Virus Diseases of the Chrysanthemum

Philip Brierley.

For more than 50 years florists have grown chrysanthemums in the greenhouse as potted plants and as cut flowers for autumn bloom, and amateurs have grown them as garden perennials. The garden chrysanthemum gained popularity with the introduction about 1935 of early-flowering sorts in a wide range of color and form.

Before the development in the 1930's and 1940's of techniques for controlling the time of flowering by adjusting the photo-period as well as the temperature, florists' chrysanthemums were seen only in the fall and the early winter months. Rooted cuttings were planted in the greenhouse in April or early May and grown on to natural flowering, which extended from September through January with a succession of early and late varieties. Precision timing of flowering enabled growers to produce cut flowers of chrysanthemums at all seasons. A great expansion in production resulted, and the chrysanthemum became one of the five leading florists' crops in terms of value to the grower. Acres of mums were produced in cloth houses out of doors. Production in greenhouses was expanded.

Together with those increases in volume and in efficiency of production, there appeared about 1945 a disease called chrysanthemum stunt, which threatened to ruin the business.

Chrysanthemum stunt was first described by A. W. Dimock, of Cornell University. He noticed the disease in florists' mums as early as 1945. He directed attention to the reduced size of plant, leaves, and flowers; the bleaching of bronze, pink, and red flowers to lighter shades; and a tendency to early flowering in plants affected with stunt. The disease became generally prevalent in the United States and Canada in 1946 and 1947. Infection reached 50 to 100 percent in many greenhouses, and affected plants were so short or so inferior that they were unsalable.

By that time the disease was familiar to most producers of florists' chrysanthemums, but its nature remained a mystery. The symptoms and the rapid extension of the stunt disease immediately suggested a virus as the causal agent, but growers who had not previously contended with any virus disease of major importance were slow to accept that explanation. Many ascribed the trouble to over-propagation, to the use of hormones in propagating, or to the lack of the normal winter rest period that mums were believed to require for normal growth.

Convincing evidence of the virus nature of stunt was presented by several workers in 1948 and 1949.

M. F. Welsh, at the Summerland Laboratory in British Columbia, produced a stunt-mottle disease, now known to include stunt and a mosaic disease, by experimental grafting. Floyd F. Smith and I found the stunt virus transmissible by grafting and by manual inoculation with sap from a stunt plant.

J. R. Keller, of Cornell University, confirmed our findings, showed that the yellow spotting in Mistletoe chrysanthemums is a symptom of stunt, and also transmitted the stunt virus from plant to plant by dodder connection. C. J. Olson, pathologist at Yoder Brothers, Inc., of Barberton, Ohio, discovered that contamination of healthy plants by the knife and hands in taking cuttings can transmit the stunt virus. He and I learned that contamination by the hands in pinching may effect transmission of the virus. Shears used in cutting flowers can also transmit it.

Olson presented evidence that stunt is not carried through the seeds of chrysanthemums. Earlier claims of transmission by insects have not been confirmed. Present evidence indicates that contaminations during commercial handling operations, such as taking cuttings, pinching, and cutting flowers, are responsible for all transmission of stunt in florists' mums. Even in garden chrysanthemums those contaminations during handling are of chief, and perhaps sole, importance in spreading stunt, for commercial propagators bring garden mums into greenhouses for increase during late winter and spring.

Symptoms of stunt are first expressed several months after contamination takes place. Most varieties show the first recognizable symptoms of stunt 6 to 8 months or longer after infection. Such a long delay is not uncommon in virus diseases in woody plants, but is exceptional in herbaceous plants, such as chrysanthemums, that make extensive and rapid vegetative growth.

This slow expression of stunt is an advantage to the grower of chrysanthemums who does not propagate his own plants. It is feasible to buy stunt-free cuttings, now available from specialists in propagation, and to bring them to flowering without taking precautions against stunt contaminations, because stunt expression is too slow to affect the quality of the first crop. Any contamination that took place during the production of the first crop, however, will be expressed in a second crop propagated from the first one. The propagator who is attempting to re-select stunt-free plants from partly contaminated stocks, therefore, must contend with recently contaminated Plants that seem perfectly normal but are stunt-affected.

Stunt was recovered from normal-appearing plants of the variety Mary MacArthur 1, 2, and 3 months after inoculation, although the plants did not show recognizable symptoms until after 6 to 7 months. Also some varieties of chrysanthemums express ill-defined symptoms or none even after longstanding infection.

Clearly some reliable method of detecting stunt is essential to any program of eliminating the disease from stocks of chrysanthemums.

Many methods have been tried. Microscopic examination of affected tissues failed to reveal any characteristic abnormalities. Studies of stunt tissues under the electron microscope by W. C. Price and R. L. Steere at the University of Pittsburgh and by James Johnson at the University of Wisconsin failed to detect any foreign particles of the types that characterize some other plant viruses.

An intensive search for plants that would express well-defined symptoms following manual inoculation has not been successful. All species of chrysanthemums that have been tested and a large number of other plants of the family Compositae are susceptible, but most of them produce no recognizable symptoms, although the stunt virus can be recovered from them in chrysanthemum. Only the florists' cineraria and Matricaria Golden Ball proved to be of some value as test plants; each became dwarfed and rosetted in 2 or 3 months after manual inoculation.

Such test plants that could be grown from seed were eagerly sought in the early stages of the stunt problem because of the difficulty of finding strictly stunt-free chrysanthemums. The need for them has diminished with the discovery of chrysanthemum varieties that express stunt symptoms clearly and relatively early.

Elimination of stunt from such varieties is a simple task. Mistletoe chrysanthemums, a group of florists' "standards" or large-flowering sorts, come in several flower colors and all react to stunt with distinctive yellow leaf spotting. Mistletoe varieties react in 4 to 6 weeks when inoculated by grafting. On manual inoculation, some stunt is expressed in 5 weeks, but it is necessary to hold the plants for at least 6 months for full expression. Blazing Gold, another florists' standard variety, expresses yellow vein banding 6 to 8 weeks after graft inoculation, and becomes typically stunted in habit later. Both Blazing Gold and the Mistletoe varieties are now used to detect stunt. Each has advantages in detecting mosaic diseases as well as stunt, as I explain later. Graft indexing is the standard procedure because of the more prompt and consistent expression of symptoms. For some purposes, such as property studies, manual methods of inoculation must be used. Mistletoe chrysanthemums are preferred for that purpose because of their distinctive expression of symptoms, but the long time required for full expression is a handicap.

The only method of controlling stunt that is known to be feasible is the reselection of healthy stock with suitable precautions against further contamination. Two systems of reselection have been used by different commercial firms with marked success.

Mikkelsen and Sons, of Ashtabula, Ohio, devised a system of reserving tip cuttings from the most vigorous plants, which are usually the healthy ones, for a propagation block, which is renewed each year. The next best cuttings are used for the flowering crop. All weak or questionable ones are discarded. The only precaution against contamination is to break off the cuttings instead of cutting them with a knife. This procedure makes use of the superior vigor of healthy shoots, and thus tends to eliminate other diseases that depress vigor as well as the stunt disease. The program, which is relatively simple and involves a minimum of records, has worked well for the Mikkelsens in supplying disease-free planting material for several acres of year-around chrysanthemums.

Yoder Brothers designed a program to eliminate stunt from the millions of plants maintained by them for propagation. The best plants selected in vegetative condition were later flowered to detect further stunt expression at the flowering stage, and they were even pruned to bring all shoots to bloom, with the result that additional partial infections, known as "splits , were detected. The Yoders have used paper shields, flamed tools, and sterilized soil to eliminate all possible hazards of re-contamination. The nucleus, or foundation, stock is maintained in a separate greenhouse and handled by a separate crew of trained workers as insurance against contaminations in handling. More recently, as suitable test varieties became known, graft indexing on Blazing Gold was adopted to speed recognition of stunt in new acquisitions. The foundation block, now free of stunt by all known tests, is a permanent one, which furnishes cuttings to the production line, where they are further increased. The success of such reselection has brought a sharp decline in the importance of stunt in the florists' chrysanthemums. Stunt-free cuttings of most florists' varieties are now available, but only a beginning has been made toward supplying similar reselected stock of the garden varieties.

Some attempts have been made to eliminate stunt from chrysanthemums by heat or by cold treatments.

Heat cure of virus disease is possible only when the virus is less tolerant of heat than the host plant, and that is true for a few viruses only. In tests by Yoder Brothers and also at the Plant Industry Station at Beltsville, the stunt persisted at all the temperatures that the chrysanthemums withstood. Some growers reported that stunt plants were cured if stock plants were wintered in outdoor frames and if cuttings were taken as early as suitable shoots were available in spring. In trials during three seasons at Beltsville, such wintering in outdoor frames retarded expression of stunt symptoms but failed to eliminate the stunt virus or to alter its final expression of symptoms.