RE: [tomato] Tolerance to tomato yellow leaf curl virus

Pete (
Tue, 14 Dec 1999 21:21:36 -0500

Tomato Yellow Leaf Curl Virus 1
J. E. Polston, R. J. McGovern, P. A. Stansly 2

Tomato yellow leaf curl virus (TYLCV) was first characterized in Israel in
1959 and has been a major limiting factor for tomato production in that
country since the 1930s. Related viruses have been reported from other
Mediterranean countries, Africa, Asia, and Australia. Recently a virus
essentially identical to TYLCV from the eastern Mediterranean was found
infecting tomato plants in the Dominican Republic (1993) and Jamaica (1994).
This virus has drastically limited tomato production in both countries and
poses a significant economic threat to the commodity throughout the Western

TYLCV is a member of the Geminiviridae group of viruses which also contains
tomato mottle virus and bean golden mosaic virus which have recently become
established in Florida. Like both these viruses, TYLCV consists of twinned
(geminate) particles ( Plate 1 ) and is spread by adult silverleaf
whiteflies ( Bemisia argentifolii Perring & Bellows). However, TYLCV
consists of a single strand of DNA unlike most other geminiviruses which
have two. Analyses of several isolates of TYLCV from various parts of the
world have indicated that different viruses can cause the tomato yellow leaf
curl disease in different areas of the world. At this time the term TYLCV
refers to those virus isolates which are genetically very similar to the
virus causing yellow leaf curl first identified in Israel.

Tomato yellow leaf curl virus infects several crop plants but has been
reported as a problem only in tomato. The incidence of TYLCV in tomato is
often very high and tomato plants are severely affected by the virus.
Symptoms vary somewhat among tomato cultivars but in general leaves produced
shortly after infection are reduced in size, distorted, cupped inward or
downward, and have a yellow mottle. Subsequent leaves become progressively
smaller and more distorted, and exhibit both marginal yellowing which
sometimes encompasses the entire leaf, and upward leaf cupping ( Plate 2 and
Plate 3 ). Infected plants are severely stunted; the younger the plant is at
the time of infection, the more severe the stunting becomes. The most
significant effect of TYLCV infection is flower abscission. Fewer than one
in ten flowers will set fruit after TYLCV infection, severely reducing
yields. The stunting and flower abscission caused by TYLCV are more severe
than those caused by tomato mottle virus. Tomato plants infected with both
tomato mottle virus and tobacco etch virus have foliar symptoms similar to
those of TYLCV, however, without the high frequency of flower abscission.
Foliar symptoms of TYLCV lack the purpling of leaf veins and the curling of
shoots caused by pseudocurly top virus, a treehopper-transmitted geminivirus
found occasionally in tomato in Florida.

Tomato yellow leaf curl virus has a broad host range which currently
includes wild and cultivated plants from seven families ( Table 1 ). This
contrasts notably with the narrow host range of tomato mottle virus
(Fabaceae and Solanaceae). The majority of the host plants infected by TYLCV
showed no symptoms, although the virus could be acquired from them and
transmitted to tomato by whiteflies. Four species of crop plants (lentil,
common bean, tobacco and tomato) have been infected experimentally but only
tomato has been found infected naturally. Surveys conducted in Israel showed
that only two weed species, Cynanchum acutum and cheeseweed ( Malva
parviflora ), were infected naturally. In Turkey, jimson weed ( Datura
stramonium ), black nightshade ( Solanum nigrum ) and nettle ( Urtica sp.)
were found to be reservoirs of the virus. Table 1 lists the known hosts of
TYLCV and whether symptoms occur.

The sweetpotato whitefly, Bemisia tabaci Genn., has recently been split into
two species, one named B. tabaci (previously referred to as biotype A) and
the other named Bemisia argentifolii the silverleaf whitefly (previously
known as B. tabaci biotype B). The two whitefly species are physically
difficult to distinguish, but the two species show several biological
differences. The silverleaf whitefly feeds and reproduces on a broader range
of plant species than the sweetpotato whitefly, including most types of
vegetables, broadleaf row crops, weeds, and many ornamentals including
poinsettia. The silverleaf whitefly also has a higher rate of reproduction
and feeds more heavily than the sweetpotato whitefly. The silverleaf
whitefly owes its name to the reaction its feeding produces on squash.
Salivary secretions injected into the plant by the immature whitefly produce
a silvering of squash leaves, irregular ripening of tomato fruit, and
blanching of broccoli stems and poinsettia leaves. In recent years the
silverleaf whitefly has become the dominant of the two species throughout
the southern United States and in many other areas. The silverleaf whitefly
is known to occur on tomatoes in the Dominican Republic and Jamaica and is
responsible for the transmission of TYLCV in those areas.

Adult silverleaf whiteflies are small (1/16 inch in length), winged insects
covered with a white powdery wax ( Plate 4 ). They usually alight on the
upper leaf surface but quickly move to the lower surface where they feed on
plant sap, mate, and lay up to 300 eggs. A tiny "crawler" emerges from each
egg and moves across the leaf in search of uninhabited surface. Once
settled, the crawler inserts its tube-like stylet and begins to feed. Three
molts followgiving rise to successively larger but immobile scale-like
stages, the last of which transforms into a yellowish, red-eyed immature
("pupa") approximately 1/32 inch in length. A few days later an adult
whitefly emerges. The entire process from egg to adult is about two to four
weeks long, depending on the temperatures present during development. Higher
temperatures decrease the time required for whitefly development. Once
emerged from the "pupa", adult whiteflies remain on the leaf for several
hours as they coat themselves with wax which they produce. The whitefly may
remain on the plant or fly. Adult whiteflies can fly for several hours and
with wind assistance can traverse significant distances.

Tomato yellow leaf curl virus is spread primarily by whiteflies. In Israel
and the Caribbean the whitefly vector of TYLCV is the silverleaf whitefly.
Studies in Israel have shown that the minimum time required for the whitefly
to acquire the virus is 15 to 30 minutes, and longer feeding periods result
in higher rates of transmission. Similar time periods are required for
transmission. Tomato yellow leaf curl virus can be acquired by immature
whiteflies but only adults can transmit the virus. Adults do not transmit
the virus to their progeny. Tomato yellow leaf curl virus is transmitted by
adults for approximately 10 days, though longer retention times have been
observed. Shorter acquisition periods result in shorter retention times.
Female whiteflies transmitted TYLCV at rates six times higher than males.

In addition to transmission by whiteflies, TYLCV can also be spread through
the movement of infected plant material. This plant material could be in the
form of infected tomato transplants or through cuttings taken from infected
plants. The virus is not transmitted through seed and not through casual
contact with infected plants. The virus can be mechanically transmitted with
great effort through the use of special laboratory buffers. Long distance
movement could be achieved through the movement of viruliferous whiteflies
"hitchhiking" on noninfected plants. It seems likely that TYLCV was imported
into the Caribbean, but how that occurred is not known.

A disease cycle for TYLCV in tomato has been proposed in Israel. The virus
probably overwinters in the roots of Cynanchum acutum , a spring weed which
matures in August. A high percent (50%) of C. acutum plants sampled were
infected with TYLCV. It is believed that whiteflies acquire TYLCV from C.
acutum plants inearly summer and then transmit the virus to tomatoes over a
period of several weeks. Whitefly populations are very low in the winter and
increase to high populations by summer. Viruliferous whiteflies are first
detected in June and their numbers increase rapidly thereafter. Tomatoes are
planted in the summer at the same time that whitefly populations are high.
The combination of a weed reservoir for TYLCV, high populations of the
whitefly vector and young tomato plants creates a devastating situation for
tomato production.

As the disease cycle discussed above might indicate, TYLCV is a very
difficult pathogen to manage. In Israel, Turkey, and Cyprus the virus
persists in natural weed reservoirs in the absence of a tomato crop.
Whiteflies in many regions readily feed and reproduce on tomato increasing
the difficulty of management. A number of different control strategies for
TYLCV have been tried with limited success. The most successful strategies
to date use a combination of management practices--yellow mulches, timely
pesticide applications, and resistant cultivars.

Whitefly Control. As with other plant viruses which can be transmitted for
long periods of time by their vectors, suppression of the vector may provide
an effective means of reducing virus spread within a field, and reducing the
number of vectors which come into the field. Biological control, which often
works well in the absence of broad spectrum pesticides to reduce the impact
of the whitefly as a pest, offers insufficient control of the vector for the
reduction of virus incidence. Insecticidal control is difficult and
expensive to maintain throughout an entire cropping season. Although
frequent applications of pesticides help to decrease whitefly populations
and suppress the spread of TYLCV, virus management through whitefly control
is not possible in years where whitefly populations are high. Several
foliar-applied insecticides are available for killing whitefly adults and
immatures. When applying foliar insecticides, it is essential to maintain
good coverage on the underside of the leaves where whiteflies reside.
Insecticides with differing modes of action should be rotated to retard
selection for whitefly resistance to any one type of pesticide. Soil-applied
systemic insecticides have been shown to be effective at reducing spread of
TYLCV within tomato fields (secondary spread), but have not been effective
at reducing the amount of virus being introduced into fields (primary

Cultural Practices. Yield loss from TYLCV is more severe the earlier the
infection begins, therefore nearby infected crops and weeds must be
destroyed well in advance of planting. Eradication of overwintering weed
hosts in Cyprus significantly reduced the incidence of TYLCV. However, the
same practice was not effective in Israel, possibly due to long distance
movement of viruliferous whiteflies. In Israel yellow mulches (plastic,
straw, sawdust) were found to be effective in decreasing virus spread.
(Reflective mulches, which disorient the whiteflies, have been shown to be
more effective than colored mulches in reducing the incidence of tomato
mottle virus in Florida). The use of trap crops of cucumber, a highly
preferred whitefly host, delayed TYLCV spread when planted in alternate rows
with, and 30 days before, tomatoes. Fine mesh screens were found to
effectively exclude whiteflies and virus from tomato transplant greenhouses.
However, this strategy requires extra cooling of the greenhouses due to
reduced air flow and may not be economically feasible in Florida. Windbreaks
have been tried but resulted in higher whitefly populations and higher
numbers of infected plants.

Resistant Cultivars. Fresh market tomato hybrid cultivars are available with
tolerance to TYLCV which are adapted to Mediterranean production areas.
Plants of the hybrid cultivar TY20 become infected but produce an acceptable
yield (22 tons/A compared to 1.6 tons/A for a susceptible cultivar) if
plants are protected for four weeks after transplanting using a combination
of available control practices.