Overview of Musa virus diseases

Plant virology in sub-Saharan Africa
Overview of Musa virus diseases
G. Pietersena and J.E. Thomasb
a
Agricultural Research Council, Plant Protection Research Institute,
PB X134, Pretoria, 0001, South Africa
b
Queensland Horticulture Institute, DPI, 80 Meiers Road,
Indooroopilly, Qld, Australia 4068
Abstract
Bananas and other Musa spp. are affected by five known, relatively well-characterized
viruses: these are Banana bunchy top virus (BBTV) genus Nanavirus; Banana streak
virus (BSV) genus Badnavirus, Cucumber mosaic virus (CMV) genus Cucumovirus, Banana bract mosaic virus (BBrMV) genus Potyvirus, and Abaca mosaic virus
(AbaMV) genus Potyvirus. Recently, new filamentous virus particles have been noted
in bananas from Africa, the Americas, southeast Asia, and Australia. The virus has been
isolated and characterized and the name Banana mild mosaic virus proposed. Another
new virus, Banana die-back virus, has also just been described from Nigeria. Currently
known properties of these viruses, their distribution and importance, diagnosis and
control will be discussed.
Résumé
Les bananes et d’autres Musa spp sont affectées par cinq virus connus relativement
bien caractérisés. Il s’agit du virus du renflement de la partie supérieure (Nanavirus) ;
du virus de la stirure de la banane (Badnavirus) ; du virus de la mosaïque du concombre (Cucumovirus), du virus de la mosaïque de la banane (Potyvirus) et du virus de la
mosaïque abaka (Potyvirus). Récemment, de nouvelles particules virales filamenteuses
ont été signalées sur la banane en provenance d’Afrique, des Amériques, d’Asie du
Sud-est et d’Australie. Le virus a été isolé et caractérisé et l’appellation « mosaïque
légère de la banane » a été proposée. Un autre nouveau virus, le virus du dépérissement
terminal de la banane vient d’être décrit au Nigeria. Cette présentation fera le point sur
les caractéristiques connus de ces virus, leur distribution et importance , ainsi que les
méthodes de diagnostic et de lutte.
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Overview of Musa viruses in sub-Saharan Africa
Introduction
The banana (including plantain, Musa spp.) is one of the world’s most important subsistence crops. It is widely grown in the tropics and subtropics in all types of agricultural
systems, from small, mixed, subsistence gardens, to large multinational commercial
monocultures. The crop serves in many developing countries as a staple food or the
cornerstone of the country’s economy. The largest producers are Latin America and
Asia, however, much of the South American production in particular is as an export
crop to the developed world.
There has been an increase in the international movement of banana germplasm in
recent years, much of it to developing countries, and especially in the form of tissue
culture propagated plants. The presence of any virus poses a risk as new viruses or
strains may be distributed in large quantities to new sites.
Bananas are affected by four known, relatively well-characterized viruses (Diekmann and Putter 1996): these are Banana bunchy top virus (BBTV) genus Nanavirus,
Banana streak virus (BSV) genus Badnavirus; Cucumber mosaic virus (CMV) genus
Cucumovirus; and Banana bract mosaic virus (BBrMV) genus Potyvirus. Recently, a
filamentous virus, Banana mild mosaic virus (BanMMV, Thomas et al. 2000; Gambley
and Thomas 2001) has been shown to be widespread in banana and plantain germplasm
material and also been noted in bananas from Africa, the Americas, southeast Asia, and
Australia (Lockhart 1995; Thomas et al. 2000). Another new virus, Banana die-back
virus, has also just been described from Nigeria (Hughes et al. 1998), Abaca mosaic
virus (AbaMV) genus Potyvirus infects Abaca (Musa textilis) in the Philippines, and is
known to infect banana experimentally. However, there is no information on its possible
natural occurrence in banana.
Banana bunchy top virus (BBTV)
Of the known virus diseases of bananas, Banana bunchy top disease (BBTD, caused
by BBTV) is the most serious. BBTD is a major constraint to banana production in
many areas of southeast Asia and the Pacific (Thomas et al. 1994). The disease has been
identified in numerous developing countries in Oceania, Africa, and Asia (Thomas et al.
1994; Diekmann and Putter 1996; Kenyon et al. 1997; Thomas and Iskra-Caruana 2000);
Kagy et al. 2001). BBTV is still absent from the countries of Central and South America.
Strains of BBTV causing mild or latent symptoms have recently been detected (Su et
al. 1993), and the virus may occur at higher incidences than previously believed.
BBTV has caused some devastating epidemics, the latest being in Pakistan, with the
disease being observed in 1988 for the first time. By 1992, it showed that the disease
was widespread in a number of districts in Pakistan with disease incidences up to 100%,
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Plant virology in sub-Saharan Africa
and that about half of the plantations had already been destroyed (Soomro et al. 1992;
Khalid et al. 1993).
The virus belongs to the genus Nanavirus and virions are icosahedral, 18–20 nm in
diameter (Wu and Su 1990, Dietzgen and Thomas 1991). The virus possesses a multicomponent genome, consisting of at least six circular ssDNA components (Burns et
al. 1995; Xie and Hu 1995; Karan et al. 1997). Additional components, which may be
satellites, occur with some isolates (Horser et al. 2001).
BBTV is transmitted in a persistent, nonpropagative manner by an aphid vector
(Pentalonia nigronervosa), and in vegetative planting material, but not by mechanical
inoculation (Magee 1927).
Successful methods of control, viz. early identification, and eradication of infected
plants and the use of virus-free planting material, are successfully applied in Australia
(Dale 1987). However, these are unlikely to alleviate the problem in developing countries, where farmers lack the structured organizations required to apply eradication
programs throughout affected districts, and funds are lacking to enforce eradication
programs. Additionally, no incentives or alternate food sources exist, so that a farmer will
not sacrifice the small source of sustenance his family may have, in order to save a larger
area. Furthermore, virus-free planting material may also not be readily available.
Banana streak virus (BSV)
BSV, believed to be distributed worldwide on Musa sp. (Lockhart and Olszewski 1993),
was not considered a serious problem of bananas until recently. The disease was first
noted in Côte d’Ivoire in 1966 (Lassoudière 1974), but the causal virus was not isolated
until 1986 (Lockhart 1986).
Since then, the disease has been, and continues to be reported from many new countries (Jones and Lockhart 1993; Diekmann and Putter 1996; Tushmereirwe et al. 1996,
Pasberg-Gauhl et al. 1996; Reichel et al. 1996; Vuylsteke et al. 1996; Lockhart and Jones
2000). The virus causes a wide range of symptoms and damage ranges from mild to
severe. It is transmitted mostly through planting materials, but also in a semipersistent
manner by some mealybug species (Planococcus citri and Pseudococcus sp.; Lockhart
and Jones 2000). Field spread appears to occur in some countries, but not in others
(Lockhart pers. comm. 1998). In Uganda, a serious outbreak of the virus was reported
in 1996, with some plantations containing 100% infected plants (Tushmereirwe et al.
1996). Damage appeared most severe when the virus was associated with a filamentous
virus particle (probably BanMMV).
BSV is a member of the genus Badnavirus. The virions are nonenveloped, bacilliform
average 130–150 nm × 30 nm in size, and contain a circular dsDNA genome (Lockhart
and Olszewski 1993). A high degree of heterogeneity exists among isolates of BSV,
52
Overview of Musa viruses in sub-Saharan Africa
and they differ serologically, genomically, and biologically (Lockhart and Olszewski
1993; Geering et al. 2000), making diagnosis difficult. It has recently been shown that
BSV genomic sequences are integrated into the genome of Musa and Ensete (LaFleur
et al. 1996). While all Musa genotypes tested appear to contain viral sequences, the
nature of these sequences is variable. Of two integrated sequences characterized so far,
one appears to be incapable of giving rise to episomal BSV infection. However, there
is good evidence that the second integrated sequence is the source of de novo episomal
BSV infection, and that this is associated with in vitro propagation and possibly other
stress factors (Ndowora et al. 1999; Harper et al. 1999). This phenomenon has prevented
the deployment of tissue cultures of improved banana and plantain hybrids (Frison and
Sharrock 1998). There is evidence that additional integrated BSV sequences can give
rise to episomal infections with other BSV strains (Geering et al. unpublished).
As vegetative propagation appears to play a large role in transmission of BSV, the
most effective means to control the disease is to ensure source plants used for propagation are virus-free. In view of the activation of some forms of the integrated genome
in vitro, propagated plantlets of hybrids should also be tested, even though source
plants appeared virus-free. High incidences of mealybugs in plantations should also
be reduced.
Cucumber mosaic virus (CMV)
CMV, the type member of the genus Cucumovirus (family Bromoviridae), is worldwide
in its distribution, has the largest host range of any plant virus, infecting more than 800
species, and is transmitted by more than 60 aphid species in a nonpersistent manner
(Palukaitis et al. 1992). Virus strains can be subdivided into two major subgroups, I
and II, by serological and molecular methods (Devergne and Cardin 1973; Piazzolla
et al. 1979; Edwards and Gonsalves 1983; Rizos et al. 1992; Singh et al. 1995; Hu et
al. 1995), but all yield essentially the same subdivisions of isolates (Rizos et al. 1992).
Subgroup I, typified by isolate DTL, occurs predominantly in the tropics and subtropics,
while subgroup II, typified by ToRS, is prevalent in temperate regions (Hasse et al.
1989). Both subgroups, however, do occur on bananas (Diekmann and Putter 1996).
Strains on banana vary from those not causing any symptoms to those inducing mild to
severe symptoms (Diekmann and Putter 1996). The heart-rot strain found in Morocco
is particularly severe (Wardlaw 1972).
The virus may cause chlorosis, mosaic, and heart rot, and is the etiological agent
of infectious chlorosis disease in this crop (Niblett et al. 1994). In general, CMV does
not have a major impact on banana production, but serious outbreaks have occurred
(Bouhida and Lockhart 1990; Li 1995). Bunch weight reductions of between 45% and
53
Plant virology in sub-Saharan Africa
62% have been reported (Estelitta et al. 1996). The virus is currently considered an
emerging threat to the cultivation of banana in Kerala, India, especially where cucurbitaceous vegetables are cultivated as intercrops in banana (Estelitta et al. 1996). It is
especially important to control CMV where mass propagation of in vitro banana material
is employed, as levels of CMV in these plantings can be high.
While considered worldwide in its distribution, CMV and CMV strains have been
reported for the first time on bananas in a number of developing countries recently, probably due to the availability of efficient detection and identification methods (Doon 1991;
Zambolim et al. 1994; Castano et al. 1994; Rivera et al. 1992; Osei 1995; Srivastava et
al. 1995; Allam et al. 1995; Li et al. 1996; Pietersen et al. 1998).
To control CMV, it is essential to ensure that source plants used for propagation
are free of virus. Highly reliable diagnostic techniques exist which allow this to be
accomplished. Elimination of weed hosts from plantations and surrounding areas also
help to control the virus. Furthermore, banana plantations should not be close to crop
hosts of CMV (e.g., cucurbits, tomatoes, and tobacco).
Banana mild mosaic virus (BanMMV)
Recently, previously uncharacterized filamentous virus particles have been noted in
bananas from Africa, the Americas, southeast Asia, and Australia (Lockhart 1995;
Thomas et al. 2000). Recent evidence suggests that the same virus is present in all these
areas (Thomas et al. 2000). The virus is widespread within international germplasm
collections (Thomas, Iskra-Caruana, and Pietersen unpublished). The widespread nature
of the virus, soon after being detected for the first time, suggests that it may be worldwide
in its distribution. The virus has not been associated with a specific disease of banana
thus far, but appears to increase the severity of the symptoms of BSV when it co-infects
plants (Tushmereirwe et al. 1996). The economic impact of the virus thus far is unknown.
The virions of BanMMV are flexuous filaments about 580 nm long and 14 nm wide.
An isolate of the virus from cv. Ducasse has been sequenced and although related to
Potex-, Carla-, and Foveaviruses, it appears distinct from all previously described virus
genera (Gambley and Thomas 2001).
Banana bract mosaic virus (BBrMV)
Banana bract mosaic disease was first noted in 1979 in the Philippines, at Davao on
the Island of Mindanao (Thomas and Magnaye 1996). It has subsequently been shown
to be widespread in the Philippines, India, and Sri Lanka (Rodoni et al. 1997; Thomas
et al. 1997). A potyvirus has been isolated from infected plants and is assumed to be
the causal agent (Thomas and Magnaye 1996). Yield losses of up to 40% have been
recorded in the Philippines on cv. Cardaba and cv. Lakatan (Magnaye 1994). The disease
54
Overview of Musa viruses in sub-Saharan Africa
is known in India as Kokkan disease. BBrMV also infects Abaca in the Philippines,
and in some plants at least, the symptoms resemble those induced in banana (Sharman
et al. 2000).
Recently, the virus has also been detected in some plants with CMV-like symptoms
from India, Thailand, and Vietnam, though only the plants from India were tested for,
and shown to contain CMV (Rodoni et al. 1999). A sample from western Samoa had
symptoms of BSV infection, and had a dual infection of BSV and BBrMV (Rodoni
et al. 1999). It is thus possible the virus is much more widespread than previously
believed. With the detection methods available now (Bateson and Dale 1995; Rodoni
et al. 1997; Thomas et al. 1997; Sharman et al. 2000), greater clarity on the distribution
and importance of the virus is likely to emerge.
Abaca mosaic virus (AbaMV)
AbaMV, belonging to the sugarcane mosaic subgroup of the genus Potyvirus, is restricted
to the Philippines. It has been a significant constraint to production of Abaca (Musa
textilis; Manila hemp) (Eloja and Tinsley 1963, Diekmann and Putter 1996).
The virus can be transmitted to edible banana, in which it causes symptoms similar
to BBrMV (Magnaye and Espino 1990; Stover 1972). However, nucleotide sequence
information and serology (Thomas et al. 1997) have confirmed that the two viruses are
distinct. This suggests that both have to be taken into account in surveys of viruses of
bananas and in the indexing of Musa germplasm.
Banana die-back virus (BDBV)
A probable Nepovirus, BDBV, has recently been recorded in Nigeria (Hughes et al.
1998). The virus causes leaf crinkling, leaf necrosis, and cigar-leaf die-back, and suckers
from the same mats are progressively more stunted, ultimately resulting in severely
stunted banana plants. The extent of the disease and implications for banana/plantain
production in sub-Saharan Africa are unknown, and are the subject of investigation
currently (Hughes et al. 1998).
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