The Tristeza Disease of Citrus

T. J. Grant, L. J. Klotz, J. M. Wallace.

The sour orange has long been recognized as a desirable rootstock for the propagation of commercial varieties of citrus. It was highly recommended and widely used until the time of the rapid spread of the tristeza disease in South America and the quick decline in California. The presence and threat of the disease and the problem of satisfactory rootstocks in affected areas continue to be of importance to citrus growers in many parts of the world.

Some 40 years ago growers in South Africa learned from experience that the sour orange was a failure as a rootstock under their conditions. In 1924, the unsatisfactory growth of sweet orange on sour orange rootstock in South Africa received some attention and was referred to as rootstock and scion incompatibility. Instances of "incompatibility" of sweet orange on sour orange rootstock were found between 1924. and 1940, and the trouble appeared in Java, Argentina, Uruguay, Brazil, California, Paraguay, and Australia. In Argentina and Uruguay, the disease was referred to as podredumbre de las raicillas. In Brazil Sylvio Moreira referred to it as tristeza, a word that describes the sad appearance of the diseased trees. Tristeza is now the common name for the disease in South America.

The disease, when it was recognized in California, was referred to as quick decline. As this particular type of rootstock problem made its appearance and became important in various parts of the world, many theories were advanced' to explain the effects produced stock-scion incompatibility, soil acidity, various types of nutrient deficiencies, soil toxins, high content of soil moisture, long dry periods, nematode infestations, pathogenic organisms, virus infection, and others.

Indications of the importance of the disease were reported by A. A. Bitancourt, Sylvio Moreira, J. C. Bertelli, and others. Guy Bush, agricultural attache at the American Embassy in Rio de Janeiro, informed the Department of Agriculture of the importance of the disease and showed visiting citrus growers and scientists from the United States the effects of the disease. He urged that cooperative investigations be undertaken.

Citrus growers in the United States, alarmed by the losses associated with the disease in South America, urged the Department to send someone to study the disease. After consideration of all available information, a virologist, C. W. Bennett, was sent in 1946 to South America. The Institute Agronomico at Campinas, in Sao Paulo, Brazil, the center of a diseased region, extended the use of its facilities for carrying out the work in the field and in screenhouses and the assistance of A. S. Costa, a virologist, and Sylvio, Moreira, a horticulturist.

H. S. Fawcett and J. M. Wallace, of the Citrus Experiment Station of the University of California at Riverside, reported in 1946 that quick decline had been transmitted by graft inoculation of healthy trees and could therefore be considered to be an infectious disease, caused by a virus. At about the same time M. Meneghini, of the Institute Biologico in SAO Paulo, reported the results of tests to demonstrate that the oriental black citrus aphid (Aphis citricidus) could transmit tristeza in Brazil an indication of the virus nature of the disease.

Henry Schneider, of the California Citrus Experiment Station, described the collapse of the phloem, or food-conducting, tissues of the sour orange rootstock of infected trees. His studies in 1946 and 1947 also led to the development of a method of detecting the presence of the disease by means of a microscopic examination of bark tissues at the graft union of the sweet Orange on the sour orange rootstock. Symptoms like those of tristeza and quick decline can be found on trees that have been girdled by gophers or have been injured on the bark or roots by one of many agencies. Such trees, however, do not show in their internal bark or phloem tissue the reactions that are characteristic of the virus-infected trees. Thus, the anatomical technique has been helpful in diagnosing the disease and determining its distribution.

C. W. Bennett's and A. S. Costa's investigations confirmed the transmissibility of tristeza by means of the oriental black citrus aphid and demonstrated transmission of the disease by buds. They laid the basis for the cooperative tests of rootstocks that followed.

Fruit growers in South Africa had learned that they could grow commercial citrus when they used their Rough lemon as a rootstock. When the tristeza disease spread through Brazil, Sylvio Moreira, at the Limeira Citrus Experiment Station, noted that the citrus varieties growing on sweet orange and Rangpur lime rootstocks continued to grow normally while the varieties on sour orange rootstock in nearby plantings died or were unthrifty.

The need for more information about the reactions of various rootstock-scion combinations then became evident. Under the direction of Frank Gardner, of the Subtropical Fruit Field Station of the Department of Agriculture at Orlando, Fla., 265 lots of seed, representing many types and varieties of citrus and citrus relatives, Were assembled, treated, and forwarded to Brazil.

They and varieties collected in Brazil were studied by A. S. Costa, T. J. Grant, and Sylvio Moreira as rootstocks for several commercial varieties of citrus tops, as tops on sour orange rootstock, and as unbudded seedlings.

Plants in all the investigations were subjected to inoculation. The oriental black citrus aphids were fed on citrus trees carrying the tristeza virus and then transferred and allowed to feed on the plants to be tested. In instances in which plants under study failed to show any response to the first inoculations, the inoculation was repeated two and three times.

On the basis of the test, the rootstocks were classed as nontolerant and tolerant.

The nontolerant rootstocks behave like the sour orange and the inoculated sweet-orange tops show disease symptoms. The citrus types in the group include grapefruit, pummelo, shad-dock, some acid lemons and limes, some tangelos, and some closely related types of citrus. All, as far as tristeza disease is concerned, are considered unsatisfactory as rootstocks for the usual commercial varieties of citrus and cannot profitably be used as rootstocks in areas where tristeza occurs.

The tolerant rootstocks include the types of citrus that (under the conditions of the tests in Brazil) continued to show no symptoms of disease in the sweet orange tops even though they were inoculated with the tristeza virus. Among them, generally speaking, are the mandarins, such as Cleopatra, some mandarin hybrids as Rangpur lime, the sweet oranges, the trifoliate orange, the Rough lemon, some citrumelos, a few citranges, and some tangelos. The fact that sweet orange tops on these rootstocks continued to grow well despite the tristeza virus showed that these rootstocks tolerated the virus and that they are the most likely to be satisfactory for use in places where tristeza occurs.

The tests of the many citrus types and varieties as tops on sour orange rootstocks showed by the early occurrence of symptoms and decline of the plants that the sweet oranges were easily infected with the tristeza virus by means of the oriental black citrus aphid. The sour orange on sour orange rootstock, on the other hand, was difficult to infect by means of this aphid and most of such plants survived the repeated inoculations. On the basis of time it took for symptoms to show, the degree of tolerance and nontolerance of different citrus types varies greatly.

From the tristeza inoculations of seedlings, it was learned that certain varieties could show disease symptoms on their own roots among them were varieties of the West Indian lime, grapefruit, some tangelos, pummelos, and some acid lemons. The use of species and varieties of citrus that show symptoms of tristeza as seedlings helped in the study of behavior of different citrus types and in the development of faster methods for detecting the presence of the virus.

Among the interesting and important results of the investigations at the agronomic institute at Campinas were the finding of mild strains of the tristeza virus and the unexpected indication that plants invaded by the mild strains are protected from showing the striking disease symptoms caused by the severe strain of the virus.