Anthracnose of lucky bamboo Dracaena sanderiana caused by the fungus Colletotrichum dracaenophilum in Egypt

Journal of Advanced Research (2016) 7, 327–335

Cairo University

Journal of Advanced Research

ORIGINAL ARTICLE

Anthracnose of lucky bamboo Dracaena sanderiana
caused by the fungus Colletotrichum
dracaenophilum in Egypt
Ahmed A. Morsy, Ibrahim E. Elshahawy *
Plant Pathology Department, Agricultural and Biological Research Division, National Research Centre, Giza, Egypt

G R A P H I C A L A B S T R A C T

A R T I C L E

I N F O

Article history:
Received 4 November 2015
Received in revised form 21 January
2016
Accepted 22 January 2016
Available online 16 February 2016

A B S T R A C T
Dracaena sanderiana, of the family Liliaceae, is among the ornamental plants most frequently
imported into Egypt. Typical anthracnose symptoms were observed on the stems of imported
D. sanderiana samples. The pathogen was isolated, demonstrated to be pathogenic based on

Koch’s rule and identified as Colletotrichum dracaenophilum. The optimum temperature for
its growth ranges from 25 to 30 °C, maintained for 8 days. Kemazed 50% wettable powder
(WP) was the most effective fungicide against the pathogen, as no fungal growth was observed

* Corresponding author. Tel.: +20 1279180670; fax: +20 57 2403868.
E-mail address: (I.E. Elshahawy).
Peer review under responsibility of Cairo University.

Production and hosting by Elsevier
/>2090-1232 Ó 2016 Production and hosting by Elsevier B.V. on behalf of Cairo University.


328
Keywords:
Anthracnose
Dracaena sanderiana
Colletotrichum dracaenophilum
Lucky bamboo

A.A. Morsy and I.E. Elshahawy
over 100 ppm. The biocontrol agents Trichoderma harzianum and Trichoderma viride followed
by Bacillus subtilis and Bacillus pumilus caused the highest reduction in fungal growth. To
the best of our knowledge, this report describes the first time that this pathogen was observed
on D. sanderiana in Egypt.
Ó 2016 Production and hosting by Elsevier B.V. on behalf of Cairo University.

Introduction

Pathogenicity tests

Lucky bamboo (Dracaena sanderiana hort. ex Mast.) is among
the ornamental plants most frequently imported into Egypt.
This bamboo is also known as Dracaena braunii [1]. Although
the word bamboo occurs in several of its common names, D.
sanderiana is actually of an entirely different taxonomic order
from true bamboos. In Egypt, lucky bamboo is the most popular
indoor plant and is frequently imported and resold in attractive
pots. Colletotrichum spp. is an imperfect fungus belonging to the
Melanconiales. Members of the genus Colletotrichum cause diseases on a number of host plants. These diseases, often referred
to as anthracnose, include strawberry black spot and key lime
anthracnose (caused by Colletotrichum acutatum), tomato fruit
anthracnose (caused by Colletotrichum coccodes), red sorghum
stalk rot (caused by Colletotrichum graminicola), coffee berry
disease (caused by Colletotrichum kawahae), bean anthracnose
(caused by Colletotrichum lindemuthianum) and many others
[2]. Additional species of Colletotrichum with conidia greater
than 20 lm have been encountered on living plants of D. sanderiana (lucky bamboo) from China [3]. In Bulgaria and Iran,
Bobev et al. [4] and Komaki et al. [5], respectively, provided
the first reports that Colletotrichum dracaenophilum infects the
stems of potted D. sanderiana plants, causing anthracnose disease. In the United States, Sharma et al. [6] isolated, characterized and tested fungicide treatments to control Colletotrichum
spp. causing anthracnose on lucky bamboo, D. sanderiana. They
also reported that C. dracaenophilum caused the most severe disease on lucky bamboo, whereas one isolate of the Colletotrichum
gloeosporioides species complex was less pathogenic to all Dracaena spp. and varieties tested. In Egypt, during March 2015,
anthracnose symptoms were recorded on D. sanderiana plants.
Therefore, the objectives of this work were (i) to describe the
symptoms of lucky bamboo anthracnose, (ii) to isolate, identify
and test the pathogenicity of the causal agent, (iii) to determine
the effect of temperature on the growth of the causal pathogen
and (iv) to evaluate the effect of certain fungicides and biocontrol agents on the growth of the pathogen.

Pathogenicity was confirmed by fulfilling Koch’s postulates on
rooted cuttings of lucky bamboo plants as well as detached
stem segments, according to Bobev et al. [4]. Twenty cuttings
of lucky bamboo plants were surface disinfected with 1.5%
sodium hypochlorite (NaOCl) for 5 min, followed by several
rinses with sterile distilled water before being sown in five glass
bottles containing 500 mL sterile water. Thirty days later, these
bamboo plants were divided into two sets. The stems of the
first set were wounded (ten wounds per plant) using a sterile
needle at 4 cm intervals. The stems of 5 plants of the first set
were inoculated by inserting small mycelial plugs from 10day-old potato dextrose agar (PDA) cultures of C. dracaenophilum into wounds, which were subsequently covered
with Parafilm strips. Pure agar plugs were used to inoculate
the wounded stems of the control plants (5 plants). Both inoculated and control plants were kept at 28 ± 2 °C. Anthracnose
symptoms were observed visually for sixty days after inoculation. The stems of the second set (5 plants) were injected with
0.5 mL plantÀ1 of C. dracaenophilum conidial suspension
(2 Â 106 conidia mLÀ1) using a sterilized syringe [9]. The
injected and un-injected (5 plants) stems of lucky bamboo
plants were covered with plastic polyethylene bags for 24 h
to provide humid conditions. Anthracnose symptoms were
observed visually. In addition, the stems of apparently healthy
lucky bamboo plants were cut longitudinally and horizontally
into 1–3 cm segments. These segments were inoculated with
one drop of C. dracaenophilum conidial suspension (2 Â 106
conidia mLÀ1) after surface disinfection. Five stem segments
from each type of longitudinal and horizontal pieces were used
as replicates, and the experiment was replicated twice. The rot
of the detached stem segments was observed visually.

Material and methods
Isolation and identification of the causal pathogen

In March 2015, disease problems on the stems of imported
(Netherlands) indoor lucky bamboo plants (D. sanderiana) were
observed. The symptoms were observed during several months
after the consumer purchased them from the retail stores located
in Giza governorate. More than 50 diseased samples with typical anthracnose symptoms were collected to isolate the pathogen based on Koch’s rule [7]. The obtained fungal colonies
were identified according to the Colletotrichum description
reported by Sutton [8] and according to Farr et al. [3].

Effect of temperature on the growth of C. dracaenophilum
Fresh potato dextrose agar (PDA) plates were inoculated with
a 5 mm mycelial disk cut with a sterile cork borer from the
margin of a 10-days-old colony of C. dracaenophilum. Plates
were incubated in an incubator at 5, 10, 15, 20, 25, 30, 35
and 40 °C. The radial growth of C. dracaenophilum was measured in two perpendicular directions at 4, 8, 10 and 14 days
after inoculation. Four Petri plates were used as replicates
for each combination of temperature and incubation period.
Inhibitor effect of fungicides on the growth of C. dracaenophilum
The inhibition effects of ten different fungicides under different
concentrations viz., 0, 25, 50, 100, 200, 300, 400, 500 and
600 ppm against the pathogen were determined. The systemic
fungicides were dimethomorph 6% + copper oxychloride
40% (Acrobat Copper 46%), carbendazim (Kemazed 50%


Anthracnose of lucky bamboo Dracaena sanderiana in Egypt
Table 1

329

Analysis of variance for RCBD.

SOV

Replication
A (temperature T or fungicide F)
B (incubation period I or concentration C)
AB
Error
Total

Table 3

Table 4

df

P-values

df

P-values

(r À 1) = 3
AÀ1=7
BÀ1=3
(A À 1) (B À 1) = 21
(AB À 1) (r À 1) = 93
(ABr À 1) = 127

0.48

<0.01
<0.01
<0.01

(r À 1) = 3
AÀ1=9
BÀ1=7
(A À 1) (B À 1) = 56
(AB À 1) (r À 1) = 237
(ABr À 1) = 314

<0.01
<0.01
<0.01
<0.01

WP), flutolanil (Moncut 25% WP), mancozeb (Tridex 80%),
metalaxyl M + mancozeb (Ridomil Glod 68%), and
thiophanate-methyl (Topsin-M 70% wettable granul (WG)
and the protective fungicides were Mancozeb 80% (Dithane
M-45), pencycuron (Monceren 25% WP) and thiram
+ tolclofos-methyl (Rizolex T 50% WP). The Metalaxyl 8%
WP + Mancozeb 64% (Tasoline) is systemic and protective
fungicide. The inhibition effect was tested using the poisoned
food technique described by Uribe and Loria [10]. Four Petri
plates were used as replicates for each treatment as well as
untreated control. The average radial growth of C. dracaenophilum was measured in two perpendicular directions
when C. dracaenophilum reached full growth in the control
plate.
Inhibitor effect of biocontrol agents on the growth of C.

dracaenophilum
Fungal and bacterial biocontrol agents viz., Trichoderma
harzianum, Trichoderma viride, Trichoderma virens, Trichoderma koningii, Pseudomonas fluorescens, Bacillus subtilis,
Bacillus megaterium and Bacillus pumilus were obtained from
the Plant Pathology Department, National Research Centre
(NRC). The inhibitor effect of the fungal biocontrol agents
against the growth of C. dracaenophilum was studied using
the method described by Bell et al. [11]. Petri plate containing PDA medium was inoculated on one side with a 5 mm
mycelial disk from a 7-day-old culture of the test fungus.
The opposite side was inoculated with a disc of C. dracaenophilum and the plates were incubated at 28 ± 1 °C.
Plates inoculated with a disc of C. dracaenophilum by itself
were used as a control. Four replicate plates were made
for each test fungus as well as the control. Colony radius
of C. dracaenophilum was recorded when the control plates
reached full growth. The inhibitory effect of the bacterial
biocontrol agents was studied using the method described
by Estrella et al. [12]. Petri plate containing PDA medium
was inoculated (by streaking) on one side with one loopful
from a 48-h-old culture of the test bacterium. The opposite
side was inoculated with a disc of C. dracaenophilum and the
plates were incubated at 28 ± 1 °C. Plates inoculated with a
disc of C. dracaenophilum by itself were used as a control.
Four replicate plates were made for each test bacterium as
well as the control. Colony radius of C. dracaenophilum
was recorded when the control plates reached full growth.
The reduction in the growth of C. dracaenophilum was calculated using the formula suggested by Pandy et al. [13] as follows: Growth reduction (%) = [(C À T)/C] Â 100, Where:

C = Average growth of C. dracaenophilum in control and
T = Average growth of C. dracaenophilum in biocontrol
agent treatment.

Statistical analysis
Statistical analysis for a randomized complete block design
(RCBD) with two factors and interaction terms was performed
for all experiments according to Gomez and Gomez [14]. Least
significant difference (LSD) values were calculated to test the
significance of differences between means according to Steel
et al. [15] (Table 1).
Results and discussion
Symptomatology and the causal pathogen
The primary symptoms of lucky bamboo anthracnose were
pale green yellowish lesions that appeared on the stems.
These symptoms extended to the upper and lower internodes, which became yellow. The hard tissues turned soft,
the plant showed wilt symptoms, and the entire stem was
covered with numerous black globose ellipsoid acervuli with
sparse, black setae Fig. 1. The pathogen was isolated and
identified as C. dracaenophilum D. F. Farr & M. E. Polm,
according to the classification of Sutton [8] and Farr et al.
[3]. C. dracaenophilum has been reported in many regions,
such as Cyprus [16], China and Kenya [18], Bulgaria, [4],
Iran [5], and the United States [17], including south Florida
and retail stores in north Florida [6]. This work is the first
report of this fungal species in Egypt. The morphological
characteristics of the pathogen are shown in Table 2 and
Fig. 2. Colonies of the fungus grown on PDA were dominated by pale aerial mycelium. The acervuli on dying stems,
numerous in the discolored areas, were arranged concentrically on the stem, forming tiny black spots, 264–382.8 lm
in the longest dimension, with septate setae, sparse, scattered
in the hymenium, black, 180–295 Â 3.75–6.25 lm, straight to
slightly curved, becoming narrow and hyaline at the rounded
apex, 4–11 septet. Acervuli were also produced on PDA
medium. On the plant and in culture, the conidia were hyaline broadly clavate to cylindrical, occasionally slightly

curved, and measured 23–33  6.6–9.9 lm (28 long  8.25
width lm). The pathogen can be expected anywhere in the
world where infected lucky bamboo cuttings are imported
from China [6]. Even in the Netherlands, the cuttings actually come from China. Sinclair [19] and Verhoeff [20] stated


330

A.A. Morsy and I.E. Elshahawy

Fig. 1 Natural symptoms of lucky bamboo anthracnose disease caused by Colletotrichum dracaenophilum: severe wilted and dead lucky
bamboo plants showing acervuli on discoloured areas (A). Magnified portion showing acervuli on stem tissue (B).

Table 2

Morphological characters of Colletotrichum dracaenophilum isolated from lucky bamboo plants.

Character

Colletotrichum dracaenophilum

Colony color
Conidia shape
Spore mass color
Spore size (lm)
Acervuli size (lm)
Acervuli on host
Acervuli on media

Pale

Hyaline, unicellular, cylindrical to ovoid, straight or slightly curved, guttulate
Pale pink
23–33 Â 6.6–9.9 lm (28 Â 8.25 lm)
180–295 Â 3.75–6.25 lm
Appear
Appear

that even in the absence of visible symptoms, Colletotrichum
spp. may persist on plants as microscopic latent infections
consisting of appressoria with limited development of infective hyphae. Sharma et al. [6] made the same observation
and reported that lucky bamboo introduced from China
might carry C. dracaenophilum, which can induce anthracnose symptoms several months after arrival in the United
States. It is not known which environmental factors might
trigger the appearance of symptoms. However, Sharma
et al. [6] mentioned that anthracnose lesions appeared on
non-inoculated stalks of D. sanderiana plants when the irrigation intervals were lengthened. Thus, water stress may
trigger symptoms.

black acervuli on senescent and dead plants Fig. 3. The pathogen infected stems segments and colonized vascular tissues,
causing rot of the stem tissue Fig. 4. It is assumed that the
maceration of stem and vascular tissues prevents water and
nutrient transportation, causing the leaves to wilt and finally
the whole plant to die. Lucky bamboo stems injected with C.
dracaenophilum conidia showed necrotic, pale green and yellowish lesions around the injection site. The obtained data
are consistent with the results obtained recently by Boven
et al. [4], Komaki et al. [5] and Sharma et al. [6], who also
reported that C. dracaenophilum infected the stems of potted
D. sanderiana plants.
Effect of temperature on the growth of C. dracaenophilum

Pathogenicity tests
Pathogenicity on lucky bamboo plants revealed that the fungus C. dracaenophilum caused 100% infection on the inoculated stems of lucky bamboo plants. Two weeks after
inoculation, pale green lesions began developing on all inoculated plants, and the fungus was successfully re-isolated. No
symptoms were found around the control wounds with pure
agar plugs. Anthracnose of lucky bamboo caused by C. dracaenophilum was characterized by the development of small

The effects of different temperatures and incubation periods
on the growth of C. dracaenophilum are presented in Table 3.
Temperature had a significant effect on the growth of C. dracaenophilum. At both low (5 °C) and high (40 °C) temperatures, fungal growth was completely inhibited during all
tested incubation periods. The optimum temperature for C.
dracaenophilum growth ranged from 25 to 30 °C, maintained
for 8 days. The minimum temperature and maximum average
temperature for fungal growth were 10 and 30 °C, respectively.


Anthracnose of lucky bamboo Dracaena sanderiana in Egypt

331

Fig. 2 Colletotrichum dracaenophilum: Pale aerial mycelium of the fungus growth during seven days at 28 ± 2 °C (A). Conidia produced
on media (B). Acervuli with setae produced on lucky bamboo stems (C).

The growth rate was increased by increasing the incubation
period from 4 to 14 days at temperatures ranging from 10 to
35 °C.
Effect of different fungicides on the growth of C.
dracaenophilum
The effects of different fungicides under different concentrations on the growth of C. dracaenophilum are presented in
Fig. 5. Fungicides had a significant effect on the growth of
C. dracaenophilum. Among them, Kemazed 50% WP had a

strong inhibition effect as no fungal growth was observed over
100 ppm. It was followed significantly by Rizolex T 50% WP,
where no fungal growth was observed over 300 ppm. Dithane
M-45 and Tridex 80% over 400 ppm completely inhibited the
fungal growth. Other fungicides showed moderate inhibitory
effect only at 600 ppm. It is also clear that the increase in
fungicide concentration had an obvious decrease in the linear
growth of C. dracaenophilum.

Effect of different bioagents on the growth of C. dracaenophilum
The antagonistic potential of the tested bioagents against the
growth of C. dracaenophilum is shown in Table 4,
Figs. 6 and 7. Data indicate that most of bioagents had significant antagonistic activity against the growth of C. dracaenophilum. Among bacterial bioagents, B. subtilis and B.
pumilus caused the highest growth reduction of C. dracaenophilum. It was followed by P. fluorescens, while B. megaterium showed no antagonistic activity. Among fungal
bioagents, T. harzianum, T. viride and T. koningii significantly
caused the highest growth reduction of C. dracaenophilum. It
was followed by T. virens. Antibiosis and competition for
space and nutrients are generally the mode of antagonism
observed for Bacillus and Pseudomonas species [21,22]. Trichoderma strains exert biocontrol against fungal phytopathogens
either indirectly, by competing for nutrients and space or
directly, by mechanisms such as antibiosis, and mycoparasitism [23].


332

A.A. Morsy and I.E. Elshahawy

Fig. 3 Artificial inoculation with Colletotrichum dracaenophilum on whole lucky bamboo plants: Dead plants 60 days after inoculation
and showing acervuli on stem (A) as compared with healthy plant (B).

A

0 Days

5 Days

15 Days

B

0 Days

5 Days

15 Days

Fig. 4 Stem rot of lucky bamboo segments artificially inoculated with Colletotrichum dracaenophilum conidia after 0, 5 and 15 days of
inoculation.


Anthracnose of lucky bamboo Dracaena sanderiana in Egypt
Table 3

333

Effect of temperature on the radial growth (mm) of C. dracaenophilum on PDA medium.

Incubation period (days)

Radial growth (mm) of C. dracaenophilum

Temperature degrees (°C)

4
8
10
14

L.S.D.0.05

5 °C

10 °C

15 °C

20 °C

25 °C

30 °C

35 °C

40 °C

0.0
0.0
0.0
0.0

00.0
08.8
11.8
20.5

11.5
23.3
33.8
45.0

21.3
32.5
48.3
77.5

41.5
90.0
90.0
90.0

50.3
90.0
90.0
90.0

16.3
34.0
47.8
55.3

0.0
0.0
0.0
0.0

Temperature (T)

Incubation period (I)

TÂI

2.19

2.05

2.16

Values are mean of four replications for each (T Â I) combination for example (5 °C, 4 days).

Fig. 5

Table 4

Effect of commercial fungicides on the radial growth (mm) of C. dracaenophilum on PDA medium.

Effect of some biocontrol agents on C. dracaenophilum grown on PDA medium.

Biocontrol agent

Radial growth (mm) and reduction (%) of C. dracaenophilum

Radial growth (mm)

T. harzianum
T. viride
T. koningii
T. virens
B. subtilis
B. pumilus
P. fluorescens
B. megaterium
Control
L.S.D.0.05

a

29.3
29.5a
30.8a
35.8a
37.5a
38.3a
66.5a
90.0b
90.0
2.8

Reduction (%)
67.4
67.2
65.8

60.2
58.3
57.4
26.1
00.0
–

Values are mean of four replications for each biocontrol agent as well as the control.
Growth reduction (%) = [(C À T)/C] Â 100, Where: C = Average radial growth of C. dracaenophilum in control and T = Average radial
growth of C. dracaenophilum in biocontrol agent treatment.
a
Significantly different from the respective control at P < 0.05.
b
Not significantly different from the respective control at P < 0.05.


334

A.A. Morsy and I.E. Elshahawy

Fig. 6 Bacterial antagonistic effect on C. dracaenophilum growth. (A) C. dracaenophilum in the presence of P. fluorescens,
(B) C. dracaenophilum in the presence of B. pumilus, (D) C. dracaenophilum in the presence of B. megaterium and (E) C. dracaenophilum in
the presence of B. subtilis.

Fig. 7 Fungal antagonistic effect on C. dracaenophilum growth. (A) C. dracaenophilum in the presence of T. harzianum,
(B) C. dracaenophilum in the presence of T. viride, (D) C. dracaenophilum in the presence of T. koningii and (E) C. dracaenophilum in
the presence of T. virens.


Anthracnose of lucky bamboo Dracaena sanderiana in Egypt

Conclusions
The occurrence of anthracnose symptoms caused by C. dracaenophilum was observed for the first time on D. sanderiana
in Egypt. The fungicide Kemazed 50% WP and different biocontrol agents viz., T. harzianum, T. viride, B. subtilis and B.
pumilus, restricted the growth of C. dracaenophilum in agar
plates.
Conflict of Interest
The authors declared that there is no conflict of interest.
Compliance with Ethics Requirements
This article does not contain any studies with human or animal
subjects.
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