Virus Diseases of Cereal Crops

H. H. McKinney.

Most of the plant viruses impair or destroy chlorophyll, the all-important food-synthesizing green pigment in crop plants. The plant struggles for its existence or dies if its chlorophyll has been impaired.

Some viruses stunt or otherwise deform or alter the growth of plants without seriously affecting the chlorophyll. Sometimes it seems that the chlorophyll even may be increased. Some plants may carry a virus but show no signs of disease.

Some viruses tend to impair or destroy the chlorophyll uniformly through the leaf. They cause chlorosis a general yellowing or bleaching. In others the impairment or destruction occurs in patches, spots, or streaks in the leaf; there is a light-green or yellow or white mosaic mottling, spotting, or streaking. The chlorotic patterns in the leaves are strikingly similar for many of the virus diseases of the grasses, even though the viruses are quite different.

Among the cereal crops in the United States the greatest losses from the virus diseases are caused by the mosaics of winter wheat. Several viruses attack cereals. Some have been controlled through the use of resistant varieties, but for a destructive group of viruses in the area between Oklahoma to South Dakota no effective control is known.

We identify the viruses of cereals and other plants largely on the basis of symptom reactions of the infected plants when grown under proper environmental conditions; the host-range characteristics; the methods by which a virus can be transmitted from diseased to healthy plants; and the ability of a virus to live in extracted plant juice or in dried tissue under different temperatures, and other physical and chemical treatments for given lengths of time.

The method of perpetuating a virus is determined by the characteristics of the virus. If the virus can be transmitted only by tissue union or by insects, it is kept alive in the living plant or sometimes in the living insects. Many viruses that can be transmitted experimentally by manual methods of inoculation are kept alive for months or years in frozen juice or in dried tissues near freezing.

The wheat, barley, oat, and cucumber viruses that can be transmitted by manual methods of inoculation are kept in clipped leaf tissue that is dehydrated over calcium chloride, and stored over anhydrone at temperatures just above freezing. At intervals the stored viruses are increased in growing plants, and new dehydrated tissues are prepared and stored. The virus of brome mosaic and viruses of the Agropyron mosaic can be maintained in that way, but usually less work is involved when they are carried in their respective native host plants, and the new cultures are started by the division of the plant stools or from the rhizomes. The virus of barley stripe mosaic can be kept in infected seeds for at least 8 years.

SOIL-BORNE wheat mosaic viruses occur in Illinois, Indiana, Iowa, Kansas, Maryland, Missouri, Nebraska, North Carolina, Oklahoma, South Carolina, and Virginia. Infected fields have been found in nearly one-half of the counties in Illinois. Indiana also has many infected areas. In many places, particularly in Illinois, the viruses would curtail the production of wheat were it not for resistant wheats.

These viruses of wheat and its close relatives also infect barley and rye, although they have shown relatively high resistance. Oats, corn, and plants outside of the grass family apparently are not susceptible to them. Bromus commutates, a wild grass, is susceptible. The viruses are not carried in the seed from the diseased plants.

The virus of wheat mosaic-rosette (Marmor tritici var. typicum), is the first virus that we knew could be carried over in the soil from season to season. The rosette phase of the disease attracted attention in 1919, near Granite City, Ill., but its virus nature was not recognized until 1925. Previously it was suspected that insects (particularly the hessian fly), cold winter temperatures, and several species of fungi were causing the trouble. In 1920 it was learned that the causal agent is associated with soils and that it can be inactivated in the soil by steaming and treatment with formaldehyde.

Many varieties of wheat were found to be immune to rosette. From 1920 to 1923 I selected rosette-immune strains from the highly susceptible varieties Harvest Queen and Illini Chief. Years later, when Illinois 2 wheat was found to be highly susceptible to mosaic rosette, O. T. Bonnett and his associates at the University of Illinois selected lines that were immune to rosette and highly resistant to mosaic and that had several of the desirable characteristics of Illinois 2. Those lines contributed to the development of Prairie and Royal varieties.

The evidence that the causal agent Of rosette was associated with the soil actually delayed the discovery that a virus caused the disease. In 1920 workers generally considered that viruses did not over-season in the soil. Even today few viruses are known to be carried over in the soil. Fortunately the rosette symptoms occur in only a few varieties, such as Harvest Queen, Illini Chief, and Missouri Bluestem. Most varieties, however, develop mosaic mottling when they are grown in infested soils.

Along with the field experiments, microscopic studies that Sophia Eckerson, R. W. Webb, and I conducted at the University of Wisconsin revealed the presence of abnormal inclusion bodies in many of the cells of both rosetted and mosaic plants. These cell inclusions were so strikingly like those associated with some known virus diseases, and the mosaic symptoms were so evident in many of the varieties of wheat, that we strongly suspected the virus nature of rosette and the mosaics.

Inoculation methods commonly used to transmit mosaic viruses in plants like tobacco and cucumber failed to transmit the disease to healthy wheat seedlings. Neither rosette nor mosaic developed when I grew winter wheat out of its natural growing season. So I got the idea that cool temperatures favor infection and disease expression.

Tests by Dr. Webb demonstrated that soil temperatures near 60 F. and comparatively high soil moisture favored natural infection from the soil. When I inoculated healthy wheat seedlings with the juice from the diseased plants and then cultured them at cool temperatures, they developed the disease.

Mosaic symptoms are transmitted most successfully by growing the inoculated plants with ample sunlight, a daily photo-period of 8 hours, and a temperature near 60 .

I observed that some of the wheat plants growing in the field developed light-green mosaic mottling. Others developed severe yellow mottling. In the inoculation tests with virus from mosaic spelt and wheat plants, I saw that some of the plants of Harvest Queen wheat developed light-green mosaic and rosette, while others developed yellow mosaic somewhat like the situation that I had observed in the study of the mosaic viruses that infect tobacco. Virus-selection techniques soon enabled the isolation of two viruses. One induced mild light-green mosaic and rosette in Harvest Queen wheat. The other induced severe yellow mosaic in Harvest Queen, but no rosette.

I found that most varieties of wheat developed only mosaic when they were inoculated with the mosaic-rosette virus. Some varieties developed light-green mosaic. Others developed mild yellow mosaic.

Some of the severe yellow mosaic viruses that have been isolated from the soil-borne series differ somewhat in their ability to destroy chlorophyll and to stunt or otherwise deform the plant. None, however, has been observed to cause the excessive stooling or bud proliferation caused by the mosaic-rosette virus. To distinguish them from other viruses that cause yellow mosaic in wheat, they are referred to as the prairie wheat yellow mosaic viruses (Marmor tritici var. fulvum). Attempts to isolate a virus that induces rosette without the mild mosaic mottling have failed.

These yellow mosaic viruses are regarded as strains of the mosaic-rosette virus, but further study is needed to determine whether they are direct mutants or more distant relatives. I have not seen the strong unilateral interference, characteristic of the tobacco mosaic virus in combination with its yellow mosaic virus mutants, in the soil-borne viruses isolated thus far from wheat. It is therefore harder to demonstrate mutation in the wheat mosaic viruses than it is in the tobacco mosaic virus.

The soil-borne wheat mosaic viruses are relatively unstable in extracted plant juices and in tissues removed from the plant and kept at ordinary temperatures. The viruses are inactive when the leaves die on the plant. When fresh mosaic leaves are dried in the laboratory, the virus becomes inactive within 2 or 3 weeks. Furthermore, the viruses soon die when fresh mosaic leaves are allowed to decompose in moist soil. The thermal death point of the yellow mosaic viruses tested thus far is 140 to 149 F., with 10 minutes exposure when in the plant juice. Traces of yellow mosaic virus passed a Schott-Jena fritted glass filter having average pore size of 880 millimicrons. The dilution end points for the rosette and the yellow mosaic viruses in distilled water are between 100 and 1,000 times.

Mosaic may occur in an infested field every year for at least 12 years, or it may fail to appear after the first year. Air-dried soil stored in the laboratory for 3 years remained infectious. Some lightly infested soils lost their infecting power when stored through one summer, however.

In a cropping test that covered 5 years on infested land, Benjamin Koehler, of the Illinois Agricultural Experiment Station, found that continuous cropping with a susceptible wheat greatly favored the occurrence of mosaic and rosette. Cropping for 4 years with an immune wheat, oats, soybeans, and corn greatly reduced or controlled completely the rosette and mosaic in the susceptible wheats grown on the land the fifth season. Four years of cropping with alfalfa also reduced the amount of disease, but less than other crops did. Under favorable conditions, which are not completely understood, Dr. Koehler found that a lightly infectious soil gradually became highly infectious after four successive croppings with susceptible wheats.

The effects of various chemicals and heat on infested soil have been tested by Koehler and me and also by Folke Johnson at Ohio State University. Infestation can be eliminated by the use of heat, formaldehyde, chloropicrin, dichloropropene-dichloropropane (D D), napthalene, calcium cyanide, carbon disulfide, methyl bromide, rotenone, napthalene, and ethyl alcohol. Ethylene dichloride was less effective than the other chemicals. Ethyl chloride gave no control. Toluene gave no control in air-dried infested soil that was saturated with the chemical for 4 days, followed by complete evaporation of the chemical and seeding within 5 days to a susceptible wheat.

We do not know the exact relation of these wheat viruses to the soil. Perhaps they live in some soil-inhabiting organism that carries the virus and introduces it into the underground parts of the young seedling in autumn.