Breeding for Multiple Disease Resistance in Cocoa (Theobroma cacao L.)
Black pod and Canker caused by Phytopthora palmivora and Phytophthora megakarya and Cocoa Swollen Shoot Virus Disease (CSSVD) caused by cocoa swollen shoot virus are important diseases of cocoa in Ghana. Host plant resistance has been considered the most effective method of controlling these diseases. This study was initiated to determine whether multiple forms of resistance to these diseases could be identified in hybrids of cocoa. Thirty six crosses of 6x6 diallel mating design of cocoa were screened for resistance to black pod (P. palmivora and P. megakarya), CSSVD (severe New Juaben CSSV Strain 1A and Nsaba CSSV strain) and Phytophthora canker (P. palmivora and P. megakarya) under a controlled environment. Of the thirty six crosses, 12, 6 and 7 were resistant to black pod, cocoa swollen shoot virus disease and Phytophthora canker, respectively. No cross was found to have combined resistance to the three diseases. This indicates that selection and breeding of cocoa genotypes for multiple disease resistance based on phenotypic data alone could be difficult. Marker assisted selection using tightly linked gene-specific molecular markers will play a larger role in future studies and could be an asset in working with quantitative resistance systems. Cocoa hybrids Alpha B36xPa7/808, Pa7/808xPound 7 and Alpha B36xT65/326 which possess high levels of resistance to more than one disease were identified through this study and would be useful in cocoa multiple disease resistance breeding programmes.
Received: March 07, 2012;
Accepted: April 09, 2012;
Published: June 08, 2012
Theobroma cacao L. (Cacao; Malvaceae sensu lato) is a small tree
endemic to the lowland rainforests of the Amazon basin (Wood
and Lass, 1985; Bartley, 2005). Cocoa is the major
export commodity in Ghana and other countries in West Africa (68% of world production).
Cocoa diseases reduce the potential crop yield by an estimated 810,000 tons
annually (30% of world production) and individual farm losses can approach 100%
(Keane, 1992; Bowers et al.,
Cocoa diseases of most economic importance in Ghana include, black pod disease,
Cocoa Swollen Shoot Virus Disease (CSSVD) and trunk canker (Opoku
et al., 2007).
Cocoa Swollen Shoot Disease (CSSD), in particular poses a serious threat to
Ghanas cocoa industry. The disease has caused enormous devastation of
cocoa farms in Ghana since its discovery in 1936 and over 200 million visibly
infected and contact trees have been cut-out from about 130,000
hectares of land during the past 50 years as a control measure (Ampofo,
1997). However, CSSVD is still prevalent and has spread to all cocoa growing
regions of Ghana (Ollennu et al., 2002). Infection
with severe strains reduced the yield of mature trees by 25% after 1year, by
50% after 2 years and almost totally after 3 years, by which time most infected
trees were dead or dying (Posnette, 1941; Brunt,
1975). Millions of cocoa trees have been killed as a result of the CSSVD
since then and the spread of the disease has been largely unimpeded in the area
of mass infection in the Eastern Region of Ghana.
The practical method of control of CSSVD has been identification and destruction
of infected and neighboring contact trees and subsequent re-inspection of treated
farms. Cutting out, however, seems unable to prevent new outbreaks which continue
to occur due to the difficulty of controlling the mealybug vectors of CSSV,
the severity of the disease in some areas and the latent infection in cocoa
and in certain forest trees and the high cost of control by cutting out diseased
trees (Legg, 1979). It was generally agreed that breeding
for resistance to the virus would be the long term solution to the problem.
There were an indication that resistance from different cocoa populations could
be accumulated to give progenies of higher resistance since resistance to CSSV
was found to be additive and polygenically inherited (Lockwood,
Black pod disease caused by Phytophthora palmivora and Phytophthora
megakarya in Ghana (Dakwa, 1987; Luterbacher
and Akrofi, 1993; Opoku et al., 1999) is
one of the most prevalent and destructive diseases of cocoa (Theobroma cacao
L.). P. megakarya is gradually spreading to all cocoa growing areas in
Ghana. The development of high-yielding, resistant material is generally agreed
to be the most effective and economic control method (Adomako,
2007, 2006; Nyadanu et al.,
2009; Cilas and Despreaux, 2004; Iwaro
et al., 2000).
The incidence of canker in Ghana dates back to the 1920s (Dade,
1928). Phytophthora canker is characterized by discolorations of
bark tissues on the trunk and branches (Firman and Vernon,
1970). Canker reduces the yield potential of the tree by destroying flower
cushions (Firman, 1974) and also serves as an important
source of inoculum for pod infection (Griffin et al.,
1981). Despite its economic importance, cocoa canker has received little
attention probably due to difficulties in field identification. Severe canker
infections resulting in the death of many cocoa trees, particularly in the P.
megakarya infected cocoa growing areas of Western, Ashanti and Brong Ahafo
Regions of Ghana was reported. At the early stage of development and under dry
conditions, scraping the bark to expose the canker lesions and or painting the
scraped lesion with fungicides generally halts the advancement of the canker.
However, under high rainfall and humidity, the canker may quickly girdle the
stem and kill the tree (Akrofi, 2003). Breeding for
resistance has been considered as the most effective to control the disease.
Efforts at developing resistant materials of major cocoa diseases in Ghana have been targeted at developing cocoa materials having resistance to only one of the pathogens at a time. Information on whether varieties resistant to one disease would necessarily be resistant to other diseases is not available. However, since the pathogens of CSSVD, black pod and canker continuous to spread to cocoa growing areas, real farm situations require cultivars having multiple disease resistance to CSSVD, black pod and canker. This is because it is only rare that only one pathogen is present in a particular field. Economic advantages of such cultivars with multiple disease resistance to the major diseases of cocoa are obvious; they are less expensive and less labour-intensive for the grower, reduce yield loss and minimize the need for pesticide applications, resulting in less pollution of the environment.
Multiple Disease Resistance (MDR) has been a major objective of research of
many pathologists and breeders working on different crops (Jansky
and Rouse, 2003). In Ghana however, MDR of cocoa varieties to the three
major cocoa diseases, that is, black pod, CSSVD and trunk canker have not been
reported. The objective of this research was to develop cocoa hybrids from parents
that have been known to be tolerant to black pod, CSSVD and trunk canker and
evaluate them for multiple disease resistance to these diseases.
MATERIALS AND METHODS
Plant material: Six cocoa genotypes, Alpha B36, Pa7/808, Pound 7, T17/524, T65/238 and T65/326 were selected for this study among the accessions held at the Cocoa Research Institute of Ghana. These cocoa genotypes were used as parents in a 6x6 full diallel mating design. The progenies from the diallel mating design were grown under shade in a polybag. The crosses were arranged in a randomized complete block design with 20 seedlings per cross. The origins of the parents are listed in Table 1.
Evaluation of black pod disease resistance
Inoculum preparation: Phytophthora
palmivora and Phytophthora megakarya were grown on carrot agar medium
and from a ten-day-old culture, a zoospore suspension was obtained by inundating
each culture plate (9 cm diameter) with 10 mL sterile distilled water (chilled
to 10°C), refrigerated for 25 min (5°C) and incubated in the dark at
25°C for 30 min. The zoospore concentration of the suspension was determined
using a haemocytometer and adjusted to 200,000 mL-1.
Leaf disc test
Field leaf sampling: The new flushes from bud break of the genotypes were
tagged to obtain average ages of the leaves for each experiment. For each of
the inoculation series, leaves were collected from all the 36 crosses. Leaves
were harvested from the progenies of each cross. The average ages of the leaves
for each treatment were established by following the growth of young flushes
from bud break. After collecting the mature leaves, they were placed in labelled
polyethylene bags into which a few drops of distilled water were sprayed before
hand. The bags were then kept in the dark till the next morning to minimize
effect of leaf sampling time that may occur with large time lapses between harvesting
of leaves (Tahi, 2003). The leaves were washed thoroughly
with tapwater, blotted dry with Whatman number 3 paper and then surface sterilised
with 70% ethanol.
Preparation of leaf discs and inoculation method: Leaf disc inoculation
as described by Nyasse et al. (1995) was carried
out. In total, 15 discs of 1.5 cm in diameter were taken per leaf from the seedling
progenies with a cork borer the next day after harvesting the leaves. All the
discs from the same cross were mixed.
|| Origin of parents of progenies
Leaf discs were placed with their abaxial surface upwards on wetted plastic
foam of 1 cm thick and imbibed with 2.5 L of distilled water in four trays of
70x60x10 cm. The discs from the same plant were aligned in totally randomized
rows of ten discs per tray. Inoculation was carried out the same day, after
preparation of all leaf discs. After the concentration of zoospores were determined
with a hemacyatometer and adjusted to 200,000 mL-1, droplets of 10
μL were placed on each disc. Leaf discs from each cross, placed in rows,
were inoculated across the rows so as to inoculate a disc from each tree in
succession in order to randomize any effect of the spore batch equally over
the different genotypes. The discs were incubated at room temperature of 25°C
in plastic trays lined with moist plastic foam and covered with another plastic
tray in the laboratory avoiding direct sunlight until observations were carried
Observation of symptoms on leaf discs: Symptoms were scored 6 days after
inoculation using a 0 to 5 point scale depending on the size of necrosis (0
= absence of symptoms, 1 = very small necrotic spots, 2 = larger number and
size of necrotic spots, 3 = coalescence of brown spots into medium-sized, 4
= large uniform brown lesions and 5 = very large brown lesions, often expanding
outside the area covered by the inoculum droplet) as described by Nyasse
et al. (1995). The experiment was repeated twice.
Evaluation of swollen shoot resistance: Patch grafting method of inoculation
(Posnette, 1940) was used to evaluate the resistance
levels of the progenies. A patch from the bark of a source plant with the phloem
tissues attached was carefully put into a slit made in the recipient rootstock
and held firmly with budding tape. Two strains of the virus were used; severe
New Juaben CSSV strain 1A and Nsaba CSSV strain. The number of plants showing
symptoms of CSSV disease in the first, second and third flush leaves after inoculation
was recorded over a period of 5 months under a controlled environment. The severity
of symptoms was rated on a 0-6 scale as follows:
|| Healthy (no symptoms)
|| Red vein banding of leaves
|| Chlorotic flecking of leaves
|| Chlorotic vein clearing and green vein banding of leaves
|| Diffused flecking of leaves
|| Fern pattern and swollen shoot
|| Dead plant
Evaluation of canker resistance: The 36 crosses were screened for resistance to Phytophthora canker. The stems of 10 month old test seedlings were inoculated with agar discs of P. palmivora and P. megakarya. About 0.5 m from the ground, the bark of each seedling was sterilized with 70th ethanol and inoculated with 1 mm-2 agar plug taken from the margins of actively growing colonies of 10-day old cultures of P. palmivora and P. megakarya. Plastic film was then wrapped over the inoculated site and tightly secured with adhesive tape. 12 months later, the tape was removed and the observed lesions (the length and width) measured with a measuring tape. The canker lesions on outer bark of the seedlings were measured and the canker lesions inside was also measured after scraping the bark.
Statistical analysis: All the data obtained were analysed using the
Genstart statistical software (Version 10.0) to perform analysis of variance.
The residual plots were inspected to confirm data conformed to normality. The
relationships among resistance of cocoa genotypes to black pod, swollen shoot
virus and Phytophthora canker diseases were tested by Spearmans
Resistance to black pod disease: The study showed significant differences
(p<0.001) in leaf disc score rating of resistance levels among the crosses
to P. palmivora and P. megakarya (Table 2).
|| Mean leaf disc and CSSV severity scores of the cocoa crosses
|*Mean CSSV tolerance score was based on the cumulative score
(severity) of all symptoms of each plant, Higher score indicates higher
level of susceptibility. Pp: P. palmivora, Pm: P. megakarya
The mean disease severity was 2.27 and 2.36 for P. palmivora and P.
megakarya, respectively. Interaction between crosses x Phytophthora species
was not significant (p>0.05). Of the 36 crosses, Alpha B36xPa7/808, Alpha
B36xPound7, Alpha B36xT65/326, Alpha B36xAlpha B36, Pa7/808xAlphaB36, Pa7/808xPound7,
Pa7/808xT65/238, Pound 7xPa7/808, T65/238xAlpha B36, T65/238xPound7, T65/326xPound7
and T65/326xT65/326 were the most resistant (Table 2). The
most susceptible crosses were T17/524xPa7/808, T65/238xT65/238 and T65/326xT17/524
Resistance to swollen shoot virus disease: Significant differences (p<0.001) were observed among the crosses in terms of severity of symptoms (tolerance) caused by New Juaben 1A virus strain and Nsaba virus strain (Table 2). The mean disease severity was 3.05 and 2.59 for 1A and Nsaba, respectively. Interaction between Crosses x virus strains was not significant (p>0.05). The most tolerant crosses were Alpha B36xT17/524, Pa7/808xT65/326, Alpha B36xPa7/808, Pa7/808xPound 7, T17/524xT65/238 and T65/326xT65/238 (Table 2). The most susceptible crosses were Alpha B36xPound 7, T65/326xAlphaB36, T65/326xPa7/808, T65/326xPound7 and T65/326xT17/524 (Table 2).
Resistance to canker: The 36 hybrids varied significantly (p<0.001)
in canker lesion sizes both before and after scraping (Table 3).
The mean of canker lesion sizes before scraping was 12.43 and 11.04 cm2
for P. palmivora and P. megakarya, respectively.
|| Mean canker lesions of the crosses before and after scraping
|Larger lesion size indicates higher level of susceptibility.
Pp: P. palmivora, Pm: P. megakarya
The mean of canker lesion sizes after scraping was 24.54 and 26.61 cm2
for P. palmivora and P. megakarya, respectively. The most tolerant
crosses were Pound 7xAlpha B36, Pound 7xPound 7, Pound 7xT65/326, Pound 7xT65/238,
Pa7/808xT17/524, Alpha B36xT65/326 and Alpha B36xT65/238 (Table
3). The most susceptible crosses were Pa7/808xPa7/808, T65/238xT65/238,
T17/524xT65/326, T17/524xPa7/808 and Pa7/808xPound 7 (Table 3).
Multiple disease resistance: Combined resistance to black pod, cocoa swollen shoot virus disease and Phytophthora canker was not observed in any of the crosses tested. Two crosses, Alpha B36xPa7/808 and Pa7/808xPound 7 had combined resistance to both black pod and cocoa swollen shoot virus diseases (Table 2). Combined resistance to black pod disease and Phytophthora canker was observed in one cross, Alpha B36xT65/326 (Table 3). No cross was found to have combined resistance to Phytophthora canker and cocoa swollen shoot virus disease.
AlphaB36xPound 7 and T65/326xPound 7 which were observed to be resistant to black pod were observed to be susceptible to swollen shoot virus (Table 2). Pa7/808xPound 7 which was observed to be resistant to both black pod disease and swollen shoot virus was found to be susceptible to Phytophthora canker (Table 2, 3).
Correlations among resistance to black pod, cocoa swollen shoot virus and
Phytophthora canker diseases: Table 4 shows that
the rank correlations between leaf disc score and severity scores of cocoa swollen
shoot virus, leaf disc score and Phytophthora canker lesion sizes and
severity scores of cocoa swollen shoot virus and Phytophthora canker
were not significant (p>0.05). Figure 1-3
show graphical presentation of relationship between black pod disease and cocoa
swollen shoot, black pod and canker and swollen shoot and canker, respectively.
The regression coefficients (r2) of Fig. 1-3
were 7.0, 1.5 and 4.5, respectively.
|| Spearmans rank correlation between black pod, swollen
shoot virus disease and Phytophthora canker in the crosses of cocoa
|| Relationship between P. megakarya caused black pod
and swollen shoot diseases resistance
|| Relationship between P. megakarya caused black pod
and canker diseases resistance
The regression coefficients shows that the associations among resistances
to black pod, cocoa swollen shoot virus and stem canker diseases are not strong.
This suggests that resistance to one disease could not be used to predict resistance
to another disease.
|| Relationship between P. megakarya caused swollen shoot
and canker diseases resistance
Due to limited availability of resources for present-day agricultural research,
an extensive evaluation of an entire germplasm for a particular disease is difficult
and also time consuming. Thus, the concept of multiple disease resistance that
involves selection of varieties with combined resistance to a number of diseases
has been put forward to save time and yield loss of crops (Steffenson
and Smith, 2006; Fetch et al., 2003; Mmbaga
and Sauve, 2004; Panella et al., 2008; Jansky
and Rouse, 2003; Pande et al., 2006).
The study shows considerable genetic variability among the hybrids of cocoa
for resistance to black pod, cocoa swollen shoot virus and Phytophthora
canker. The differential response of cocoa hybrids further suggested that these
characters are under genetic control and should therefore be liable to genetic
improvement. This agrees with findings of Iwaro et al.
(1997), Nyadanu et al. (2009), Nyasse
et al. (2002) and Tahi et al. (2006).
Adomako (2006) and Thresh et
al. (1988) reported significant differences among genotypes of cocoa
for resistance to swollen shoot virus. Resistance to CSSV has been found to
be largely polygenic (additive) (Lockwood, 1981). The
significant differences among cocoa genotypes for CSSV resistance indicates
that it might be possible to increase resistance by accumulating the different
resistant factors, since CSSV resistance genes are neither confined to one particular
population nor to any type of progeny but scattered among them (Adomako,
2006). The significant differences in Phytophthora canker in this
study agrees with reports of Firman and Sundaram (1970)
and Okey et al. (1996) who also reported genetic
variability among cocoa genotypes for resistance to Phytophthora canker
Interaction of the hybrids with the Phytophthora species and the viral
strains was not significant, indicating that the hybrids did not change their
relative ranking for black pod, swollen shoot and Phytophthora canker
resistance across the Phytophthora species and the viral strains. The
non-significance of the host genotypes x Phytophthora species and host
genotypes x viral strains has important implications in cocoa breeding for resistance
to black pod, cocoa swollen shoot virus disease and Phytophthora trunk
canker. The levels of resistance of cocoa genotypes could be identified using
any of the Phytophthora species and viral strains since resistance has
been shown to be Phytophthora species or viral strain non-specific in
this study. However, the use of the most aggressive species of Phytophthora
or viral strains could lead to the identification of useful levels of resistance
against the pathogens. The results of the present study support the previous
results of Van der Vossen (1997), Iwaro
et al. (1997) and Surujdeo-Maharaj et al.
(2001) who reported that interaction between Phytophthora species
and cocoa genotypes was not significant.
Combined resistance to black pod, cocoa swollen shoot virus disease and
Phytophthora canker was not observed in any of the crosses tested. The results
show that Alpha B36xPound 7 and T65/326xPound7 which were observed to be resistant
to black pod were susceptible to swollen shoot virus. Pa7/808xPound 7 which
was observed to be resistant to both black pod disease and swollen shoot virus
was found to be susceptible to Phytophthora canker. These findings suggest
that, a cocoa cultivar resistant to one disease may not necessarily be resistant
to another disease of cocoa. These findings agrees with the results of Okey
et al. (1996) who observed SCA 6, a well known black pod disease
resistant cocoa variety, to be susceptible to Phytophthora trunk canker.
The insignificant Spearmans rank correlations among results of resistance
to black pod, cocoa swollen shoot virus and Phytophthora canker further
suggest that cocoa genotypes resistant to one disease may not be resistant to
another disease of cocoa. These findings suggest that selecting cocoa genotypes
for multiple disease resistance to the major diseases of cocoa could be difficult.
This agrees with works of other authors. Wang et al.
(2007) reported that breeders frequently face complex choices in designing
efficient crosses and selection strategies aimed at combining desired genes
into a single target genotype. Mohler and Singrun (2004)
also reported that is difficult to select plants with multiple resistance genes
based on phenotype alone due to epistatics. Gene pyramiding using Marker Assisted
Selection (MAS) is a practical approach to achieving multiple and durable resistance
(Schafer and Roelfs, 1985; Mundt,
1990; Singh et al., 2001; Castro
et al., 2003). Pyramiding of genes for all the three major diseases
of cocoa could be accomplished through MAS using tightly linked gene-specific
molecular markers. The establishment of related molecular studies would enhance
selection especially regarding the accumulation of resistance genes in one genotype
in order to increase resistance level and the durability of such new cacoa cultivars.
Alpha B36xPa7/808 and Pa7/808xPound7 with combined resistance to black pod and cocoa swollen shoot virus diseases and Alpha B36xT65/326 with combined resistance to black pod disease and Phytophthora canker are potential promising materials for multiple disease resistance breeding in cocoa.
Selection and breeding of cocoa genotypes for multiple disease resistance to black pod, cocoa swollen shoot and Phytophthora canker diseases of cocoa based on phenotypic data alone would be difficult. Future studies should consider pyramiding of genes for these diseases using tightly linked gene-specific molecular markers. The study identifies Alpha B36xPa7/808 and Pa7/808xPound 7 to have multiple disease resistance to black pod and cocoa swollen shoot virus and Alpha B36xT65/326 to have multiple disease resistance to black pod and Phytophthora canker. These crosses could therefore be valuable sources of resistance for cocoa breeding programs for multiple disease resistance.
Financial support provided by Ghana Cocoa Growing Research Association (GCGRA), UK, is much appreciated. Technical support provided by Messrs Mawuli Adoblanui, Emmanuel Ewe and Ernest Akortia and Madam Mercy Ofori, all of CRIG is highly acknowledged.
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