Plant Cell Biotechnology and Molecular Biology 21(15&16):23­33; 2020 ISSN: 0972­2025

FIRST REPORT OF Rhizoctonia solani CAUSING

DAMPING-OFF AND ROOT ROT DISEASE ON
Tetraclinis articulata SEEDLINGS
R. EL HADDADI, A. ERRIFI, S. MSAIRI, A. OUAZZANI TOUHAMI AND A. DOUIRA*
Laboratoire de Botanique, Biotechnologie et Protection des Plantes, Faculté des Sciences,
Université Ibn Tofail, Kenitra, Morocco [REH, AE, SM, AOT, AD].
[*For Correspondence: E­mail: allal.douira@uit.ac.ma]

Received: 10 April 2020

Accepted: 16 June 2020
Published: 25 June 2020 Original Research Article
_______________________________________________________________________________________________

ABSTRACT
Rhizoctonia solani (Kühn) is a soil-borne, necrotrophic fungus causing damping off, root rot and
stem canker in many cultivated plants worldwide. Recently, R. solani was isolated from thuya
[Tetraclinis articulata (Vahl.) Mast.] seedlings showing damping-off disease in Sidi Amira Forest
nursery, northwest Morocco. A pure culture of R. Solani, originally isolated from (5 weeks) T.
articulata diseased seedlings, was used as inoculum of growing media with a (3:1,v,v) mixture of
peat/vermiculite filled in 400 ml plastic containers with 50 wells. For the control containers, mock
inoculum was added in each well. Pregerminated seeds of T. Articulata, brought from a Kourifla
forest stand, were sown in a set of 4 containers for each treatment. Seedlings were grown up in a
glasshouse in separated blocks to avoid any risk of contamination. After 3 weeks, pre-emergence,
post-emergence damping-off, root rot and stem necrosis were observed in seedlings grown in
containers with inoculated substrate while control sets remained asymptomatic. Koch’s postulate is
verified by reisolating R. Solani from roots and hypocotyl of seedlings grown in inoculated growing
media. Pathogenicity test revealed that pre-emergence, post-emergence mortality rate, disease index
and growth parameters were significantly different comparing to control.

Keywords: Damping­off disease; Tetraclinis articulata; Rhizoctonia solani; symptoms; Koch’s postulate;
pathogenicity; Morocco.

INTRODUCTION Damping­off was considered “the most serious

Production of seedlings in the nursery is an
integral part of forest regeneration and restoration
programs. Damage to seedlings in the nursery
may result in crop losses or poor field
performance after outplanting in the field [1].
Diligent record keeping, evaluation and
reporting of seedling performance is critical to
correctly identify the cause of damage and its
etiology, so effective and economically viable
treatments can be applied to check future
damage.
problem encountered in raising nursery
seedlings,” and consequently was one of the most
focused research subject since the beginning of its
description by Hartley and Pierce in 1917 [2].
Dampingoff involves non­germination, prevention
of seedling emergence after germination, or the
rotting and collapse of seedlings at the soil level
[3,4,5]. Damping­off can be caused by a number
of biotic or abiotic factors, which prevent seeds to
germinate or seedlings to emerge. As a
consequence, the symptoms associated with
damping­off widely vary depending on the

23

stresses associated and time of its occurrence [2].
In general, many fungi and fungi­like species have
been reported as the most important biotic stress
weakening or destroying seeds and seedlings of
almost all species including fruit, vegetable, field,
ornamental, and forestry crops [6]. However,
Fusarium sp., Rhizoctonia sp., Pythium sp. and
Phytophthora sp. are the most frequently
associated fungi with damping­off and are
considered causal agents of this problem in the
literature [3,7,8,9].
Recently a damping­off disease of thuya
[Tetraclinis articulata (Vahl.) Mast.] seedlings
caused by Fusarium solani was identified in Sidi
Amira Forest nursery, northwest Morocco
(34.050341°N, 06.671741°W; 130 m elevation)
[10]. The symptoms include scattered chlorotic or
curled needles followed by tip dieback, root rot
with reduced secondary roots development and
stunting of plants as the disease progresses.
However, some diseased seedlings showed other
symptoms else those described above. Such
randomly distributed diseased seedlings of 3­5
weeks age showed constricted cankered stem on
the ground line with roots rot. In such plants, the
epicotyl stayed green until the seedling collapses
as if it were sheared at ground level (Fig. 1).
Preliminary isolation of fungal species from roots
and stem of seedlings showing symptoms of
Fig. 1. (A) Newly emerged Tetraclinis articulata seedling killed by post-emergence damping-off;
(B): Diseased seedlings showing (b) discoloured, constricted area of stem just above the ground line
and (c) primary root rot
24
El Haddadi et al.
damping­off revealed 9% presence of Rhizoctonia
solani in isolated lot [10].
R. solani is a ubiquitous soil borne necrotroph
that inflicts damage on a wide range of
economically important crops [11]. Considerable
diversity in colony morphology, biochemical and
molecular markers, pathogenicity and
aggressiveness exist among members of this
species, which has permitted their classification
into 14 somatically incompatible groups otherwise
termed anastomosis groups (AGs) [12,13,14,15].
R. solani attacks members of the Poaceae ( maize,
rice, wheat, barley, oat), Fabaceae (soybean,
peanut, dry bean, alfalfa, chickpea, lentil, field
pea), Solanaceae (tobacco, potato),
Amaranthaceae (sugar beet), Brassicaceae
(canola), Rubiaceae (coffee), Malvaceae (cotton),
Asteraceae (lettuce), Araceae (pothos), Moraceae
(ficus) and Linaceae (flax) family [11,13]. R.
solaniwas reported to cause damping­off disease
of many forest species around the world: Pinus
nigra (France) [16], Eucalyptus sp. (China [17],
Brazil [18] and South Africa [19]), Caragana
arborescens (Canada) [20], Picea smithiana
(India) [21], Pinus palustris (USA: Florida [22]
and Poland [23]), Acacia mangium (Phillipines)
[24], Rosmarinus officinalis (S. korea) [25],
Abies alba , Alnus glutinous, Betula pendula,
Larix decidua and Picea abies (Norway)
[26].

Symptoms on diverse hosts include seed rot, root
rot, hypocotyl rot, crown rot, stem rot, limb rot,
pod rot, stem canker, black scurf, seedling blight,
and pre­ and post­emergence damping off [13].
Losses caused by Rhizoctonia sp. damping­off
disease increase with increasing level of soil
temperatures and dryness [27] and decrease with
excessive moisture [28]. Rhizoctonia sp. is less
affected by pH [29] and the activity of the fungus
in the soil is greatly stimulated by nitrogen: In
soils with high carbon to nitrogen ratios, the
activity of Rhizoctonia decreases [30]. This
fungus can be transmitted through seeds, water or
by airborne spores, but spread by infected soil is
most common because the fungus overwinters in
soil as sclerotia [31]. Sclerotia, which arise from
undifferentiated hyphae or monilioid cells [32],
germinate to form mycelia and serve as an
inoculum source for infection [33] and disease
spread.
The objective of the present study was to isolate
the pathogens responsible for damping­off
symptoms newly observed on T. articulata
seedlings, and to prove its pathogenicity to fulfil
the Koch’s postulate.
MATERIALS AND METHODS
Isolation of Fungi
Diseased seedlings were brought to the laboratory
and isolations were made from roots, hypocotyls,
and leaves (needles) segments. The segments were
cut into 1 cm fragments, disinfected with alcohol
for five minutes, rinsed with sterile distilled water,
dried on sterile filter paper and then deposited on
PSA medium (Potato Sucrose Agar: 200 g potato,
20 g sucrose, 15 g agar­agar, 1000 ml of distilled
water) and incubated in darkness at 25°C. The
identification of the fungi imperfect was based on
morphological criteria using microscopic
observations of the culture after purification on
different culture media. Isolation percentage Pi
(%) was obtained by applying the following
formula:
Pi (%) = (NSX/NT)*100
With: NSX is the number of segment containing the
fungal species X and NT is the total number of
colonies of all isolated species.
25
El Haddadi et al.
Preparation of Inoculum and Growing Media
A pure culture of R. Solani originally isolated
from 5 weeks diseased T. articulata seedlings in
the Sidi Amira forest nursery was made on PSA
medium (Potato Sucrose Agar: 200 g potato, 20 g
sucrose, 15 g agar­agar, 1000 ml of distilled
water). The fungus was maintained on PSA in
petri plates (at 25°C) for a week. For inoculum
preparation, 250 ml conical flaks, each containing
about 10 g of barley grains soaked overnight in
sterilized distilled water were used. The media in
flaks were autoclaved for 30 min for two
consecutive days. After the flaks were cooled each
one was inoculated with a small block (5 mm
diameter) taken from the periphery of the seven
day­old cultures on PSA. The flaks were, then,
incubated at 27°C for two weeks. During
incubation the flaks were shaken twice a day to
ensure homogeneous growth of fungal mycelium
on the barley seeds. 5 g plugs of the fungal­
colonized barley seeds were used as inoculum.
T. articulata seeds previously collected (25
September 2018) in a Kourifla forest stand
(33.713122°N, 06.707834°W, 220 m elevation),
stratified at 4°C, were surface sterilized in 2%
NaOCl for 15 minutes, soaked in distilled water
for 48 hours in room temperature (18­20°C) then
surface sterilized in 2% NaOCl for 5 minutes,
followed by two rinses with distilled water and
then pre­germinated on soaked filter paper and
kept in dark at room temperature (18­20°C) for 6
days.
New 400 ml plastic containers with 50 wells were
filled with a (3:1,v,v) mixture of free­pathogen
peat and vermiculite up to 1 cm and then each
well was inoculated with one mycelia plug at
(50:1,w/w) growing medium/inoculum of
Rhizoctonia solani. A layer (0.5 cm) of growing
medium was added above the inoculum and one
pre­germinated sterile seed of T. Articulata was
softly placed in each well and covered with
growing medium in order to fill up the well (0.5
cm layer). For the control wells, 1 barely meal
plug without inoculum (mock inoculum) was
added in each well. The containers were kept in a
glasshouse in separated blocks to avoid any risk of
contamination during sowing seeds and growing­
up the seedlings.

Experimental Design
Pathogenicity test experimental design was carried
out by adopting a completely randomized design
with four replicates and every single container
with 50 seedlings constituted one experimental
unit. In all, 4 containers were allocated for
Rhizoctonia­inoculated substrate and 4 containers
as control.
Measured Parameters and Plant
Characteristics
After the appearance of damping­off symptoms,
emergence and survival were assessed daily and
final counts were taken on the 62 days post
inoculation and then seedlings were removed from
the wells, washed and assessed for diseases. Shoot
and roots length (primary and lateral), leaves, and
secondary root number was recorded for each
seedling to estimate the degree of R. solani species
on juvenile thuya seedlings. Reduction in growth
was calculated for each plant characteristic using
the following formula:
Reduction in growth (%) = [(G1­
G2)/G1]*100
Where: G1 is the mean of the measured parameter
for control plants and G2 is the mean of measured
parameter for inoculated plants.
Disease Assessment
Disease assessment was made with using disease
severity category scales [34,35,36]: For
hypocotyls disease, the seedlings were categorised
on a scale of 0­4 (0 = no lesions or discoloration, 1
= small lesion on the hypocotyl with reddish to
brown coloration affecting < 25% of the hypocotyl
length, 2 = dark to brown, brown, or black lesions
covering 25­50% length of the hypocotyl, 3 =
necrosis affecting more than 50% length of the
hypocotyl , 4 = completely dead or not emerged),
primary root disease, on 0–6 scale (0 = no lesions,
1 = small lesions on primary root, 2 =
discoloration or necrosis covering less than 25%
of the primary root, 3 = necrosis covering up to
25­50% of primary root, 4 = necrosis covering 50­
75% of primary root, 5 = necrosis covering >75%
of primary roots, 6= completely dead or not
emerged) and lateral roots disease, on 0­6 scale (0
26
El Haddadi et al.
= no symptoms, 1 = 1 lateral root girdled, 2 = 2 to
5 lateral roots girdled, 3 = 6 to 9 lateral roots
girdled, 4 = 10 to 13 lateral roots girdled, 5 = >14
lateral roots girdled, 6= dead or not emerged).
Disease index DI (%) was calculated as:
∗
(%) = ∗ 100
∗
Where Ni: Number of plants in disease category;
di: Numerical value of disease category; N:
Number of plants in all categories; D: Maximum
value on rating scale.
Pathogen Reisolation
Following disease assessments, thirty six roots,
hypocotyls and leaves segments were randomly
taken from plants grown in inoculated substrate
and controls, washed with water, disinfected with
90° alcohol for 1 to 2 minutes, rinsed thoroughly
with sterile water, dried on a sterile filter paper
and then deposited in Petri dishes containing PSA
medium to reisolate the respective pathogen
strains to fulfil Koch’s postulate. The observation
of the cuts were done after seven days.
Parmeter and Whitney [12] defined a certain
number of morphological criteria to determine R.
solani. But this sterile vegetative form is common
to 2 Basidiomycetes: Thanatephorus cucumeris
(Frank­Donk) and Ceratobasidium sp. (Rodger).
The strains attached to T. cucumeris correspond to
the species R. solani and have more than two
nuclei per mycelial septa (article); those related to
Ceratobasidium sp. are always binucleate [11]. A
simple technique [37] makes it possible to count
the nuclei and to separate the strains of the 2
genera: A drop of aniline blue (at 1%) in alcoholic
solution (at 2%) is deposited on a thin layer of the
fringe of cultures carried out on 1.5% malt
medium. After covering with a cover slip, the
nuclei are counted under a microscope (G x 40)
after 2 to 4 h of staining at laboratory temperature
under lighting.
Statistical Analysis
Fisher’s variance test was performed to test for
homogeneity of variance between the trial repeats
 El Haddadi et al.

and the Shapiro­Wilk test was performed to test
for normality. The student’s t­test was calculated
at the 5% confidence level to compare treatment
means. All statistical analysis was performed
using XLSTAT software (2016).
RESULTS AND DISCUSSION
Fungi Characteristics in Culture
Fungi identification was based on vegetative
characters. Cultures vary in colour from pale
yellow to dark brown. Septate multinucleate (more
than two nucleus) hyphae appear hyaline when
young, but turn brown with age. The fungi do not
produce spores in culture. However, cultures
develop gray to dark brown sclerotia (Fig. 2).
Conidia, clamp connections, rhizomorphs, and
cultural pigmentations other than brown were not
observed. Microscopically, the fungus is
recognized by the characteristic right­angle
branching of the hyphae, which have constrictions
at the points where they connect with parent
hyphae (Fig. 3). Largest hyphae diameter range
between 6 and 10 µm. In older cultures, cross
walls usually develop just beyond the hyphal
constrictions. Our morphological observations are
in conformity with those described by Parmeter &
Whitney [12], Barnett & Barry [38] and Genhua &
Chengyun [39].

Fig. 2. Typical culture of Rhizoctonia solani showing: (A) Young (5 days) hyaline cottony culture
with gray sclerotia and (B) Characteristic brown sclerotia on old culture (15 days) culture

Fig. 3. Hyphae of Rhizoctonia solani showing: (A): Characteristic right-angle branching and
(B): (a) constrictions near septa and (b) multinucleate septa

27

Disease Symptoms on Thuya Seedlings
Three different types of disease symptom are
recognized:
1. Pre-emergence damping-off: This disease
affects seeds and germinants before they emerge.
Pre­emergence damping­off is a difficult disease
to diagnose because the affected seeds are not
visible; consequently, the losses are often
attributed to “poor seed”. If the germinants have
not emerged after a reasonable period, the seed
should be excavated and examined; if the seed
contents are decayed, then damping­off fungi may
be involved. Sometimes, germinating seeds are
killed after the radicle has emerged.
2. Post-emergence damping-off: This affects
young seedlings until their stems become woody.
The classic symptoms of post­emergence
damping­off include decay of the seedling
hypocotyl at the ground line (Fig. 4), causing the
seedling to topple over (Fig. 5). The symptoms of
post­emergence damping­off of thuya seedlings
occur at or slightly below the ground line and
result in water­soaked (Fig. 6), brownish or
blackish lesions that rapidly become sunken or
constricted. Lesions can progress along the stem
to reach the roots (Fig. 7). Other stresses such as
Fig. 4. Constriction and Fig. 5. Post-emergence
decay of the seedling damping-off causes a
hypocotyl at the ground constriction and decay
line (2 weeks old post- of the seedling stem (5
sowing) weeks old post-sowing)
28
El Haddadi et al.
heat or chemicals can facilitate the occurrence of
damping­off symptoms; for instance, the surfaces
of dark soils or mulches can become so hot that
they kill seedling stem tissue. For damping­off
caused by heat injury, the stem affected tissues are
always sun­sided located (South exposed), in
contrary, R. solani girdles all collar tissues and
causes its constriction. The distinguishing
characteristic between biotic and abiotic damping­
off is the presence of decayed root tissue.
3. Roots rot: Both primary root and lateral roots
are affected; brownish and blackish lesions extend
along the root system and form necrosis of the
cambium tissues which result in its decay. The
disease destroys lateral roots and makes it
fragmented (Fig. 8). Root rot is often associated
with lack of feeders (Fig. 9).
Pathogenicity of Rhizoctonia solani on Thuya
Seedlings
Pathogenicity test for R. solani proved the ability
of this fungus to cause damping­off disease in
young T. articulata seedlings. This fungus attacks
in particular the root system and the collar of
young seedlings without extending to the aerial
system (Table 1). Indeed, reisolation percentage of
the fungus from the epicotyl region remains zero
Fig. 6. water-soaked, Fig. 7. Necrosis
brownish to blackish extending from
lesions turning into a diseased primary
stem canker root along the stem

Fig. 8. Decay and Fig. 9.Lack of lateral roots on a diseased (left) compared to a healthy
fragmentation of a an (right) seedlings (4 weeks old post-sowing)
affected lateral root
compared to that recorded in the hypocotyl (70%),
primary roots (70%) and lateral roots (65%). The
pathogenic effect of R. solani was also confirmed
by the significant level of difference (p value
=0.01) in survival rate of inoculated (69%) and
non­inoculated seedlings (92.5%) (Table 2, Fig.
10).
Damping­off disease is particularly pronounced
during pre­emergence phase with severity of
26.5% compared to 4.5% under post­emergence
phase (Table 2). This shows that this fungus
inhibits the completion of seeds germination
process. Pre­emergence damping­off occurs when
fungi infect developing radicals and kill seedlings
while shoot tissues are still below ground.
However other problem can cause similar effects,
including non­uniform seeds, poor seed vigour
and development, seed decay, and removal of
substrate by wind or irrigation splashes.
Post­emergence damping­off occurs when fungi
infect the succulent tissue of germinate of above
ground shoots, causing decay, wilting, and death.
Infection occurs on the stem but only slightly
29
El Haddadi et al.
below the ground line and on the roots. The
infected tissue appears as a purple to brown lesion
or as a dark water­soaked area that becomes
sunken and constricted in advance stage. Post­
emergence damping­off results in wilting and
collapse of the seedling.
Plants that may have passed the juvenile stage (>
60 days post­planting), the fungus continues to
attack the root system. Infection of older seedlings
results in progressive root rot with root systems
lacking an actively growing tip and having few
laterals. Such infected seedlings may continue to
grow as asymptomatic, but with drastic reduction
in shoot growth (Table 3).
Disease index (DI) recorded for the inoculated
plants reached respectively to the level of 50.5%,
56.92% and 59% for lateral roots, primary root
and hypocotyl. R. solani affected majority of
morphological attributes of seedlings grown in
infested soil. Shoots height was reduced by
18.85%, decreasing from 6.771 cm for the control
plants to 5.494 cm for the inoculated plants (p­
value <0.0001). Leaves number was reduced by
 El Haddadi et al.

10.74%, decreasing from an average of 41.622 to
37.152 (p­value <0.0001). Shoots growth
reduction suggests that the normal flow of water
and nutrients from the substrate through root
system and stem is disrupted. Indeed, the root
system also shows a clear reduction both in
laterals number (22.38%) and their average length
(21.01%) with total root system length reduction
by 24.68 per cent. Primary root length did not
record any difference between inoculated
seedlings and control (p­value = 0.736). This
shows that R. solani is more virulent at the level of
fine roots and collar than at primary roots which
continues its development despite the presence of
brown and dark lesions observed on superficial
tissues (cortex).
Preventing the pathogens from entering the
nursery is the best control but this is not always
possible, especially if we know that a necrotrophic
pathogen like R. solani with a wide host range
[13,40] is able to overwinter as long­lived
sclerotia in the soil, machines, containers and tools
or as a mycelia in crop debris which is a
characteristic feature of the fungus. Effective
management involve several control measure such

Fig. 10. Six weeks old thuya sedlings showing the pathogenic effect of R. solani: Control seedlings at
left and innoculated seedlings with reduced survival rate at right

Table 1. Reisolation percentage of Rhizoctonia solani from epicotyl, hypocotyl and root system of
inoculated and control thuya seedlings

Treatment Reisolation percentage (%) (*)

Epicotyl Hypocotyl Primary root Lateral roots
Inoculated seedlings 0a 70a 70a 65a
Control seedlings 0b 0b 0b 0b

(*) The results of the same column followed by different letters differ significantly at 5% level of significance

Table 2. Effect of Rhizoctonia solani on percent seedling emergence and disease index (DI %) (*) on
thuya seedlings

Treatment Pre-emergence Post-emergence Survival Hypocotyl Primary root Lateral root

damping-off (%) damping-off (%) (%) DI(%) DI(%) DI(%)
Inoculated seedlings 26.5 a 4.5 a 69 a 59 a 56.92 a 50.5 a
Control seedlings 7b 0.5 b 92.5 b 7.75 b(**) 8 b(**) 8.33 b(**)

(*)Mean of four replicates and based upon number of 50 seedlings. The results of the same column followed by different letters
differ significantly at 5% level of significance.
(**) seedlings not emerged

30
 El Haddadi et al.

Table 3. Thuya seedlings characteristics (*) under inoculated and un-inoculated (control) conditions

Treatment Shoot length Leaves Lateral root Lateral root Primary root Root system
(cm) number number length (cm) length (cm) length (cm)
Control seedlings 6.771 a 41.622 a 11.324 a 3.036 a 16.259 a 51.723 a
Inoculated seedlings 5.494 b 37.152 b 8.790 b 2.399 b 16.381 a 38.957 b
Reduction in growth 18.85% 10.74% 22.38% 21.01% ­ 24.68%

(*)Mean of four replicates and based upon number of 30 seedlings. The results of the same column followed by different letters
differ significantly at 5% level of significance

as the use of clean certified seeds, cleaning seed Pests, USDA, Forest Service; Agriculture
coats with a running water rinse [41] or sterilizing Handbook. 2012;680.
them with quick soak in dilute (1:10) bleach 2. Hartley C, Pierce RG. The control of
solution prior to sowing [4], use low pH pathogen­ damping­off of coniferous seedlings.
free growing media as mixture of commercial peat USDA Bull. 1917;453:32.
and vermiculite/perlite, reduce soil splash effect, 3. Lamichhane JR, Durr C, Schwanck AA,
use sterilised containers and keep them on raised Robin MJPH, Sarthou. Integrated
benches to prevent contact with surface water and management of damping­off diseases. A
runoff which can be contaminated. Likewise, review. Agronomy for Sustainable
keeping soil or growing media “moist, but not Development, Springer Verlag/EDP
wet” discourages damping­off [5]. Sciences/INRA. 2017;37(2):25.
4. Landis TD. Forest nursery pests: Damping­
CONCLUSION off. Forest Nursery Notes. 2013;2:25–32.
5. James RL. Damping­off. In: Cram M.M,
Rhizoctonia solani is able to prevent seedlings Frank M.S, Mallams KM, (Eds) For. Nurs.
emergence (pre­emergence damping­off), kills Pests. Agric. Handbook, vol. 680.USDA
seedlings directly (post­emergence damping­off) Forest Service, Washington DC. 2012;115–
or causes stem canker and root rot disease 116.
inducing stunting symptoms on T. articulata 6. Kraft JM, Haware MP, Halila H, et al.
seedlings. The affected root system often lacks Soilborne diseases and their control. In:
active growing root tips: this anomaly may cause Knight R, (Ed) Link. Res. Mark. Oppor.
establishment problems of young plants in the Pulses 21st Century. Kluwer Academic
field especially in harsh sites as in semi­arid areas. Publishers, Dordrecht. 2000;457–466.
To our knowledge, this is the first report of R. 7. Cram MM. Damping­off in tree nursery.
solani on thuya [Tetraclinis articulata (Val) Pacific Northwest­ Pest Management
Mast.] hitherto to unreported in Morocco and Handbooks; 2012.
throughout the world. Available:https://pnwhandbooks.org/node/3
AUTHORS’ CONTRIBUTIONS 88
8. Pérrin R. Les agents pathogènes du sol en
This work was carried out in collaboration among pépinières forestières: Prévision des risques
all authors. All authors read and approved the final –lutte. Revue Forestière Française
manuscript. XXXVIII­3. 1986;243­248.
9. Landis TD, Tinus RW, McDonald SE,
COMPETING INTERESTS Barnett JP. The container tree nursery
manual. The biological component: nursery
Authors have declared that no competing interests pests and mycorrhizae. Washington (DC):
exist. USDA Forest Service. Agriculture
Handbook. 1990;674(5):171.
REFERENCES 10. EL Haddadi R, Errifi A, Msairi S, Ouazzani
Touhami A, Douira A. First report of
1. Mallams MK. Starkey T. Evaluating Fusarium solani causing damping­off
damage to nursery crops. In: Forest Nursery disease on Tetraclinis articulata seedlings;

31

Plant Cell Biotechnology and Molecular
Biology. 2019;20(23&24):1106–1114.
11. Ajayi­Oyetundea OO, Bradleyb CA.
Rhizoctonia solani: Taxonomy, population
biology and management of Rhizoctonia
seedling disease of soybean. Plant
Pathology. 2018;67:3–17.
12. Parmeter JR, Whitney HS. Rhizoctonia
solani: Biology and pathology. Berkeley:
University of California Press. 1970;255.
13. Farr DF, Rossman AY. Fungal databases,
U.S. National Fungus Collections, ARS,
USDA; 2020.
Available:https://nt.ars­
grin.gov/fungaldatabases/
14. Hawksworth DL. A new dawn for the
naming of fungi: Impacts of decisions made
in Melbourne in July 2011 on the future
publication and regulation of fungal names.
MycoKeys. 2011;1:7–20.
15. Carling DE. Anastomosis groups and
subsets of anastomosis groups of
Rhizoctonia solani. Abstract in Proceedings
of the Third International Symposium on
Rhizoctonia. National Chung Hsing
University, Taichung, Taiwan. 2000;14.
16. Camporota P, Perrin R. Survey for
damping­off in forest nurseries in France.
Preliminary results. In: Perrin R, Sutherland
JR, Eds. Diseases and insects in forest
nurseries. Paris: Institut National de la
Recherche Agronomique. INRA. 1994;68:
51­58.
17. Dequn Z, Sutherland JR. Diseases of
eucalyptus forest nursery seedlings and
their management in forest nurseries in
Yunnan Province, China. In: Perrin R,
Sutherland JR, Eds. Diseases and insects in
forest nurseries. Paris: Institut National de
la Recherche Agronomique. INRA.
1994;68:45­49.
18. Ferreira FA, Garcia MCC, Sanfuentes EVS.
Evaluation of fungi for biocontrol of
Cylindrocladium scoparium, Rhizoctonia
solani and Botrytis cinerea to be used in
suspended Brazilian eucalyptus nurseries.
In: James RL, Ed. Proceedings of the 3rd
meeting of IUFRO Working Party
S7.03.04. Missoula (MT): USDA Forest
Service, Northern Region. Forest Health
Protection Report. 1997;97(4):134­137.
32
El Haddadi et al.
19. Viljoen A, Wingfield MJ, Crous PW.
Fungal pathogens in Pinus and Eucalyptus
seedling nurseries in South Africa: A
review. South African Foresty Journal.
1992;161:45­51.
20. Vaartaja O, Cram WH. Damping­off
pathogens of conifers and of Caragana in
Saskatchewan. Phytopathology. 1956;46:
391­397.
21. Singh O, Chaukiyal SP, Sharma HP.
Control against damping off in spruce
nurseries. Indian Journal of Forestry.
1985;8(4):321­322.
22. Starkey T, Enebak SA. Rhizoctonia blight
of southern pines. In: Cram MM, Frank
MS, Mallams KM, Tech. Coords. Forest
Nursery Pests. Washington (DC): USDA
Forest Service. Agriculture Handbook.
2012;680:63­65.
23. Belka M, Malgorzata M. Characteristics
and diversity of Rhizoctonia spp.
population in soil of selected bare­root
nurseries in Poland. Acta Mycologica.
2014;49(2):279­290.
24. Zethner O, Jorgensen J, Husaeni EA. The
current status of diseases and pests of forest
tree seeds in South East Asia, especially
diseases in Indonesia. In: ISTA Tree Seed
Pathology Meeting, Proceedings, 1996.
International Seed Testing Association.
1997;86­94.
25. Aktaruzzaman MD, Kim JY, Afroz T,
Kim BS. First report of web blight of
rosemary (Rosmarinus officinalis) caused
by Rhizoctonia solani AG­1­IB in
Korea. Mycobiology. 2015;43(2):170­
173.
26. Duda B, Orlikowski LB. Rhizoctonia solani
on coniferous seedlings in forest nurseries.
Journal of Plant Protection Research.
2004;44(3):175­180.
27. Wright E. Influence of temperature and
moisture on damping­off of American and
Siberian elm, black locust and
desertwillow. Phytopathology. 1957;47:
658­662.
28. Roth LF, Riker AJ. Influence of
temperature, moisture and soil reaction on
the damping­off of red pine seedlings by
Pythium and Rhizoctonia. Journal of
Agricultural Research. 1943;67:273­293.

29. Jackson LW. Effects of H­ion and Al­ion
concentrations on damping­off of conifers
and certain causative fungi. 36. Drizou F, Graham NS, Bruce TJA, Ray
Phytopathology. 1940;30:563­579.
30. Papavizas CG, Davey CB. Saprophytic
behavior of Rhizoctonia in soil.
Phytopathology. 1961;51:693­699.
31. Starkey T, Enebak SA. Rhizoctonia blight
of southern pines. In: Cram MM, Frank
MS, Mallams KM. Forest nursery pests.
Washington (DC): USDA Forest Service.
Agriculture Handbook. 2012;680:63­
65.
32. Sumner DR. Sclerotia formation by
Rhizoctonia species and their survival. In:
Sneh B, Jabaji­Hare S, Neate S, Dijst G,
Eds. Rhizoctonia species: Taxonomy,
Molecular Biology, Ecology, Pathology and
Disease Control. Dordrecht, Netherlands:
Kluwer Academic Publishers. 1996;207–
15.
33. Keijer J. The initial steps of the infection
process in Rhizoctonia solani. In: Sneh B,
Jabaji­Hare S, Neate S, Dijst G, Eds.
Rhizoctonia Species: Taxonomy, Molecular
Biology, Ecology, Pathology and Disease
Control. Dordrecht, Netherlands: Kluwer
Academic Publishers. 1996;149–62.
34. Lilja A, Lilja S, Poteri M, Ziren L. Conifer
seedling root fungi and root dieback in
finish nurseries. Scandinavian Journal of
Forest Research. 1992;7:547­556.
35. Khangura RK, Barbetti MJ, Sweetingham
MW. Characterization and pathogenicity of
_____________________________________________________________________________________
© Copyright International Knowledge Press. All rights reserved.
El Haddadi et al.
Rhizoctonia species on canola. Plant
Disease. 1999;83(8):714–21.
RV. Development of high­throughput
methods to screen disease caused by
Rhizoctonia solani AG 2­1 in oilseed rape.
Plant Methods. 2017;13:4.
37. Camporota P, Lucas P, Aouchiche H.
Variabilité du genre Rhizoctonia. In:
Variation et variabilité des agents
phytopathogènes Avignon 10­11 mai 1984,
Coll. de l’INRA. 1984;26:187­191.
38. Barnett HL, Barry BH. Illustrated genera of
imperfect fungi. American Phytopatho­
logical Society; Fourth Edition. 1998;240.
39. Genhua Y, Chengyun L. General
description of rhizoctonia species complex.
In: Cumagun CJ. (Ed.), Plant Pathology;
2012.
Available:http://www.intechopen.com/book
s/plant­pathology/general­description­of­
rhizocotonia­species­complex
40. Hielta AM, Sen R. Rhizoctonia associated
with forest trees. In: Sneh B, Jabaji­Hare S,
Neate S, Dijst G, Eds. Rhizoctonia Species:
Taxonomy, Molecular Biology, Ecology,
Pathology and Disease Control. Dordrecht,
Netherlands: Kluwer Academic Publishers.
2012;351­358.
41. Fraedrich SW, Cram MM. Seed fungi. In:
Cram MM, Frank MS, Mallams KM. Forest
nursery pests. Washington (DC): USDA
Forest Service. Agriculture Handbook.
2012;680:132­134.
33