Phytobiomes Journal  2023  7:29-41 https://doi.org/10.1094/PBIOMES-06-22-0038-RVW
REVIEW
Changing Dynamics in the Spread and Management of Banana
Xanthomonas Wilt Disease in Uganda Over Two Decades
Jerome Kubiriba,1 Rockefeller Erima,1 Arthur K. Tugume,2,† William Tinzaara,3 and Wilberforce K. Tushemereirwe1
1 National Banana Research Program, National Agricultural Research Organization (NARO), P.O. Box 7065, Kampala, Uganda
2 Department of Plant Sciences, Microbiology and Biotechnology, College of Natural Sciences, Makerere University, P.O. Box 7062, Kampala,
Uganda
3 Alliance of Bioversity International and CIAT, P.O. Box 6247, Kampala, Uganda
Accepted for publication 17 January 2023.
ABSTRACT
Banana Xanthomonas wilt (BXW) is a destructive disease action; hence, only 30% impact in controlling BXW was
caused by Xanthomonas vasicola pv. musacearum (Xvm), a registered. In contrast, participatory approaches mobilized
bacterium that indiscriminately infects all banana varieties grown farming communities into action and effectively controlled BXW
in East and Central Africa (ECA). In this region, BXW was first at field and community levels to near eradication. The
reported in 2001 in Uganda and was projected to eliminate approaches effectively controlled BXW in Uganda and,
>90% of Uganda’s banana crops (worth USD4 billion) if not consequently, in eastern Kenya, northern Tanzania, Rwanda,
controlled in less than 10 years. Lack of basic information led to Burundi, and the Democratic Republic of Congo. This article
application of control approaches that were based on similarity reviews step-wise processes leading to success over the 2
of BXW symptoms to those of Moko disease of banana. decades and identifies critical research gaps. Deployment of
However, the approaches were unsuccessful and, in 7 to 9 resistant genotypes is urgently needed as a significant addition
years, BXW had covered six countries and threatened to wipe to the BXW management toolbox to create BXW-free banana
out the banana industry in ECA. However, BXW has been tamed cropping systems in ECA.
to date, mainly due to relentless and systematic deployment of
carefully crafted and packaged cultural control practices based
on epidemiological information generated within target banana Keywords: banana (Musa spp.), banana Xanthomonas wilt
cropping ecosystems. In Uganda, the initial “top-down” (BXW), community participatory approaches, disease
communication approaches reached >85% of banana farming management, East and Central Africa, plant disease
communities but did not mobilize the communities enough into epidemiology, Uganda
Banana (Musa spp.) is the main food and cash crop for 400 kg/capita/year (Kabahenda et al. 2010; Kalyebara et al. 2006;
over 70 million smallholder farmers in East and Central Africa PIBID 2007). The ability of banana to be amenable to a diversity
(ECA), with an annual production worth US$4.3 billion, equiv- of food, feed, and industrial uses places the crop strategically in
alent to approximately 6% of ECA’s gross domestic product transforming economies of some countries in ECA such as Uganda
(Arvanitoyannis et al. 2008; FAOSTAT 2020; Kakuru et al. 2018; (Padam et al. 2014). Because alternative food security staples such
Nyombi 2013). Although the crop is important in ECA, the world’s as cassava (Manihot spp.) and sweetpotato (Ipomoea spp.) in ECA
per capita consumption of banana is highest in Uganda at 220 to had been damaged by the emergence of devastating viral disease
epidemics in the region since the late 1990s (Alabi et al. 2011;
†Corresponding author: A. K. Tugume; arthur.tugume@mak.ac.ug Alicai et al. 2007; Clark et al. 2012; Rey and Vanderschuren 2017;
Thresh et al. 1997; Valverde et al. 2007), the pressure to sustain the
Funding: Financial support was provided by “Feed the Future Project” (USAID). region’s food security system remained anchored on banana.
e-Xtra: The productivity and ability of banana to support ECA food
Supplementary material is available online.
security, however, became severely constrained with the emergence
The author(s) declare no conflict of interest. of a highly destructive disease, banana Xanthomonas wilt (BXW)
(Drenth and Kema 2021; Tushemereirwe et al. 2004). BXW de-
Copyright © 2023 The Author(s). This is an open access article stroyed entire household banana farms in some areas of East Africa
distributed under the CC BY-NC-ND 4.0 International license. because it successfully and indiscriminately infects all banana
Vol. 7, No. 1, 2023 29
varieties grown in this region (Geberewold 2019; Karamura et al. yellowish bacterial oozes that appear 5 to 20 min after cutting
2008; Smith et al. 2008b). Currently, BXW is known only in Africa diseased pseudostems (Tripathi et al. 2009; Tushemereirwe et al.
(Uganda, the Democratic Republic of Congo [DRC], Rwanda, 2004). These symptoms develop rapidly and the infected plants
Burundi, Kenya, Tanzania, and Ethiopia) (Mbaka et al. 2008; wilt and rot within 3 to 4 weeks under field conditions (Smith et al.
Ndungo et al. 2006; Niko et al. 2011; Ocimati et al. 2019; 2008a). Under conditions of water stress, banana plants are physi-
Tushemereirwe et al. 2003; Yirgou and Bradbury 1974). Prior ologically weak and, hence, more vulnerable to BXW and express
to 2001, BXW was only historically known in and restricted to symptoms faster (Ochola et al. 2015).
Ethiopia on a cultivated relative of banana, enset (Ensete ventri- BXW is transmitted by insects, birds, and bats during natural
cosum) (Yirgou and Bradbury 1968), and on banana (Yirgou and process of pollination by these agents (Buregyeya et al. 2014;
Bradbury 1974). In ECA, the disease soon became an epidemic, Rutikanga et al. 2015; Ssekiwoko et al. 2006a; Tinzaara et al. 2006).
quickly destroyed banana plantations, caused close to 100% loss Moreover, disease spread is promoted by repeated use of contam-
of production, and threatened people’s livelihoods and the banana inated farm tools during crop husbandry practices, and using in-
industry in the region (Kalyebara et al. 2006; Tripathi et al. 2009; fected suckers as planting materials (Mwangi and Nakato 2007).
Tinzaara et al. 2011). The spread of BXW differs between cropping systems because
Lack of information in the early 2000s led to application of in- farming practices in different areas may predispose the plants to
effective control methods that were based on similarities between BXW differently (Smith et al. 2008a). Over 90% of banana cul-
BXW and another bacterial wilt disease of banana, Moko disease tivars grown in Uganda belong to the subgroup of East African
(Blomme et al. 2011, 2017a; Lehmann-Danzinger 1987; Tushe- highland banana (EAHB, matooke, AAA-EA) compared with DRC
mereirwe et al. 2004). Unfortunately, these methods were ineffec- where Kayinja (Pisang Awak, ABB) constitutes the main variety
tive and, consequently, BXW quickly spread to all major banana- grown (Blomme et al. 2014). The flowers of Kayinja are sweeter
growing regions in Uganda between 2001 and 2006 and, within and contain more nectar than the EAHB cultivars, which promotes
only 9 years, the disease had spread across the six countries of more frequent visitations of airborne vectors to Kayinja (Kagezi
the ECA (Ndungo et al. 2006; Niko et al. 2011; Tushemereirwe et al. 2006; Mwangi and Nakato 2007). In contrast, EAHB cultivars
et al. 2003). Since then, with accumulated epidemiological infor- are predominantly grown on a larger-scale plantation, characterized
mation on the BXW, various control and management options have by intensive husbandry practices, which presents a greater risk of
been developed and applied with varying success levels (Blomme mechanical or tool-mediated spread of BXW (Drenth and Kema
et al. 2014; Kikulwe et al. 2019; Kubiriba et al. 2016; McCampbell 2021; Karamura et al. 2013; Tinzaara et al. 2009; Tushemereiwe
et al. 2018; Smith et al. 2008a). Because Uganda’s food security et al. 2006). Therefore, whereas in the less-managed Kayinja-based
system was the first to be most severely affected by BXW, and be- system, vector-mediated transmission is the dominant route, tool-
ing the first recorded BXW incidence outside Ethiopia (Tripathi mediated transmission is the main route of BXW transmission in
et al. 2009; Tushemereirwe et al. 2004), the national agricultural the highly managed EAHB-based cropping system.
research system in Uganda launched initial multipronged, rapid
control strategies against BXW. Rapid rural appraisal and partic- XANTHOMONAS VASICOLA PV. MUSACEARUM
ipatory approaches were mounted involving active participation
of banana farming communities, local leaders, and government. Xanthomonas vasicola pv. musacearum (Xvm), previously des-
Most of these strategies were scalable to the region (Blomme et al. ignated as X. campestris pv. musacearum (Studholme et al. 2020),
2014, 2017b; Gotor et al. 2022; Karamura et al. 2006; Kubiriba and is a rod-shaped, aerobic, Gram-negative, flagelled, xylem-limited
Tushemereirwe 2014; Kubiriba et al. 2014; Mbabazi et al. 2021; proteobacterium and the causative agent of BXW (Bradbury 1986;
Pagnani et al. 2021). Despite the success, resurgences of BXW Smith et al. 2008a). Isolates of Xvm collected from various areas
were recorded where the disease had been successfully managed affected by BXW showed a high level of genetic homogeneity and
(Kubiriba et al. 2012b). Furthermore, there are reports that BXW close phylogenetic relationships (Aritua et al. 2007; Odipio et al.
is still spreading in areas of DRC (Blomme et al. 2014; Ocimati 2009). Observed close phylogenetic relationships within Xvm iso-
et al. 2019), partly because of not fully implementing recommended lates in Uganda were strange, given the high level of severity of
control and management strategies (Gotor et al. 2022). Recently, the disease in the field and rapidly spreading nature of the disease.
Mozambique was listed at high risk of BXW due to the abundance It could possibly be explained by recent spread originating from a
of Bluggoe (Musa ABB genotype), which is highly susceptible to single introduction event of Xvm.
insect-, bird-, and bat-vectored disease transmission (Ocimati et al. Using single-nucleotide polymorphism analysis, two major sub-
2019). Therefore, there is no guarantee that BXW will not resurge lineages of Xvm (named sublineages I and II) were later identi-
or that its spread to new areas will be halted. fied (Wasukira et al. 2012). This was suggestive of two introduc-
The aim of this review is to summarize information on achieve- tory events: one event represented by sublineage I (isolates from
ments and experiences on BXW management in Uganda over the DRC and Rwanda) and another represented by sublineage II (iso-
last two decades and how these provide a springboard for research lates from Uganda, Tanzania, Burundi, and Kenya) (Wasukira et al.
and development efforts in relation to the BXW epidemic in ECA. 2012). Using polymorphic multilocus number of tandem repeat
This will enable stakeholders to identify areas of successful ap- analysis markers on a larger Xvm collection, 12 clusters were iden-
proaches for deployment at scale. We stimulate scholarship by iden- tified (Nakato et al. 2018a). Although most of the clusters were
tifying the most urgent research gaps as well as action points for consistent with the sublineage classification suggested earlier by
regional governments on more effective management and possibili- Wasukira et al. (2012), more diversity was observed in the clusters
ties of BXW eradication for sustainable banana production in ECA. that were not assigned to any of the earlier reported sublineages
(Nakato et al. 2018a). However, symptom expression does not dif-
SYMPTOMS, TRANSMISSION, AND SPREAD fer significantly between sublineages because the Xvm diversity
OF BXW observable at a molecular level is not obvious phenotypically. Thus
far, the management practices have not changed but may need to
Symptoms of BXW include progressive yellowing and wilting change for effective control of future BXW epidemics if the variants
of leaves, premature and uneven ripening of fruit, and creamy- continue to be become apparent.
30 Phytobiomes Journal
INITIAL EFFORT FOR THE CONTAINMENT AND to develop BXW resistance. Otherwise, the only current, feasi-
MANAGEMENT OF BXW ble way to improve BXW resistance is using transgenic technol-
ogy (Lorenzen et al. 2008; Shotkoski et al. 2010; Tripathi et al.
A “fire-fighting” strategy that never put out the fire. Because 2016) or genome editing approaches (Tripathi et al. 2022). There-
the BXW outbreak was abrupt and new in Uganda, and no epi-
demiological information was available on which to base action
(Tushemereirwe et al. 2004), all of the initial methods of con-
tainment were in a “fire-fighting” mode, based on experiences of
another banana bacterial wilt (Moko) disease control in Central
America (Blomme et al. 2017a; Fegan and Prior 2006; Lehmann-
Danzinger 1987; Munar-Vivas et al. 2010). Uganda government,
through the Ministry of Agriculture, Animal Industry and Fisheries
(MAAIF), responded by constituting a task force in December 2001
to develop a strategy for disease eradication. This strategy empha-
sized massive creation of awareness and measures aimed at eradi-
cation of BXW by massive cutting and burying of infected banana
stools (Fig. 1), quarantine, decapitation of male buds to block fur-
ther vector transmission, and disinfection of farm tools used in the
affected fields (Tushemereiwe et al. 2006). The strategy was admin-
istered in the two affected districts of central Uganda (Mukono and
Kayunga), which temporality reduced disease incidence to <10%.
However, due to high costs, limited awareness about the need for
BXW control by the farming communities, and nonsystematic de-
ployment of the measures, implementation of the strategy became
unsustainable and soon BXW escalated into 11 new neighboring
districts, necessitating a change of approach from disease “eradi-
cation” to “containment and management”.
Consequently, in 2003, the National Agricultural Research Orga-
nization (NARO) constituted another taskforce to formulate a more
comprehensive research strategy for a country-wide containment of
BXW. The strategy emphasized surveillance, generating scientific
information and technologies for disease management, improving
policies appropriate for control of BXW, and monitoring the impact
of implementing these activities (Tushemereiwe et al. 2006). The
development of BXW resistance was one of the key objectives un-
der this strategy but this was only feasible in the long run (Tripathi
et al. 2016, 2017, 2022).
Identifying sources of resistance to BXW in banana
germplasm. Some banana cultivars such as Mbwazirume (AAA-
EA), Nakitembe (AAA-EA), and M9 (AAA-EA hybrid), all of
which belong to the EAHB group, can escape vectored BXW
infection because they have persistent or semipersistent bracts on
the male inflorescence (Mudonyi et al. 2019). Persistent flowers
or bracts remain attached to the flower stalk (peduncle), leaving
no room for insect contamination because there is no entry point
left, whereas dehiscent inflorescences of other varieties create
room for insect contamination (Fiaboe et al. 2010). In rare cases,
cultivars such as Scambia (AAB) lack male buds (Kubiriba and
Tushemereirwe 2014), which eliminates vector-mediated trans-
mission. Deployment of such cultivars can only reduce the cost
of cultural control of BXW, eliminating vectored BXW infection.
However, these cultivars are susceptible to tool-mediated BXW Fig. 1. Some of the early methods of controlling banana Xanthomonas
infection. Thus, a more durable form of resistance is desired, and wilt (BXW) that were not sustainable. A, Massive uprooting and burying
this can only be achieved through conventional or nonconventional of BXW-infected plants into a ditch dug in the middle of the plantation.
breeding. The banana plantation (background) had just undergone intensive prun-
Early studies confirmed the inedible wild progenitor of banana, ing by tool-mediated removal of fresh leaf sheath from the base of the
Musa balbisiana (BB genome), as a potential source of resistance pseudostem, a practice known to enhance tool-mediated transmission
among several tested Musa genotypes (Ssekiwoko et al. 2006c, of BXW (Photo taken by Dr. Guy Blomme in Rwanda). B and C, Banana
2015). In addition, Nakato et al. (2019) screened 72 banana ac- farmers in Kayunga district, central Uganda in June 2002 undertaking
massive destruction of banana plantations where BXW-infected plants
cessions from the International Institute of Tropical Agriculture had been identified during the very early stages of BXW epidemic. Part
(IITA) germplasm collection, including male parents widely used of the plantation that had just been cut down (B) and the same farmers
in banana breeding programs. M. balbisiana was reconfirmed as disinfecting their hands by washing with JIK (sodium hypochlorite) (C).
resistant, while other genotypes were either tolerant or suscepti- Kayunga is where the first record of BXW was made in Uganda and
ble. This increases the possibility of using conventional breeding East and Central Africa (Photos taken by Jerome Kubiriba).
Vol. 7, No. 1, 2023 31
fore, IITA in collaboration with NARO and the African Agricul- (Blomme et al. 2008; Kubiriba and Tushemereirwe 2014; Kubiriba
tural Technology Foundation tested constitutive expression of a et al. 2014). SDSR was successfully applied in Uganda, Kenya,
hypersensitive response-assisting protein (Hrap) gene and a plant and DRC and significantly reduced BXW incidence (Kubiriba and
ferredoxin-like protein (pflp) gene from sweet pepper (Capsicum Tushemereirwe 2014; Kubiriba et al. 2014). The advantage of us-
annuum) (Chen et al. 2000; Lin et al. 1997). Both genes showed ing SDSR is that there are no costs of uprooting or replanting the
stable and specific resistance against BXW in banana (Nimusiima whole mat or the entire plantations, which allows the remaining un-
et al. 2015; Shotkoski et al. 2010; Tripathi et al. 2014, 2016, 2017, infected plants to continue yielding harvestable fruit (Blomme et al.
2019). Currently, the most used biotechnology tools revolve around 2008; Kikulwe et al. 2022; Kubiriba et al. 2014). Therefore, SDSR
use of transgenes; however, with better understanding of the Xvm has been essential in rehabilitating sections of plantations infected
pathosystem (Wasukira et al. 2014), other tools such as gene edit- by BXW without the necessity of uprooting the entire plantation
ing may be used to develop BXW resistance in the future. For ex- and planting afresh. Such local sections in banana plantations are
ample, broad-spectrum disease resistance that has been developed characterized by an open space of newly planted or sprouted young
in cotton through CRISPR/Cas9 genome editing of specific host- shoots (Fig. 2).
susceptibility genes has been demonstrated in banana against BXW Utilizing knowledge of disease transmission routes to con-
and other diseases (Ntui et al. 2020; J. N. Tripathi et al. 2021; L. trol BXW. In addition to tool-mediated transmission, BXW is also
Tripathi et al. 2021, 2022). spread by insects, birds, and bats from male buds of diseased plants
Applying knowledge of disease etiology and epidemiology to to those of healthy plants (Kubiriba and Tushemereirwe 2014).
manage BXW. Studies were designed to generate etiological and Therefore, to tame the spread of BXW, early removal of male buds
epidemiological information within the areas of disease outbreak. from banana plants using a forked stick eliminated the spread of the
These included survival of the bacteria in the soil, refuse and hosts, disease by vectors within or into new fields (Tinzaara et al. 2006).
disease spread dynamics, and possible ways to stop spread in new Tools used for pruning create wounds on diseased plants, pick up
fields or within fields. This then formed a basis for development the sap with bacteria, and spread it to nondiseased plants (Mwangi
of cultural control practices for the management of BXW (Smith and Bandyopadhay 2006; Mwangi et al. 2007; Yirgou and Bradbury
et al. 2008a; Tushemereiwe et al. 2006). Use of clean planting ma- 1968). Live Xvm bacterial cells were recovered from knives and ma-
terial was the first recommendation for BXW management in the chetes up to 20 days after inoculation (Buregyeya 2010). Banana
early years of the epidemic in ECA, because it was thought to be a traders in Uganda travel over 300 km a day with nondisinfected
major means of limiting long-distance spread of the disease. The as- tools, indicating possibilities of spreading BXW between banana-
sumption at the time was that infected mats could not produce clean growing regions of Uganda. In one household, a single tool that is
suckers and that a single infected plant on a mat meant that all plants not disinfected with either sodium hypochlorite solution or flame is
of that mat were infected because they were all anatomically con- able to transmit BXW 20 days after inoculation (Buregyeya 2010).
nected to the same corm (Tushemereirwe et al. 2004). Later, it was Recently, Ocimati et al. (2021) showed that a thorough washing of
observed that corms of infected mats were not uniformly colonized farm tools with cold water and different locally available laundry
by Xvm bacteria (Ocimati et al. 2015), suggesting a possibility of soaps that had no antibiotics and detergents, just like household
obtaining disease-free suckers from previously infected mats for bleach, eliminated all of the Xvm bacteria on farm tools.
establishment of new plantations, especially if BXW was not ob- The method of disposing of diseased plant materials is impor-
served in the field for 10 to 12 months. Recently, Xvm infection was tant in controlling BXW successfully; however, this depends on
shown to induce organ-specific defence responses in banana plants the longevity of pathogen in soil or debris. Initially, it was recom-
(Mustafa et al. 2022), providing additional support to nonuniform mended that infected plant material be burned or buried immedi-
bacterial colonization of tissues as well as differential responses to ately after rogueing (Blomme et al. 2008). This was based on the
infection. The corm was postulated to be an important organ for assumption that Xvm is easily spread from debris of infected plants,
ensuring disease-free lateral shoots (Mustafa et al. 2022; Ocimati as is the case for Fusarium wilt disease of banana, caused by the
et al. 2013; Ssekiwoko et al. 2006b). fungal pathogen Fusarium oxysporum f. sp. cubense, which sur-
Uneven colonization of banana corms by Xvm and the fact that vives in the soil for more than 20 years (Stover 1962). However,
most BXW infection starts from the shoot system and progresses burning colossal masses of fresh succulent banana tissues was not
slowly down to the corm (Ssekiwoko et al. 2006c) indicated a pos- feasible and the effort of digging large, deep pits to bury the mate-
sibility to limit movement of Xvm into lateral shoots by timely re- rial was prohibitively labor intensive (Rutikanga et al. 2013; Smith
moval of the diseased plants from the mat. This led to the emergence et al. 2008a). Fortunately, studies also showed that Xvm did not sur-
of a new technique of BXW management, named “single diseased vive beyond 35 days in soil or plant debris (Mwebaze et al. 2006).
stem removal” (SDSR) (Blomme et al. 2017b; Kikulwe et al. 2022; Consequently, farmers were advised to chop infected material into
Kubiriba et al. 2014, 2016). In SDSR, only a BXW-diseased plant is small fragments to accelerate both desiccation and decomposition
aseptically removed at the soil level from the mat while leaving the (Kubiriba et al. 2014). The poor survival of Xvm in soil and plant
other, symptomless plants on the same mat (Kubiriba et al. 2014). debris also implied that banana can be replanted in fields that were
Initially, the control of BXW included rouging of entire ba- previously infested by BXW after a fairly short period of time.
nana mats, including symptomatic and symptomless plants. Imple- Hence, a fallow period of at least 6 months following the destruction
mentation of this practice became an extremely laborious process of entire mats was recommended in central Uganda agroecological
and most farmers in the severely affected areas did not adopt it conditions, whereas no fallowing is required where SDSR is more
(Bagamba et al. 2006; Mwangi 2007). Where it was practiced, it widely used as a means of inoculum removal.
exposed land on steep slopes to soil erosion agencies (Niko et al.
2011). Moreover, it proved costly for the farmer to reestablish ba- ROLE OF LOCAL COMMUNITIES IN DEPLOYING
nana production because plantations take approximately 2 years to BXW CONTROL PRACTICES
revert to previous production levels (Blomme et al. 2008). There-
fore, early removal of flower-infected (symptomatic) pseudostems Use of participatory approaches for BXW control among the
at the mat base (SDSR) at the onset of first floral symptoms pre- communities. An earlier action plan of 2001 aimed at eradicating
vented the disease from spreading to the rest of the plants on the mat BXW around the initial outbreak areas was top-down, denoting a
32 Phytobiomes Journal
hierarchical system of government or management in which actions lem instead of individual farmers’ problem. It was emphasized that
and policies are initiated at the highest level, and could not be sus- every member of the community had to control the disease to save
tained, while BXW persisted (Tushemereirwe et al. 2006). Indeed, other banana crops in the community.
where banana farming communities are the primary formulators of Using community bylaws to enforce implementation BXW
the methods, high rates of adoption are likely (Gold et al. 1993; control measures. Due to an eradication campaign of cocoa trees
Kikulwe et al. 2019; Tinzaara et al. 2019, 2021). Therefore, partic- infected with cocoa swollen shoot virus launched in 1946, the virus
ipatory approaches to proactively engage the banana farmers and was largely under control by early 1960 and only resurfaced when
other stakeholders in the community were used to improve BXW the government stopped the campaign (Thresh and Owusu 1986).
control. This involved facilitation of dialogue among the different Similar campaigns were successfully implemented in controlling
stakeholders with the aim of developing and implementing an ac- Citrus tristeza virus in Israel (Fishman et al. 1983) and banana
tion plan to solve the problem (Supplementary Table S1). Because bunchy top virus in Australia (Allen 1983). Legislation seems to
BXW was highly devastating and could also be spread by itinerant have been one of the important components of the above successful
vectors able to fly several kilometres in a very short time, one in- programs. It mainly involved guidelines on movement of planting
fected farm or plant could act as source of inoculum for all banana material from infected fields or from one region to another and
farms in a community. Thus, it was considered a community prob- required growers to destroy any diseased plants (Magnaye 1994).
Fig. 2. A, Unmanaged banana plan-
tation with banana Xanthomonas wilt
(BXW) leaf symptoms (inset: banana
bunch showing uneven fruit ripening
with blackening of fruit pulp) compared
with B and C, managed plantations
in Uganda in which no single dis-
eased stem removal (SDSR) is done.
Upon identification of BXW, infected
plants are rogued by D, uprooting
or E, cutting above soil level, which
creates open spaces in the planta-
tions, allowing new shoot growth after
SDSR. Open spaces begin to fill again
progressively; for example, F, which
is 7 weeks after SDSR. G, In more
severe BXW, many plants are elimi-
nated, which creates much larger open
spaces and allows intercropping while,
at the same time, enforcing plantation
reestablishment through replanting.
Vol. 7, No. 1, 2023 33
The governments in West Africa in the colonial era enforced these tendance, including the subcounties and villages participants came
rules, though farmers were not happy with some of them (Thresh from, were taken. The participants were asked if they had ever ob-
and Owusu 1986). In Australia and Honduras, however, farmers served similar symptoms in their localities. The occurrences were
cooperated to organize an efficient system for detecting and de- recorded and followed up for verification and mapped by district or
stroying diseased plants and generally enforcing rules constituted national BXW control partners. Therefore, it was possible to map
by them. most new occurrence by engaging the public, instead of going to
In Uganda, compelling all banana farmers in the community to every household (Tushemereiwe et al. 2006).
control BXW necessitated a “localized legislative mechanism”. One The BXW control initiative used participatory monitoring and
option was a law issued by central or local government, where ev- evaluation (M&E) which emphasizes involvement of target com-
erybody must comply or face dire consequences. Instead, commu- munities and stakeholders to facilitate the process. To execute par-
nities formulated and enforced their own bylaws (Supplementary ticipatory M&E, the community stakeholders, including farmers,
Table S2). The bylaws included a set of rules and penalties that were facilitated to select quantifiable and monitorable indicators,
compelled members of the community to meet regularly to discuss record data on them, and report to fellow farmers and village BXW
progress towards BXW control, effectively detect the disease in the taskforces regularly. Progress in BXW control observed by farm-
fields, execute actions aimed at limiting its spread, and ensuring ers and discussed at community level built farmers’ confidence that
that the community members abided by the bylaws (Kubiriba and BXW can be controlled. This encouraged reluctant farmers to de-
Tushemereirwe 2014). Implementation of community bylaws vote more efforts to BXW control. During community meetings,
started in Ntungamo District (southwestern Uganda) in 2005, were farmers were able to modify the recommended practices and also
adopted in Kyazanga-Lwengo District in 2006 (central Uganda), resolve the hindrances to BXW control peculiar to the community.
and, by 2014, all major banana-growing areas of Uganda had The unique approach of involving farmers as key players in the
adopted the bylaws (Kubiriba et al. 2016). management of a devastating plant disease burden proved effective
Participatory surveillance for mapping and tracking BXW because there is a great sense of personal and community respon-
distribution and spread. Traditionally, crop disease outbreaks are sibility for the outcomes of these efforts (Tinzaara et al. 2019).
mapped based on formal surveys and transects, which normally
target only representative samples of disease outbreaks. Currently, STATUS OF BXW CONTROL AND MANAGEMENT
frontline remote sensing tools coupled with machine learning meth- (2005 TO 2018)
ods have a significant role in crop monitoring and disease surveil-
lance (Kreuze et al. 2022; Selvaraj et al. 2019, 2020). The devastat- BXW control between 2005 and 2013. The above M&E sys-
ing and fast-spreading nature of BXW dictated that control efforts tems were complemented with formal surveys with structured ques-
could not ignore the presence of even one outbreak in the major tionnaires and checklists between 2006 and 2018. Consequently,
banana-growing areas. To halt economic loss, a new system was de- BXW prevalence decreased between 2005 and 2008 from higher
vised to track all outbreaks in real time as they occurred in Uganda than 75 to 45% in central Uganda, where the disease had become
(Kubiriba and Tushemereirwe 2014), which consisted of the fol- endemic (Tushemereirwe et al. 2006). In the areas between Lake
lowing: (i) massive and aggressive awareness creation through mass Victoria basin and Mountain Rwenzori, BXW prevalence decreased
media, posters, and brochures, aimed at building capacity for the from 55 to 24%, whereas it was reduced to <5% in the main
farming communities to identify the disease; (ii) farmers were urged banana-growing areas of the southwestern Uganda (Kubiriba and
to report to the nearest extension worker or via hotline telephone Tushemereirwe 2014). Apparently, BXW had been effectively con-
numbers indicated on posters and brochures; (iii) symptoms were trolled in the most important southwestern, Lake Victoria, and
described, as well as details of the location of the outbreak; (iv) Mt. Rwenzori regions (Fig. 3) which, together, produce >80% of
a return call was made by the nearest trained extension officer or Uganda’s banana crops (Bagamba 2007; Gold et al. 1999; Katungi
extension staff was sent to the location to verify and confirm the 2007; Nyombi 2013; Rubaihayo and Gold 1993; Tushemereirwe
presence of the outbreak; and (v) data were continuously compiled et al. 2006). Other banana-growing areas, grouped as endemic to
into a database at NARL-Kawanda and used to generate disease dis- the disease, still had high levels of BXW incidence; however, this
tribution maps. This reporting system was key in showing the dis- did not affect the overall national banana production because they
ease spread, supporting mobilization of the stakeholders for BXW were not key in banana production. There was only a slight decrease
control, and targeting the control measures in real time. However, it in value of banana production at the national level against predicted
was heavily dependent on the vigilance of the farmers. Therefore, BXW damage between 2003 and 2007 (Fig. 4).
this was complemented by other reporting systems such as going However, in 2008, there was a resurgence of BXW with preva-
public. At the time of the epidemic, disease mapping was based on lence of up to 51% at the national level and, by 2010, it had spread
the subcounty-generated information; fortunately, the current and to new areas with a 60% prevalence (Kubiriba et al. 2012b, 2014).
more accurate GIS tools for disease mapping tools can provide ac- Some of the reasons for the resurgence were (i) trained extension
curate data on disease incidence (Kreuze et al. 2022; Selvaraj et al. agents had been replaced by new, untrained staff; (ii) laxity and
2019, 2020). abandonment of the surveillance system; and (iii) lack of coherent
Going public and participatory monitoring and evaluation institutional frameworks for organizing communities for BXW con-
of BXW control. The aforementioned participatory surveillance trol, inadequate mobilization and sensitization of key stakeholder
system was backed up with another one, dubbed “going public” platforms along the production-consumption chain, and less effec-
(Tushemereiwe et al. 2006). This was used to trace new BXW out- tive surveillance methods (no application of digital tools) leading to
breaks in areas of southwestern Uganda, where >75% of Uganda’s untimely actions. Therefore, this information was the basis for the
banana crops are produced (Kalyebara et al. 2006). The team would revision of the national BXW control strategy that was launched in
go to public places such as open markets, trading centers, and places 2013 (Kubiriba and Tushemereirwe 2014).
of worship to display posters of BXW symptoms in a way that the Controlling BXW under the revised national BXW strategy
team would attract public attention. The public was then mobi- of 2013. The revised national BXW strategy aimed at reducing
lized around the posters and sensitized about BXW symptoms and disease prevalence from 51% to <1% by the end of 2015. It was
spread, and how it can be controlled. Meanwhile, records of at- observed that the recommended cultural control practices were still
34 Phytobiomes Journal
effective in controlling BXW, and the main challenge was mass mo- local governments (Bagamba et al. 2006). Under the 2013 BXW
bilization of farmers to deploy them (Kubiriba and Tushemereirwe control strategy, information was picked from the participating
2014). Therefore, the revised strategy of 2013 aimed at (i) aggres- communities as they implemented BXW control and packaged by
sively and widely disseminating information on BXW spread and the media houses that eventually disseminated it. Information was
control, (ii) mobilizing communities for BXW control, (iii) sup- more focused on organization of stakeholders to control BXW:
porting the development and implementation of legal instruments, farmer mobilization and implementation of bylaws. It was antic-
and (iv) monitoring and evaluation of implemented BXW control ipated that capturing information from farmers free of technical
activities. jargon and disseminating it through radio and newsprint would im-
Like the previous BXW control efforts, implementation of the prove information access and be used for decision making by fellow
2013 control strategy was driven by participatory approaches, with farmer beneficiaries (Kubiriba et al. 2016).
modifications. Previously, awareness campaigns were based on in- Successful BXW control at the selected hotspots became obvi-
formation generated and spearheaded by the research teams, sup- ous, with the value of giving confidence to the surrounding, less-
ported by inspectors at the MAAIF and production departments at affected communities that BXW can be controlled, as demonstrated
Fig. 3. Map of Uganda showing
banana bacterial wilt (BBW) occur-
rence and control in major banana-
growing areas of Uganda as of 2008.
Fig. 4. Value of banana crops pro- 700,000
duced in Uganda during the banana y = 5982x4 - 5E+06x3 + 1E+10x2 - 2E+13x + 1E+16
R2 = 0.99
Xanthomonas wilt epidemic: 2001 and
600,000
2007.
Estimate with control
500,000
Predicted without control
400,000
300,000
200,000 y = 2424x3 - 1E+07x2 + 3E+10x - 2E+13
R2 = 0.98
100,000
-
2001 2002 2003 2004 2005 2006 2007 2008
Year
Vol. 7, No. 1, 2023 35
Value of banana  production (US$ '000) 
by hundreds of farmers (Kubiriba et al. 2016). Linking of farm- Characteristics of a technology are key in influencing farmers
ers with networks of organizations and individuals which focused to adopt it. BXW control was based on epidemiology information
on getting more people to use the technologies for greater eco- generated within the ecological set up of the BXW outbreaks. The
nomic benefit (Bentley et al. 2006) was executed through field days ease with which BXW insect-vectored or tool-mediated spread was
(Kubiriba et al. 2016). Clearly, lessons were learned by peer farmers blocked through timely removal of male buds with the right tools
in how to drastically reduce BXW incidence through surveillance and disinfection of cutting tools (Blomme et al. 2008), short Xvm
for diseased plants in a community and the significant contribution survival in the soil (Mwebaze et al. 2006), and nonuniform col-
of administrative and political support through effective formula- onization of the corm and pseudostem (Ocimati et al. 2015) all
tion and implementation of bylaws at subcounty level (Kubiriba contributed to development of a cultural management package that
et al. 2016). was significantly effective at controlling BXW. This package was
Between 2006 and 2008, except for the southwestern region, suited to controlling a rapidly spreading and destructive epidemic,
which produced most banana crops, all other regions had 30% as demonstrated in the affected farming communities in Uganda and
higher BXW prevalence (Fig. 5). During the time of BXW resur- successfully applied across the banana-growing regions of ECA,
gence in 2010 and 2013, all regions, including the southwestern with minor modifications (Blomme et al. 2017b, 2019; Kubiriba and
region, experienced >30% BXW prevalence and, by 2018, this Tushemereirwe 2014; Kubiriba et al. 2012a, b, 2014, 2016). Such a
was reduced to <5% BXW. This successful control of BXW in all strategy could be applicable to any phytopathosystem of compara-
banana-growing areas in Uganda resulted in weekly banana sales ble epidemiology and etiology, provided the farming communities
recovery to approximately 72% in 2018 (Fig. 5). The successes in attach this value to the enterprise and the approach is participatory.
the management of BXW could only be sustained with institutional
support through key players at the community level. CONCLUSIONS AND FUTURE RESEARCH
PERSPECTIVES
TECHNOLOGY ADOPTION FOR EFFECTIVE
CONTROL OF BXW The challenges associated with plant disease threats of food se-
curity in developing countries are enormous (Jeger et al. 2021;
Many initiatives, innovations, and technologies that target small- Sherman et al. 2019) and the challenge is exacerbated when essen-
holder farmers in sub-Sarahan Africa struggle with adoption and tial food staples such as banana are affected (Ristaino et al. 2021;
scaling up, even when returns are proven in pilot studies (Franzel Rizzo et al. 2021; Savary et al. 2019; Strange and Scott 2005). This
et al. 2001; Lynam and Twomlow 2014). Successful scaling up re- demands careful and immediate application of approaches based
quires that the factors affecting adoption as well as the spaces or con- on basic scientific and social science structures of the communities
texts that scaling up has to navigate are well understood, iteratively for ease of adoption (Garcia-Figuera et al. 2021; Mills et al. 2011).
evaluated, and incorporated into the scaling-up process (Linn 2012). Over the last two decades, the most fundamental progress made in
Key attributes of a successful scaling-up strategy include effective addressing BXW disease problem in ECA is that it can be controlled
communication, peer learning, and strong leadership, altogether or eradicated. The rigor of interventions against BXW in Uganda
contributing to the quality of community participation (Gillespie represent a success story of disease management that is comparable
2004; Kolavalli and Kerr 2002; Ndah et al. 2015). with transgenic management of papaya ringspot disease in Hawaii
One of the key determinants of farmers’ acceptance and adop- (Gonsalves and Gonsalves 2014; Gonsalves et al. 2007). However,
tion of the technology is the importance that end-users attach to the success in combatting a threatening epidemic of BXW’s magni-
the enterprise. Ndah et al. (2015) categorized this under conditions tude hinges on the importance of informing farmers about the effec-
of the output markets at both village and regional level. This ex- tiveness and benefits of control strategies as opposed to emphasizing
plains why, between 2005 and 2008, only banana farmers in the the risk posed by the disease (Milne et al. 2020). Hence, the fol-
southwestern region of Uganda were able to keep BXW incidence lowing additional information is needed to guide further evidence-
below 5% (Kubiriba and Tushemereirwe 2014). It is in this region based efforts in controlling BXW.
that banana fruit not only provide food security but also are key for First, Xvm bacterial isolates have not been sufficiently analyzed
daily income, and the region produces >75% of Uganda’s banana for their population biology. Whereas Xvm isolates show close phy-
fruit. logenetic relationships (Nakato et al. 2018b; Wasukira et al. 2012),
Fig. 5. Proportion of banana fields
infected with banana Xanthomonas
wilt (BXW) in the different regions of
Uganda between 2006 and 2018.
36 Phytobiomes Journal
there is no description of Xvm population genetics parameters. Pop- specific studies of bacteriophages against Xvm in banana are still
ulation parameters such as haplotype diversities, gene flow, and limited or lacking. Previously, Xvm was shown to be unable to sur-
population contraction or expansion indices are means of examin- vive beyond 35 days in soil or plant debris (Mwebaze et al. 2006);
ing pathogen demographic trajectory that require profiling. Also, however, whether this inability is enhanced by phaging activities
the sublineages may differ in their rate of evolution or direction and of soilborne bacteriophages against Xvm or competing saprophytic
magnitudes of Darwinian selection pressures but this has not been microbes or other factors is an interesting topic for further study.
investigated. Fifth, the plethora of microbial communities associated with
Second, uneven colonization of the corm by Xvm results in in- BXW-infested or healthy banana plants (plant microbiota or plant
complete systemic movement of the bacteria and subsequent escape microbiome) require in-depth studies because healthy plants host
from BXW of some lateral shoots on the same corm as the infected taxonomically diverse and structured communities of microorgan-
banana plant (Blomme et al. 2017b; Mustafa et al. 2022; Ocimati isms. These plant–microbiome associations have long coevolved
et al. 2015). However, the mechanism for uneven colonization of the to have a direct influence on rhizosphere functioning, plant devel-
corm is unknown. One plausible hypothesis is that, upon entry into opment, and disease processes (Dastogeer et al. 2020; Gao et al.
the corm, Xvm gets “weakened” to a level below the threshold re- 2021; Trivedi et al. 2020). Apparently, the plant microbiome, now
quired to induce disease in the lateral shoots. This possibility is sup- viewed as an extension of the host plant genome, can be modu-
ported by the finding that the corm is an organ highly responsive to lated or enhanced for better plant health and productivity (Beck
Xvm attack when compared with other organs (Mustafa et al. 2022). et al. 2022; Compant et al. 2019; Trivedi et al. 2020, 2022; Turner
The anatomical connectivity between corm, pseudostem, and “true et al. 2013). Also, plant microbiome research has revolutionized our
stem” implies that Xvm may associate with the corm transiently to view of plant health, in which the classic disease triangle (host, envi-
perpetually, depending on the point of inoculation. Further studies ronment, and pathogen) has expanded to include plant-associated
describing the anatomical assembly and physiological traits of the microbial communities (Gao et al. 2021; Malacrinò et al. 2022;
corm and associated Xvm histopathology are needed urgently. Trivedi et al. 2020). Studies on the core banana microbiome show
Third, a link between the stage of plant growth and rate of BXW differences between plant compartments and soils but not geno-
disease development is not well known, although the assumption types (Birt et al. 2022), which opens up opportunities to manage
is that disease progresses faster in younger than in older plants. banana diseases (Ali and Imran 2022; Malacrinò et al. 2022). If
Accordingly, depending on the developmental stage, banana plants the BXW-infected banana microbiome can be segregated between
may show varied speeds of Xvm systemic spread within the plant. different parts, Xvm mobility and multiplication can be curtailed.
This knowledge is important because a single banana plant lasts for However, although there are a few descriptions under conditions
9 to 14 months between sprouting on the corm and its removal by for banana Fusarium wilt fungal disease (Kaushal et al. 2020; Liu
harvesting mature fruit, which gives a broad window for the plant to et al. 2019; Xue et al. 2015), there is a limitation in the analysis
become infected. Recently, the spread of Xvm within banana mats of scenarios under BXW disease. Other than showing that BXW-
was shown to be influenced by the amount of inoculum and the phys- resistant transgenic banana plants have the same stable rhizosphere
iological stage of the mother plant and attached suckers (Ocimati microbiome as nontransgenic plants (Nimusiima et al. 2015), how
et al. 2022). Our unpublished observations show that there is a long banana microbiome composition and modulation may contribute to
delay of 8 to 12 weeks postinoculation with Xvm to the appearance the management of BXW is not well known. Alteration in and com-
of systemic BXW leaf symptoms when inoculations are made on position of the plant microbiome can be induced by climate change,
the male banana buds. In contrast, faster development of systemic which can subsequently modulate the disease development process
leaf (but not necessarily fruit) BXW symptoms was observed upon (Trivedi et al. 2022). Generally, reports show that, whereas banana
leaf inoculations with Xvm. In more than 200 mats for which the plants have benefited from the effects of climate change since 1961,
mother plants were inoculated and no SDSR was practiced, <7.5% this situation will be reversed in the future and, by 2050, all pre-
of lateral shoots developed BXW compared with>95% that showed vious gains will be lost (Fernandez et al. 2022; Machovina and
no BXW 40 weeks postinoculation, indicating the corm’s natural Feeley 2013; Varma and Bebber 2019). Plant disease can be driven
ability to limit disease progression into lateral shoots despite con- by climate change that modulates microbiomes and plant adaptation
tinuous Xvm loading from the infected mother (our unpublished (Gao et al. 2021; Trivedi et al. 2022). Short-term (years to decades)
observations). This topic requires extended studies. adaptation of plants to climate change will be mainly driven by the
Fourth, although methods of biocontrol for banana fungal plant microbiome whereas, in the long term (century to millennia),
and bacterial diseases could be feasible (Blomme et al. 2017a; the adaptation of plants will be driven equally by ecoevolutionary
Dadrasnia et al. 2020; Premabati and De Mandal 2020), application interactions between the plant microbiome and its host (Gao et al.
of these methods to the control of Xvm is still limited or underde- 2021; Trivedi et al. 2022). Therefore, urgent studies of the banana
veloped. For example, bacteria antagonistic against Xvm showed microbiome in relation to Xvm and BXW incidence are required as
a reduction in disease incidence on enset (Abayneh 2010). Also, an alternative strategy for further management and eradication of
endophytic bacterial isolates of Burkholderia, Herbaspirillum, and this disease from banana farming communities of ECA.
Enterobacter spp. isolated from banana in Uganda were shown to Taken together, BXW has been largely controlled in Uganda by
suppress Xvm (Were 2016). Consequently, suppression of Xvm by a package of cultural methods in the last two decades. However,
endophytes at the banana corm level was postulated to account for complete BXW eradication and management is not guaranteed un-
incomplete systemic spread of Xvm at the mat level (Blomme et al. der this framework because of the need for continuous active in-
2017a; Karamura et al. 2016). However, empirical evidence sup- volvement of farmers and supportive stakeholder community. These
porting this hypothesis is still lacking. Of current interest, yet also gains are applicable to the greater ECA where BXW is a problem,
not fully developed, is biocontrol of Xvm in banana using bacterio- including Mozambique, which is currently at high risk of BXW
phages. The potential of bacteriophages as biocontrol agents against (Ocimati et al. 2019). Banana microbiome modulation presents a
Ralstonia solancearum (causative agent of Moko disease of banana) new opportunity for BXW management because banana plants tend
or various pathogenic species of Xanthomonas spp. has been shown to establish compartment-specific microbiomes at an early age that
(Domingo-Calap et al. 2022; Erdrich et al. 2022; Nakayinga et al. persist to maturity (Birt et al. 2022). Moreover, a missing yet feasi-
2021; Ramírez et al. 2020; Romero-Suarez et al. 2012). However, ble alternative element in the management of BXW is the deploy-
Vol. 7, No. 1, 2023 37
ment of resistance, either introgressed from the wild M. balbisiana control options over the past decade in East and Central Africa. Eur. J. Plant
or by transgenic methods. Transgenic resistance against BXW in Pathol. 139:271-287.
banana is available (Tripathi et al. 2016, 2017); however, it suf- Blomme, G., Ocimati, W., Sivirihauma, C., Lusenge, V., Bumba, M., and
fers legislative and political impediments in the region, including Ntamwira, J. 2019. Controlling Xanthomonas wilt of banana: Influence of
collective application, frequency of application, and social factors on the ef-
in Uganda. A promising alternative is to employ CRISPR/Cas9- fectiveness of the single diseased stem removal technique in eastern Demo-
mediated genome editing, which has shown promise and could cratic Republic of Congo. Crop Prot. 118:79-88.
deliver acceptable BXW-resistant banana varieties (Schaart et al. Blomme, G., Ocimati, W., Sivirihauma, C., Vutseme, L., Mariamu, B., Kamira,
2021; J. N. Tripathi et al. 2021; L. Tripathi et al. 2021, 2022). Ur- M., van Schagen, B., Ekboir, J., and Ntamwira, J. 2017b. A control package
gent deployment of BXW resistance is paramount and would be a revolving around the removal of single diseased banana stems is effective
significant addition to the existing BXW control and management for the restoration of Xanthomonas wilt infected fields. Eur. J. Plant Pathol.
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