of the disease was demonstrated and preventive Diseases and their control measures were developed by CES scientists in the 1930s. Clean planting stock was found essential to Edmond C. Calavan, Professor, Emeritus, prevention. Department of Pathology; Seymour D. Van Gundy, Professor, Tristeza, exocortis, and stubborn Department of Nematology; Joseph W. Eckert, Professor, A mysterious malady called “quick decline” Department of ; and began killing trees in southern California in Edward L. V. Johnson, Staff Research Associate, 1939. Within 25 years it caused the loss of three Department of Plant Pathology million trees, mostly sweet orange on gummosis- resistant sour orange rootstock. Some trees wilted quickly, others declined slowly and lost foliage. everal times in the past 75 years, California’s CES began a crash research program in the early S industry faced catastrophic losses from 1940s. J.M. Wallace and H.S. Fawcett showed that fruit and tree diseases. In every case, timely tristeza virus caused the disease, and R.C. Dickson research greatly reduced the damage. and colleagues found that it was transmitted in California by the melon aphid. Further research Gummosis and psorosis, old maladies determined that Troyer and Carrizo were Heavy losses of trees from gummosis (foot rot) in tolerant to tristeza, so these rootstocks were used 1900-15 alarmed citrus growers and stimulated extensively for replants and new orchards. their interest in research, thus providing impetus Tristeza was, for a time at least, brought under to the new Citrus Experiment Station (CES). substantial control. Recent spread of new strains Gummosis-affected trees turn yellow, decline, and of tristeza virus that cause severe damage to sweet die if the trunk or primary roots are girdled. The orange and trees on all rootstocks has gummosis outbreaks led, in 1913, to the appoint- stimulated additional studies at the Citrus Re- ment of a plant pathologist, H.S. Fawcett, to the search Center to contain the new threat. CES staff. Dr. Fawcett determined that phytoph- and rootstocks are, un- thora fungi were killing citrus bark near the soil fortunately, susceptible to exocortis, shown by level and were causing both the gummosis disease pathologists in the experiment station to be caused and brown rot of fruits, which were especially by a viroid, which is much smaller than any virus. destructive in orchards. Dr. Fawcett and Dr. Exocortis viroid causes stunting and bark scaling L. J. Klotz developed practical con- of these two rootstocks. It is spread by tools and trol measures with applications of Bordeaux mix- through grafting, but can be largely prevented by ture and surgical excision of lesions. the use of clean stock, sanitation, and resistant Dr. Klotz and colleagues subsequently worked rootstocks, such as sweet orange, grapefruit, and extensively on the life cycles of these water . molds, and refined brown rot control measures When CES was less than 10 years old, a strange using copper-bearing sprays. Sour orange root- stunting and fruit deforming disease, then called stocks were found gummosis-resistantand were sheepnose, appeared on navel oranges in the Red- soon extensively used in California. Recently, lands area. Growers found it was perpetuated by plant pathologists have obtained good control of propagation and called it stubborn, because af- root, trunk, and fruit infections of Phytophthma fected trees would not respond to treatment. CES spp. by treatments with the systemic fungicides, scientists and growers worked together to show its metalaxyl (Ridomil) and fosetyl-A1(Aliette). transmissibility. Nearly 50 years after its discovery, Gummosis is not the only potentially catas- several CES, U.S. Department of Agriculture trophic disease the California citrus industry has (USDA), and overseas scientists discovered that faced in this century. Psorosis (California scaly citrus stubborn disease is caused by a subbacterial bark), an incurable graft-transmissible disease organism new to science, the mycoplasma Spiro- destructive to oranges, grapefruit, and plasma citri, and that the stubborn organism also trees, though rare among the seedling trees of Cal- infects many ornamentals, vegetables, and weeds ifornia’s citrus industry more than a century ago, after transmission by beet leafhoppers and two became widespread and destructive in grafted of Scaphytopius (leafhoppers). Control is trees before 1900. Apparently due to virus infec- by prevention and by removal of stubborn trees. tion, psorosis caused bark scaling and death of in- ner wood, followed by gradual decline of affected The clean stock program trees. It remained the most important graft- The need for disease-free propagative budwood transmissible citrus disease in California until the was evident long ago, but efforts to find such 1940s, when it was overshadowed by tristeza. material were thwarted for many years by numer- Scraping the bark of lesioned areas delayed or ous symptomless carrier trees and the lack of tech- reduced tree damage by psorosis. Transmissibility niques for eliminating disease organisms from otherwise desirable trees. The first effective move toward a clean stock program for citrus was taken by the CES and the California Department of Agriculture in the 1930s, mnafter psorosis was found graft-transmissible. A registration program was established to identify parent trees from which nurseries could obtain

CR - 10 budwood free of the psorosis pathogen. This pro- to turgid citrus fruits. Recently, experiment station gram prospered until tristeza virus overran most researchers found that metalaxyl (Ridomil) erad- registered trees in the 1940s. With losses from icates phytophthora infections as well as hot water virus and other bud-perpetuated diseases mount- without the iqjury potential. ing in the 1950s, sought help Alternaria stem-end rot is a major factor limit- from CES in establishing a “Variety Improvement ing the storage period of . Bartholomew Program” to provide disease-free, true-to-name showed in 1926 that Altmnaria infected the stem budwood for increase by nurseries. The psorosis buttons of the fruit early in their development on registration program was reactivated quickly, but the tree and, at harvest, the was deeply it took about 10 years for the experiment station imbedded in the tissue, where it survived post- to produce trees that indexed free of all known harvest fungicidal treatment. Many buttons were diseases. infested, but the fungus attacked the fruit only Despite some problems with stubborn disease, after the buttons became senescent. W.S. Stewart expanded citrus registration and certification, now demonstrated in the early 1950s that postharvest called the “Citrus Clonal Protection Program,” treatment of fruit with 2,4-D delayed senescence has, thanks to strong support by the industry and and postponed the attack. Today, all lemons pro- excellent cooperation by the California Depart- duced in California are treated with 2,4-D in the ment of Food and Agriculture, Cooperative Exten- packinghouse to control alternaria stem-end rot sion, and USDA, provided a good supply of clean during storage. budwood for increase by nurseries during the past Work continues at the Citrus Research Center to 13 years. This goal was achieved only by develop- reduce losses caused by blue and green molds, the ing methods, or adapting those developed else- most serious market diseases of citrus fruits pro- where, for detection by indexing and elimination duced in California. These investigations have two of all pathogens present in desirable clones. The purposes- to prevent infection of injuries on the ongoing program at the Citrus Research Center is a fruit by Penicillium and to inhibit sporulation on joint effort of the departments of Botany and diseased fruit, thereby preventing spoilage of Plant Sciences and of Plant Pathology to discover sound fruit. Research was started in the 1950s to ways of eliminating and avoiding Phytophthora find a substitute for biphenyl, a postharvest fungi- and other fungi, psorosis, tristeza, stubborn dis- cide then severely criticized in European markets. ease, vein enation-woody gall, exocortis, cachexia, See-butylamine (2-aminobutane), discovered in ringspot, concave gum, infectious variegation, this program and released to the industry in the crinkly leaf, tatter leaf-citrange stunt, and others. early 1960s, has been widely used to prevent Thenno-therapy and shoot-tip grafting have been infection of lemons during storage and of oranges effective in eliminating pathogens. during ethylene degreening. During the past 15 Thus far, the clean trees have been successfully years, several new fungicides have been investi- maintained and the more important ones are es- gated, each more effective than its predecessor in tablished in the Lindcove Foundation Block east of preventing infection and inhibiting sporulation of Visalia. The California program has reduced citrus Penicillium. tree disease losses and has been used as a model The intensive use of see-butylamine, thiabenda- for similar projects in other countries. A compre- zole, and benomyl has selected strains of Penicil- hensive clean stock program is essential to the lium resistant to these fungicides, resulting in continued production of healthy citrus trees. their failure to control decay. Packinghouse man- agement strategies for controlling the resistance Postharvest decay, a costly mess problem are being actively investigated. Two new Decay of citrus fruits after harvest has caused fungicides, imazalil and etaconazole, not yet avail- substantial losses to growers and consumers for able for commercial use, can control strains of more than a century. The California citrus industry Penicillium resistant to fungicides now in use. estimated loss due to decay during 1979 at $84 Investigations at Riverside have shown that million. The major postharvest diseases of citrus etaconazole also effectively controls sour rot, a fruits are blue and green molds (Penicillium), disease not controlled by any existing commercial sour rot (Geotrichwm), brown rot (Phytophthora), treatment. and alternaria stem-end rot. Brown rot and alter- naria rot begin from infections of fruit on the tree; Some fungi are good for citrus blue and green molds and sour rot start from Mycorrhizae are beneficial fungi that grow in spores deposited in iqjuries. symbiotic association with roots and aid in the up- L.J. Klotz found that copper fungicides were in- take of many nutrients, particularly phosphorus. effective against brown rot if the fungus had These fungi are sometimes described as “biotic penetrated the peel, but submerging fruit with in- fertilizers,” because they can be partially substi- cipient infections in hot water (115°-1180 F) for tuted for high fertilization. Unfortunately, concen- two to four minutes killed the fungus. Various trations of methyl bromide used for fumigating modifications of this treatment have been used in citrus nurseries to kill soil pathogens are also lethal California packinghouses for many years to control to mycorrhizal fungi. brown rot, despite the potential for heat damage U.C., Riverside, researchers collected, screened, and selected the most efficient strain of Glomus fasciculatus, a mycorrhizal fungus associated with citrus. The relative dependencies of various citrus

CR - 11 rootstocks on mycorrhizae in fumigated low- root development and growth of young citrus nutrient soil were determined. Information from trees. Thomas also called attention to the danger responses in 26 soils was computer analyzed, pro- of distributing this nematode on nursery trees. ducing formulae for predicting citrus growth. A Some 30 years later, after the development of soil commercial production system for mycorrhizal ino- fumigation, the California Department of Food culum was developed recently and has been and Agriculture established a nursery certification adopted by one California nursery. program, which continues to ensure the produc- tion of clean planting stock. Citrus nematode Although Thomas showed the importance of Since the citrus nematode, Tylenchulus semi- citrus nematode, no means were available for con- penetrans Cobb (slow decline), was first dis- trolling it on bearing trees and little attention was covered in Los Angeles County by J.R. Hodges in focused on this problem until 1912, the CES has been the international center Richard C. Baines joined the experiment station for research on its biology and control. Nathaniel in 1947. At about that time, the chemicals A. Cobb, who had just joined the Bureau of Plant 1,3-dichloropene (1,3-D) and ethylene dibromide Industry in Washington, D.C., immediately des- (EDB) were discovered to be effective soil fumi- cribed this species and organized an international gants for the control of nematodes in pineapple. survey, which established that this pest was Baines seized the opportunity to study these and worldwide in distribution. He used this example of other chemicals for control of the citrus nematode. a plant parasitic nematode to draw attention to During the 1950s and the 1960s the station con- the scientific and economic importance of soil- ducted two major interdisciplinary programs to inhabiting nematodes to agriculture and soon find solutions to the “citrus replant” and the established the first Nematology Laboratory. ‘‘citrusgrove rejuvenation” problems. The Results of a thorough study by Edward E. research by Baines and his colleagues in Nema- Thomas of the CES, completed in 1923, demon- tology, Plant Pathology, Plant Sciences and Soil strated that the parasite was widespread on citrus Sciences clearly demonstrated that these problems rootlets in California and that it greatly retarded could be solved by control of the citrus nematode by soil fumigation and use of tolerant rootstocks. The citrus nematode is a semi-endoparasitic worm, feeding internally in citrus roots while a major portion of the body remains external to the root surface. Severely infected rootlets may con- tain as many as 5,000 females per gram. Each fe- male produces 100 to 200 eggs, which hatch into larvae that reinfect the spring root flush. Feeding by the nematodes reduces the number of new root tips, decreases uptake of nutrients and water, and increases the root’s susceptibility to soil fungi. During the late 1940s and early 1950s, Baines showed that young nematode-free citrus trees replanted in heavily infested citrus orchard soil were stunted as much as 60 percent when com- pared with trees planted in fumigated soil. Fumi- A. Phytophthora gummo- gation of citrus soil before replanting is now sis, the worst fungus standard practice throughout the California citrus disease of California areas. citrus trees. In the search for nematode resistance in citrus species and close relatives, CES scientists iden- 6. Indexing for tristeza virus. Disc from leaf of tified the trifoliate orange as highly resistant to candidate tree is placed the citrus nematode and to Phytophthora. They in Mexican , which tested and released the Troyer citrange, now a will develop symptoms if widely used rootstock in California and other candidate is infected. citrus growing regions. In about 1950 Baines also pioneered in the de- C. The first certified velopment and use of the soil fumigant, citrus nursery tree pro- 1,2-dibromo-3-chloropropane(DBCP) on produc- duced in California and ing citrus. DBCP was the first nematicide that its developers in 1970: D.A. Newcomb, S.M. could be used around living , and it im- Mather, W. Reuther, E.C. proved growth and production of citrus by 10 to Calavan, H.W. Duncan. 32 percent. Unfortunately, use of DBCP was can- celled in 1977, a loss that caused major concern to D. Small, misshapen the citrus industry and a renewed research effort fruits caused by stub- at the University for new chemical and biological born disease, compared alternatives. with normal orange.

E. Spiroplasrna citri, cause of citrus stubborn disease.

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