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African Journal of Agricultural Research Vol. 6(3), pp. 521-531, 4 February, 2011
Available online at http://www.academicjournals.org/AJAR
ISSN 1991-637X ©2011 Academic Journals
Full Length Research Paper
Response of improved cassava varieties in Uganda to
cassava mosaic disease (CMD) and their inherent
resistance mechanisms
J. Adriko
1
*, W. S. Sserubombwe
2
, E. Adipala
1
, A. Bua
2
and J. M. Thresh
3
and R. Edema
1
1
Department of Crop Science, P.O. Box 7062, Kampala, Uganda.
2
National Crop Resources Research Institute (NACRRI), P.O. Box 7084, Kampala, Uganda.
3
Natural Resources Institute, University of Greenwich, Chatham, ME4 4TB, UK.
Accepted 14 January, 2011
Field based trials were setup to evaluate response and inherent resistance mechanisms to cassava
mosaic disease (CMD) of four improved varieties; Nase 9, Nase 11, 00036 and 00057 together with Nase
4 and Bao as resistant and susceptible standards, respectively. These were grown in a CMD epidemic
hotspot at Namulonge in Central Uganda. There were differences in sensitivity to CMD and whitefly
populations among tested varieties. The improved varieties were less affected by CMD than the
susceptible standard Bao. Three resistance mechanisms were exhibited by the varieties tested, namely;
low infectibility (00036), recovery (Nase 9 and Nase 11) and reversion. Two of the varieties, that is, Nase
4 and 00057 showed all three resistance mechanisms. High whitefly populations characterized Bao,
Nase 4 and 00057. Most of the varieties had a higher infestation of whiteflies on healthy than diseased
plants. Results also showed that growth and yield parameters depended on the variety, growth stage at
infection and health status of the cuttings used with improved varieties recording lower yield losses
than the susceptible Bao. Also, plants infected earlier in the growth period suffered higher yield losses.
Furthermore, plots planted from diseased cuttings recorded higher yield losses compared to those
planted from healthy cuttings.
Key words: Cassava mosaic disease, improved cassava varieties, resistance mechanisms.
INTRODUCTION
Cassava mosaic disease (CMD) caused by whitefly-
transmitted cassava mosaic geminiviruses has been a
major constraint to cassava production in Uganda since
1988 when a severe epidemic of the disease was first
reported. The current epidemic of (CMD) in Uganda has
been controlled mostly by use of disease-resistant
varieties (Thresh and Otim-Nape, 1994; Otim-Nape et al.,
2000), whose introduction and dissemination has
*Corresponding author. E-mail: johnadriko@agric.mak.ac.ug.
Abbreviations: MAP, Month after planting; CMD, cassava
mosaic disease.
restored cassava production in many districts. However,
there is inadequate information on their susceptibility and
resistance to infection, the mechanism of resistance, and
the yield loss due to CMD. Resistance mechanisms
exhibited by cassava varieties include tolerance,
recovery, low infectibility, low virus systemicity and
reversion (Thresh et al., 1998). Therefore, understanding
resistance and integrating it into a holistic strategy for
management of CMD is of significant importance.
Considerable epidemiological data have already been
collected on Nase 2, Nase 3 and Nase 4 (Otim-Nape et
al., 1994; Otim Nape et al., 1998; Sserubombwe et al.,
2001; Byabakama et al., 1997; Alicai et al., 1998;
Sseruwagi et al., 2003). However, there is little
information available on the subsequently released Nase
522 Afr. J. Agric. Res.
5 through to Nase 12 as well as breeding lines at
advanced evaluation stages, especially their performance
in epidemic areas. The effect of CMD on yield also needs
to be assessed since yield loss studies have so far been
done only on a few improved varieties (Otim-Nape et al.,
1994; Osiru et al., 1999; Sserubombwe et al., 2001;
Byabakamam, 1996; Alicai et al., 1998; Egabu, 2002).
MATERIALS AND METHODS
The experiments were set up at Namulonge Agricultural and Animal
Production Research Institute (NAARI) in Wakiso district near
Kampala. This area continues to experience rapid spread of CMD
(Otim-Nape et al., 2000). Two newly released varieties (Nase 9
(30555 – 17) and Nase 11 (TC 1)), and two advanced stage
varieties 00036 and 00057 (generated from crosses using locals)
were studied together with a susceptible farmer-selected (Bao) and
resistant (Nase 4 also SS4) standard. Experimental plots were
established with cuttings obtained from either diseased or healthy
plants of each variety. Treatments consisted of healthy and
diseased plots of each variety, where selection was based on visual
assessment of the standing plants. The 12 treatments (6 varieties x
2 health status) were arranged in a Randomized Complete Block
Design with four replications. The plots measured 10 m x 10 m,
each containing 121 plants spaced 1 m by 1 m. The central core (7
x 7) of the ‘diseased’ plots comprised ‘diseased’ plants and
surrounding these were “guard rows” of healthy cuttings, while in
the healthy plots all the 121 plants were healthy. Where necessary,
sprouts with incorrect health status 1 month after planting (MAP)
were replaced.
Data were collected on CMD incidence, CMD severity and adult
whitefly population. These observations were made monthly from 1
month after planting (MAP) to 6 MAP. CMD incidence was
expressed as a percentage based on the number of diseased
plants compared to the total number of plants present, and
calculated for the whole plots and for the ‘Guard’ plants. CMD
severity was scored for each plant in the plot based on the scale of
1 - 5 (Terry and Hahn, 1980) and average CMD severity was
calculated as the total severity score per plot/number of plants
showing disease symptoms. The populations of adult whiteflies
were monitored on each of the central 49 plants. To do this, a
representative shoot of each plant was chosen and counts were
made of adults on the top-most four expanded leaves of the
selected shoot.
To investigate yield losses associated with CMD infection, yield
of plants of various stages of infection, that is, ‘early’ (2 - 4 MAP),
and ‘late’ (> 4 MAP) - by whitefly, and ‘cutting’ (infected from outset)
were taken. Also yield records were made for healthy plants and
those that lost disease symptoms (recovered). Records included
number, fresh weight (kg) and yield (kg/plant) of tuberous roots.
The raw data were summarized and then subjected to analysis of
variance (ANOVA) using Genstat computer package. Means were
separated using the Least Significant Difference (L.S.D) at P=0.05.
Actual disease progress (incidence %) curves (based on diseased
plants at each time of assessment) were plotted to follow the
progress of CMD for each variety. Plots of histograms and line
graphs of CMD incidence in the core plants of the diseased plots
were used to study the reversion and recovery characteristics of the
different varieties, while the guard row CMD incidences were used
for comparing the effect of inoculum source on the spread of CMD
to healthy neighbours in the different varieties.
Areas under disease progress curves (AUDPCs) were calculated
using % incidence as described by Campbell and Madden (1990)
as follows:
AUDPC ∑
1
n
-
1
= (i
1
+ i
2
)/2 (t
2
–
t
1
)
Where, ∑, summation; i
1,
disease incidence at time t
1;
i
2,
disease
incidence at time t
2.
Symptom severity curves were also fitted for different varieties as
whole plot severity curves as well as separate central core and
guard row severities and adult whitefly population curves were
made to illustrate the adult whitefly population dynamics in the
different varieties.
Yield loss due to CMD was calculated in relation to yield of the
healthy controls using the formula;
% Yield loss = (Yield of healthy – Yield of CMD infected)/ Yield of
healthy x 100%
RESULTS
Analysis of variance (ANOVA) showed significant
differences (p<0.001) in the incidence of CMD among
varieties. The lowest incidences of CMD occurred in plots
of Nase 4, irrespective of the “health status” of plots
(Figure 1). In contrast, for plots planted from “healthy
cuttings” the highest incidence of CMD was recorded in
the variety Nase 9, 00057 and 00036 in that order (Figure
1a). However, when plots of the same varieties were
planted with “diseased cuttings”, the highest CMD
incidence was recorded on the susceptible variety Bao
(65.4%) followed by Nase 9 (47%), Nase 11 (45%),
00036 (42.2%) and 00057 (22.9 %) (Figure 1b). There
was a progressive increase in incidence of CMD in all the
improved cassava varieties, followed by a decline
occurring after 5 MAP in varieties Nase 11, 00057 and
Nase 9, indicating symptom recovery. However, in plots
planted with Nase 11, much spread occurred between
the first and second MAP (Figure 1). Similarly, some
amount of recovery was observed in plots planted with
diseased cuttings of Nase 11, 00036 and 00057. This,
however, occurred only after 5 MAP. In Nase 4, recovery
started 4 MAP, whereas in the susceptible Bao, spread
was continuous (Figure 1b).
To determine the effect of CMD inoculum pressure on
the spread of disease, the amount and rate of disease
spread in the initially healthy guard rows of ‘healthy’ and
‘diseased’ were monitored. The results showed that
amount of CMD inoculum variedly influenced CMD
spread in the healthy guards of the different varieties.
Where the core plants were derived from diseased
cuttings, significantly higher CMD spread was recorded in
the guard rows of the varieties Bao and Nase 11 (Figure
2). In contrast, disease inoculum in the core had no
significant effect on Nase 9, 00057, 00036 and the Nase
4 (Figure 2). Nase 4 recorded the lowest incidences in
the guard rows.
Plot severities allowed the comparison of disease
intensity in different varieties tested while severity in the
guard rows allowed us to assess influence of inoculum
pressure on CMD development in plants of the different
varieties. The highest CMD severity was recorded in plots
planted with the susceptible variety Bao (2.8 and 3.0 in
the “healthy” and “diseased” plots, respectively), while the
lowest severities were recorded in plots containing Nase 4 and
Adriko et al. 523
0
20
40
60
80
0 1 2 3 4 5 6 7
CMD Incidence (%)
MAP
00036 00057 Bao Nase 11 Nase 4 Nase 9
a
0
20
40
60
80
0 1 2 3 4 5 6
7
MAP
b
Figure 1. Monthly incidence (%) of CMD observed in whole plots of each of six cassava varieties at
Namulonge when grown from either healthy (a) or diseased (b) cuttings.
524 Afr. J. Agric. Res.
0
10
20
30
40
50
00036 00057 Bao Nase 11 Nase 4 Nase 9
Guard CMD incidence (%)
Variety
Healthy
Diseased
L.s.d (0.05) = 4.2
Figure 2. Percentage incidence of CMD recorded at 6 MAP in the initially healthy “guard rows” of ‘healthy’ and ‘diseased’ plots of
six cassava varieties grown at Namulonge.
00057 (Figure 3). The highest CMD severity was
recorded in guard rows surrounding plots planted with the
susceptible variety, Bao, irrespective of the health status
of original cuttings used, while the lowest severities were
observed in the initially healthy guard rows surrounding
the variety Nase 4 and 00057 (Figure 4). Reduced
disease severities were observed in rows surrounding
plots of Nase 9 and Nase 11 from 5 MAP (Figure 4). In
general, the amount of inoculum (“diseased plots” versus
“healthy plots”) significantly affected the severity of
disease in the guard rows surrounding Bao (p<0.001).
However, this was not true in guard rows surrounding the
improved varieties, viz., 00057, Nase 4, Nase 11 and
00036 (Figure 4).
Whitefly populations were monitored because of their
key role in CMD transmission. The mean number of adult
whiteflies recorded differed among varieties (p<0.001).
During the trial, the largest number of adult whiteflies was
recorded on plots planted with varieties Nase 4, Bao, and
the lowest in those planted with 00036 (Figure 5). Health
status had differing effects on the varieties. For example,
in plots planted with the varieties 00036, 00057 and Nase
4 whitefly numbers were greater on plants derived from
“healthy” cuttings compared to those from “diseased”
cuttings. The opposite was true for plots planted with
varieties Bao, Nase11 and Nase 9 (Figure 5). For all
varieties, the whitefly population peaked at 4 MAP before
declining (Figure 6). A second cycle of whitefly numbers
occurred after 5 MAP, but this varied with variety and
health status of the cuttings used.
Results showed that the total amount of disease
(AUDPC) over the period of experimentation differed
among the varieties tested and with the initial health
status of cuttings used (p<0.001). Nase 4 had the lowest
AUDPC value in both “healthy” and “diseased” plots
(Figure 7). Whereas in the plots planted with “healthy”
cuttings, Nase 11 (16.9) recorded the highest AUDPCs
followed by Bao (6.1), 00057 (5.1), Nase 9 (4.1) and
00036 (1.9) in that order. In contrast, in plots containing
“diseased” cuttings, plots for Bao had the highest
AUDPCs (52.6) followed by Nase 9 (42.1), 00036 (41.9),
Nase 11 (39.9) and 00057 (21.2) (Figure 7).
Plots of histograms and line graphs of CMD incidence
in the core plants of the diseased plots were used to
study the reversion and recovery characteristics of the
different varieties. The proportion of cuttings obtained
from infected plants that sprouted without disease
symptoms (reversion) differed among the varieties
(p<0.001). The variety 00057 displayed the highest level
of reversion (75.6%) (Figure 8a). This was followed by
Nase 4 (60.8%), Nase 11 (33.1 %), Bao (23.2%) and
Nase 9 (15.8 %). The lowest amount of reversion (10.3%)
was however, recorded on the variety 00036 (Figure 8a).
In general higher amounts of reversion were recorded in
the first rains planting of 2003 compared to those in the
second rains planting of 2002.
The extent of the partial or complete loss of symptoms
on originally diseased plants (recovery) also differed
among varieties. Recovery was observed in the varieties
Nase 4, 00057, Nase 11 and Bao, while none was seen
in the varieties 00036 and Nase 9 (Figure 8b). Most
recovery was noticed after 4 MAP, although for Nase 11
it began much earlier at 2 MAP (Figure 8b).
To evaluate the effect of CMD on cassava yield,
Adriko et al. 525
0.0
1.0
2.0
3.0
4.0
0 1 2 3 4 5 6
7
MAP
00036 00057 Bao
Nase 11 Nase 4 Nase 9
a
CMD Severity
0.0
1.0
2.0
3.0
4.0
0
1
2
3
4
5
6
7
MAP
b
Figure 3. Monthly mean severities of CMD recorded on six varieties in plots containing either “healthy” (a) or
“diseased” (b) cuttings at Namulonge.
different yield parameters including tuberous root
number, weight and yield were studied. Yield parameters
indicated that there were significant effects of variety
used and stage of CMD infection on these parameters (p
< 0.001). The variety 00057 produced the highest
number of tuberous roots, while Bao and Nase 9 had the
lowest (Table 1). Except for Nase 11, cutting-infected
plants had the lowest tuber numbers compared to
“healthy” plants (Table 1). In comparing effects of CMD
infection stage, healthy plants of 00057 had the highest
526 Afr. J. Agric. Res.
0.0
1.0
2.0
3.0
4.0
0 1 2 3 4 5 6
7
Guard row CMD severity
MAP
00036 00057 Bao Nase 11 Nase 4 Nase 9
a
0.0
1.0
2.0
3.0
4.0
0 1 2 3 4 5 6 7
MAP
b
Figure 4. Monthly mean severities of CMD recorded on plants in the “guard rows” of six varieties containing
either “healthy” (a) or “diseased” (b) cuttings at Namulonge.
numbers of tuberous roots compared to other stages of
infection. However, with 00036, Bao and Nase 11; the
late-infected plants had the highest root numbers. In
varieties Nase 4 and Nase 9, plants that recovered from
CMD produced more tubers than other categories of
infection (Table 1).
Bao and Nase 9 produced the largest average tuberous
root weights followed by Nase 11, 00036, 0057 and Nase
Adriko et al. 527
0
2
4
6
8
10
12
14
16
00036 00057 Bao Nase 11 Nase 4 Nase 9
Variety
Healthy Diseased
L.s.d (0.05) = 3.39
Mean adult Whitefly population
Figure 5. Mean adult whitefly infestation recorded over 6 months on top four expanded leaves of either
‘healthy’ or diseased’ plants of each of six cassava varieties at Namulonge.
4 in that order (Table 1). In general, lower average
tuberous roots weights were recorded in CMD-affected
plants compared to un-infected ones (Table 1). However,
Nase 4 differed with plants infected as cuttings having the
highest root weights. Similarly, in Nase 11, cutting
infected plants had higher average root weights
compared to those infected early or late (Table 1).
Like the previous yield parameters, the yield (Kg/plant)
of cassava depended on the variety and stage of CMD
infection (p<0.001). Nase 9 produced the highest
tuberous root yield followed by Nase 11, 00057, 00036,
Bao and Nase 4 (Table 1). For varieties 00036, Bao and
Nase 9, plants grown from infected cuttings had the
lowest tuberous root yields. Except for Nase 9, uninfected
plants, in general produced the highest yields. For Nase
9, the highest root yields were from plants that recovered
from infection (Table 1).
Yield loss arising from CMD infection was also
calculated in relation to the healthy controls and
depended on variety and stage of infection (Figure 9).
Bao had the highest overall yield losses with the most
affected plants being those that got infected from cuttings
(Figure 10) while 00057 had the lowest yield losses,
followed by Nase 11 and Nase 4. The stage of infection
did not affect yield loss in these three improved lines
(Figure 9). In fact for Nase 4 highest yield losses
occurred in plants that were infected late while for in
00057 and Nase 11 higher yield losses were recorded in
early-infected plants rather than those from cutting
infection.
The results showed generally low CMD spread in the
tested varieties (CMD incidence (< 50% respectively at 6
MAP) contrary to earlier findings that Namulonge is an
epidemic area, where over 80 % CMD spread would be
expected in susceptible varieties. Further, there was
more disease spread in plots originally planted with
‘diseased’ cuttings of the varieties Bao, Nase 9 and Nase
11 than those planted with ‘healthy’ cuttings. This is
expected of low or medium disease pressure areas but in
epidemic areas due high external inoculum, equally high
disease spread would be expected in both the ‘healthy’
and ‘diseased’ plots (Byabakama et al., 1999). The
findings of this study thus suggest that Namulonge could
currently be in a post-epidemic or recovery phase.
From the results (CMD incidence, Disease progress,
severity and AUDPC), we see different responses of the
cassava varieties to CMD. It is apparent that Nase 4 was
the most resistant of the cassava varieties tested. The
two advanced varieties namely 00036 and 00057 were
next, although the infected 00036 plants developed
conspicuous (severe) symptoms. In these varieties,
presence of ‘diseased’ cuttings had no influence on CMD
spread, while in plots of Bao, Nase 9 and Nase 11 as
shown above, ‘diseased’ cuttings significantly contributed
to CMD spread. The improved varieties also showed
varying levels of reversion and recovery. The varieties
Nase 4 and 00057 had mild inconspicuous symptoms,
some of which disappeared at later stages of growth.
Nase 9 and Nase 11 had high disease severities, but
these either declined or disappeared with plant age. The
528 Afr. J. Agric. Res.
0
5
10
15
20
25
30
0 1 2 3 4 5 6 7
Adult whitefly population
MAP
a
0
5
10
15
20
25
30
0 1 2 3 4 5 6 7
MAP
00036 00057 Bao
Nase 11 Nase 4 Nase 9
b
Figure 6. Monthly records of adult whitefly population on the top four expanded leaves of either ‘healthy’ (a) or
‘diseased’ (b) plants of 00036, 00057, Bao, Nase 11, Nase 4 and Nase 9 grown at Namulonge.
high severities in Nase 9 and Nase 11 are contrary to
earlier findings (Alicai, 2003) that CMD-affected improved
cassava varieties mainly express mild symptoms. The
varieties also differed in whitefly infestation confirming
previous findings (Otim-Nape et al., 1998; Omongo,
2003). Bao, Nase 4 and 00057 had the highest whitefly
populations and this was associated with high CMD
spread in Bao but not in the improved varieties as found
in earlier studies (Fargette et al., 1993; Otim-Nape, 1993;
Otim-Nape et al., 1997, 1998, 2000; Legg and Ogwal,
Adriko et al. 529
0
10
20
30
40
50
60
70
00036
00057
Bao
Nase 11
Nase 4
Nase 9
AUDPC
Variety
Healthy
Diseased
L.s.d (0.05) = 10.56
Variety
Figure 7. Area under disease progress curve (AUDPC) calculated for each of six
cassava varieties grown at Namulonge.
0
20
40
60
80
100
00036 00057 Bao Nase 11 Nase 4 Nase 9
Variety
Core Incidence (%) % Reversion
L.s.d (0.05) = 4.60
a
Core CMD incidence and reversion (%) at 1
MAP
0
20
40
60
80
100
0 1 2 3 4 5 6
7
MAP
00036
00057
Bao
Nase 11
Nase 4
Nase 9
b
Diseased Core CMd Incidence
Diseased
core CMd incidence
Figure 8. Comparison of amount of reversion exhibited by six cassava varieties based on CMD incidences
(%) recorded in the “core” diseased rows (a) and monthly records of CMD incidence in the “core plots”
planted with diseased cuttings at Namulonge used to show recovery trends (b).
530 Afr. J. Agric. Res.
Table 1. Effect of cassava variety and CMD infection stage on the tuber number, tuber weight (Kg/tuber) and tuberous root yield (Kg/plant) of six different cassava varieties grown in
Namulonge.
C = Cutting infected; E = early infected; L = lately infected; H = healthy; Rec = recovered; Rev = reverted.
Figure 9. Yield loss (Kg/plant) calculated in relation to yield of healthy controls for six different cassava varieties grown at Namulonge
discussion.
Variety
Tuber number Individual tuber weight (kg) Total tuber yield (Kg/plant)
C E L H Rec Rev C E L H Rec Rev C E L H Rec Rev
00036 7.1 9.0 9.4 8.8 4.2 8.4 0.3 0.4 0.2 0.5 0.2 0.4 2.4 3.6 2.3 3.9 1.2 2.7
00057 9.7 9.7 11.2 11.7 10.8 8.8 0.3 0.3 0.3 0.4 0.3 0.3 3.0 2.9 3.5 4.4 3.4 2.6
Bao 2.9 5.7 6.0 5.7 4.6 3.1 0.4 0.6 0.6 1.0 0.7 0.4 1.3 3.2 3.3 4.7 3.6 1.4
Nase 11 8.3 6.8 11.2 9.3 4.7 7.1 0.4 0.4 0.4 0.7 0.8 0.4 3.4 2.8 3.7 5.2 2.5 3.0
Nase 4 6.9 10.8 6.9 11.8 12.4 7.5 0.4 0.2 0.2 0.3 0.3 0.3 2.5 2.5 2.1 4.0 3.9 2.0
Nase 9 3.5 4.0 5.6 5.8 8.2 4.2 0.5 0.7 0.7 1.0 0.8 0.7 2.0 2.8 3.7 5.8 9.4 3.9
L.s.d (0.05) = 1.203 CV % = 6.6 L.s.d (0.05) = 0.899 CV % = 17.9 L.s.d (0.05) = 0.0836 CV % = 15.1
1998; Omongo et al., 2001; Legg et al., 2003; Omongo,
2003; Sserubombwe et al., 2001).
The occurrence of these mechanisms among the
varieties tested offer options for their deployment in
different epidemiological backgrounds. For example the
highly resistant ones like Nase 4, 00057 and 00036 have
a wide range of deployment options, that is, can be
deployed in both low and high disease pressure areas,
while the moderately immune and recovery types are
suitable for low to moderate disease pressure areas.
These results imply that Nase 4, 00036 and 00057 are
considerably resistant to CMD irrespective of inoculum
pressure and therefore can be deployed in CMD
epidemic areas. However, Nase 9 and Nase 11 should
only be grown using clean planting materials to avoid
high CMD spread due to presence of disease inoculum.
The findings call for a further investigation as to whether
recovered plants cannot act as foci for the spread of
disease to healthy plants. From such a study, recovering
varieties, if proved safe could be recommended for use
since there is still a high demand for improved planting
materials. If further studies on reversion prove that
cuttings from the reverted plants give rise to symptomless
plants (Thresh et al., 1998), it will allow the use of the
reversion phenomenon to generate more planting
materials to meet the need for improved planting
material.
The improved varieties gave moderate yields of
between 2.5 and 10 kg per plant. The improved varieties
generally had lower yield losses than the susceptible
check, Bao. Results indicate occurrence of yield losses
due to CMD infection in all the tested varieties. Except in
Nase 9 where cutting infected plants had high yield
losses, time of infection did not influence yield loss in the
improved varieties. These findings indicate that good
yields can be obtained from the improved varieties, with
less yield losses likely to occur even though the plants
get infected with CMD. However, in some of the varieties,
for example Nase 9, the farmer needs to use clean
planting material to avoid the high yield losses associated
with the cutting infected plants.
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