Text-only Preview

Meisaku Koizumi
Okitsu Branch, Fruit Tree Research Station
Ministry of Agriculture, Forestry and Fisheries, Japan
Okitsu, Shimizu, Shizuoka 424-02, Japan
The production of new commercial fruit crops in the Asian and Pacific region has meant
the appearance of new virus diseases. This paper reviews virus or virus like-diseases vectored
by insects found in passionfruit, longan and other fruit crops in Asia. It warns that some dis-
eases which now appear minor have the potential of causing severe damage in the future.

Insect-borne virus or virus-like diseases are
Passionfruit (Passiflora edulis Sims.) origi-
a major constraint to fruit production in Asia. Many
nated in South America, and has now become popu-
of them have a harmful effect on production, with
lar in tropical and subtropical Asia. The fruit is either
lower yields, poor fruit quality, and a decline in the
eaten fresh, or is used commercially for juice produc-
vigor of the tree. Some have been introduced from
tion. The golden passionfruit (P. edulis f. flavicarpa
foreign countries, while others have broken out
Deg.) is the most important cultivar. Many viruses
spontaneously in a particular place. In the early
or virus-like diseases occur in the plants.
stages they are found only within a small area, but
they become prevalent when favorable conditions
Potyvirus Group
appear. The dissemination of infected plants and
insect vectors is an important factor. The appear-
Passionfruit Woodiness Virus (PWV)
ance of a new host or interhost, and the occurrence
of mutations, are also possible factors in disease
This virus disease was first reported in 1953
in Australia, although the disease ‘woody fruit’ had
This paper reviews insect-borne virus or
been recognized since 1901 (Taylor and Greber
virus-like diseases which have occurred over the
1973). An outbreak of PWV in Taiwan occurred in
past ten years in various fruit (not including major
1980. PWV has been found in Brazil (Kitajima et al.
fruit crops such as citrus, banana or papaya). Some
1986) and South Africa (Brand et al. 1993) and is
of these diseases are widespread in Asia, while others
probably present in tropical Asia.
are still local or not yet found in Asia, (i.e. they are
Symptoms of mosaic, rugosity and distor-
exotic). Even if they are fairly unimportant, they
tion of leaves, with yellow spots on older leaves,
have the potential of becoming prevalent and causing
develop on infected P. edulis plants. Ringspots,
severe damage in the future. We should pay atten-
which vary in color from pale green to chlorotic, are
tion to these minor diseases, as well as to the major
found together with leaf mosaic on the spring growth
of golden passionfruit and hybrid passionfruit (P.
edulis/P. e. f. flavicarpa
). The fruit is frequently
distorted, and the pericarp is hard and thick, giving
the disease the common name of ‘woody fruit’. The
Keywords: Chinese jujube, cucumber mosaic virus, insect vectors, kaki, longan, passionfruit mottle
virus, passionfruit, passionfruit woodiness virus, soursop, virus disease

productive life of the plant is greatly shortened
ing a wide range of Leguminosae.
(Taylor and Greber 1973).
The particles are filaments approximately
The virus particles are flexible filaments
841 nm in length. Two polypeptids of molecular
about 12 nm wide and 750 nm in length (Taylor and
weight 33.2 and 28.7 kDa can be detected. The
Greber ibid). They are transmitted in a non-persis-
aphids Myzus persicae, Aphis spiraecola, A. gossypii
tent manner by the aphids Myzus persicae and Aphis
and A. craccivora transmit the virus. SLPFMV
gossypii. They are sap-transmissible to a wide range
reacts with antisera to PWV, Passionfruit Ringspot
of hosts, particularly leguminous plants. However,
Virus, and Potato Virus Y, but reacts only weakly to
there is no evidence of transmission through seed.
Watermelon Mosaic 2, and not at all to Bean Com-
Several strains have been recognized, dis-
mon Mosaic Virus.
tinguished by the severity of the symptoms they
produce in Passiflora edulis. The virus also occurs
Passionfruit Ringspot Virus (PFRSV)
naturally in some tropical legumes, including Ara-
chis hypogea
, Centrosema pubescens, Crotalaria
This virus, found in Ivory Coast, West
usaramoensis, Glycine max and Phaseolus
Africa, causes leaf mottling and ring-spotting in
atropurpureus, but does little damage to these spe-
golden passionfruit (De Wijs 1974). The virus
particles are 15 x 810-830 nm, and react with antis-
In Australia, the use of a hybrid P. edulis/P.
era to PWV from Australia, but not in an identical
e. f. flavicarpa (Taylor and Greber 1973) or pre-
way. The virus seems to belong to the potato virus
inoculation with a mild strain of PWV (Pares et al.
Y group.
1985) reduced the damage from severe strains of
The Puerto Rican Passionfruit Virus (PRPFV)
Passionfruit Mottle Virus (PaMV)
This virus, from Puerto Rico and the Do-
minican Republic, is considered to be an isolate of
This virus was found in Taiwan in 1987
Watermelon Mosaic Virus 2. This identification is
(Chang 1992). The particles are similar to those of
based on host reactions, serological relations, and
PWV in morphology. The capsid protein of PaMV
the capsid protein molecular weight (Niblett et al.
is 38 kDa, while that of PWV is 37 kDa. The
cylindrical inclusion bodies are large and bundle-
shaped, while those of PWV are short and plate-like.
Both viruses share a common host range, with the
exception of a few leguminous species. The most
Infection of passionfruit with Cucumber
important difference between the two is the symp-
Mosaic Virus (CMV) is found in many countries.
toms produced in a hybrid cultivar, Tainung No. 1
Golden passionfruit infected with CMV show both
(P. edulis/P. e. f. flavicarpa). When this cultivar is
mosaic and striking coalescent yellow rings on the
infected with PaMV, it shows only mild mottling of
leaves, with occasional slight deformation of the
the leaves, while PWV induces severe foliage mosaic
foliage (Colariccio et al. 1987). Dual infection with
and woody, misshapen fruits. PaMV is transmitted
CMV and PWV causes severe symptoms.
by the aphid Myzus persicae, and there is no evi-
Woodiness disease of passionfruit in South
dence of seed transmission. PaMV is antigenically
Africa was shown to be associated, not only with a
related to, but distinct from, PWV, Bean Common
single potyvirus infection, but also with multiple
Mosaic Virus and Blackeye Cowpea Mosaic Virus.
infection by at least three different viruses, including
It reacts weakly with Soybean Mosaic Virus, but is
CMV (Brand and Wechmar 1993). Recently, it was
unrelated to other potyviruses.
reported from Australia that a double infection with
CMV and a mild strain of PWV caused vine-tip
Sri Lankan Passionfruit Mottle Virus (SLPFMV)
necrosis, so that the vines died back (Pares et al.
This virus is found in golden passionfruit in
The use of vegetatively propagated hybrids
Sri Lanka (Dassanayake and Hicks 1992). Typical
in Australia, coupled with pre-inoculation with a
symptoms are mottled leaves with numerous chlo-
mild strain of PWV, has been claimed to control a
rotic spots, reduction of vigor, and fruit with a
severe strain of PWV, so that CMV became more
shrunken, blotchy appearance. The virus infects
important (Pares et al. ibid).
systemically 23 species in five plant families, includ-

Tymovirus Group
tal and berry crops (Stace-Smith 1984).
Passionfruit Yellow Mosaic Virus (PYMV)
This virus has been found in Brazil (Crestani
Passionfruit Leaf Mottle
et al. 1986). Infected golden passionfruit showed
characteristic bright yellow mosaic, with yellow
This disease, caused by a geminivirus, is
netting, and crinkling on the leaves. The particles are
found in P. edulis in Puerto Rico (Brown and Fletcher
isometric, around 30 nm in diameter. The host range
1993). The virus is transmitted by the whitefly
is definitely limited to the genus Passiflora. A
Bemisia tabaci (Gennadius), as well as by grafting,
chrysomelid beetle (Diabrotica speciosa Germ) trans-
but not by sap inoculation, or aphids, nor can it be
mits the virus, and there is no evidence of seed
transmitted through seed.
transmission. The disease is still of little importance
in Brazil.
Mycoplasma-like Organisms (MLO)
Purple Granadilla Mosaic Virus
Witches’ broom disease, caused by MLO,
is prevalent in some parts of Brazil (Kitajima et al.
This virus was also found in Brazil, where
1986). Its vector and host range are unknown.
it was identified on P. edulis (Chagas et al. 1984). It
is characterized by leaf mosaic, vein clearing and
irregular chlorotic bands on the vines, deformation
and hardening of the fruit, and poor fruit-set. The
Witches’ broom of longan (Euphoria lon-
host range, morphology, and vectors of the virus are
gan Lam.) is found in China (Chen et al. 1992) and
similar to those of PYMV. However, the virus did
neighboring countries. A flexible virus has been
not react serologically to 33 different isometric
isolated from infected longan trees. The virus is
viruses, including PYMV (Oliveira 1994).
transmitted by a stinkbug, Tessaratoma papillosa
Drury, and a psylliid, Cornegenapsylla sinica Yang
et Li. It is transmitted from one longan tree to
another, and also from longan to litchi (Litchi
Passionfruit Vein Clearing Virus
chinensis Sonnerat). The symptoms in longan are
very similar to those produced by litchi witches’
This virus has been prevalent in golden
broom disease. A close relationship between the two
passionfruit plantations in Brazil since 1981 (Kitajima
diseases is indicated.
and Crestani 1985, 1986). Vines infected with the
disease have short internodes and brittle leaves with
characteristic clear veins. Infected trees have poor
yields of deformed (and sometimes woody) fruit.
Witches’ broom of Chinese jujube (Ziziphus
Mixed infection with PWV or witches’ broom myco-
jujuba Mill.) is found in China and Korea. The causal
plasma is common. The effective vector has not yet
agent has been confirmed to be a mycoplasma-like
been confirmed, but since plant rhabdoviruses are
organism (Zhang et al. 1991, Zhu et al. 1988). The
transmitted by plant-sucking arthropods, mostly
MLO is transmitted by a leaf hopper, Hishimonoides
Hemiptera (Peter 1981), the presence of a vector can
chinensis Anufrive.
be assumed. The relationship between Passionfruit
Vein Clearing Virus and other rhabdoviruses is still
Soursop (Annona muricata L.), also known
as guanabana, is a fruit tree belonging to the
Annonaceae, and is native to the American tropics.
Tomato Ringspot Virus (TRV) is found in P.
Soursop Yellow Blotch Virus (SYBV), a rhabdovi-
edulis in Peru (Koenig and Fribourg 1986). It is well
rus, has been found in Brazil. The symptoms are
known that the nematode Xiphinema americanum
yellow blotches on the leaves (Kitajima and Martins
transmits TRV. TRV and X. americanum have been
1993). The presence of a vector is assumed.
endemic in North America, but the virus became
worldwide with the movement of infected ornamen-

An effective propagation system which can supply
sufficient healthy plants to growers is also necessary.
Kaki, or Japanese persimmon (Diospyros
The development and application of protective mild
kaki L.), is free of any virus or virus-like disease in
strains is also useful, but some fear still remains of a
Japan. However, a disease characterized by leaf
synergistic reaction with other viruses.
yellowing, the dieback of young shoots and tree
In conclusion, the breeding or selection of
decline has been found in Brazil since around 1979
resistant varieties is the most important and conve-
(Matsuoka and Carvalho 1987). The disease has
nient way of controlling virus and virus-like diseases
become locally widespread and is destructive. A
of fruit which are vectored by insects. For this
mycoplasma-like organism (MLO) is associated with
purpose, the collection of genetic resouces and a
the disease. The cultivars Fuyu, Gimbo, Rama Forte
search for useful genes should be carried out.
and IAC hybrids are susceptible.
Over the last ten years, new findings of
Brand, R.J. and M.B. von Wechmar. 1993.
insect-born virus or virus-like diseases of fruits,
Characterization of two viruses implicated
particularly in tropical and subtropical areas, have
in the woodiness disease complex of
increased. In many cases, the vector, interhost and
South African passionfruit: Cucumber mo-
mode of infection are still unknown. Why are new
saic virus and a new potyvirus. Journal
diseases occurring one after another? The most
of the Southern African Society for Horti-
probable cause is the movement of infected materials
cultural Science 3: 28-33.
from the endemic area to disease-free countries.
Brown, J.K., J. Bird and D.C. Fletcher.
However, another possibility should be con-
1993. First report of passiflora leaf
sidered. For example, kaki, the Japanese persimmon
mottle disease caused by a whitefly-trans-
which originated in Japan or China, has been free of
mitted geminivirus in Puerto Rico. Plant
any insect-born virus or virus-like disease for several
Disease 77: 1264.
thousand years. However, a disease of kaki caused
Chagas, C.M., P.P. Joazeiro, M. Kudamatsu,
by MLO occurred in Brazil (Matsuoka and Carvelho
and J. Vega. 1984. Mosaic of purple
1987), where the plant had been introduced only 50
granadilla, a new virus in Brazil.
years earlier. This suggests that the pathogen and its
Fitopatologia Brasileira 9: 241-247.
vector had been endemic in Brazil, affecting some
Chang, C.A. and Y.D. Lin. 1992. Ecology
other plant species, and was then given the opportu-
of passionfruit virus transmission and the
nity to infect kaki. At some stage, either the patho-
evaluation of the effectiveness of using vi-
gen or its vector may have undergone a change in
rus-free seedlings to control passionfruit
pathogenicity or transmissibility, so that it became
virus diseases in Taiwan. Plant Pathol-
able to infect the kaki plant. To prove whether this
ogy Bulletin, Taiwan Agricultural Re-
assumption is true or not, we need much more
search Institute 1: 140-146.
information about the host range of both the patho-
Chang, C.A. 1992. Characterization and
gen and the vector, and about the taxonomic situa-
comparison of passionfruit mottle virus, a
tion of the pathogen.
newly recognized potyvirus, with
Chang and Lin (1992) demonstrated the
passionfruit woodiness virus. Phytopathol-
effectiveness of annual eradication of all passionfruit
ogy 82: 1358-1363.
trees and replanting of virus-free seedlings, even in a
Chen, J.Y., C.F. Xu, K.B. Li, and Y.H. Xia.
situation where insect-born viruses have become
1992. On transmission of longan witches’
established. These results are an encouraging ex-
broom disease by insect vectors. Acta
ample of the control of insect-born diseases. How-
Phytopathologica Sinica 22: 245-249.
ever, difficulties in eradication may arise if the patho-
Colariccio, A., C.M. Chagas, M. Mizuki, J.
gen has become widely established, not only in
Vega, and E. Cereda. 1987. Natural in-
cultivated plants but also in wild ones. In this
fection of golden passion fruit with cu-
situation, considerable effort and funding will be
cumber mosaic virus in Brazil.
needed for many years if eradication is to be achieved.
Fitopatologia Brasileira 12: 254-257.
Whatever method is used to control vector-
Crestani, O.A., E.W. Kitajima, M.T. Lin, and
born diseases, rapid and reliable indexing is needed.
V.L.A. Marinho. 1986. Passion fruit

yellow mosaic virus, a new tymovirus
bly caused by an isolate of water-melon
found in Brazil. Phytopathology 76: 951-
mosaic virus 2. Phytopathology 81: 698.
Oliveira, C.R.B., V.L.A. Marinho, F.S. Astolfi,
Dassanayake, E.M. and R.G.T. Hicks. 1992.
M. Azevedo, C.M. Chagas, and E.W.
Sri Lanka passion fruit mottle virus, a
Kitajima. 1994. Purification, serology
potyvirus infecting golden passion fruit in
and some properties of the purple grana-
Sri Lanka. Annals of applied Biology
dilla (Passiflora edulis) mosaic virus.
120: 459-469.
Fitopatologia Brasileira 19: 455-462.
De Wijs, J.J. 1974. A virus causing
Pares, R.D., A.B. Martin, and R.D. Fitzell.
ringspot of Passiflora edulis in the Ivory
1985. Virus-induced tip necrosis of
Coast. Annals of applied Biology 77:
passionfruit (Passiflora edulis Sims).
Australasian Plant Pathology 14: 76-78.
Kitajima, E.W. and O.A. Crestani. 1985.
Peters, D. 1981. Plant Rhabdovirus Group.
Association of a rhabdovirus with
CMI/AAB Description of Plant Viruses,
passionfruit vein clearing in Brazil.
No. 244.
Fitopatologia Brasileira 10: 681-688.
Stace-Smith, R. 1984. Tomato Ringspot Vi-
Kitajima, E.W., C.M. Chagas, and O.A.
rus. CMI/AAB Description of Plant Vi-
Crestani. 1986. Virus and mycoplasma-
ruses, No. 290. (No. 18 revised).
associated diseases of passionfruit in Bra-
Taylor, R.H. and R.S. Greber. 1973.
zil. Fitopatologia Brasileira 11: 409-432.
Passionfruit Woodiness Virus. C.M.I./
Kitajima, E.W., C.R.F. Martins, and A.A.
A.A.B. Descriptions of Plant Viruses, No.
Santos. 1993. Identification of a rhabdo-
virus in soursop (Annona muricata).
Zhang, X.G., Z.W. Chen, Z.A. Chen, S.M.
Plant Disease 77: 276-278.
Sun, F.G. Zhang, and X.D. Tiang. 1991.
Koenig, R. and C.E. Fribourg. 1986. Natu-
Study on the infection of MLO of jujube
ral occurrence of tomato ringspot virus in
witches’ broom disease to periwinkle
Passiflora edulis from Peru. Plant Dis-
(Vinca rosea). International Journal of
ease 70: 244-245.
Tropical Plant Disease 9: 251-256.
Matsuoka, K. and M.G. Carvalho. 1987.
Zhu, B.M., Z.Y. Chen, C.Y. Shen, P.Z. Zhou,
Mycoplasma-like organisms associated with
C.A. Chang, C. Wang, and X.F. Liu.
kaki decline in Brazil. Plant Pathology
1988. Isolation of mycoplasma like or-
36: 417-419.
ganisms from Chinese jujube infected with
Niblett, C.L., A.C. Monllor, R. Provvidenti, P.
witches’ broom disease and preparation of
E. Still, J. Escudero, J. Bird, and K.
its antiserum. Acta Biochimica et
Gough. 1991. A disease of passionfruit
Biophysica Sinica 20: 247-252.
(Passiflora edulis) in Puerto Rico, possi-