree even two weeks later. The incidence of robust
survivors varied greatly within series, the root system of
such individuals was not retarded with exception of most
susceptible varieties (Bodri, Lona, Lucilla, Menüett). The
reaction of germlings to the presence of Rhizoctionia in
the soil was extremely heterogenic, the coefficient of
variation was over 30 percent within pot that made im-
possible the reliable statistical analysis. This was the
reason of use of the six fold scale for assessment of plant
response to Rhizocton ia infection. In several cases half of
seedlings survived while the other half was killed inde-
pendently of host/pathogen pair, most probably due to
environmental effects.
The behaviour of small grains was similar to that of
wheat including symptoms and development of disease
syndrome. The leaf spots on Eleusine appeared rarely,
but this was not in direct contact with virulence of
Rhizoctonia strains. The survivors of small grains were
not analyzed in details.
3.3. Susceptibility of Wheat Varieties
The test plants tolerated the Rhizoctonia in strain de-
pendent manner (Table 1). Among T. aestivum cultivars
Lona, Menüett and Bodri proved to be less tolerant,
while Emese, Palotás and Petrence exhibited low suscep-
tibility. The response of T. monococcum and T. turg idum
was similar to more tolerant T. aestivum cultivars. The
Eleusine was less susceptible than other small grains.
Unfortunately, none of the test plants tolerated the ma-
jority of Rhizoctonia strains at high degree.
The response of wheat cultivars to R. zeae, the new
pathogen in Europe, altered significantly of that of R.
solani strains. This difference manifested clearly, when
variety dependent virulence of R. zeae and associated R.
solani strain (B-433) was compared (R2 = 0.317, n = 19),
although their average pathogenicity (AP) was similar
(2.9 and 3.1, respectively). R. cerealis proved to be mod-
erately aggressive against germinating cereals (AP = 3.6),
and the similarity between activity spectrum of R. solan i
strains and R. cerealis was low (r2 < 0.23).
The susceptibility of wheat varieties to Ceratorhiza
(B-438) isolated of strawberry and Athelia (B-442) was
low, however, the C. ramic ola (B-427) isolated of orchid
heavily injured five T. aesticum cultivars (Toborzó, Bodri,
Lucilla, Toldi and Lona). The orchid symbiont R. stah lii
(B-441) exhibited low pathogenicity. Test plants were
related applying Nonlinear Mapping based on data com-
prised in Table 1 (Figure 3). Plants similarly responding
to soil borne Rhizoctonia infection formed a loose group,
but no clear patterns were revealed.
The taxonomic position did not influence the grouping.
This type of plotting did not gave information on the
structure of relationships among wheat cultivars, so an-
other nonlinear method, the Cluster Analysis was carried
out (Figure 4).
Wheat cultivars clustered into two well separated groups
on the dendrogram. Triticum aestivum cultivars were dis-
tributed between groups, however T. monoco cum and T.
turgidum were in different clusters. The average toler-
ance level of groups was similar (A = 3.1 and B = 2.7),
but alterations were revealed in the spectrum of suscepti-
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
Em ese
Kol o
Ki kelet
Kar izm a
Al kor
El eusine
Figure 3. Nonlinear map of test plants. The size of balls is proportional to potential tolerance of test plant to Rhizoctonias.
Triticum aestivum cultivars are marked with light grey, those correlated by their response to Rhizoctonia strains (r > 0.5) are
linked with lines. The clusters P and S comprise varieties of Pannon Standard and Pannon Pre mium sortiments. The c urve A
marks possible pattern.
Linkage Distance (1- Pearson’s r)
0.200.25 0.30 0.35 0.40 0.45 0.50 0.55 0.60
M enüett
Magv as
Eme se
1. 2
Lona 2. 5
3. 2
3. 3
3. 5
3. 5
3. 5
2. 3
2. 4
AG 8
C(3 )
1.4 3.3 4.1
2.4 4.7 2.6 3. 7
0.6 3.5 4.0
3.3 3.0 2.7 2.8
Mea n (6)
Figure 4. Grouping of wheat varieties based on their responses to soil borne Rhizoctonia infection. The data of Table 1 were
clustered of Pearson’s correlation matrix applying Unweighted Group Average method. Tolerance values to A. rolfsii (1), C.
cerelae (2), C. ramicola (3), Thanatephorus anamorphs (4), W. circinata (5) and anastomosis groups (AG1, AG8 and AG10) of
R. solani are of Table 1 (0 = susceptible, 5 = tolerant). (6) Average values of tolerance calculated for groups A and B.
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection 2247
bility. The difference was particularly spectacular in the
case of AG-1 strain of R. solani isolated in Australia,
which proved to be especially virulent against T. tur-
gidum and cultivars of Pannon Standard sortiment.
3.4. Analysis of Survivors
The inhibition of growth and mass accumulation of sur-
vivors were proportional to the potential susceptibility
and inhibition of emergence (Figure 5). The rates of in-
hibition of growth and mass accumulation well correlated
to each other: (p < 0.001):
Length = 0.8149Mass + 0.8876 (FG = 18, r2 = 0.8066).
Consequently, the response of survivors can be charac-
terized with inhibition of growth. This has importance
when survivors have to be grown up for selection or fur-
ther studies.
3.5. Factors Influencing the Plant Response
Four substantial factors could be revealed by PCA (Table
2) that explained 71% of total variation of data matrix
edited of the Table 1. None of principal components
(PCs) comprised dominant part of variation, and the cul-
tivars clustered into four well defined groups (A = 6, B =
5, C = 3 and D = 4 varieties, respectively). The perform-
ance of majority of cultivars was determined by one
dominant factor except three (Toborzó, Suba and Karizma)
where two factors influenced the response (Table 2). All
this indicates, that tolerance of wheat cultivars to soil
borne Rhizoctonia infection was regulated by different
genetic factors.
3.6. Virulence of Rhizoctonia Strains
Majority of Rhizocton ia strains holded back the germina-
tion (Figure 6) in the case as minimum as one cultivar.
However, this effect was not strictly related to response
of seedling in posterior stages of evolution of wheat/
Rhizoctonia association. For example, the AG-1 strain of
R. solani proved to be later more aggressive than R. ce-
realis, although these two strains altered the germination
by similar manner. Seemingly, the genetic background
regulating the formation of anastomosis between hyphae
is not connected directly to expression of pathogenicity
against wheat, the host spectrum of two AG-4 strains was
different, and these strains inhibited the emergence at
various degree. The AG-8 strain of R. solani that causes
severe yield losses in China and Australia altered the
dynamics of emergence insignificantly, contrary to iso-
lates of imported propagating material of China and
Netherlands (B-245, B-521).
Based on results shown in the Figure 4 two matrices
were edited of the data of Table 1. The Canonical Cor-
relation Analysis resulted three significant canonic func-
tions (R2 = 0.886, 0.847, 0.684 and χ2 = 103.2, 70.5, 42.4,
P a nnon S t a nd a rdPannon PremiumOther varieti es 5.5
Susceptibility (1)
To bor zó
Palotá s
Mazur ka
* Hegyes
** Alkor
4.0 4.55.0 5.5
Mass accumulation(4)
To bo rzó
Palotá s
To l di
* Hegyes
** Alkor
4.05.0 6.0
To bo rzó
To l di
* Hegyes
** Alkor
4.55.0 5.5
To bo rzó
To l di
* Hegyes
** Alkor
Figure 5. Responses of wheat varieties to Rhizoctonia strains. Inhibition rates (%) as related to control are given in probits.
The varieties marked with one and two asterisks are T. monococcum and T. turgidum, while non-marked are T. aestivum cul-
tivars, respectively. 1 = proportion of seedlings bearing symptoms of disease syndrome, 2 = proportion of killed germinating
seeds and seedlings suffered damping off, 3 = growth inhibition, 4 = inhibition of mass accumulation. r1,2 = 0.797, r1,3 = 0.772,
r1,4 = 0.728, r2,3 = 0.941, r2,4 = 0.742, r3,4 = 0.802 < r0,01 = 0.515 (FG = 18).
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
Table 2. Factors influencing the response of wheat varieties to soil-borne Rhizoctonia infection.
Pricipal Components
No. Varieties Groups PS% PC-1 PC-2 PC-3 PC-4
1 Toborzó A 52 0.513 0.244 0.508 0.182
2 Bodri C 55 0.416 0.231 0.674 0.080
3 Emese A 27 0.561 0.278 0.107 0.379
4 Petrence D 25 0.459 0.154 0.380 0.683
5 Lucilla - 47 0.435 0.262 0.376 0.407
6 Magvas B 56 0.146 0.575 0.465 0.295
7 Palotás D 27 0.426 0.436 0.312 0.536
8 Menüett B 60 0.234 0.852 0.039 0.230
9 Toldi B 58 0.076 0.683 0.214 0.338
10 Suba C 48 0.015 0.248 0.656 0.508
11 Ködmön C 53 0.083 0.316 0.765 0.385
12 Kolo B 43 0.241 0.701 0.404 0.146
13 Mazurka D 34 0.306 0.332 0.028 0.744
14 R23 D 34 0.121 0.364 0.245 0.661
15 Kikelet A 32 0.841 0.229 0.017 0.113
16 Karizma A 31 0.626 0.095 0.500 0.251
17 Lona B 76 0.232 0.662 0.224 0.177
18 Hegyes A 25 0.820 0.100 0.146 0.300
19 Alkor A 35 0.558 0.494 0.422 0.204
Eigenvalue 3.73 3.64 3.11 3.01
Proportion (%) of total variation 19.61 19.18 16.37 15.86
The PC loadings influencing the response of cultivars significantly were underlined. Varieties 1-6 and 7-13 are of Pannon Standard and Pannon Premium sorti-
ments, respectively. G = Varieties influenced by the same factor were marked with the same letter. PS = potential susceptibility of variety to Rhizoctonia calcu-
lated in percents of the Table 1.
Emergence (days)
Thanatephorus anamo rphs
R.cereali s
R.stahli i
Ma lus
Figure 6. Influence of Rhizoctonia strains on germination of wheat seeds. The gray strips mark strains that significantly de-
layed the germination. F and L are the limits of emergence of first and last seeds calculated as average for 19 wheat cultivars.
The skew lined area mark the interval (p = 0.05) of germination of seeds in Rhizoctonia free soil.
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
Open Access AJPS
morphs, indicating that these properties have no decisive
role in expression of pathogenicity. The physiological
characters, which take place in anastomose contact have
also minor importance, for example two R. solani strains
of AG-4 anastomosis group (B-417 and B-430) are in
notably different position. Similarly, the source of strain
had no influence on clustering. For example, the strains
isolated of potato tubers were located in different clusters,
while anamorphs (B-441 and B-427) of Ceratorrhi za and
Thanatephorus of orchid and potato, respectively, were
closely related. The taxonomic position of source (host
plant) also had no importance, the strains of mono- and
dicot plants were placed into the same cluster (see B-417
of Citrus and B-433 of Festuca). Unfortunately, we have
few data on exact geographic origin, but surprisingly, all
isolates of Hungarian origin were separated into the same
cluster. The strains B-413 and B-521 were of imported
propagating material. This might be related to role of
environmental (biogeographic and bioclimatic) factors.
Being typical soil habitants and forming mycelial web in
soil [38,39], the soil biota plays a crucial role in the
microevolution of Rhizocton ia species, while the assem-
blage of soil biota significantly depends on both structure
and composition of mineral matrix and climatic condi-
tions [40].
respectively). Plotting the strains as canonic scores by
first two roots strict linear relationship was revealed, where
only few strains deviated (AG-1, AG-5). However, the
strains on plot of third canonic function (Figure 7) clus-
tered into two well separated groups (p < 0.001). The
members of each group differ by their virulence, and the
strains of the same anastomosis group split within two
clusters, indicating, that the properties responsible for
separation into anastomosis groups have minor impor-
tance in formation of these clusters.
3.7. Relationships among Rhizoctonia Strains
The Rhizo ctonia strains were clustered on the base of
their pathogenicity against wheat cultivars (Table 1) based
on correlation matrix applying Unweighted Pair Group
Average method (Figure 8). No clear patterns can be
revealed on dendrogram. Two highly virulent strains iso-
lated of onion (B-245) and garden jewelweed (B-521)
with poorly virulent AG-E strain separated of others,
most probably due to low diversity of response data. The
properties responsible for taxonomic position of strains
seemingly have minor importance as the anamorphs of
Athelia, Cerato basidium, Ceratorrhiza and Waitea spe-
cies formed mixed clusters with Thanatephorus ana-
G-E B-411
Figure 7. Separation of Rhizoctonia strains with Canonical Correlation Analysis. According to groups shown in Figure 3 two
submatrices were edited of the data comprised in Table 1 and were related by means of CCA. Strains B-409 and B-430 (AG-4)
were omitted of calculations. The size of black (A) and gray (B) balls is proportional to potential aggressivity of strains to
wheat, respectively. The fitness of regression was over r = 0.97 (p < 0.001) for both function.
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
R. solani
R. solani
R. solani
R. solani
A. rolfsii
R. stahlii
C. cereal e
C. ramicola
R. solani
W. circinata
R. solani
R. solani
C. fraga r ia e
AG-1 0
Strain (1)
tala j
Solanu m
Solanu m
Source (2)
S (5)
P (6)
Origin (3)
Linkage Distance (UW PGA, 1-Pearson’s r) 0.8 1.0
Figure 8. Grouping of Rhizoctonia strains based on their inhibitory effect on germinating seeds of various wheat varieties.
The data of Table 1 were clustered of Pearson’s correlation matrix applying Unweighted Group Average method. (1) Strains
underlined were isolated of monocots, (2) Source, the monocots are underlined, (3) Location, (4) Code. The codes of members
of the group I on Figure 4 are marked with asterisks. The columns S(5) and P(6) comprise potential tolerance values of varie-
ties of Pannon Standard and Pannon Premium sortiments, respectively (0 = tolerant, 100 = susceptible). H = isolated of
sources collected in Hungary.
3.8. Factors Influencing Virulence of Rhizoctonia
The Principal Component Analysis resulted in nine nota-
ble components that explain 82% of total variance (Ta-
ble 3). Similarly to factors influencing the response of
wheat cultivars none of them was superior, the major PC
has about twice more weight than the minimally signifi-
cant one. The groups were sharply separated and formed
by strains of various taxonomic positions. Only in two
cases was the performance of strains (B-419 and B-410)
affected by two factors. The quantitative aspect of viru-
lence was not connected per se to groupping, for exam-
ple the most virulent AG-1 strain of R. solani (B-415)
was linked to significantly less virulent AG-10 strain
(B-423). The findings support the concept of multilocal
character of interaction between wheat and attacking
4. Discussion
We focused on soil borne Rhizoctonia infection that has
the greatest effect on the growth and yield of wheat
among soil borne pathogens [41], and the brown patch
disease became devastating in last two decades. This
might be related to the changes in both pest management
practices and cultivation techniques that resulted the in-
creased frequency of the specialized pathogen genotype
in some geographic areas [42,43]. The metalloorganics of
broad antimicrobial spectrum of activity applied formerly
for seed dressing have been banned, and the monosite
inhibitors either do not inhibit Rhizoctonia like fungi or
they loose activity rapidly due to acquired resistance.
Moreover, the formerly dominant tillage based wheat
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection 2251
Table 3. Factors influencing virulence of Rhizoctonia strains against wheat cultivars.
Rhizoctonia strains Principal Components
No. Code Group PV% PC-1 PC-2 PC-3 PC-4 PC-5 PC-6 PC-7 PC-8 PC-9
1 B-415 A 82 0.03 0.24 0.07 0.07 0.15 0.16 *0.81 0.07 0.27
2 B-432 B 13 0.11 0.11 0.05 0.14 0.02 *0.94 0.04 0.10 0.03
3 B-446 C 24 0.09 0.27 0.05 0.07
*0.89 0.06 0.28 0.14 0.02
4 B-417 D 32 0.47 0.27
*0.64 0.26 0.14 0.15 0.03 0.28 0.22
5 B-430 D 20 0.04 0.26 *0.90 0.04 0.10 0.04 0.11 0.11 0.02
6 B-418 E 52 0.14 0.03 0.14 0.20 0.14 0.16 0.09
*0.90 0.01
7 B-419 DF 25 0.07 0.16 *0.76 0.17 0.20 *0.53 0.08 0.07 0.01
8 B-420 F 36 0.05 0.22 0.14 *0.85 0.05 0.04 0.01 0.23 0.16
9 B-421 C 32 0.17 0.20 0.01 0.10 *0.51 0.18 0.40 0.48 0.31
10 B-422 G 52 0.41 *0.56 0.45 0.01 0.21 0.08 0.41 0.01 0.17
11 B-423 A 19 0.31 0.44 0.19 0.09 0.25 0.17
*0.57 0.19 0.35
12 B-424 B 33 0.17 0.11 0.33 0.13 0.27
*0.78 0.20 0.05 0.03
13 B-434 F 28 0.08 0.17 0.17
*0.61 0.37 0.07 0.25 0.31 0.16
14 B-411 H 58 *0.67 0.19 0.38 0.02 0.34 0.16 0.17 0.04 0.14
15 B-410 HG 64 *0.54 0.31 0.36 0.14 0.07 0.09 *0.51 0.03 0.34
16 B-413 F 48 0.37 0.33 0.22
*0.59 0.13 0.01 0.06 0.02 0.49
17 B-409 I 36 0.07 0.01 0.06 0.10 0.11 0.05 0.17 0.08
18 B-245 G 99 0.00 *0.93 0.03 0.13 0.05 0.10 0.14 0.07 0.04
19 B-521 G 99 0.00 *0.93 0.03 0.13 0.05 0.10 0.14 0.07 0.04
20 B-433 H 42 *0.61 0.11 0.31 0.21 0.16 0.04 0.19 *0.51 0.22
21 B-441 H 47 0.24 0.19 0.02 0.15
*0.68 0.26 0.02 0.03 0.15
22 B-405 C 20 *0.67 0.20 0.05 0.22 0.30 0.02 0.09 0.10 0.04
23 B-438 H 38 *0.56 0.25 0.24 0.11 0.02 0.39 0.44 0.12 0.07
24 B-427 H 27 *0.60 0.03 0.34 0.48 0.35 0.04 0.10 0.06 0.22
25 B-447 H 54 *0.86 0.05 0.15 0.09 0.11 0.11 0.10 0.17 0.001
26 B-442 F 41 0.19 0.19 0.36
*0.60 0.14 0.04 0.05 *0.50 0.01
Eigenvalues 3.81 3.10 2.96 2.45 2.38 2.22 2.15 1.95 1.80
Proportion of total variance 14.6 11.9 11.4 9.4 9.2 8.5 8.3 7.5 6.9
Strains 1-13 refer to anastomosis groups AG-1-AG-11 and AG-E of R. solani, respectively, of CBS collection, strains 14-20 are Hungarian isolates of R. solani
and R. stahlii (21), all are Thanatephorus anamorphs. Rhizoctonia strains 22 - 26 are anamorphs of Waitea (22), Cerathorrhiza (23, 24), Ceratobasidium (25)
and Athelia (26). PV% = potential virulence of Rhizoctonia strains against wheat cultivars calculated of the Table 1 applying Potency Mapping. The PC load-
ings influencing the virulence of strains significantly, were marked with asterisks. The small grains were omitted of calculations.
cropping system in dryland farming has been changed to
minimum or not-till cropping systems that favours to
survival of mycelial web forming Rh izoctonia [39,44-47].
The efforts to control soil borne infections applying
various eubiotic preparations were not successful yet in
large scale, mainly due to the low reproducibility of the
effect in field conditions which makes the calculation of
cost/benefit ratio unreliable. Actually, seed dressing re-
sults only sufficient control of pathogens threatening the
cultivated plant in early stage of development. Thus the
importance of selection of resistant wheat cultivars in-
4.1. Performance of Wheat/Rhizoctonia
Rhizoctonia species are abundant in soils as mutualistic
members of microbial consortium associated with plants.
Their relationship with host plants may change from sym-
biosis (as in various orchids) to destructive parasitism,
and these fungi usually do not cause visible disease symp-
toms. The infection may remain latent for a long period
and can rapidly generalize, when environmental stress
factors overhelm the homeostatic regulation of host plant,
i.e., the disposition of host favours to pathogen either in
phyllosphere of in roots. The amount of thallus varies
within large limits (0.09 - 6 ng per g tissue) in symptom-
less plants [48]. The symptomatic picture is usually vari-
able to a high extent as stunting growth, decrease in mass
accumulation, leaf spots of various size, deformations of
various organs and rooting tissues can be observed on
infected plant alone or in combinations together, the dis-
ease syndrome may evolve rapidly to a fatal consequence
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
in formerly symptomless host (damping off and wilting).
In our experiments all the above mentioned variations
were observed, and the overall susceptibility of one re-
spective variety influenced only the frequency of various
symptoms of disease syndrome caused by soil borne
Rhizoctonia infection independently on taxonomic posi-
tion or origin of the strains. This indicates that some
traits used for taxonomic classification can not be tightly
associated with the properties determining the character
of wheat/Rhizoctonia interaction. The small black spots
that were occasionally observed on scutellum and meso-
cotyl of surviving individuals may be result of hypersen-
sitive reaction (HR) suggesting the defense mechanism
against Rhizoctonia attack rapidly activates. Further stud-
ies requested to connect this property with wheat re-
sponse to soil borne Rhizoctonia infection as the in-
volvement or manipulation of HR into breeding pro-
grams may open door towards to the control of brown
patch disease [49]. Furthermore, the role of Rhizoctonia
toxins in pathogenesis has to be elucidated as well as
factors regulating development of survivors in presence
of Rhizoctonia should be identified.
The genetic background of tolerance to Rhizoctonias is
not elucidated yet. Discoveries show that both anatomic
and physiological features are involved into manifesta-
tion. Thus, the structure and composition of cell wall
might have importance; the resistance to fungal xylanase
is a tolerance factor [50]. The multivariate analysis of our
experimental results supports the multigenic character of
wheat response, although no dominant factor was revealed.
Unfortunately, the screening of tolerance to Rhizoctonia
in microscale provocative experiments can give data for
only preliminary selection of wheat lines, and the survi-
vors should be evaluated in field conditions as well [51].
Nevertheless, the data obtained are encouraging and on
our opinion the screening of gene banks applying the
method demonstrated here can result germlings useful for
further manipulations (for example cultivars Emese,
Petrence and Toldi). The high variation observed in re-
sponse of wheat to soil borne Rhizoctonia might be
caused by lack of preliminary selection of tested plants.
Members of the genus Rhizoctonia are considered as a
complex mixture of filamentous fungi, having in com-
mon the possession of a non-spored imperfect state, usu-
ally referred to as the anamorphs of five genera: Athelia,
Ceratobasidium, C eratocys t is, Thanathephorus and Waitea.
Here we included data on virulence of strains of the above
five teleomorph genera, all of them attacked germinating
seeds of cereals tested. Our results approve presumtion of
Tomaso-Peterson and Trevathan [52] that the new for
Europe pathogen, R. zeae, is considered as a hazard for
wheat cultivation, with special regard to warm climate
The multivariate analysis of experimental data re-
vealed nine significant factors influencing the aggressiv-
ity of these strains; moreover, these factors are clearly
not related to traits used for taxonomic purposes. The
hyphal anastomosis interactions has been widely used for
clustering of Rhizoctonia anamorphs within the complex,
since other types of diagnostic features are usually scarce
in these fungi [53]. It was considered, that the anastomo-
sis groups are specialized to defined host plants [54]. Our
experiments do not support this presumption in the case
of wheat. Seemingly, the host range of single strains
might be different, and reversely, strains clustered into
different taxons, may have similar host range. By this
reason, on our opinion, —based on presented results here,
—for primary screening of wheat cultivars as minimum
as six different strains should be used, including A. rolfsii,
C. cerealis and W. circinata.
4.2. Future Prospects
The plant rhizosphere is a dynamic environment in which
many parameters may influence the population structure,
diversity and activity of the microbial community. The
soil C:N ratio has critical role in disease incidence caused
by Rhizoctonia as it was demonstrated by Kuhn et al.
[55]. The roles of mycorrhiza in facilitating the acquisi-
tion and transfer of carbon (C) and nitrogen (N) is well
known. A considerable amount of bidirectional transfer
of C between host plant and its fungal symbiont, and a
fungus-dependent pathway for organic N can be realized
rapidly, thus influencing positively the stress tolerance of
plant [56]. The micro- and mesofauna also can alter the
disease incidence either wounding the roots [57] or de-
creasing the size of inoculum [58]. Induction of suppres-
sive soil by using mixed cropping or applying eubiotic
preparations is contradictory, as the iron deficiency may
harm the wheat although this can be overcame by leaf
nutrition. Nevertheless, we can expect new, usable knowl-
edge of the environmental research on microbial com-
munities and plant microbe interaction studies, which can
help to design and sustain suppressive soil that would be
the most convenient and economic method for comatting
yield losses caused by soil-borne diseases [59].
High number of papers describe antifungal effect of
various plant extracts, but only few of them report con-
vincing comparative data on efficacy, and in minority of
cases these effects have been comparable with marketed
fungicides [60,61]. Most of the active substances identi-
fied are terpenoids, and on our view there is a few prob-
ability to develop potentially effective and environmen-
tally safer alternative fungicide to xenobiotics. However,
these plants might be sources for transgenic modification
to upgrade the sheath blight tolerance of wheat (Table 4).
The breading is the most promising measure to improve
the tolerance to soil-borne pathogen complex, because
the use of any xenobiotic has adverse effects on soil biota
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
Open Access AJPS
Table 4. Potential candidates for tr ansge nic manipulation of wheat for improvement of tolerance to Rhizoctonia.
Plant Factor Results (example) Ref.
Hordeum vulgare rip30 increased tolerance (potato) [71]
Hordeum vulgare chitinase increased tolerance (tobacco) [72]
Pennisetum glaucum lipid transfer protein antifungal [73]
Triticum sp. puroindoline increased tolerance (rice) [74]
Celastrus hypoleucus pristimerin inhibiting the formation of infective body [75]
Celastrus hypoleucus celastrol inhibiting the formation of infective body [75]
Prokaryote 5-enolpyruvoyl-shikimate-3-phosphate synthetase Increased tolerance (wheat/Puccinia) [76]
Oryza sativa thaumatin like protein increased tolerance (rice) [70]
Oryza sativa OsPR-4b gene encoding pathogenesis related proteinenhanced resistance [77]
Solanum tuberosum Potide G proteinase inhibitor [78]
Bacillus subtilis Iturin A Antifungal [79]
Bacillus subtilis flagellin Antifungal [80]
Raphanus sativus defensin increased tolerance (wheat) [81]
Solanum tuberosum Snakin 1 enhanced resistance [82]
Dasypyrum villosum unknown tolerance to AG 8 [83]
Oryza sativa Rice chitinase increased tolerance (Musa/Mycosphaerella) [84]
Oryza sativa Rice chitinase increased tolerance (Eleusine/Magnaporthe) [85]
Tichoderma harzianum glucanase inhibiting the formation of infective body [86]
Tephrosia villosa defensin increased tolerance (tobacco) [87]
Arabidopsis thaliana NADPH oxydase induced resistance [88]
Oryza sativa ACCA synthase induced resistance [89]
as well as can predispose host plant to pathogen [62,63].
In our experiments individual resistant to some Rhizocto-
nia, which attack the majority of its fellows, occurred in
each variety, likely to observations of other authors [64].
Such survivors can be objects of further breeding or ge-
netic engineering. Unfortunately, the mechanistic ap-
proach on concern surrounding the genetically modified
maize with Bacillus thuringiensis toxin or the glyphosate
tolerant crops borne overall social resistance to gene tech-
nology. We should clarify, most of these concerns have
no scientific base. First of all, the usefulness of geneti-
cally modified (GM) crops can be sustained with careful
management [65].
Although, Rhizoctonia species, which cause bare-patch
disease and sharp eyespot in wheat are not among the top
ten pathogens [66], economic improtance of their control
is increasing from severe to catasrophic yield losses re-
ported from main wheat cultivating areas [67-69]. There
is an urgent need in sustainable management strategy to
combat damages induced by soil habiting Rhizoctonia
complex, first of all, new tolerant wheat cultivars. No
major resistance genes to this pathogen have been identi-
fied so far inspite of increasing efforts in studies of
physiology and genetic background of wheat/ Rhizoc tonia
interaction. Nevertheless, candidates for transgenic ma-
nipulation can be selected (Table 4). The possible im-
provement of tolerance demonstrated on rice [70] might
serve as example for wheat.
Some terpenoid phytoanticipins of Pelargo nium grav-
olens [90], Artemisia arborescens [91], Helianthus tube-
rosus [92] exhibited good antifungal effect, but on our
opinion the use of antifungal polypeptides seems to be
more promising for transgenic manipulation. For exam-
ple, a basic oligopeptide of Bacillus subtilis exhibited
excellent and broad spectrum antimicrobial activity in
our experiments [93] and would fit for control of all four
important soil borne pathogens of wheat. The incorpora-
tion of Rhizoctonia specific mycovirus into genome of
cereals also is a promising possibility [94], with special
regard to root border cells. These, detached living cells
form the “front line” in the soil, the special part of
rhizosphere, described as a system first by Hawes [95],
where the plant controls the microenvironment with these
specially progammed cells [96]. The border cells have
indisputably key function in plant defense controlling the
dynamics of adjacent microbial populations in the soil to
foster beneficial associations and inhibit pathogenic in-
vasion [97], thus these cells are plausible objects of ge-
netic engineering to desing wheat plant with optimum
characteristics for root health management.
PCR based molecular methods enable the comparative
analysis of genes involved in plant defense [98]. The task
is complex because the design of PCR based molecular
markers linked to the Rhizoctonia resistance genes of
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
wheat cultivars seems to be complicated due to high
number of factors influencing on the type of plant re-
sponse. Synergic joint action of several minor factor may
result more stabile repel than a single major one as one
gene mutation can not eliminate this type of defense [90].
However, we understand little about how genes interact
because very few possible genetic interactions have been
explored experimentally [99], thus depending on the
insertion event, a particular transgene can have large
effects on the entire phenotype of a plant and that these
effects can sometimes be reversed when plants are
moved from the glasshouse to the field [100]. On our
opinion the more intense research of complex repertoire of
small RNAs (microRNAs [miRNAs] and siRNAs) used
as guides for post-transcriptional and epigenetic regula-
tion would help to design new, either intraspecific or
intrageneric wheat varieties. To promote research in this
field it is necessary to make public the data on cereal
crop genomes and discuss the contribution: what proteins,
and their genome sequence organisation, play in plant
defence. Although these data are extremely valuable tool
for detailed analysis, and the emergence of informatic
market makes difficulties as patent applications back out
of scientific disputation [101], nevertheless, such free
disputation in large scale of scientific community would
significantly accelerate the progress in breeding of wheat
tolerant to soil borne diseases.
5. Conclusions
No relationship was found between taxonomic position
and origin of Rhizoctonia strains, indicating that traits
used for their classification are not closely related to ex-
pression of their pathogenicity against wheat cultivars.
Nine factors were revealed that significantly affect their
virulence in wheat/Rhizoctonia system.
We have got empirical evidence from plant/pathogen
system on the possibility of selection; the wheat phenol-
type resistant to soil-borne Rhizoctonia, that verifies our
approach of using simplified scale for disease assess-
6. Acknowledgements
This study was supported by The National Office for
Research and Technology, Grant No. K67688.
[1] L. Vajna and G. Oros, “First Report of Rhizoctonia zeae
in Hungary,” Plant Pathology, Vol. 54, No. 2, 2005, p.
[2] G. Oros, “Rhizoctonia Species. Gaps to Be Filled in the
Hungarian Soil Science,” Tiszántúli Növényvédelmi Fórum
Előadásai, Debrecen, 18-20 October 2004, pp. 321-329.
[3] G. J. Kövics and N. Lőrincz, “Causal Agents of Stem-
Base Diseases of Winter Wheat in Eastern Hungary,” In:
Proceedings of Conference, Resources of the Environ-
ment and Sustained Development, Oradea, 24-26 May
2001, Analele Universitátii din Oradea. Tom. VII. Scien-
tific Communication Session: Partea I-a. Fascicula Agri-
cultură-Horticultura, pp. 37-44.
[4] E. I. Simay, “Outbreak of Rhizoctonia solani Kuhn on oat
(Avena sativa) in Hungary,” Cereal Research Communi-
cations, Vol. 17, No. 3-4, 1998, pp. 233-235.
[5] F. Unal and F. S. Dolar, “First Report of Rhizoctonia
solani AG 8 on Wheat in Turkey,” Journal of Phytopa-
thology, Vol. 160, No. 1, 2012, pp. 52-54.
[6] L. Chen, Y. Y. Zhang, H. X. Liang, H. X. Liu, L. P. Du,
H. J. Xu and Z. Y. Xin, “Overexpression of TiERF1 En-
hances Resistance to Sharp Eyespot in Transgenic Wheat,”
Journal of Experimental Botany, Vol. 59, No. 15, 2008,
pp. 4195-4204.
[7] M. S. Hamada, Y. N. Yin, H. G. Chen and Z. H. Ma,
“The Escalating Threat of Rhizoctonia cerealis, the
Causal Agent of Sharp Eyespot in Wheat,” Pest Man-
agement Science, Vol. 67, No. 11, 2011, pp. 1411-1419.
[8] Y. P. Guo, W. Li, H. Y. Sun, N. Wang, H. S. Yu and H.
G. Chen, “Detection and Quantification of Rhizoctonia
cerealis in Soil Using Real-Time PCR,” Journal of Gen-
eral Plant Pathology, Vol. 78, No. 4, 2012, pp. 247-254.
[9] E. Demirci, “Rhizoctonia Species and Anastomosis Groups
Isolated from Barley and Wheat in Erzurum, Turkey,”
Plant Pathology, Vol. 47, No. 1, 1998, pp. 10-15.
[10] B. Tunali, J. M. Nicol, D. Hodson, Z. Uckun, O. Buyuk,
D. Erdurmus, H. Hekimhan, H. Aktas, M. A. Akbudak
and S. A. Bagci, “Root and Crown Rot Fungi Associated
with Spring, Facultative, and Winter Wheat in Turkey,”
Plant Disease, Vol. 92, No. 9, 2008, pp. 1299-1306.
[11] R. G. Grogan, “The Science and Art of Plant Disease
Diagnosis,” Annual Review of Plant Pathology, Vol. 19,
1981, pp. 333-351.
[12] J. S. Gill, K. Sivasithamparam and K. R. J. Smettem,
“Soil Types with Different Texture Affects Development
of Rhizoctonia Root Rot of Wheat Seedlings,” Plant and
Soil, Vol. 221, No. 2, 2000, pp. 113-120.
[13] J. Keijer, “The Initial Steps of the Infection Process In
Rhizoctonia solani,” In: B. Sneh, S. Jabaji-Hare, S. Neate,
and G. Dijst, Eds., Rhizoctonia Species: Taxonomy, Ecol-
ogy, Pathology and Disease Control, Kluwer, Dordrecht,
1996, pp. 149-162.
[14] V. N. Armentrout anf A. J. Downer, “Infection Cushion
Development by Rhizoctonia solani on Cotton,” Phyto-
pathogy, Vol. 77, 1987, pp. 623-630.
[15] D. I. L. Murray, “Penetration of Barley Root and Coleoptile
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection 2255
Surfaces by Rhizoctonia solani,” Transactios of British
Mycological Society, Vol. 79, No. 2, 1982, pp. 354-360.
[16] D. K. Roget, S. M. Neate and A. D. Rovira, “Effect of
Sowing Point Design and Tillage Practice on the Inci-
dence of Rhizoctonia Root Rot, Take-All and Cereal Cyst
Nematode in Wheat and Barley,” Australian Journal of
Experimental Agriculture, Vol. 36, No. 6, 1996, pp. 683-
[17] R. J. Cook and R. J. Veseth, “Wheat Health Manage-
ment,” APS Press, St. Paul, 1991, p. 152.
[18] W. W. Bockus and J. P. Shroyer, “The Impact of Reduced
Tillage on Soilborne Plant Pathogens,” Annual Review of
Phytopathology, Vol. 36, 1998, pp. 485-500.
[19] T. C. Paulitz, R. W. Smiley and R. J. Cook, “Insights into
the Prevalence and Management of Soilborne Cereal
Pathogens under Direct Seeding in the Pacific Northwest,
USA,” Canadian Journal of Plant Pathology-Revue
Canadienne de Phytopathologie, Vol. 24, No. 4, 2002, pp.
[20] D. K. Roget, S. M. Neate and A. D. Rovira, “Effect of
Sowing Point Design and Tillage Practice on the Inci-
dence of Rhizoctonia Root Rot, Take-All and Cereal Cyst
Nematode in Wheat and Barley,” Australian Journal of
Experimental Agriculture, Vol. 36, No. 6, 1996, pp. 683-
[21] S. A. Frank, “Recognition and Polymorphism in Host-
Parasite Genetics,” Philosophical Transaactions of the
Royal Society, London Series B, Vol. 346, No. 1317, 1994,
pp. 283-293.
[22] R. K. Voorhees, “Sclerotial Rot of Corn Caused by Rhi-
zoctonia zeae, n. sp.,” Phytopathology, Vol. 24, No. 11,
1934, pp. 1290-303.
[23] L. Vajna and G. Oros, “Turfgrass Blight in Hungary. The
Role of Rhizoctonia solani and R. zeae in the Disease
Development,” Plant Protection, Vol. 59, 2005, pp. 149-
157. [in Hungarian]
[24] M. H. F. Hashmi and A. Ghaffar, “Seed-Borne Mycoflora
of Wheat, Sorghum and Barley,” Pakistan Journal of
Botany, Vol. 38, No. 1, 2006, pp. 185-192.
[25] T. C. Streeter, Z. Rengel, S. M. Neate and R. D. Graham,
“Zinc Fertilisation Increases Tolerance to Rhizoctonia
solani (AG 8) in Medicago truncatula,” Plant and Soil,
Vol. 228, No. 2, 2001, pp. 233-242.
[26] J. A. Lewis, R. D. Lumsden and J. C. Locke, “Biocontrol
of Damping-Off Diseases Caused by Rhizoctonia solani
and Pythium ultimum with Alginate Prills of Gliocladium
virens, Trichoderma hamatum and Various Food Bases,”
Biocontrol Science and Technology, Vol. 6, No. 2, 1996,
pp. 163-173.
[27] R. J. Cook, D. M. Weller, A. Y. El-Banna, D. Vakoch and
H. Zhang, “Yield Responses of Direct-Seeded Wheat to
Rhizobacteria and Fungicide Seed Treatments,” Plant
Disease, Vol. 86, No. 7, 2002, pp. 780-784.
[28] S. J. Barnett, D. K. Roget and M. H. Ryder, “Suppression
of Rhizoctonia solani AG-8 Induced Disease on Wheat by
the Interaction between Pantoea, Exiguobacterium, and
Microbacteria,” Australian Journal of Soil Research, Vol.
44, No. 4, 2006, pp. 331-342.
[29] S. A. Wakelin, S. T. Anstis, R. A. Warren and M. H. Ry-
der, “The Role of Pathogen Suppression on the Growth
Promotion of Wheat by Penicillium radicum,” Austral-
asian Plant Pathology, Vol. 35, No. 2, 2006, pp. 253-258.
[30] O. V. Mavrodi, N. Walter, S. Elateek, C. G. Taylor and P.
A. Okubara, “Suppression of Rhizoctonia and Pythium
Root Rot of Wheat by New Strains of Pseudomonas,”
Vol. Biological Control, 62, No. 2, 2012, pp. 93-102.
[31] D. V. Mavrodi, O. V. Mavrodi, J. A. Parejko, R. F. Bon-
sall, Y. S. Kwak, T. C. Paulitz, L. S. Thomashow and D.
M. Weller, “Accumulation of the Antibiotic Phenazine-1-
Carboxylic Acid in the Rhizosphere of Dryland Cereals,”
Applied and Environmental Microbiology, Vol. 78, No. 3,
2012, pp. 804-812.
[32] S. Kildea, V. Ransbotyn, M. R. Khan, B. Fagan, G. Leo-
nard, E. Mullins and F. M. Doohan, “Bacillus megaterium
Shows Potential for the Biocontrol of Septoria tritici
Blotch of Wheat,” Biological Control, Vol. 47, No. 1,
2008, pp. 37-45.
[33] J. Sváb, “Biometrical Methods in Research Work,” Me-
zőgazdasági Kiadó, Budapest, 1981 (in Hungarian).
[34] J. W. Sammon, “A Nonlinear Mapping for Data Structure
Analysis,” IEEE Transactions on Computers, Vol. 18, No.
5, 1969, pp. 401-407.
[35] P. J. Lewi, “Spectral Mapping, a Personal and Historical
Account of an Adventure in Multivariate Data Analysis,”
Chemometrics and Intelligent Laboratory Systems, Vol.
77, No. 1-2, 2005, pp. 215-223.
[36] D. Magyar and G. Oros, “Application of the Principal
Component Analysis to Disclose Factors Influencing on
the Composition of Fungal Consortia Deteriorating Re-
mained Fruit Stalks on Sour Cherry Trees,” In: P. San-
guansat, Ed., Principal Component Analysis, InTech, Ri-
jeka, 2012, pp. 89-110.
[37] K. Pearson, “On Lines and Planes of Closest Fit to Sys-
tems of Points in Space,” Philosophical Magazine, Vol. 6,
No. 2, 1901, pp. 559-572.
[38] T. C. Paulitz and K. L. Schroeder, “A New Method for
the Quantification of Rhizoctonia solani and R. oryzae
from Soil,” Plant Disease, Vol. 89, No. 7, 2005, pp. 767-
[39] J. S. Gill, K. Sivasithamparam and K. R. J. Smettem,
“Size of Bare-Patches in Wheat Caused by Rhizoctonia
solani AG-8 Is Determined by the Established Mycelial
Network at Sowing,” Soil Biology & Biochemistry, Vol.
34, No. 6, 2002, pp. 889-893.
[40] I. M. Szabó, “The Microbiology of the Biosphere,” Aka-
démiai Kiadó, Budapest, 1989.
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
[41] A. H. A. Al-Abdalall, “Assessment of Yield Loss Caused
by Root Rots in Wheat and Barley,” Journal of Food Ag-
riculture & Environment, Vol. 8, No. 2, 2010, pp. 638-
[42] R. J. Cook, “Management of Wheat and Barley Root
Diseases in Modern Farming Systems,” Australasian
Plant Pathology, Vol. 30, No. 2, 2001, pp. 119-126.
[43] R. A. Davis, D. Huggins, R. J. Cook and T. C. Paulitz,
“Can Placement of Seed Away from Relic Stubble Limit
Rhizoctonia Root Rot in Direct-Seeded Wheat?” Soil &
Tillage Research, Vol. 101, No. 1-2, 2008, pp. 37-43.
[44] J. S. Gill, K. Sivasithamparam and K. R. J. Smettem,
“Influence of Depth of Soil Disturbance on Root Growth
Dynamics of Wheat Seedlings Associated with Rhizoc-
tonia solani AG-8 Disease Severity in Sandy and Loamy
Sand Soils of Western Australia,” Soil & Tillage Research,
Vol. 62, No. 1-2, 2001, pp. 73-83.
[45] T. C. Paulitz, R. W. Smiley and R. J. Cook, “Insights into
the Prevalence and Management of Soilborne Cereal
Pathogens under Direct Seeding in the Pacific Northwest,
USA,” Canadian Journal of Plant Pathology-Revue Ca-
nadienne de Phytopathologie, Vol. 24, No. 4, 2002, pp.
[46] C. E. Pankhurst, H. J. McDonald, B. G. Hawke and C. A.
Kirkby, “Effect of Tillage and Stubble Management on
Chemical and Microbiological Properties and the Devel-
opment of Suppression towards Cereal Root Disease in
Soils from Two Sites in NSW, Australia,” Soil Biology &
Biochemistry, Vol. 34, No. 6, 2002, pp. 833-840.
[47] W. T. Schillinger, A. C. Kennedy and D. L. Young,
“Eight Years of Annual No-Till Cropping in Washing-
ton’s Winter Wheat-Summer Fallow Region,” Agricul-
ture Ecosystems & Environment, Vol. 120, No. 2-4, 2007,
pp. 345-358.
[48] M. Su’udi, J. M. Park, W. R. Kang, D. J. Hwang, S. Kim
and I. P. Ahn, “Quantification of Rice Sheath Blight Pro-
gression Caused by Rhizoctonia solani,” Journal of Mi-
crobiology, Vol. 51, No. 3, 2013, pp. 380-388.
[49] E. T. Iakimova, L. Michalczuk and E. J. Woltering, “Re-
view. Hypersensitive Cell Death in Plants—Its Mech-
nisms and Role in Plant Defence against Pathogens,”
Journal of Fruit and Ornamental Plant Research, Vol. 13,
2005, pp. 135-158.
[50] J. Wu, Y. Wang, S. T. Kim, S. G. Kim and K. Y. Kang,
“Characterization of a Newly Identified Rice Chitinase-
Like Protein (OsCLP) Homologous to Xylanase Inhibi-
tor,” BMC Biotechnology, Vol. 13, 2013, p. 4.
[51] J. D. Smith, K. K. Kidwell, M. A. Evans, R. J. Cook and
R. W. Smiley, “Assessment of Spring Wheat Genotypes
for Disease Reaction to Rhizoctonia solani AG-8 in Con-
trolled Environment and Direct-Seeded Field Evaluations,”
Crop Science, Vol. 43, No. 2, 2003, pp. 694-700
[52] M. Tomaso-Peterson and L. E. Trevathan, “Characteriza-
tion of Rhizoctonia like Fungi Isolated from Agronomic
Crops and Turfgrasses in Mississippi,” Plant Disease,
Vol. 91, No. 3, 2007, pp. 260-265.
[53] D. E. Carling, “Grouping in Rhizoctonia solani by Hyphal
Anastomosis Interactions,” In: B. Sneh, S. Jabaji-Hare, S.
Neate and G. Dijst, Eds., Rhizoctonia Species: Taxonomy,
Ecology, Pathology and Disease Control, III.1., Kluwer,
Dordrecht, 1996, pp. 35-48.
[54] V. G. Garcia, M. A. P. Onco and V. R. Susan, “Review.
Biology and Systematics of the Form Genus Rhizocto-
nia,” Spanish Journal of Agricultural Research, Vol. 4,
No. 1, 2006, pp. 55-79.
[55] J. Kuhn, R. Rippel and U. Schmidhalter, “Abiotic Soil
Properties and the Occurrence of Rhizoctonia Crown and
Root Rot in Sugar Beet,” Journal of Plant Nutrition and
Soil Science-Zeitschrift fur Pflanzenernahrung und Boden-
kunde, Vol. 172, No. 5, 2009, pp. 661-668.
[56] T. J. Lewandowski, K. E. Dunfield and P. M. Antunes,
“Isolate Identity Determines Plant Tolerance to Pathogen
Attack in Assembled Mycorrhizal Communities,” PLOS
One, Vol. 8, No. 4, 2013, Article ID: E61329.
[57] M. Mazzola, “Manipulation of Rhizosphere Bacterial Com-
munities to Induce Suppressive Soils,” Journal of Nema-
tology, Vol. 39, No. 3, 2007, pp. 213-220.
[58] J. Varga, Z. Naár and C. Dobolyi, “Selective Feeding of
Collembolan Species Tomocerus longicornis (Müll.) and
Orchesella cincta (L.) on Moss Inhabiting Fungi,” Pedo-
biologia, Vol. 46, No. 6, 2002, pp. 526-538.
[59] M. Mazzola and Y. H. Gu, “Wheat Genotype-Specific In-
duction of Soil Microbial Communities Suppressive to
Disease Incited by Rhizoctonia solani Anastomosis Group
AG-5 and AG-8,” Phytopathology, Vol. 92, No. 12, 2002,
pp. 1300-1307.
[60] S. A. Deepak, G. Oros, S. G. Sathyanarayana, H. Shekar
Shetty and S. Sashikanth, “Antisporulant Activity of Wa-
tery Extracts of Plants against Sclerospora graminicola
Causing Downy Mildew Disease of Pearl Millet,” Ameri-
can Journal of Agricultural and Biological Sciences, Vol.
2, No. 1, 2007, pp. 36-42.
[61] S. A. Deepak, G. Oros, S. G. Sathyanarayana, N. P. Shet-
ty, H. S. Shetty and S. Sashikanth, “Antisporulant Activi-
ty of Leaf Extracts of Indian Plants against Sclerospora
graminicola Causing Downy Mildew Disease of Pearl
Millet,” Archives of Phytopathology and Plant Protec-
tion, Vol. 38, No. 1, 2005, pp. 31-39.
[62] C. A. Bradley, G. L. Hartman, L. M. Wax and W. L. Pe-
dersen, “Influence of Herbicides on Rhizoctonia Root and
Hypocotyl Rot of Soybean,” Crop Protection, Vol. 21,
No. 8, 2002, pp. 679-687.
[63] H. Lee, S. E. Ullrich, I. C. Burke, J. Yenish and T. C.
Paulitz, “Interactions between the Root Pathogen Rhizo-
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection 2257
ctonia solani AG-8 and Acetolactate-Synthase-Inhibiting
Herbicides in Barley,” Pest Management Science, Vol. 68,
No. 6, 2012, pp. 845-852.
[64] J. B. S. Haldane, “Disease and Evolution,” La Ricera Sci-
entifica Supplemento, Vol. 19, 1949, pp. 1-11. Reproduced
in Current Science, Vol. 63, No. 9-10, 1992, pp. 599-603.
[65] D. J. Lyon, A. J. Bussan, J. O. Evans, C. A. Mallory-
Smith and T. F. Peeper, “Pest Management Implications
of Glyphosate-Resistant Wheat (Triticum aestivum) in the
Western United States,” Weed Technology, Vol. 16, No. 3,
2002, pp. 680-690.[0680:PM
[66] R. Dean, J. A. L. Van Kan, Y. A. Pretorius, K. E. Ham-
mond-Kosack, A. Di Pietro, P. D. Spanu, J. J. Rudd, M.
Dickman, R. Kahmann, J. Ellis and G. D. Foster, “The
Top 10 Fungal Pathogens in Molecular Plant Pathology,”
Molecular Plant Pathology, Vol. 13, No. 4, 2012, pp. 414-
[67] M. G. Cromey, R. C. Butler, H. J. Boddington and A. R.
Moorhead, “Effects of Sharp Eyespot on Yield of Wheat
(Triticum aestivum) in New Zealand,” New Zealand Jour-
nal of Crop and Horticultural Science, Vol. 30, No. 1,
2002, pp. 9-17.
[68] K. L. Schroeder and T. C. Paulitz, “Effect of Inoculum
Density and Soil Tillage on the Development and Sever-
ity of Rhizoctonia Root Rot,” Phytopathology, Vol. 98,
No. 3, 2008, pp. 304-314.
[69] M. Anees, V. Edel-Hermann and C. Steinberg, “Build up
of Patches Caused by Rhizoctonia solani,” Soil Biology &
Biochemistry, Vol. 42, No. 10, 2010, pp. 1661-1672.
[70] K. Kalpana, S. Maruthasalam, T. Rajesh, K. Poovannan,
K. K. Kumar, E. Kokiladevi, J. A. J. Raja, D. Sudhakar, R.
Velazhahan, R. Samiyappan and P. Balasubramanian,
“Engineering Sheath Blight Resistance in Elite Indica
Rice Cultivars Using Genes Encoding Defense Proteins,”
Plant Science, Vol. 170, No. 2, 2006, pp. 203-215.
[71] M. M’hamdi, H. Chikh-Rouhou, N. Boughalleb and J. I.
R. de Galarreta, “Ribosome Inactivating Protein of Barley
Enhanced Resistance to Rhizoctonia solani in Transgenic
Potato Cultivar ‘Desiree’ in greenhouse conditions,” Bio-
technologie Agronomie Societe et Environnement, Vol. 17,
No. 1, 2013, pp. 20-26.
[72] P. A. O’Brien, G. C. MacNish and N. M. K. Milton,
“Transgenic Tobacco Plants Show Different Resistance to
Rhizoctonia solani AG 4 and AG 8,” Australasian Plant
Pathology, Vol. 30, No. 3, 2001, pp. 221-225.
[73] R. Velazhahan, R. Radhajeyalakshmi, R. Thangavelu and
S. Muthukrishnan, “An Antifungal Protein Purified from
Pearl Millet Seeds Shows Sequence Homology to Lipid
Transfer Proteins,” Biologia Plantarum, Vol. 44, No. 3,
2001, pp. 417-421.
[74] K. Krishnamurthy, C. Balconi, J. E. Sherwood and M. J.
Giroux, “Wheat Puroindolines Enhance Fungal Disease
Resistance in Transgenic Rice,” Molecular Plant-Microbe
Interactions, Vol. 14, No. 10, 2001, pp. 1255-1260.
[75] D. Q. Luo, H. Wang, X. Tian, H. J. Shao and J. K. Liu,
“Antifungal Properties of Pristimerin and Celastrol Iso-
lated from Celastrus hypoleucus,” Pest Management Sci-
ence, Vol. 61, No. 1, 2005, pp. 85-90.
[76] J. A. Anderson and J. A. Kolmer, “Rust Control in Gly-
phosate Tolerant Wheat Following Application of the
Herbicide Glyphosate,” Plant Disease, Vol. 89, No. 11,
2005, pp. 1136-1142.
[77] T. Zhu, F. Song and Z. Zheng, “Molecular Characteriza-
tion of the Rice Pathogenesis-Related Protein, OsPR-4b,
and Its Antifungal Activity against Rhizoctonia solani,”
Journal of Phytopathology, Vol. 154, No. 6, 2006, pp.
[78] M. H. Kim, S. C. Park, J. Y. Kim, S. Y. Lee, H. T. Lim,
H. Cheong, K. S. Hahm and Y. Park, “Purification and
Characterization of a Heat-Stable Serine Protease Inhibi-
tor from the Tubers of New Potato Variety ‘Golden Val-
ley’,” Biochemical and Biophysical Research Communi-
cations, Vol. 346, No. 3, 2006, pp. 681-686.
[79] S. M. Zhang, Y. X. Wang, L. Q. Meng, J. Li, X. Y. Zhao,
X. Cao, X. L. Chen, A. X. Wang and J. F. Li, “Isolation
and Characterization of Antifungal Lipopeptides Pro-
duced by Endophytic Bacillus amyloliquefaciens TF28,”
African Journal of Microbiology Research, Vol. 6, No. 8,
2012, pp. 1747-1755.
[80] X. Y. Zhao, X. M. Zhao, Y. M. Wei, Q. X. Shang and Z.
P. Liu, “Isolation and Identification of a Novel Antifungal
Protein from a Rhizobacterium Bacillus subtilis Strain
F3,” Journal of Phytopathology, Vol. 161, No. 1, 2013,
pp. 43-48.
[81] Y. Li, M. P. Zhou, Z. Y. Zhang, L. J. Ren, L. P. Du, B. Q.
Zhang, H. J. Xu and Z. Y. Xin, “Expression of a Radish
Defensin in Transgenic Wheat Confers Increased Resis-
tance to Fusarium graminearum and Rhizoctonia cerea-
lis,” Functional & Integrative Genomics, Vol. 11, No. 1,
2011, pp. 63-70.
[82] P. Faccio, C. Vazquez-Rovere, E. Hopp, G. Gonzalez, C.
Decima-Oneto, E. Favret, A. D. Paleo and P. Franzone,
“Increased Tolerance to Wheat Powdery Mildew by Hete-
rologous Constitutive Expression of the Solanum chaco-
ense Snakin-1 Gene,” Czech Journal of Genetics and Plant
Breeding, Vol. 47, 2011, pp. S135-S141.
[83] J. D. Smith, K. K. Kidwell, M. A. Evans, R. J. Cook and
R. W. Smiley, “Evaluation of Spring Cereal Grains and
Wild Triticum germplasm for Resistance to Rhizoctonia
solani AG-8,” Crop Science, Vol. 43, No. 2, 2003, pp.
[84] G. Kovacs, L. Sagi, G. Jacon, G. Arinaitwe, J. P. Buso-
Open Access AJPS
Susceptibility of Wheat Varieties to Soil-Borne Rhizoctonia Infection
Open Access AJPS
goro, E. Thiry, H. Strosse, R. Swennen and S. Remy,
“Expression of a Rice Chitinase Gene in Transgenic Ba-
nana (‘Gros Michel’, AAA Genome Group) Confers Re-
sistance to Black Leaf Streak Disease,” Transgenic Re-
search, Vol. 22, No. 1, 2013, pp. 117-130.
[85] S. Ignacimuthu and S. A. Ceasar, “Development of Trans-
genic Finger Millet (Eleusine coracana (L.) Gaertn.) Re-
sistant to Leaf Blast Disease,” Journal of Biosciences,
Vol. 37, No. 1, 2012, pp. 135-147.
[86] S. Alamri, M. Hashem and Y. S. Mostafa, “In Vitro and
In Vivo Biocontrol of Soil-Borne Phytopathogenic Fungi
by Certain Bioagents and Their Possible Mode of Ac-
tion,” Biocontrol Science, Vol. 17, No. 4, 2012, pp. 155-
[87] S. Vijayan, N. K. Singh, P. Shukla and P. B. Kirti, “De-
fensin (TvD1) from Tephrosia villosa Exhibited Strong
Anti-Insect and Anti-Fungal Activities in Transgenic To-
bacco Plants,” Journal of Pest Science, Vol. 86, No. 2,
2013, pp. 337-344.
[88] R. C. Foley, C. A. Gleason, J. P. Anderson, T. Hamann
and K. B. Singh, “Genetic and Genomic Analysis of
Rhizoctonia solani Interactions with Arabidopsis; Evi-
dence of Resistance Mediated through NADPH Oxi-
dases,” PLoS ONE, Vol. 8, No. 2, 2013, Article ID:
[89] E. E. Helliwell, Q. Wang and Y. N. Yang, “Transgenic
Rice with Inducible Ethylene Production Exhibits Broad-
Spectrum Disease Resistance to the Fungal Pathogens
Magnaporthe oryzae and Rhizoctonia solani,” Plant Bio-
technology Journal, Vol. 11, No. 1, 2013, pp. 33-42.
[90] H. Bouzenna and L. Krichen, “Pelargonium graveolens
L’Her and Artemisia arborescens L. Essential Oils: Che-
mical Composition, Antifungal Activity against Rhizoc-
tonia solani and Insecticidal Activity against Rhysopertha
dominica,” Natural Product Research, Vol. 27, No. 9,
2013, pp. 841-846.
[91] C. H. Liu, W. X. Zou, H. Lu and R. X. Tan, “Antifungal
Activity of Artemisia annua Endophyte Cultures against
Phytopathogenic Fungi,” Journal of Biotechnology, Vol.
88, No. 3, 2001, pp. 277-282.
[92] F. J. Chen, X. H. Long, M. N. Yu, Z. P. Liu, L. Liu and H.
B. Shao, “Phenolics and Antifungal Activities Analysis in
Industrial Crop Jerusalem Artichoke (Helianthus tubero-
sus L.) Leaves,” Industrial Crops and Products, Vol. 47,
2013, pp. 339-345.
[93] S. Pietr and G. Oros, “Antifungal Properties of Polypep-
tide Antibiotics Produced by Some Strains of Bacillus
subtilis,” Tagungsbericht der Akademie der Landwirts-
chafts-Wissenschaften DDR, Vol. 253, 1987, pp. 261-266.
[94] L. Zheng, H. Q. Liu, M. L. Zhang, X. Cao and E. X. Zhou,
“The Complete Genomic Sequence of a Novel Mycovirus
from Rhizoctonia solani AG-1 IA Strain B275,” Archives
of Virology, Vol. 158, No. 7, 2013, pp. 1609-1612.
[95] S. McGinley, “Rott Border Cells Defense Plants.”
[96] M. C. Hawes, U. Gunawardena, S. Miyasaka and X. Zhao,
“The Role of Root Border Cells in Plant Defense,”
Trends in Plant Science, Vol. 5, No. 3, 2000, pp. 128-133.
[97] M. C. Hawes, L. A. Brigham, F. Wen, H. H. Woo and Y.
Zhu, “Function of Root Border Cells in Plant Health:
Pioneers in the Rhizosphere,” Annual Review of Phyto-
pathology, Vol. 36, 1998, pp. 311-327.
[98] S. A. Deepak, K. R. Kottapalli, K. G. Rakwal, G. Oros, K.
S. Rangappa, H. Iwahashi, Y. Masuo and G. K. Agrawal,
“Real-Time PCR: Revolutionizing Detection and Expres-
sion Analysis of Genes,” Current Genomics, Vol. 8, No.
4, 2007, pp. 234-251.
[99] F. O. Amulaka, J. N. Maling’a, M. Cakir and R. M. S.
Mulwa, “Development and Characterization of Wheat
Germplasm with Combined Resistance to Russian Wheat
Aphid and Stem Rust (Race ‘Ug99’) in Kenya,” Ameri-
can Journal of Plant Sciences, No. 4, 2013, pp. 767-773.
[100] S. L. Zeller, O. Kalinina, S. Brunner, B. Keller and B.
Schmid, “Transgene 6 Environment Interactions in Gene-
tically Modified Wheat,” PLoS ONE, Vol. 5, No. 7, 2010,
Article ID: E11405.
[101] G. K. Agrawal, R. Rakwal and A. Sarkar, “‘Cost of
Knowledge’ and ‘Quality of Knowledge’: Looking to-
ward Future,” International Journal of Life Sciences, Vol.
7, No. 1, p. i.