How Insects Transmit Viruses

L. M. Black.

Most viruses that cause plant disease are transmitted by insects, principally those that have sucking mouth parts aphids, leafhoppers, white flies, mealy-bugs, and tingids. Leafhoppers and aphids are the most important.

Although many plant viruses are without known insect vectors, it is generally expected that insect carriers will eventually be discovered for most of them. There are exceptions. Tobacco mosaic virus and potato latent virus are two viruses that occur in high concentration in infected plants and are stable enough to be spread readily from one plant to another by almost any means that releases juice from a wound in an infected plant and transfers the juice to a fresh wound in a healthy plant. Tobacco mosaic virus is thus transferred by the hands of men working with tobacco plants even though the wounds may be only microscopic in size. It can also be thus transferred by the mouth parts of grasshoppers. Potato latent virus can be transferred from plant to plant when the wind blows the leaves of diseased plants against healthy ones so as to injure both. The mystery about these two viruses is not their transmission by such methods but why potato latent virus is apparently not transmitted by sucking insects and why tobacco mosaic virus is so poorly transmitted.

A few viruses, such as wheat rosette virus and lettuce big-vein virus, contaminate the soil in which diseased plants are grown and infect healthy plants subsequently grown therein. Just how inoculation takes place in such diseases is not known. Dodders (Cuscuta species), parasitic flowering plants, can transmit plant viruses by means of the natural graft unions they make with their hosts. Most plant viruses, however, depend on insects for their dispersal.

APHIDS transmit more plant viruses than any other group. Aphid-borne viruses induce in plants a great variety of symptoms, the most important of which are the mosaics. One of the most efficient aphid vectors is the green peach aphid, Myzus persicae, which transmits more than 50 different plant viruses.

Much remains to be learned about what actually occurs during transmission by aphids. Many aphid vectors transmit virus after very brief feedings on diseased plants. Studies on this type of transmission have reached a point where the feeding intervals of individual aphids are closely observed and timed by a stop watch. For example, the vector of beet mosaic virus requires an acquisition feeding of only 6 to 10-seconds. During subsequent consecutive inoculation feedings of 10 seconds each on healthy plants, the virus is gradually lost by the aphids and fewer than 2 percent of them can transmit to more than four plants without fresh access to virus. This virus is said to be non-persistent in the vector. Usually such a virus is lost more rapidly from feeding aphids than from fasting ones the virus of cucumber mosaic disease, for instance, is lost by the aphid within 6 to 8 hours when fasting, but within 10 to 20 minutes when feeding on healthy plants. In other instances this relation may be reversed. The loss of virus from aphids during feeding may be due to a virus-inactivating enzyme secreted by the aphids while feeding but not while fasting. Such a substance has not been demonstrated, however, and in reality We do not know the explanation for such loss and for many other features of aphid transmission. A virus transmitted by aphids, particularly if it is of this non-persistent type, is usually transmissible by several or, indeed, many species. The virus of onion yellow dwarf can be transmitted by more than 50 species of aphids, but not by thrips, mites, grasshoppers, beetles, caterpillars, or maggots.

That kind of transmission is in contrast to another type in which, following acquisition of virus, a latent period must elapse before the aphid is able to transmit. The aphid may then do so for many days without fresh access to virus. A minority of viruses transmitted by aphids are spread in that manner. One of them, the virus of potato leaf roll, is not transmitted by the aphid until 24 to 48 hours have elapsed after acquisition. The virus may then be retained by the insect for 7 to 10 days, even through molts, without fresh access to virus from plants.

That an aphid may transmit one virus in the persistent manner and another in the non-persistent from the same host plant clearly indicates that persistence or non-persistence is determined by the virus.

Why do we concern ourselves with such minute details of transmission? Simply because such knowledge may make the difference between success and failure in finding a vector of a virus. For instance, no transmission of a certain mosaic virus could be obtained after extensive trials with three species of aphids when they were fed one day on diseased plants and then transferred to healthy ones. When the aphids were fasted for 30 minutes before an acquisition feeding of 5 to 10 minutes and were then allowed an inoculation feeding of 5 to 10 minutes, however, transmissions were obtained.

LEAFHOPPERS, next to aphids, are the most important vectors of plant viruses. Experiments by a Japanese grower in 1884 demonstrated a connection between rice stunt and leafhoppers. That might be considered the first virus shown to be insect-transmitted, but actually it was not realized until more than 20 years later that the causal agent of the disease was not the leafhopper but some autonomous agent carried by the insect.

Viruses transmitted by leafhoppers cause a variety of symptoms in plants, including chlorotic streaking of leaves (as in corn streak), necrosis or death of tissues (as in elm phloem necrosis), tumors (as in wound-tumor disease), and yellows (as in aster yellows). All known vectors for virus diseases with a symptom picture like that of aster yellows are leafhoppers.

Although many aphid-borne viruses can be transmitted by rubbing leaves with juice from diseased plants, only two leafhopper-borne viruses have been so transferred. In other cases transmission has been accomplished only by the use of insects, dodder, or grafting. This has accordingly made the study of the viruses themselves very difficult. For such researches it has been necessary to permit the leafhoppers to feed on virus solutions through membranes or to inject the virus solution into leafhoppers. The insects must then be tested for infectivity on plants because none of the leafhoppers themselves has ever been observed to be diseased.

Practically all of the leafhopper-borne viruses (alfalfa dwarf virus is apparently an exception) are considered to have a latent or incubation period in their vectors. In some, this latent period may be so short (curly top virus) as to suggest that the virus does not multiply in the insect. Nevertheless, it reaches relatively high concentrations and is retained for weeks, not only in the beet leafhopper, which transmits it, but also in a number of other arthropods that cannot do so.

In most leafhopper vectors that have been studied, however, the period that occurs between acquisition of the virus and its transmissibility by the vector is much longer. In many it varies from 1 to 2 weeks or more. This is a true incubation period, during which the viruses multiply to an infective concentration in their vectors.

Although most leafhopper vectors do not transmit virus to their progeny through the egg, certain exceptions exist. Rice stunt virus and clover club leaf virus may be passed to 95 or 100 percent of young insects through the eggs of the vectors. A single female leafhopper carrying clover club leaf virus has originated at least 21 generations of infective progeny during a 5-year period without fresh access to virus from plants. The virus in the original female had been diluted at least 100,000,000,000,000,000,000,000,000 times. That would be impossible had not the virus multiplied in the leafhopper.

There may be, then, two main types of transmission of virus by leafhoppers. One type, exemplified by curly top virus, may be characterized by a very short incubation period and no multiplication in the vector; the other type by a long period of incubation and multiplication in the vector.

Once infective, leafhoppers tend to remain so for many days without fresh access to virus, often until they die. Nevertheless, such insects may fail to infect susceptible plants for many days in succession. Some that obtain virus from their parent through the egg may in turn pass virus to their progeny through the egg and yet may fail to infect any susceptible plants although fed on them for their entire life.

Often scientists have tested so many species of insects before finding a leafhopper vector that when they attained success they regarded the vector as specific. Only one species is known even today to transmit North American curly top virus. Very likely that is because it is the only species of the genus that occurs in North America where tests have been made.

The concept of specificity which envisioned a single leafhopper species as the vector of a virus has been broken down by recent research. For example, it is now known that Pierce's disease of grapes is transmitted by 24 different species of leafhoppers in two families. on the other hand, work with yellow dwarf and with curly top viruses has revealed a new type of specificity, of considerable complexity. In the former, there are two varieties of virus, each specifically transmitted by related leafhoppers. In the case of curly top, We have evidence of a complex of related viruses, with different vector and plant-host relationships.