Xanthomonas Wilt – A threat to banana production in East and Central Africa
Authors:
Leena Tripathi and Maina Mwangi
International Institute of Tropical Agriculture,
Kampala, Uganda
Steffen Abele
International Institute of Tropical Agriculture,
Dar Es Salaam, Tanzania
Valentine Aritua and Wilberforce Kateera Tushemereirwe
National Agricultural Research Laboratories, Kawanda,
Kampala, Uganda
Ranajit Bandyopadhyay
International Institute of Tropical Agriculture,
Ibadan, Oyo State, Nigeria
Bananas and plantains (Musa spp.) are
the world’s fourth most important food
crop after rice, wheat, and maize. Annual
banana production in the world is estimated
at 1 × 1011 kg, of which less than
10% enters the commercial market, indicating that the crop is more important for local consumption than for export (19).
Approximately one-third of the bananas
produced globally are grown in sub-Saharan
Africa, where the crop provides more
than 25% of food energy requirements for
more than 100 million people. East Africa
(including Burundi, Kenya, Rwanda, Tanzania, and Uganda) is the largest banana producing and -consuming region in Africa.
Uganda is the world’s second largest
producer after India, with a total of about
10.5 × 109 kg (18). Banana production is threatened by various constraints such as declining soil fertility, socioeconomic problems, pests, and diseases (45).
The banana Xanthomonas
wilt (BXW) disease caused by the bacterium
Xanthomonas campestris pv.
musacearum endangers the livelihood of
millions of farmers in East Africa (64).
Low soil fertility and BXW are considered
to be the two greatest threats to banana
productivity in the Great Lakes region of
eastern Africa including Burundi, Rwanda,
northeastern Democratic Republic of
Congo, Uganda, northwestern Kenya, and
Tanzania (26).
The disease was first reported about 40 years ago in Ethiopia on Ensete, which is closely related to banana (70). Outside Ethiopia, BXW was first reported in Uganda in 2001 and has now spread to almost all major banana-producing districts of the country. The disease has also been reported in Democratic Republic of Congo (43), Rwanda (48), Tanzania (32), Kenya (31), and Burundi (5) (Fig. 2).
Pest risk analysis of BXW has been recently published for several French overseas departments (10) and countries in eastern, central, and southern Africa (50). The disease affects almost all commonly
grown banana cultivars (65), although field
observation and laboratory experiments
indicate that beer banana cultivar Pisang
Awak (Kayinja) is most susceptible
(16, 56). The banana cultivars grown in the
Great Lakes region include the following:
East African Highland banana subgroup
(AAA-EA genome) used to make “matooke” (steamed and mashed fruit) and
beer; brewing cultivar Pisang Awak (ABB
genome); the dessert cultivars Sukali Ndiizi (AAB genome) and the Cavendish subgroup (AAA genome); and plantains (Gonja, AAB genome).
The impacts of BXW are both extreme
and rapid, unlike those of other diseases,
which cause gradually increasing losses
over years. The economic impact of BXW
is due to death of the mother plant that
would otherwise contribute to the ratoon
plant production cycles (60).
Fields infested with X. campestris pv.
musacearum cannot be replanted with
banana for at least 6 months due to carryover of soilborne inoculum (62). BXW has similarities to other bacterial wilts of banana, caused by Ralstonia solanacearum,
including Moko, blood, and bugtok diseases
(53). Once these pathogens have
become established, disease control is very
difficult and eradication impossible (16).
Economic and Social Impact
Bananas are important in the Great
Lakes region, not only in Uganda, but also
in adjacent countries, where they are both
a food security and a cash crop (17). Food
security studies reveal that in Uganda,
Rwanda, and Burundi, bananas constitute
more than 30% of the daily per capita
caloric intake, rising to 60% in some regions
(2). Bananas also provide a major
source of cash income for the farmers in
the Great Lakes region (44).
Between 2001 and 2007, BXW spread
into more than 35 districts in Uganda,
apparently from central Uganda, where
banana production is less intensive and
mainly subsistence-oriented, to the highly
intensive production areas in western
Uganda. In central Uganda, BXW incidence,
measured as the proportion of affected
sites within a district, reached up to
60%, but the major banana production
areas in southwestern Uganda showed little
or no infestation by 2006 (65).
In response to the outbreak of BXW, the Ministry of Agriculture, and Animal Industry and Fisheries (MAAIF) in Uganda formed a task force in December 2001 to develop a strategy to eradicate the disease (65). The strategy emphasized cutting and burying infected banana plants, restricting movement of banana materials, decapitating male buds, sterilizing tools, and raising awareness about the disease. BXW management strategies reduced disease incidence to less than 10% in areas where they were adopted, but implementation was not sustainable due to the high costs.
As yet, there has been little analysis of
the economic impact of BXW in countries
neighboring Uganda. However, if uncontrolled, BXW would spread at a rate of 8% per annum in cooking banana plantations (27), causing an estimated production loss of about 53% over a 10-year period, equivalent to a reduction from the current 4.5 × 109 kg to 2.1 × 109 kg/year (1).
Overall economic losses were estimated at $2 billion (1) to $8 billion over a decade,
arising from price increases and significant
reductions in production (68). According
to Abele and Pillay (1), consumers bear the
major share of the losses due to reduced
supply and increasing prices of bananas,
whereas producers benefit from higher
prices and tend to lose less than consumers.
Kayobyo et al. (27) predicted declines
in per capita consumption of bananas by
42% and total household incomes by about
32% by the end of 2004 in the BXW-affected areas compared with the nonaffected counterparts.
Similar scenarios are likely for the other countries in the region that depend on bananas as a main staple crop. The scenario described above has significant implications for the management of BXW. Generally, management measures for crop diseases are taken based on economic threshold, when losses are greater than the costs of management (46).
BXW management in this respect has three problems. First, producers will probably begin to manage the disease too late from an
overall economic perspective, not taking
into account the much higher losses to
consumers that occur early. Second, there
are no curative measures for BXW. Third,
the disease affects banana populations
quite rapidly, so that by the time the farmer
begins to respond, it may be too late (12).
Disease management technologies have
to be assessed for their financial viability
in terms of development and dissemination
costs against adoption and returns for
farmers (and thus on research investment).
Adoption of exotic or hybrid improved
cultivars in East Africa is still low, whereas
adoption of improved management techniques is significantly higher (17). The
most promising technologies are those that
can be delivered in a short time, require
little adaptation of existing management
systems, and offer high returns. For banana
production, improved agronomic practices
rank highest in returns on investment, followed by genetic modification for disease
resistance (26). Traditional breeding methods are less profitable, as they take longer to achieve usable outputs (26).
These observations favor genetic modification for resistance to BXW as a low-cost preemptive measure with minimal market distortion as old stands are gradually replaced by improved material. However, genetic modification has to take into account the potential loss of natural biodiversity that
could lead to a higher risk of losses due to
other diseases.
Causal Organism
The causal agent of BXW is a motile,
gram-negative, rod-shaped bacterium possessing a single polar flagellum, for which the name Xanthomonas campestris was adopted in the 1960s and 1970s (70,71),
but which was subsequently renamed Xanthomonas campestris pv. musacearum in
the 1980s (72).
As a typical member of
Xanthomonadaceae, the bacterium produces
yellow, circular, mucoid, slimy colonies
on nutrient agar and semi-selective
medium YTSA-CC (60). Recently, phylogenetic relationships were evaluated for 20 isolates of the bacterium collected
within a period of about four decades,
between 1968 and 2005, from Ethiopia,
Uganda, Democratic Republic of Congo,
Tanzania, and Rwanda. Sequence analyses
of the internally transcribed spacer (ITS)
locus (6) and the gyrase B (gyrB) gene
revealed only limited (<2%) nucleotide
divergence among the isolates (6). This
was consistent with fatty acid methyl esters
(FAME) analysis and genomic amplicon
fingerprinting with repetitive sequence
polymerase chain reaction (rep-PCR) profiling, both of which indicated that populations of X. campestris pv. musacearum are homogenous (6,7).
Absence of any notable differences with respect to time of isolation, geographic location, or host (banana and enset) suggests a recent introduction of X. campestris pv. musacearum, first from Ethiopia to Uganda and then across the Great Lakes region. In a laboratory-based pathogenicity test, the isolates from Uganda were observed to induce the same level of severity on all banana genotypes tested (6,56), which is additional evidence that the isolates have originated recently.
Comparison of X. campestris pv.
musacearum with other Xanthomonas spp.,
based on FAME and partial nucleotide
sequences of the gyrB gene and ITS,
showed that all strains of X. campestris pv.
musacearum are similar to X. vasicola
which formerly comprised a sorghum
pathogen, X. vasicola pv. holcicola, and a
sugarcane and maize pathogen, X. vasicola
pv. vasculorum (15,67).
In addition, pathogenicity studies revealed that X. campestris pv. musacearum is able to induce a hypersensitive response in maize. Based on phylogenetic and biochemical analyses and pathogenicity studies, X. vasicola pv. musacearum has been proposed as the new identity of the bacterium causing BXW (6).
However, more data on the pathogenicity
characteristics of the X. vasicola
pathovars are needed to support the new
pathovar classification. The very high
similarity among all banana/enset strains
indicates that pathovar evolution occurred
in relatively recent history (47).
Symptoms
Affected banana plants develop symptoms
characterized by a progressive yellowing
and wilting of leaves, and uneven
and premature ripening of fruit with sections
showing unique yellowish blotches in
the pulp and dark brown placental scars
(64). Symptoms on floral parts include wilting of bracts, shriveling and rotting of the male buds, and yellowbrown
flower stalks .
Cross-sections of diseased pseudostems reveal yellowish bacterial ooze (55). When pseudostems and rachis are cut, pockets of pale yellow bacterial ooze appear within 5 to 15 min . Yellow or brown streaks
occur in the vascular tissues of infected
plants. Eventually, infected plants wither
and the plant rots. Symptom development is
rapid under favorable conditions and typically evident within 3 to 4 weeks under field conditions and 2 to 3 weeks after inoculation under screenhouse conditions (56).
Symptom expression varies depending
on cultivar, growth stage, and the mode of
disease transmission (35). When flowering
plants are infected by insect-transmitted
bacteria, the initial symptoms are wilting
and withering of the male bud, with a
gradual shrinking along the rachis extending
toward the fingers. The shrunken part
of the rachis often acquires an ashen discoloration before turning black.
As the infection progresses over time, the fruits (most often those nearer to the male bud) start turning yellow prematurely, giving an appearance of ripening. By the time these infected fingers turn yellow on the outside, infection is usually advanced and the pulp within is already rotted and discolored. As the disease progresses, the infected leaves turn yellow, wilt, and eventually die.
In the terminal stages of infection, the whole
bunch rots completely, all leaves dry out
and die back, and stems die and collapse
gradually from the top downward.
Plants can also be infected by X.
campestris pv. musacearum before flowering, usually as a result of transmission
through contaminated tools (4), although
soilborne infection can also occur through
the roots (36). When plants are infected
before flowering, the initial symptom is
progressive yellowing of leaves from the
leaf tip toward the petioles. During the wet
season, water-soaking symptoms may
appear first in patches on the leaf before
the leaf turns yellow.
Generally, symptoms seem to progress faster during the wet season than during the dry season. The time taken to reach different stages of symptom expression may differ with cultivar and environmental conditions, but generally plants show symptoms within 3 weeks of infection.
Disease Diagnosis
BXW can be diagnosed from the typical
symptoms it induces on banana, including:
premature ripening of fruits, internal
brown discolorations of fingers and vascular
tissues, pale yellow ooze from cut surfaces,
wilting of bracts and male buds, and
progressive yellowing leading to complete
wilting.
Diseases with similar symptoms,
such as Moko disease, are not known to
occur in Africa. A prominent symptom of
Panama disease (caused by Fusarium oxysporum f. sp. cubense) is wilting, but cut
sections of the stem show vascular discoloration without any yellow bacterial ooze and fruits are not directly affected.
For more precise diagnosis, several
pathogen characteristics have been examined, including a variety of biochemical tests, substrate utilization (BIOLOG), and FAME analysis (6). However, affordable, accurate, and reliable diagnostic tools are necessary and important for detecting the pathogen, studying disease epidemiology, and developing management measures.
The BXW pathogen grows slowly when
cultured on synthetic media and can be
overgrown easily by contaminants, thus
precise diagnostic techniques are needed.
Recently, two semi-selective media have
been developed for X. campestris pv.
musacearum: CCA (39) and YTSA-CC
(60). On these media, X. campestris pv.
musacearum is easily identified as yellowish, mucoid, circular colonies, and the
bacterium can be isolated from infected
banana tissues, contaminated insect vectors,
and infested soil.
Efforts are underway to develop DNAbased
diagnostic methods (6,7,33). PCR assay was developed for detection of X. campestris pv. musacearum (7). Due to their close genetic
relatedness, this assay also detects other X.
vasicola pathovars, including all 36 X.
vasicola strains currently available at National Collection of Plant Pathogenic Bacteria, Central Science Laboratory, York, UK.
Negative results were obtained with 52
other Xanthomonas spp. Two pairs of
primers were developed for detection of X.
campestris pv. musacearum in a conventional PCR assay. The primers amplified products of 358 and 272 bp, respectively, from DNA extracts of the 36 X. vasicola isolates but not the 52 other xanthomonads.
The primers were developed from a 685-bp
fragment for a rep-PCR (6) that encodes
methylase of chemotaxis methyl-accepting
protein. Specific assays are still needed for
each of the bacterial strains. The complete
genomes of two isolates of X. campestris
pv. musacearum and one of X. vasicola pv.
Vasculorum have been sequenced (V. Aritua, personal communication) and would provide opportunities to develop additional primers.
In addition to selective media and PCR,
progress has been made in developing
ELISA-based diagnostic kits. Polyclonal
antibodies have been generated, but initial
tests showed cross-reaction with other
Xanthomonas isolates occurring in the
same niche with X. campestris pv. musacearum.
Efforts are also underway to generate
monoclonal antibodies (MAbs) that
would be precise and specific for X.
campestris pv. musacearum. The MAb
approach is particularly interesting as it
could be used to test plant sap in the field
in a simple immunostrip format.
Disease Cycle/Epidemiology
The major sources of pathogen inoculum
are infected banana plants and residues,
contaminated soil, and traded banana
products (seedlings, fruits, leaves, and
fibers). The mode of disease spread
can vary significantly, depending on the
production system (subsistence or commercial), agroecology, and cultivar grown.
Insects, cutting tools, wind-driven rain,
and infected seedlings are the major means
by which the pathogen spreads within or
across fields. The importance of insect
vectors varies with ecological conditions,
being lower in cold, higher altitude regions
(41), and the importance of farm tools
depends on how intensively farmers manage
their crops, which to an extent is determined
by the local economic importance
of bananas. Male bud infection has not
been observed in Ethiopia at altitudes over
1,700 meters above sea level (masl) (3).
Reports from the Democratic Republic of
Congo suggest that infection through the
banana inflorescence is not common at an
altitude of 1,700 masl (43), perhaps due to
lack of adequate insect transmission.
Inflorescence infections are common around
Lake Victoria, which has an altitude of
1,135 masl. Several aspects of insect transmission (e.g., efficiency of transmission by various insect species, nature of transmission, acquisition of bacterial inoculum, etc.) require further investigations (10,54).
In central Uganda, the beer cultivar
Pisang Awak is popularly grown in less
intensive subsistence farming systems. In
this region, field observations indicate that
the primary means of disease spread is
insects that transmit bacteria through the
moist cushions that are exposed when male
flowers are shed from the inflorescence
(Fig. 6).
The pathogen can infect both male and female parts of inflorescences through fresh scars left by fallen flower bracts (21), but the natural infection through female flowers is unlikely to be of importance because plants are not infected when the male flower parts are removed as a BXW management practice. X. campestris pv. musacearum has been isolated from the nectar and from the ooze exuding through the cushions revealed by the fallen male flowers and the fresh openings made by the fallen bracts of flowers (54).
Insects pick up the bacteria, externally on body parts or internally within organs, when
they visit the banana inflorescence (20).
The most abundant insects visiting banana
flowers are stingless bees, Plebeina denoiti,
fruit flies, grass flies (54), and wasps
(20). The agroecology in this region, at
800 to 1,500 masl, is more suitable for
insect vectors of the pathogen (41). In
western Uganda, where cooking bananas
are dominant and produced under more
intensive commercial systems, contaminated
tools are the major means of disease
spread.
Although the altitude, higher than 1,600 masl, is less favorable for insect vectors, the major factor here is the close attention paid to plantations by farmers, which is characterized by repeated use of
cutting tools such as machetes that can
spread the pathogen. In addition to insects
and tools, bacteria could also penetrate
into plants through roots, especially if
injured by soilborne pests, e.g., nematodes
and weevils (36), but clear experimental
evidence is lacking.
Besides banana, the only other known
natural host of X. campestris pv. musacearum is enset (70,71) although the
pathogen has been reported to be able to
infect Canna indica after artificial inoculation (51). X. campestris pv. musacearum can infect and produce symptoms on Musa zebrina and M. ornata and Canna lily (Canna × generalis), an ornamental plant, in Uganda (51). Yirgou and Bradbury (71) inoculated aubergine, barley, bean, broad bean, castor oil, lettuce, lucerne, maize, peanut, pelargonium, potato, sorghum, sunflower, sweet pepper, tobacco, tomato, and wheat with X. campestris pv. musacearum, but no symptoms were observed.
Ashagari (8) inoculated plants commonly
found in enset growing regions to determine
host range. Chenopodium album,
Colocasia antiquorium, Commelina sp.,
Guizotia scabra, Kalanchoe quartinia,
Snowdenia polystachya, Solanum nigrum,
and Tagetes minuta were unaffected after
10 weeks, but the ornamental Canna orchoides had disease symptoms within 4 to
6 weeks, as did banana and enset controls.
The role of alternate hosts in the disease
cycle is unclear. The pathogen survives for
up to 3 months in the soil in the absence of
a host (42). In a separate study, banana
seedlings replanted in infested fields were
not reinfected after all the diseased mats
were completely uprooted from the field
followed by a 6-month fallow period (62).
This implies that bananas can be replanted
after a relatively short period of time in
fields where the crop was destroyed by X.
campestris pv. musacearum.
Susceptibility of Commonly
Grown Cultivars
Although BXW has been observed on
both East African Highland bananas and
exotic dessert and beer bananas, incidence
varies by clone (63). Disease incidence
was higher in brewing bananas compared
with East African Highland cooking bananas
in severely affected central Uganda.
The exotic cultivars Pisang Awak (ABB),
Bluggoe (ABB), and dessert cultivars Gros
Michel (AAA) and Sukali Ndiizi (AAB),
have higher sugar content in their nectar,
which might make them more attractive to
insect vectors (25). In some regions of
Ethiopia and central Uganda where Pisang
Awak is abundant and de-budding is rarely
practiced, higher rates of BXW spread
have been noted at altitudes below 1,700
masl (3,25).
In a study conducted in Lira district (northern Uganda), disease incidence was highest on Bluggoe (73.5%), followed by Pisang Awak (30.4%), cooking bananas (11.7%), and least in Sukali Ndiizi (2.8%) (66).
Where disease spread is predominantly
through tools, relative susceptibility of
cultivars is also important. For example,
farmers vigorously practice de-budding in
Ntungamo and Mbarara districts of
Uganda where cooking East African Highland bananas are more abundant, but some of the recent outbreaks were difficult to eradicate due to use of contaminated tools
on susceptible cultivars (65).
Control and Management
Strategies
Management of diseases in tropical perennial crops such as banana is a challenge due to continuous association of host and inoculum over a long period of time (47).
The recommended measures for BXW
management involve a mixture of approaches combining exclusion, eradication, host resistance, and protection. Control of BXW and similar bacterial diseases of banana depends on prevention of disease spread (containment), reduction of
disease impact in affected farms (management), and rehabilitation of previously affected areas. Awareness campaigns, advocacy and support from policy makers and the donor community are critical for managing transnational epidemics such the one experienced in the Great Lakes region.
The experiences of various countries in
managing BXW have been variable. In
Uganda and Tanzania, regions with active
political leadership have achieved >90%
control of BXW, whereas the disease
prevalence has almost quadrupled in eastern
Democratic Republic of Congo due to
civil instability (38).
The United States Agency for International Development (USAID) funded a Crop Crisis Control project (C3P) during 2005 to 2008 to help prepare for and mitigate the effects of BXW, so that sudden declines in the productivity of banana will not tip large numbers of people into food insecurity in Burundi, Kenya, Rwanda, Tanzania, and
Uganda.
The specific measures taken to prevent
and/or manage BXW depend on the intensity or threat of the disease in the target
area (35). Areas in which less than 50% of
the farms are affected, each with fewer
than 50% mats infected, are included in the
“epidemic expansion” phase (34). Areas
with more than 75% of the farms affected,
each with more than 75% mats infected,
are included in the “post-epidemic” phase.
A “critical transition phase” describes an
area where more than 50% of farms are
affected, each with less than 50% mats
infected.
In fields where disease incidence is below
50%, removing infected mats is recommended to reduce the inoculum load. In this case, mat removal is urgent because
delays are likely to result in increased
disease incidence. Where conditions are
favorable and insect vectors abundant, the disease spreads sporadically but continuously from infected mats to new plants as soon as they flower. Where insect vectors are important, disease spread can be contained by removal of the male flowers and bunch of infected plants to reduce sources of inoculum. Eventually, entire infected mats should be removed to ensure that no infected suckers reach flowering, providing a source of inoculum for insect vectors.
Where contaminated tools are the main
means of pathogen dissemination, disease
will most likely spread in a systematic
manner starting from the infected mat and
expanding outward. Unless tools are disinfested after use on each mat, the number of infected mats increases rapidly.
In areas where disease incidence exceeds
70% (post-epidemic phase), there is
very little chance of harvesting anything
from the few remaining mats.
For farmers with small pieces of land, it becomes necessary to remove the infected mats so the land is available for alternative crops or livestock integration. Mat removal also starts the process of pathogen reduction in the soil, which is essential if banana is to
be replanted in the same field. The majority
of small-holder farmers in East and
Central Africa would grow other crops on
the farm where banana was uprooted .
The most appropriate replacement
crops are annuals that are nonhosts of Xanthomonas, including beans, cassava,
maize, taro, sweet potato, sorghum, tobacco,
or napier grass.
Cultural practices. Timely removal of
the male bud interrupts the insect transmission cycle and prevents the spread of the disease in banana types that are considered to be at greatest risk of infection. Removal of male buds (de-budding) by twisting the peduncle with a forked stick instead of cutting tools is one of the emphasized practices for preventing disease spread . The disease can be contained in
fields where de-budding is effectively
practiced. However, adoption of de-budding
has been inconsistent among farming
communities (25), where farmers feel that
de-budding affects the quality of the banana,
especially for the juice cultivars (9).
Once BXW occurs in a field, there is no
remedy other than to cut down all infected
plants, completely dig out the
rhizomes, and place the field under fallow
or a prolonged crop rotation regime. A 6-
month fallow period is adequate to avoid
reinfection from soilborne inoculum (62) if
all infected plant material is removed. X.
campestris pv. musacearum can survive
more than 4 months if host debris and
residues are present. Soilborne X. campestris
pv. musacearum may be more important
in the presence of nematodes and weevils
that can create injuries on roots and
thereby enhance penetration by the pathogen
(36).
Bananas reproduce by forming suckers
from vegetative buds on the rhizome, with
several suckers arising from each rhizome.
Where new plantings are to be established,
suckers are dislodged from the mother
plants and transferred to the new plot.
Adjustments in planting practices can reduce
disease incidence and support efforts to
rehabilitate banana productivity on farms
devastated by X. campestris pv. musacearum (36,37).
Pared corms have less risk of infection by X. campestris pv. musacearum if cured for 2 to 3 days before planting. Use of pest- and pathogen-free suckers produced in tissue culture can control the spread of a range of pests and diseases, including BXW (Fig. 11A). A less expensive alternative is macropropagation of suckers, for which production nurseries can be located closer to farming communities, and the suckers can be made available at much lower costs than those for tissue culture.
Wilt-escaping cultivars. As yet, there
are no banana cultivars known to be completely resistant to BXW; however, some cultivars escape infection through the inflorescence because they have persistent
male flowers and bracts , therefore
the cushions on which insects could
land and deposit the bacteria are not exposed.
This characteristic allows the plants
to escape insect-transmitted infections
only, and these cultivars might not possess
cell-mediated resistance. The cultivars that
are known to express this trait are East
African Highland cooking bananas including
Nakitembe and Mbwazirume. Germplasm
with similar inflorescence traits is
also available in Indonesia (I. Buddenhagen,
personal communication).
Some cultivars which shed their male
flowers and expose the cushions also escape
BXW infection through the inflorescence
(40). These include Yangambi km5,
Kikundi, Kisubi, Nakasebera, and
Nakitengu. Some of these cultivars do not
produce exudates on the male cushions,
hence the cushions remain dry and unattractive to insects. Other cultivars have low sap pH, which could be unfavorable for
growth of Xanthomonas within tissues
(40).
Tolerant and resistant cultivars. The
use of resistant cultivars is a cost-effective
method of managing bacterial diseases.
Development of disease-resistant bananas
through conventional breeding requires
resistant donor parents. High levels of cellmediated resistance to X. campestris pv.
musacearum have not been identified in
banana germplasm. Screening for resistance
requires a reliable and rapid method
to unambiguously discriminate host reaction.
Evaluating material in the field is
laborious and hampered by variations in
environmental conditions and nonuniform
distribution of the pathogen. Early evaluation under controlled conditions with artificial inoculation is an important requirement to screen large numbers of Musa spp. for resistance to BXW. An in vitro screening method was developed for early identification of BXW resistance in small tissueculture- grown plantlets (56).
Eight cultivars of banana were screened with 16 isolates of X. campestris pv. musacearum by this method. There were significant differences in reaction among the cultivars,
whereas no significant difference in virulence was observed among the pathogen
isolates. The cultivar Pisang Awak (Kayinja,
ABB) was found to be highly susceptible,
and Musa balbisiana (BB) was
resistant. These reactions corresponded
well with those of artificially inoculated
potted plants.
Therefore, the in vitro screening test can serve as a convenient, cheap, and rapid alternative for the evaluation of Musa germplasm for resistance to BXW in the field.
Even if resistant germplasm sources are
identified, conventional breeding of banana
is a difficult and lengthy process due
to sterility of most cultivars coupled with
long generation times. To circumvent these
difficulties, transgenic technologies may
provide a cost-effective alternative solution
to the BXW pandemic. Some success in
genetic engineering of banana has been
achieved recently (11,22,28,30,49,57,61).
An efficient method for direct gene transfer
via particle bombardment of embryogenic
cell suspensions has been reported in
the cooking banana Bluggoe, the plantain
Three Hand Planty (49), and Cavendish
banana Grand Nain (11). Hernandez et al.
(23) reported that Agrobacterium tumefaciensis compatible with banana and transgenic plants of banana have been obtained by means of A. tumefaciens–mediated transformation of embryogenic cell suspensions (22,28). At present, most transformation protocols use cell suspensions, but establishing cell suspensions is lengthy and cultivar-dependent. Protocols have also been developed with meristematic tissues from various cultivars of Musa (30,57,61), which are applicable to a wide range of Musa cultivars irrespective of ploidy or genotype (57,58,61).
An attractive strategy for bacterial disease
control in crops is to improve plant
defense mechanisms. Recent advances in
genetic engineering offer ways to transfer
resistance genes found in other organisms
into crop varieties without changing favor-
able traits. Plant defense genes from other
plants and antimicrobial proteins are now
potential sources of plant resistance (55).
The state of genetic engineering of banana
for disease resistance, including BXW
resistance, has been extensively reviewed
(55,59).
Of particular interest are the ferredoxinlike
amphipathic protein (pflp, formerly
called AP1) and hypersensitive responseassisting protein (hrap), isolated from sweet pepper (Capsicum annuum), which can intensify the harpinPSS-mediated
hypersensitive response (14,24). These
proteins have dual function: iron depletion
antibiotic action and harpin-triggered hypersensitive response enhancing action.
The transgenes enhanced the hypersensitive
response induced by various pathogens,
such as Erwinia, Pseudomonas, Ralstonia,
and Xanthomonas spp., in nonhost
plants through release of the proteinaceous
elicitor, harpinPSS, in dicots including
tobacco, potato, tomato, broccoli, and the
monocots orchid and rice (24,29,52).
Elicitor- induced resistance is not specific to
particular pathogens, so it could be a very
useful strategy (69). The International
Institute of Tropical Agriculture (IITA) has
negotiated a royalty-free license from the
patent holder Academia Sinica, Taiwan,
through the African Agricultural Technology Foundation (AATF) for access to the pflp gene for production of bananas resistant to BXW in sub-Saharan Africa.
Genetic transformation of banana with the
pflp gene is in progress at IITA in collaboration with the National Agriculture Research Organization (NARO) in Uganda.
Several transformed lines of banana cultivars Pisang Awak (ABB), Mpologoma
(AAA-EA), and Nakitembe (AAA-EA)
have been generated, and are currently
being evaluated for disease resistance under
laboratory conditions.
Conclusion
The BXW pandemic in the Great Lakes
region of East and Central Africa has
threatened the livelihoods of people who
depend on banana. The pathogen kills
plants quickly and spreads rapidly over a
large area in a short time, making the dis-
ease one of the most dreaded in banana.
The recommended measures for BXW
management involve a mixture of approaches combining exclusion, eradication, host resistance, and protection. Although much of the emphasis on BXW has focused on management options based on information on other bacterial wilt diseases, more basic and strategic information on the pathogen is required. The development of disease resistant banana cultivars remains a high priority because farmers are reluctant to employ labor-intensive disease control measures.
Nevertheless, some countries such as Uganda and Tanzania have achieved remarkable success in containing
the impact of the disease through a
mix of various management approaches.
Literature Cited
1. Abele, S., and Pillay, M. 2007. Bacterial wilt
and drought stresses in banana production and
their impact on economic welfare in Uganda:
Implications for banana research in East African
highlands. J. Crop Improv. 19:173-191.
2. Abele, S., Twine, E., and Legg, C. 2007. Food
security in Eastern Africa and the Great Lakes.
Crop Crisis Control Project final report. International
Institute of Tropical Agriculture,
Ibadan, Nigeria.
3. Addis, T., Handoro, F., and Blomme, G. 2004.
Bacterial wilt (Xanthomonas campestris pv.
musacearum) on Enset and banana in Ethiopia.
InfoMusa 13:44-45.
4. Addis, T., Turyagyenda, L. F., Alemu, T.,
Karamura, E., and Blomme, G. 2008. Garden
tool transmission of Xanthomonas vasicola pv.
musacearum on banana and enset in Ethiopia.
Pages 109-110 in: Program and Book of Abstracts
in Banana 2008: Banana and Plantain in
Africa: Harnessing International Partnerships
to Increase Research Impact. International Institute
of Tropical Agriculture, Ibadan, Nigeria.
5. Anonymous 2006. CRS/USAID/IITA Press
Release. Bujumbura - October 31, 2006. Catholic
Relief Services, Crop Crisis Control Project
(C3P). http://www.reliefweb.int/library/
documents/2006/crs-bdi-31oct.pdf
6. Aritua, V., Parkinson, N., Thwaites, R.,
Heeney, J. V., Jones, D. J., Tushemereirwe, W.,
Crozier, J., Reeder, R., Stead, D. E., and
Smith, J. 2008. Characterization of the Xanthomonas
sp. causing wilt of enset and banana
and its proposed reclassification as a strain of
X. vasicola. Plant Pathol. 57:170-177.
7. Aritua, V., Parkinson, N., Thwaites, R., Tushemereirwe,
W., and Smith, J. 2007. Molecular
epidemiology of Xanthomonas campestris
pv. musacearum, the causal agent of Xanthomonas
wilt of banana and enset. Page 32 in:
Program and Abstracts of ISHS/ProMusa symposium:
Recent Advances in Banana Crop Protection
for Sustainable Production and Improved
Livelihoods. Greenway Woods Resort,
White River, South Africa, September 10-14,
2007.
8. Ashagari, D. 1985. Studies on the bacterial
wilt of enset (Ensete ventricosum) and prospects
for its control. Ethiopian J. Agric. Sci.
7:1-14.
9. Bagamba, F., Kikulwe, E., Tushemereirwe, W.
K., Ngabeki, D., Muhangi, J., Kagezi, G.,
Ragama, P. E., and Eden-Green, S. 2006.
Farmer’s awareness of Banana Bacterial Wilt
and its control in Uganda. Afr. Crop Sci. J.
14:157-164.
10. Baker, R., Caffier, D., Choiseul, J. W., De
Clercq, P., Dormannsné-Simon, E., Gerowitt,
B., Karadjova, O. E., Lövei, G., Lansink, A.
O., Makowski, D., Manceau, C., Manici, L.,
Perdikis, D., Puglia, A. P., Schans, J., Schrader,
G., Steffek, R., Strömberg, A., Tiilikkala, K.,
van Lenteren, J. C., and Vloutoglou, I. 2008.
Scientific opinion of the panel on plant health
on a request from the European Commission
on pest risk assessment made by France on
Xanthomonas campestris pv. musacearum,
considered by France as harmful in French
overseas departments of French Guiana, Guadeloupe,
Martinique and Réunion. EFSA J.
669:1-30.
11. Becker, D. K., Dugdale, B., Smith, M. K.,
Harding, R. M., and Dale, J. L. 2000. Genetic
transformation of Cavendish banana (Musa
spp. AAA group) cv. Grand Nain via microprojectile
bombardment. Plant Cell Rep. 19:229-
234.
12. Biruma, M., Pillay, M., Tripathi, L., Blomme,
G., Abele, S., Mwangi, M., Bandyopadhyay,
R., Muchunguzi, P., Kassim, S., Nyine, M.,
Turyagyenda, L., and Eden-Green, S. 2007.
Banana Xanthomonas wilt: A review of the disease,
management strategies and future research
directions. Afr. J. Biotechnol. 6:953-
962.
13. Bouwmeester, H., Abele, S., Manyong, V. M.,
Legg, C., Mwangi, M., Nakato, V., Coyne, D.,
and Sonder, K. 2008. The Potential Benefits of
GIS Techniques in Disease and Pest Control:
An Example Based on a Regional Project in
Central Africa. Page 59 in: Program and book
of Abstracts in: Banana 2008: Banana and
Plantain in Africa: Harnessing International
Partnerships to Increase Research Impact. International
Institute of Tropical Agriculture,
Ibadan, Nigeria.
14. Chen, C. H., Lin, H. J., Ger, M. J., Chow, D.,
and Feng, T. Y. 2000. cDNA cloning and characterization
of a plant protein that may be associated
with the harpinPSS-mediated hypersensitive
response. Plant Mol. Biol. 43:429-
438.
15. Dookun, A., Stead, D. E., and Autrey, L. J. C.
2000. Variation among strains of Xanthomonas
campestris pv. vasculorum from Mauritius and
other countries based on fatty acid analysis.
Syst. Appl. Microbiol. 23:148-155.
16. Eden-Green, S. 2004. Focus on bacterial wilt.
How can the advance of banana Xanthomonas
wilt be halted? Infomusa 13:38-41.
17. Edmeades, S., Smale, M., Kikulwe, E. M.,
Nkuba, J., and Byabachwezi, M. S. R. 2007.
Characteristics of banana-growing households
and banana cultivars in Uganda and Tanzania.
Pages 49-74 in: An Economic Assessment of
Banana Genetic Improvement and Innovation
in the Lake Victoria Region of Uganda and
Tanzania. M. Smale and W. K. Tushemereirwe,
eds. IFPRI Research Report 155. IFPRI, Washington,
DC.
18. FAOSTAT Agriculture Data. 2004. http://apps.
fao.org
19. FAOSTAT Agriculture Data. 2006. http://apps.
fao.org
20. Fiaboe, K. K. M., Beed, F., Mwangi, M.,
Katembo, M., and Ndungo, V. 2008. Survey of
insects visiting banana male buds in eastern
Democratic Republic of Congo and their contamination
with the bacterium causing wilt.
Pages 97-98 in: Program and Book of Abstracts
in Banana 2008: Banana and Plantain in
Africa: Harnessing International Partnerships
to Increase Research Impact. International Institute
of Tropical Agriculture, Ibadan, Nigeria.
21. Fiaboe, K. K. M., Kubiriba, J., Beed, F.,
Mwangi, M., and Tushemereirwe, T. 2008.
Comparative importance and epidemiology of
BXW transmission through female and male
inflorescences. Page 84 in: Program and Book
of Abstracts in Banana 2008: Banana and Plantain
in Africa: Harnessing International Partnerships
to Increase Research Impact. International
Institute of Tropical Agriculture, Ibadan,
Nigeria.
22. Ganapathi, T. R., Higgs, N. S., Balint-Kurti, P.
J., Arntzen, C. J., May, G. D., and Van Eck, J.
M. 2001. Agrobacterium-mediated transformation
of the embryogenic cell suspensions of the
banana cultivars Rasthali (AAB). Plant Cell
Rep. 20:157-162.
23. Hernandez, J. B. P., Remy, S., Sauco, V. G.,
Swennen, R., and Sagi, L. 1999. Chemotactic
movement and attachment of Agrobacterium
tumefaciens to banana cells and tissues. J.
Plant Physiol. 155:245-250.
24. Huang, S. N., Chen, C. H., Lin, H. J., Ger, M.
J., Chen, Z. I., and Feng, T. Y. 2004. Plant
ferredoxin-like protein AP1 enhances Erwiniainduced
hypersensitive response of tobacco.
Physiol. Mol. Plant Pathol. 64:103-110.
25. Kagezi, G. H., Kangire, A., Tushemereirwe,
W., Bagamba, F., Kikulwe, E., Muhanji, J.,
Gold, C. S., and Ragama, P. 2006. Banana
Bacterial wilt incidence in Uganda. Afr. Crop
Sci. J. 14:83-91.
26. Kalyebara, R., Wood, S., and Abodi, P. M.
2007. Assessing the potential impact of selected
technologies on the banana industry in
Uganda. Pages 141-156 in: An Economic Assessment
of Banana Genetic Improvement and
Innovation in the Lake Victoria Region of
Uganda and Tanzania. M. Smale and W. K. Tushemereirwe,
eds. IFPRI Research Report 155.
IFPRI, Washington, DC.
27. Kayobyo, G., Aliguma, L., Omiat, G.,
Mugisha, J., and Benin, S. 2005. Impact of
BXW on household livelihoods in Uganda.
“Assessing the impact of the banana bacterial
wilt (Xanthomonas campestris pv. musacearum)
on household livelihoods in East Africa”,
workshop held on Dec. 20, 2005, Kampala,
Uganda.
28. Khanna, H., Becker, D., Kleidon, J., and Dale,
J. 2004. Centrifugation Assisted Agrobacterium
tumefaciens-mediated Transformation
(CAAT) of embryogenic cell suspensions of
banana (Musa spp. Cavendish AAA and Lady
finger AAB). Mol. Breed. 14:239-252.
29. Liau, C. H., Lu, J. C., Prasad, V., Lee, J. T.,
Hsiao, H. H., You, S. J., Yang, N. S., Huang, H.
E., Feng, T. Y., Chen, W. H., and Chan, M. T.
2003. The sweet pepper ferredoxin-like protein
(pflp) conferred resistance against soft rot disease
in Oncidium orchid. Transgenic Res.
12:329-336.
30. May, G. D., Rownak, A., Mason, H., Wiecko,
A., Novak, F. J., and Arntzen, C. J. 1995. Generation
of transgenic banana (Musa acuminata)
plants via Agrobacterium-mediated transformation.
Bio/Technology 13:486-492.
31. Mbaka, J., Ndungu, V., and Mwangi, M. 2007.
Outbreak of Xanthomonas wilt (Xanthomonas
campestris pv. musacearum) on banana in
Kenya. Pages 58-59 in: Program and Abstracts
of ISHS/ProMusa symposium: Recent Advances
in Banana Crop Protection for Sustainable
Production and Improved Livelihoods.
Greenway Woods Resort, White River, South
Africa, September 10-14, 2007.
32. Mgenzi, S. R. B., Eden-Green, S. J., and Peacock,
J. 2006. Overview of banana Xanthomonas
wilt in Tanzania. Page 107 in: Abstract
Book of the 4th International Bacterial Wilt
Symposium, 17-20 July 2006. G. Saddler, J.
Elphinstone, and J. Smith, eds. Central Science
Laboratory, York, UK.
33. Miller, S. A., Kinyua, Z. M., Beed, F., Harmon,
C. L., Xin, J., Gilbertson, R., and Garcia, L.
2008. The International Plant Diagnostic Network
(IPDN) in Africa: Improving capacity for
diagnosing diseases of banana and other Afri450
Plant Disease / Vol. 93 No. 5
can crops. Page 59 in: Program and Book of
Abstracts in Banana 2008: Banana and Plantain
in Africa: Harnessing International
Partnerships to Increase Research Impact. International
Institute of Tropical Agriculture,
Ibadan, Nigeria.
34. Mwangi, M. 2007. Removing infected banana
mats to contain Xanthomonas wilt: Experiences
in Uganda, Rwanda and the Democratic
Republic of Congo. A brief prepared for the
Crop Crisis Control Project. IITA-C3P, IITA,
Kampala, Uganda. http://c3project.iita.org/
DOC/A4-C3PBriefBananaMatRemoval.pdf
35. Mwangi, M., and Bandyopadhyay, R. 2006.
Managing Banana Xanthomonas Wilt. http://
eastafrica.usaid.gov/proxy/Document.1017.aspx
36. Mwangi, M., Bandyopadhyay, R., Ragama, P.,
and Tushemereirwe, W. K. 2007. Assessment
of banana planting practices and cultivar tolerance
in relation to management of soil-borne
Xanthomonas campestris pv. musacearum.
Crop Prot. 26:1203-1208.
37. Mwangi, M., Bandyopadhyay, R., Tushemereirwe,
W., and Ragama, P. 2006. Developing
technologies to support replanting of banana
to rehabilitate farms affected by Xanthomonas
wilt. Page 63 in: Abstract Book of the
Dr. Tripathi is a biotechnologist at the International
Institute of Tropical Agriculture (IITA) based in Uganda.
She obtained her Ph.D. in plant molecular biology in 1999
from National Botanical Research Institute, Lucknow,
India. She worked as a research scientist at the
University of North Carolina, Greensboro, before joining
IITA in 2000. Her primary research focuses on
development of disease and pest resistant cultivars of
banana and plantain. She is extensively involved in
research on banana bacterial wilt disease.
Dr. Mwangi is a plant pathologist at the International
Institute of Tropical Agriculture (IITA) based in Uganda.
He obtained his Ph.D. in plant pathology from the
University of Bonn in Germany in 2003. He has been
working at IITA since 2003, first on diseases of root and
tuber crops in the tropical forests of west and central
Africa, and since 2005 on banana bacterial wilt in east
and central Africa.
Dr. Abele is an agricultural economist who is focusing
on farming systems, market, and impact analysis. He
obtained his Ph.D. in agricultural sciences from the
University of Hohenheim, Germany, in 2000, and has
been working with various agricultural research institutes
since 1995. He joined the International Institute of
Tropical Agriculture (IITA) in 2002 and is at present based
in Tanzania.
Dr. Aritua is a molecular biologist at the National
Agricultural Research Organization (NARO), Uganda
based at National Agricultural Research Laboratories
Institute, Uganda. He obtained his Ph.D. in molecular
virology from Makerere University following dissertation
research at Federal Biological Research Center for
Agriculture and Forestry, Germany. He worked as a
research scientist at Central Science Laboratory, UK on
molecular characterization of Xanthomonas campestris
pv. musacearum. His research focuses on molecular
epidemiology of pathogens of banana.
Dr. Tushemereirwe is a plant pathologist and
coordinator of the National Banana Research Programme
at the National Agricultural Research Organization
(NARO), Uganda. He has a Ph.D. in plant pathology from
the University of Reading, UK. His primary research
focuses on the improvement of banana for the better
livelihood of the resource-poor farmers of Uganda.
Ranajit Bandyopadhyay is a plant pathologist at the
International Institute of Tropical Agriculture (IITA) based
in Nigeria. He obtained his Ph.D. in plant pathology in
1980 from Haryana Agriculture University in India. He has
been working in international agriculture research centers
since 1980, first as a sorghum pathologist at the
International Crops Research Institute for the Semi-Arid
Tropics (ICRISAT, India) from 1980 to 2001, and then as a
plant pathologist at IITA, Nigeria from 2002 to the
present. He spent two sabbatical leaves at Cornell
University during 1990-91 and at Texas A&M University
during 1998-99. He is responsible for IITA’s Africa-wide
research and development activities related to diseases
of maize, soybean, cassava, banana, cowpea, and yam.
Valentine Aritua
Wilberforce Kateera Tushemereirwe
Ranajit Bandyopadhyay
Leena Tripathi
Maina Mwangi
Steffen Abele
Plant Disease / May 2009 451
4th International Bacterial Wilt Symposium,
17-20 July 2006. G. Saddler, J. Elphinstone,
and J. Smith, eds. Central Science Laboratory,
York, UK.
38. Mwangi, M., Kubiriba, J., and Tushemereirwe,
W. 2008. The political perspective of banana
Xanthomonas wilt control in Eastern and Central
Africa. Pages 197 in: Program and Book of
Abstracts in Banana 2008: Banana and Plantain
in Africa: Harnessing International Partnerships
to Increase Research Impact. IITA,
Ibadan, Nigeria.
39. Mwangi, M., Mwebase, M., Bandyopadhyay,
R., Aritau, A., Eden-Green, S., Tushemereirwe,
W., and Smith, J. 2007. Development of a
semi-selective media for the isolation of Xanthomanas
campestris pv. musacearum from insect
vectors, infected plant material and soil.
Plant Pathol. 56:383-390.
40. Mwangi, M., Pillay, M., Bandyopadhyay, R.,
Tushemereirwe, W., and Ragama, P. 2006. Progress
in understanding mechanisms of host
plant tolerance to banana bacterial wilt. Page
65 in: Abstract Book of the 4th International
Bacterial Wilt Symposium, 17-20 July 2006.
G. Saddler, J. Elphinstone, and J. Smith, eds.
Central Science Laboratory, York, UK.
41. Mwangi, M., Tinzaara, W., Vigheri, N., Namu,
F. N., Ragama, P., and Bandyopadhyay, R.
2006. Comparative study of banana Xanthomonas
wilt spread in mid and high altitudes of the
Great Lakes region of Africa. Tropentag symposium
2006, Bonn, Germany. http://elewa.
org/pestdseagric.html
42. Mwebaze, J. M., Tusiime, G., Tushemereirwe,
W. K., and Kubiriba, J. 2006. The survival of
Xanthomonas campestris pv. musacearum in
soil and plant debris. Afr. Crop Sci. J. 14:121-
128.
43. Ndungo, V., Eden-Green, S., Blomme, G.,
Crozier, J., and Smith, J. 2006. Presence of banana
xanthomonas wilt (Xanthomonas campestris
pv. musacearum) in the Democratic Republic
of Congo (DRC). Plant Pathol. 55:294.
44. Okech, H. O., Gold, C. S., Abele, S., Nankinga,
C. M., Wetala, P. M., Van Asten, P.,
Nambuye, A., and Ragama, P. 2004. Agronomic,
pests and economic factors influencing
sustainability of banana-coffee systems of
Western Uganda and potentials for improvement.
Uganda J. Agric. Sci. 9:432-444.
45. Ortiz, R., Frison, E., and Sharrock, S. 2002.
The CGIAR - Future Harvest program for
Musa in Africa. Chronica Hortic. 42:18-24.
46. Peterson, R. K. D., and Hunt, T. E. 2003. The
probabilistic economic injury level: Incorporating
economic uncertainty into pest-management
decision making. J. Econ. Entomol.
96:536-542.
47. Ploetz, R. C. 2007. Diseases of tropical perennial
crops: Challenging problems in diverse environments.
Plant Dis. 91:644-663.
48. Reeder, R., Opolot, O., Muhinyuza, J., Aritua,
A., Crozier, J., and Smith, J. 2007. Presence of
Banana Bacterial Wilt (Xanthomonas campestris
pv. musacearum) in Rwanda. http://www.
bspp.org.uk/ndr/jan2007/2007-01.asp
49. Sagi, L., Panis, B., Remy, S., Schoofs, H., De
Smet, K., Swennen, R., and Cammus, B. 1995.
Genetic transformation of banana (Musa spp.)
via particle bombardment. Bio/Technology
13:481-485.
50. Smith, J. J., Jones, D. R., Karamura, E.,
Blomme, G., and Turyagyenda, F. L. 2008. An
analysis of the risk from Xanthomonas campestris
pv. musacearum to banana cultivation
in Eastern, Central and Southern Africa.
http://www.promusa.org/images/stories/infomu
sa/features/pdf/pra.pdf
51. Ssekiwoko, F., Taligoola, H. K., and Tushemereirwe,
W. K. 2006. Xanthomonas campestris
pv musacearum host range in Uganda. Afr.
Crop Sci. J. 14:111-120.
52. Tang, K., Sun, X., Hu, Q., Wu, A., Lin, C. H.,
Lin, H. J., Twyman, R. M., Christou, P., and
Feng, T. Y. 2001. Transgenic rice plants expressing
the ferredoxin-like protein (AP1)
from sweet pepper show enhanced resistance
to Xanthomonas oryzae pv. oryzae. Plant Sci.
160:1035-1042.
53. Thwaites, R., Eden-Green, S., and Black, R.
2000. Diseases Caused by Bacteria. Pages 213-
239 in: Diseases of Banana, Abacá and Enset.
D. R. Jones, ed. CABI Publishing, Wallingford,
UK.
54. Tinzaara, W., Gold, C. S., Ssekiwoko, F.,
Bandyopadhyay, R., Abera, A., and Eden-
Green, S. J. 2006. Role of insects in the transmission
of banana bacterial wilt. Afr. Crop Sci.
J. 14:105-110.
55. Tripathi, L. 2005. Transgenic technologies for
developing bacterial disease resistance in
plants. Pages 200-220 in: Genetic Resources
and Biotechnology, Vol. 3. D. Thangadurai, T.
Pullaiah, and L. Tripathi, eds. Regency Publications,
New Delhi.
56. Tripathi, L., Odipio, J., Tripathi, J. N., and
Tusiime, G. 2008. A rapid technique for
screening banana cultivars for resistance to
Xanthomonas wilt. Eur. J. Plant Pathol. 121:9-
19.
57. Tripathi, L., Tripathi, J. N., and Hughes J. d’A.
2005. Agrobacterium-mediated transformation
of plantain cultivar Agbagba (Musa spp.). Afr.
J. Biotechnol. 4:1378-1383.
58. Tripathi, L., Tripathi, J. N., Oso, R. T.,
Hughes, J. d’A., and Keese, P. 2003. Regeneration
and transient gene expression of African
Musa species with diverse genomic constitution
and ploidy levels. Trop. Agric. 80:182-187.
59. Tripathi, L., Tripathi, J. N., and Tushemereirwe,
W. K. 2004. Strategies for resistance
to bacterial wilt disease of banana
through Genetic Engineering. Afr. J. Biotechnol.
3:688-692.
60. Tripathi, L., Tripathi, J. N., Tushemereirwe, W.
K., and Bandyopadhyay, R. 2007. Development
of a semi-selective medium for isolation
of Xanthomonas campestris pv. musacearum
from banana plants. Eur. J. Plant Pathol.
117:177-186.
61. Tripathi, L., Tripathi, J. N., and Tushemereirwe,
W. K. 2008. Rapid and efficient production
of transgenic East African Highland
banana (Musa spp.) using intercalary
meristematic tissues. Afr. J. Biotechnol.
7:1438-1445.
62. Turyagyenda, L. F., Blomme, G., Ssekiwoko,
F., and Eden-Green, S. 2007. Determination of
the appropriate fallow period to control Xanthomonas
wilt following infection of banana.
Pages 58-59 in: Program and Abstracts of
ISHS/ProMusa symposium: Recent Advances
in Banana Crop Protection for Sustainable Production
and Improved Livelihoods. Greenway
Woods Resort, White River, South Africa, September
10-14, 2007.
63. Tushemereirwe, W. K., Kangire, A., Smith, J.,
Ssekiwoko, F., Nakyanzi, M., Kataama, D.,
Musiitwa, C., and Karyeija, R. 2003. An out
break of bacterial wilt on banana in Uganda.
InfoMusa 12:6-8.
64. Tushemereirwe, W., Kangire, A., Ssekiwoko,
F., Offord, L. C., Crozier, J., Boa, E., Rutherford,
M., and Smith, J. J. 2004. First report of
Xanthomonas campestris pv. musacearum on
banana in Uganda. Plant Pathol. 53:802.
65. Tushemereirwe, W. K., Okaasai, O., Kubiriba,
J., Nanakinga, C., Muhangi, J., Odoi, N., and
Opiuo, F. 2006. Status of banana bacterial wilt
in Uganda. Afr. Crop Sci. J. 14:73-82.
66. Tushemereirwe, W. K., Ssekiwoko, F., and
Ojeke, C. 2003. An outbreak of banana bacterial
wilt in Lira. Page 25 in: NBRP, Kawanda
Agriculture Research Institute.
67. Vauterin, L., Hoste, B., Kersters, K., and
Swings, J. 1995. Reclassification of Xanthomonas.
Int. J. Syst. Bacteriol. 45:472-489.
68. Wamboga-Mugirya, P. 2006. Uganda ‘needs
biotech law’ to save banana sector. SciDevNet.
http://www.scidev.net/en/news/uganda-needsbiotech-
law-to-save-banana-sector.html
69. Wei, Z. M., and Beer, S. V. 1996. Harpin from
Erwinia amylovora induces plant resistance.
Acta Hortic. 411:427-431.
70. Yirgou, D., and Bradbury, J. F. 1968. Bacterial
wilt of enset (Ensete ventricosum) incited by
Xanthomonas musacearum sp. nov. Phytopathology
58:111–112.
71. Yirgou, D., and Bradbury, J. F. 1974. A note on
wilt of banana caused by the enset wilt organism
Xanthomonas musacearum. East Afr. Agric.
For. J. 40:111-114.
72. Young, J. M., Bradbury, J. F., Davis, R. E.,
Dickey, R. S., Ercolani, G. L., Haywood, A.
C., and Vidaver, A. K. 1991. Nomenclature revisions
of plant pathogenic bacteria and list of
names 1980-1988. Rev. Plant Pathol. 70:211-
221.
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