If"'"*. Division of Agricultural Sciences UNIVERSITY OF CALIFORNIA ^jhsfr? ..,.. VIRUS AND VIRUSLIKE DISEASE! OF CITRUS ~\ L. J. KLOTZ E. C. CALAVAN L. G. WEATHERS ^m*-^ - CALIFORNIA AGRICULTURAL Experiment Station Extension Service , CIRCULAR 559 CAECA 559, 1-44, (1972) Virus diseases . . . are a threat to California's citrus industry. They are less readily identifiable than some other types of plant diseases, and treatment for affected trees consists largely of preventive rather than curative measures. This circular . . . lists the major virus and viruslike citrus diseases, based on recent research by workers in citrus-growing areas around the world. It describes symptoms and indicates possible control meas- ures. Illustrations are included, for help in identification, and a table is also provided for easy reference to specific diseases. JANUARY, 1972 The Authors: L. J. Klotz is Professor of Plant Pathology, Emeritus, Riverside. E. C. Calavan is Professor of Plant Pathology and Plant Pathologist in the Experi- ment Station, Riverside. L. G. Weathers is Professor of Plant Pathology and Plant Pathologist in the Experi- ment Station, Riverside. VIRUS AND VIRUSLIKE DISEASES OF CITRUS Diseases caused by viruses and myco- plasmalike bodies are among the greatest threats to citrus. Viruses consist of either ribonucleic acid (RNA) or deoxyribo- nucleic acid (DNA), usually surrounded by a very thin protein coat. Mycoplasmas resemble small "L" (irregularly shaped) forms of certain bacteria, and are thou- sands of times larger than viruses. Myco- plasmas contain both RNA and DNA, and have a complex internal structure, includ- ing ribosomes, all enclosed within a mem- brane. Mycoplasmas reproduce them- selves, whereas virus replication is an activity of the infected host under the in- fluence of the virus. Viruses are incapable of reproducing themselves in vitro. Re- cent evidence suggests that stubborn dis- ease (34)* and greening disease (41), long considered to be caused by viruses, may instead be caused by mycoplasma- like bodies. Mycoplasmalike diseases and virus diseases are graft-transmissible. (Certain other diseases with viruslike symptoms, but apparently not transmis- sible by grafting, are discussed at the end of the text.) The citrus industry is being greatly benefited by international cooperation in exchange of information on the culture and diseases of citrus. In 1957, the Inter- national Organization of Citrus Virolo- gists was formed at Riverside, California. Since then, the group has held its con- ferences in several of the world's citrus- growing areas, and has published its pro- ceedings and accounts of current research (23, 52, 53, 54, 74) . The first conference, in 1957, was held in California. Follow- ing ones have been held in Florida, Brazil, the Mediterranean countries of Italy, France, Spain, and Morocco, and in Japan, Taiwan, and the Philippines. The control of virus and mycoplasma- like diseases of citrus is achieved prin- cipally by the planting of trees that are disease-free and either tolerant of or rarely susceptible to infection under field conditions. While occasional transmission through seed has been noted for some virus diseases, the use of nucellar seed- lings is still an important means of free- ing a desirable citrus variety from de- structive viruses. Heat therapy, tissue culture, and chemicals are also useful in obtaining propagative stock free of graft- transmissible diseases. Citrus registration and certification programs, pioneered in California and designed to secure the best disease-free propagative materials, are being put into effect in much of the citrus-growing world. Citrus tree regis- trations and certifications in California are processed by the Nursery Service of the California Department of Agricul- ture, Sacramento. VIRUS DISEASES PSOROSIS Psorosis, also called "scaly bark" in Cali- fornia, is worldwide in distribution. It should not be confused with leprosis, which is called "scaly bark" in Florida (23, 70) , where psorosis also occurs. The different forms of psorosis and their pos- * Numbers in parentheses refer to "Literature citrus virus diseases and some comprehensive or sible relationships have been discussed elsewhere (20, 23, 30, 31, 36, 73, 74). Psorosis virus causes symptoms on leaves as well as on the bark. On leaves, many small, elongated, light-colored areas occur in the region of the small veinlets (fig. 1) . On young, tender leaves not only the Cited," in which many general publications on special articles on certain diseases are listed. [3 -«**-. Fig. 1 . Psorosis symptoms (upper) on sweet orange leaves; (lower) on lemon leaves. veinlets themselves, but also adjacent tis- sue may show faint to pronounced clear- ing. These small, cleared places, about 1 to 3 mm long and % to 1 mm broad, may be numerously scattered over the entire blade, or may occupy only certain por- tions. Sometimes only a small percentage of young leaves shows these symptoms, but at other times a majority will show them. Often the pattern is not distinct; [ spots either fade out gradually at the margins or run together. Under hot sum- mer conditions the flecks fade and are difficult or impossible to detect. In some specimens only the clearings along the veinlets are apparent. To see these symptoms most readily, observe young fourth- to half-grown leaves shaded, but with the light of the sky coming through them. Such symptoms are found in trees affected by different strains or varieties of the virus that have several degrees of virulence. Great caution is necessary to avoid mistaking injuries for psorosis symptoms. Thrips, aphids, mites, small hailstones, or minute sand grains driven by wind may all produce markings of similar size on young leaves. Occasionally symptoms occur on ma- ture leaves and fruit (fig. 2), especially in advanced stages of the disease. On water sprouts, leaves, and fruit, these appear as circular spots or rings that may become sunken and necrotic. Psorosis is indicated by at least two types of bark symptoms (fig. 3) : a lo- calized type and a rampant type, which is rare. Similar young-leaf symptoms ac- company both types and, especially with the rampant form, some leaves may show large blotches or rings that may become necrotic. Necrotic rings on fruit are oc- casionally found associated with psorosis. The more common type usually begins either as scales of bark, with or without gum formation, or as aggregations of small pustules under which are brown specks. The scales of outer bark are dry. irregular flakes, 1/12 to 1/8 inch thick, with live, tan to buff-colored bark under- neath. This form usually occurs first in localized areas on some of the older bark of trunks or limbs of trees six to 12 or more years of age. As the scaling ad- vances, the deeper layers of bark and even the wood become visibly affected, even though still alive. Small or large amounts of gum often form, depending 4] ^^^ 4 ^B w r ? ,v-- 11 1 sTT 1 ■ jjl W J t::!,,,:- ■■■;';•"■.... » .*4C .*•"<* ^ 1 Illl j& *v3 ■ IHk i%» 1 ■ ■ ifl ' .' "'"'"■" "■■'■'- '4 "■' v ^ :V V\ p Fig. 2. Psorosis ring-type symptoms on navel orange fruit and on grapefruit leaves. [5 MJ& Fig. 3. Psorosis (scaly bark) localized form (left) and rampant form (right) on sweet orange. on weather and growth conditions. The rate of scaling varies on different trees. After the lesion has been present for some years, gummy deposits occur be- neath the bark and between the growth layers of wood. Later the wood dies and becomes light drab to brown or reddish- brown; the discoloration progresses in an irregular fashion, not necessarily fol- lowing the grain of the wood. The af- fected portions of the tree then deterio- rate rapidly and have only a few small, yellow leaves. The anatomy of psorosis lesions has been described {20) . The rampant type of common psorosis occurs infrequently, and differs from the usual, more localized type by showing gum formation in advance of, rather than after, scaling. It also may show a rapid advance of scaling in a continuous strip or area, usually along one side of the trunk or branch and even into much smaller limbs and twigs than is normal for the common form of psorosis. The rampant type probably is not caused by a distinct strain of psorosis virus, for it can be produced by grafting a piece of bark from a localized psorosis bark lesion into a healthy orange tree (73). No treatment other than pruning or tree removal is known for advanced pso- rosis. Treatment of beginning bark le- sions of psorosis consists of scraping the bark, only before the tree shows any vis- ible deterioration in the top, in order to prolong its usefulness (28) . No perma- nent cure is known. After noticeable de- terioration has set in, it is not as a rule profitable to treat the malady. When lesions are small, not larger than one's hand, scrape deep enough to eliminate discolored layers. Scrape surrounding bark, not visibly affected, for a distance of 6 to 8 inches above and below and 4 to 6 inches on each lateral margin. To disinfect the scraped area, use either po- tassium permanganate — about 1 per cent or 1 teaspoon of crystals to a pint of water — or other safe disinfectant. If scraping is done in dry weather it is not necessary to treat the scraped area, but the scraping tool should be disinfested before each tree is treated to avoid spreading other virus or fungus diseases. Declined branches may be pruned out. In scaling areas covering more than one- third the circumference of the trunk, it is not possible to scrape deeply enough to eliminate all discoloration. As soon as deterioration of the top begins, further treatment is usually uneconomical. A rapid chemical treatment for scaly bark developed in 1944-1946 was abandoned because its use necessitated extreme care to avoid injuring healthy bark and be- cause production of the chemical "dini- tro" (dinitro-o-cyclohexylphenol) was stopped (36) . Scraping or chemical treatment appar- ently delays the staining and plugging that cause rapid deterioration of the tree, but precise data for effects of treatment on production are not available. The obvious step in controlling pso- roris and some other virus diseases of citrus is to use only virus-free plant ma- terials for propagation. This does not assure the grower that trees will remain free of all virus diseases, since insect vectors can carry some viruses that may infect even carefully selected materials. The method is effective, however, against psorosis and other diseases that are trans- mitted mostly by union of living tissues, such as artificial budding and grafting, or natural root grafting, and against vec- tored diseases in areas where vectors are absent. Psorosis virus is rarely transmit- ted through seeds or by root grafting, and apparently has no vector in Califor- nia. In Argentina, eruptive gummosis, a disease with symptoms similar to those of psorosis, appears to be spread by an unknown vector (23). The infrequency of psorosis virus transmission by natural root grafting is indicated by an experi- ment in which a row of psorosis-affected trees set out at Rancho Sespe, California, 40 years ago, at the normal planting dis- tance of 22 feet from a row of healthy trees, has not yet transmitted the disease to the latter. Many nurserymen, under the procedure specified by the California Department of Agriculture, produce and sell trees from budwood sources registered or cer- tified as apparently free of psorosis and several other viruses. Registration is based on absence of the leaf symptoms described above and of the psorosis bark disorders described in the following pages, and indexing, on sensitive indi- cator plants, for psorosis (24) and other viruses. Planting only trees known to be free of any forms of psorosis virus is the way to avoid the losses caused by this important group of maladies. BLIND POCKET Blind pocket, until recently, was re- ported only in California (35) but is now known to be in Florida (51) and Brazil (53, 57), and is very common in Chile (60) and in some orchards of the [7] Fig. 4. Blind pocket disease of sweet orange. Mediterranean basin (6) . It is associ- ated with young leaf symptoms similar to those seen with common psorosis. Blind pocket has two forms, one with plain blind pockets in bark and wood; in the other the concavities are accompanied by course, psorosislike eruptions. The erup- tive form may result from infection by two or more viruses of the psorosis group. Blind pocket usually differs from con- cave gum disease (see page 11) in that it has narrower, more abruptly de- pressed, troughlike regions, frequently with two almost straight or even convex sides coming together at an acute angle at the bottom and top (fig. 4). Some cases show longer or shorter depressions with less abrupt slopes more nearly re- sembling the concavities of concave gum disease. Under each depression is an ocherous-salmon core of tissue that even- tually is impregnated with a hard, gum- [8] like substance. Only rarely is gum forced out to the surface from these blind pock- ets. Within an area occupied by several blind pockets an eruptive lesion may oc- casionally occur, somewhat resembling a lesion of psorosis, but with thicker bark scales. No effective treatment is known for blind pocket. CRINKLY LEAF AND INFECTIOUS VARIEGATION It is generally agreed that crinkly leaf and infectious variegation are caused by strains of the citrus infectious variega- tion virus. Crinkly leaf has been found especially in lemon trees. In addition to the fleck- ing in young leaves characteristic of pso- rosis, blades of mature leaves show warp- ing and pocketing on certain branches or over the entire tree (fig. 5) . The fruit is frequently, but not always, coarse, rough, and misshapen on affected trees or branches. In severe cases, fruits are covered with irregular bumps. Somewhat similiar temporary effects may result from improper nutrition, scarring by the Botrytis fungus, or from mites, aphids, or other insects. Another type of rough- ened fruit appears to be an inherent bud variation. Workers in several countries have reported that purified preparations of citrus infectious variegation or crin- kly leaf virus are highly infectious (6, 20,23). Infectious variegation has been found a few times associated with a crin- kly leaf condition of lemons (fig. 5). Portions of the leaf blade of some leaves lack green, and are white to yellow. In some leaves the chlorotic areas are en- tirely on one side of the midrib and in others they are scattered over the entire blade but not arranged in any definite pattern. Some leaves near affected ones appear entirely normal. The young leaves also show flecking symptoms like those of psorosis. The virus strains causing infectious variegation and crinkly leaf have been [ transmitted by budding to healthy lemon, sweet orange, and sour orange trees. Trees that have crinkly leaf or infectious variegation should not be topworked be- cause the virus will enter the new scion and produce the same effect in the new top. Infectious variegation virus has been transmitted mechanically from citrus to other citrus and to herbaceous plants (6, 35) . Sap inoculations with a mixture of infectious variegation and psorosis viruses transmitted only infectious vari- egation (26) . SATSUMA DWARF This disease is of economic importance on citrus in Japan (23, 53) . Many leaves of affected trees are abnormally small and narrow, and curled downward along lateral margins. Shortened internodes of twigs produce a dwarfed, bushy effect. Environment influences the type of leaf symptoms produced. Narrow, boat-shaped leaves are produced at cool to moderate temperatures (24), whereas small, dwarfed leaves (spoon-shaped) are pro- duced at warmer temperatures. The small fruit is of poor quality with thickened rind at the stem end. These symptoms appear only on the spring flush of growth, not on the summer and fall flushes. The virus is readily transmitted to healthy citrus by budding and graft- ing. It is also mechanically transmissible from extracts of infected citrus and her- baceous hosts to healthy plants of host species. A number of legumes and white sesame are good indicator plants, show- ing, after a few days, chlorotic spots which become necrotic, with a yellowing halo. Infection then spreads into the mesophyll and kills the leaf. While the tristeza virus (p. 13) is gen- erally demonstrably present in Satsuma trees in Japan, Satsuma dwarf virus can usually be separated from it by passing inoculum from Satsuma dwarf-affected trees through trifoliate orange, which is resistant to the tristeza virus but suscepti- 9] Fig. 5. Crinkly leaf and infectious variegation: top, sour orange; bottom, lemon. ble to the Satsuma dwarf virus. This in- dicates that Satsuma dwarf disease is caused either by a distinct virus or by that virus together with tristeza virus. Moreover, while Satsuma mandarin in Japan is generally a carrier of tristeza virus, the Satsuma dwarf disease is rela- tively uncommon in Japanese plantings. [10 Fig. 6. Concave gum disease symptoms: (left) on trunk and branches of sweet orange; (right) on orange leaves. Possible relationships between Satsuma dwarf virus and citrus infectious varie- gation virus are suspected (20) . CONCAVE GUM DISEASE Concave gum disease, reported in many countries, may show symptoms similar to those of common psorosis on young leaves — that is, small, clear areas or flecks in the region of the small veinlets. The relationship between concave gum virus and psorosis virus may not be as close as originally believed (23, 53). The oakleaf or watermark pattern is a distinguishing symptom (fig. 6). Most conspicuous are the broad concavities of various sizes on the trunk or limbs formed by the arrested or retarded growth of wood tissue in localized re- gions (35, 62, 82). These are for the most part covered with normal bark, with a crevice or crack through which gum may ooze to the surface at certain seasons. Under the bark of these con- cavities are masses of gummy, granu- lated tissue often cinnamon to tawny or [ii] russet in color (28). The underlying layers of wood, which are usually thin- ner than normal, are impregnated with a semiliquid to cheesy or gummy sub- stance. A few to many successive gum- filled layers of wood, alternating with layers of nearly normal wood, are found. The injurious effects may develop slowly over many years, but in time numerous lesions on a tree may result in serious deterioration. No effective treatment is known for concave gum disease. DWEET MOTTLE When a certain selection of Cleopatra mandarin (Citrus Research Center #270) was indexed on Dweet tangor it was noted that leaves of the latter devel- oped a type of mottle that slightly re- sembled some patterns caused by psorosis Fig. 7A. Below: Tristeza (quick decline) of Valencia orange on sour orange. or concave gum viruses (23). However, the mandarin, which showed none of these three types of symptoms, had twig dieback and produced little new growth and only small fruits. Further indexing with approved indicator plants showed that the mandarin was free of other known viruses except a mild strain of exocortis. Other common commercial citrus vari- eties inoculated with Dweet mottle virus showed no symptoms but could act as carriers. When plants were inoculated with both the Dweet mottle virus and any other citrus virus, symptoms of the latter were not increased. Moreover, since Dweet mottle virus did not protect sweet oranges against psorosis, concave gum disease, and in- fectious variegation-crinkly leaf viruses, and visibly affected only Dweet tangor, it is considered distinct from any pre- viously reported. However, Dweet mottle virus has not yet been observed causing damage to commercial citrus. TRISTEZA (QUICK DECLINE) of SWEET ORANGE on SOUR ORANGE and CERTAIN OTHER COMBINATIONS The malady now known as tristeza, also called quick decline or bud union de- cline, or podredumbre de las raicillas, has been killing trees in California since as early as 1939 (5). By 1942 it was noted that the affected sweet orange trees were on sour orange rootstocks. In the early days of the industry in South Africa and Java, failure of trees on sour orange was thought by some to be a mat- ter of horticultural incompatibility. Later, in South America, the fact that sweet orange on sour orange stock ap- peared to do well when grown in glass- houses, but soon failed when placed out- doors, led investigators to believe that the trouble was caused by a virus carried by insects. The nature of the disease was indicated when the virus was transmitted [12] in Brazil by means of the aphid Toxop- tera citricidus, and in California by tis- sue grafts and by the cotton or melon aphid (Aphis gossypii) (27). In Florida, A. spiraecola and T. aurantii were also found capable of transmitting the virus (48, 51), and other vectors have been reported from India (20) . Flexuous, threadlike rods, about 10 to 12 nm x 2000 nm, are consistently present in the phloem of tristeza-infected citrus and are believed to be the cause of tris- teza (2, 23) . The existence of different strains of tristeza virus has been reported by several workers (23, 53, 74) . The disease has caused serious losses of susceptible citrus throughout much of the world with the exception of most countries in the Mediterranean basin, Mexico, and several countries of Central and South America. It is present world- wide, however, in most Meyer lemon trees and in certain tangerine selections. The infected trees in some countries and in some major areas of Arizona and of California, such as the San Joaquin and Coachella valleys, are being eradicated. Because of the high proportion of trees on sour orange rootstock in the Mediter- Fig. 7B. Below: Tristeza symptoms on leaves (top) and wood (right) of Mexican lime indicator plant. Bottom, seedling yellows of Eureka lemon. Three seedlings at left are diseased; healthy control plant at right. [13] ranean areas, the disease could cause calamitous losses there. It has already caused losses in many orchards in Spain. Estimates indicate that tristeza destroyed about 25 million trees on sour orange in South America and about 3 million in southern California. Symptoms of trees with tristeza (fig. 7A, B) are similar to those of trees in which roots have been injured or killed either by girdling due to gophers or by oak root fungus (Armillaria) , or dam- aged directly by waterlogging, high con- centrations of fertilizer, by kerosene or orchard heater oil, or by plant-growth regulators. The first noticeable symptom in the aboveground parts is a dull, ashen color and curling of the leaves lengthwise and upward (3). In the early stages, affected trees frequently have a large crop with many inside fruits. Diseased young trees usually begin to fruit one or more years before healthy trees of the same age. New growth in the fall is sparse, and navel orange fruits develop high color more rapidly than do fruits from healthy trees. Below-ground symptoms precede those above ground. Even before anything ab- normal is evident in the top, the small, fibrous roots at the periphery of the root system die, and their bark sloughs. Even in the early stages, the iodine test reveals a reduction in and, frequently, disap- pearance of starch in apparently other- wise unaffected roots. The process of starvation and destruction of roots pro- ceeds from the tips inward toward the trunk of the tree, affecting more and larger roots. Microscopic examination (20, 63) reveals that the primary diag- nostic symptom of tristeza is the presence of darkly staining material in the clear cytoplasm of parenchyma cells, called chromatic cells, adjacent to the sieve tubes (food-conducting tubes). Next, these food-conducting tubes in sour orange bark near the bud union are de- stroyed, which accounts for symptoms resembling girdling. At some stage fol- lowing destruction of sieve tubes, symp- toms begin to appear in the top. Generally the deterioration in the top is a gradual curling, wilting, and droop- ing of leaves and dying back of twigs, the process apparently keeping pace with root destruction. Frequently, however, during periods of low humidity, particu- larly those accompanied by a soil-water deficit, the trees (especially young ones) will collapse, and the leaves suddenly wilt and dry on the tree. This effect suggested the name "quick decline." Most trees so affected die. Others affected with the chronic form of the disease continue to produce. They retain too few functional sieve tubes for normal growth, however, but are able to live, commercially unpro- ductive, for several years. The leaves and roots make feeble growth. Starch reap- pears in the roots if new, functional sieve tubes are formed. Another symptom fre- quently found is a netting, pinholing, or honeycombing of the inner bark of the sour orange rootstock of affected trees. The symptom is indicative but not diag- nostic for tristeza. A good indicator plant for diagnosis of tristeza is Mexican lime (24) . When seedlings of this are budded with bud- wood from an infected tree, some of the newly forming lime leaves develop fleck- like vein clearings readily seen by trans- mitted light. The diseased leaves are also often cupped and chlorotic (fig. 7B). Wood of affected lime stems develops pits and grooves (74) (fig. 7B) . Similar stem pitting is caused by tristeza virus in many citrus varieties, including Pera sweet orange (53) . In addition to quarantine, suppressive measures, and propagation only from tested, disease-free trees in clean or lightly affected areas, the only practical suggestion for control known at present is to avoid using sour orange and other susceptible rootstocks for sweet orange varieties, grapefruit, or tangerines. Sus- ceptible rootstocks include Citrus macro- phylla, sweet lime, citremon, grapefruit. [ 14 some tangelos and shaddocks, and, in some areas, citranges and trifoliate orange. C. macrophylla, now one of the most popular rootstocks for lemon in California, is highly susceptible to tris- teza and, when exposed to aphids carry- ing tristeza virus, is likely to acquire the virus in the seedbed or nursery. Preven- tion consists of use of virus-free bud- wood, production of seedlings and nur- sery trees in tristeza-free areas, and prompt removal of C. macrophylla suck- ers from orchard trees. In some areas, where the virus is infrequently found in lemon trees, the infected lemon trees should be eliminated (8) . The rootstocks now in use for orange trees in areas where tristeza is present include sweet orange, Cleopatra manda- rin, Rough lemon, Troyer and Carrizo citranges, trifoliate orange, and Rangpur lime (in South America). Of these, only the trifoliate oranges show much resist- ance to Phytophthora gummosis, foot rot, and root rot, which are of great impor- tance especially where basin and flooding types of irrigation are practiced. Troyer citrange is intermediate in resistance to Phytophthora infection. The resistance of some trifoliates to both tristeza and Phy- tophthora offers a solution, provided scion budwood free of exocortis virus can be obtained. Some trifoliate selections, however, are known to be very suscepti- ble to lime-induced chlorosis. Recently Troyer and some other citrange root- stocks have shown considerable suscepti- bility to tristeza in certain citrus areas of California (12). Use only true-to-type seedlings of trifoliate and citrange selec- tions known to be tristeza-resistant in any tristeza-infested areas where the trees will be planted. The performance of 77 tristeza-resistant rootstocks in Brazil has been reported (53). Heat treatment was successfully used to obtain tristeza virus-free budwood in Florida and California experiments (74) . New branch growth free of tristeza and psorosis viruses was secured by exposing infected Mexican limes to 95° to 110°F in a heat chamber for 40, 78, or 107 days. Young tissue free from the tris- teza-seedling yellows virus complex was obtained from lime seedlings grown for four weeks at 100° to 104°F (74). This virus complex has recently been elim- inated from some plants of Meyer lemon and some other selections by heat treat- ment (54). Seedling yellows is a virus disease found only in association with tristeza, and may be caused by one or more forms of the tristeza virus (74). It causes a stunting and chlorosis of seedlings of sour orange, grapefruit, Eureka lemon, and citron (45, 72, 74) (fig. 7B). Leaves of severely affected plants are small, green- ish-yellow in color, and remain under- developed. Internodes of the stem and shoots are short, and multiple buds may appear at the nodes. The virus that pro- duces these effects on the seedlings ap- parently occurs naturally in sweet orange and mandarin trees affected by tristeza in Australian orchards, and can be trans- mitted to seedlings by grafting. The or- ange and mandarin trees that were reser- voirs for the virus suffered no serious injury if they were on their own roots, but were damaged if they were on sour orange or grapefruit rootstocks. Under natural conditions for infection by an in- sect vector, lemon as a scion escapes severe injury. South African and American investi- gators offered the possible explanation that tristeza is caused by two disease- producing entities, one that causes the tristeza stem pitting and one that causes stunting and yellowing of the seedlings. In Australia the seedling yellows virus is known to be generally present in sweet orange and mandarin orchards of coastal New South Wales (23, 74) ; in California it has been found in Meyer and South African lemon, Satsuma and some other mandarins, Waialua orange, and kum- quat (72) ; and it is widespread in Japan (81). Sweet orange trees naturally in- [15] 9H ■ Fig. 8. Hassaku dwarf — effect on Mexican lime seedlings. A and B, vein clearing; C, stunted seedlings; D, vein corking and cupping of leaves; E, healthy seedlings; F, stem pitting. (Photos by Dr. Shoichi Tanaka.) [16] fected by seedling yellows virus have not been found in California. While control measures suggested for tristeza should also apply here, it is rec- ommended that propagation from seed- ling yellows trees be avoided in North American, Mediterranean, and other areas where the virus is not already well established in commercial plantings. HASSAKU DWARF This disease (fig. 8) of Citrus hassaku differs from Satsuma dwarf (p. 9) in that it does not produce symptoms on legumes or sesame, but causes vein cork- ing and stem pitting and retards growth of Marumera (C. obovoidea) (53). Leaves of diseased trees are small, chlo- rotic, and wrinkled, and the leaf margins fold upward, producing a spoonlike ap- pearance. Bark of branches and trunk be- comes rough and bumpy and develops vertical concavities, with corresponding pitting in the wood. Mexican lime plants grafted with material from dwarfed Has- saku trees develop vein clearing, vein corking, and stem pitting (67), indicat- ing that the disease may be caused by a strain or complex of tristeza virus prob- ably similar to that involved in stem pit- ting of grapefruit (30, 31, 38, 47, 53). (See table 1.) C. hassaku on the resistant trifoliate rootstock is very susceptible, and on Rough lemon, severely stunted, possibly implying that a pathogen in addition to tristeza virus is involved. The Hassaku dwarf pathogen spreads in the orchard and apparently Toxoptera citri- cidus transmits it to various species of citrus (20, 47) . It is obvious that pro- pagation from Hassaku dwarf-affected trees should be avoided. VEIN ENATION and WOODY GALL Vein enation and woody gall are caused by a virus that has become widespread in citrus in southern California except in the eastern section (75, 76). The symptoms that give the disease its name are the small enations or lobes of tissue Fig. 9. Woody gall, vein enation on Rough lemon. (Photographed from specimens supplied by J. M.Wallace.) or galls that develop on the undersides of leaves, with corresponding depressions on the upper surfaces, and the gall-like growths that form on the roots, trunk, branches, and twigs. The vein enation symptom is rarely seen except in young plants, and woody gall is not common in most orchards, although under some con- ditions large woody galls develop near the bud union on rootstocks of Rough lemon and Citrus volkameriana (fig. 9). Such galls are common on Rough lemon rootstocks in Peru (20) . Woody galls are characteristically lightly pitted on the cambial surface of the wood by numerous undeveloped or latent buds and, if above- ground, the cambial surface is light green. The galls tend to form near thorns and at graft unions or wounds on sus- ceptible plants (24) . The green peach aphid, Myzus persicae, and the cotton aphid, Aphis gossypii, are vectors (24, [17] Table virus and mycoplasmalikt: Disease (common name) Literature* Symptoms Indexing plants 4 -. PSOROSIS (Scaly bark) 20, 23, 24, 36, 73,74 Clearing flecks along veinlets; local or gen- eral bark lesions, occasional ring type marks on mature leaves. Sweet orange, mandarin, Mexican lime, C. excelscf sour orange BLIND POCKET 35,53 Abrupt concavities on trunk ; occasionally coarse shelling lesions. Mandarin, sweet orange, lemon ^ CRINKLY LEAF 20,23 Distorted crinkled leaves; flecking and stip- pling in young leaves. Mandarin, sweet orange, sour orange, lemon r-4j INFECTIOUS VARIEGATION 26,35 See crinkly leaf; plus variegation in leaves. - Mandarin, sweet orange, sour orange, lemon A SATSUMA DWARF 20, 23, 24, 53 Leaves bent downward, boat-shaped or cupped (spoon-shaped) ; psorosislike leaf symptoms. Sesamum indicum CONCAVE GUM 23,53 Oak-leaf pattern and flecks in young leaves, concavities on trunk. Mandarin, sweet orange - DWEET MOTTLE 23 Psorosislike mottle on leaves. Dweet tangor TRISTEZA (Quick decline) 2, 5, 8, 12, 23, 24,27,30,31, 45, 48, 53, 54, 63, 72, 74, 81 Veinlet clearing in young leaves; necrotic sieve tubes at bud union; honey-combing (inverse pits) ; decline of top. Pits in wood of lime. Chromatic cells in various hosts. Mexican lime, C. macro- phylla ■ -4 -*- SEEDLING YELLOWS 23, 45, 72, 74, 81 Stunting and yellowing of foliage of sour orange, grapefruit and lemon; stem pitting of Mexican lime. - --i Lemon, sour orange, grape- fruit, Mexican lime STEM PITTING 23, 38, 47, 53 Pits and grooves in wood of trunks and branches; decline of top with small mottled chlorotic leaves; tree stunted; small acid fruit, low production. Grapefruit, Mexican lime * HASSAKU DWARF 20, 47, 53, 61 Small, pale, upfolded leaves; furrows or concavities on bark; stem pitting. Marumera (C. obovoidea) and Mexican lime VEIN ENATION, WOODY GALL 20, 24, 42, 44, 75, 76 Undersurface of veins with small projections (enations) ; corresponding concavities on upper surface of young plants; woody galls on trunk, branches, and roots. Enations and galls on sour lime, C. volkameriana, some mandarin-limes, Rough lemon. Enations only on various other / hosts. . *-% "See " Literature Cited," p. 39. [18 1 DISEASES OF CITRUS Distribution Vector Other means of transmission Varieties attacked Control Worldwide None yet found Budding, grafting, Leaf and bark symptoms; Use disease-free budwood and »- natural root sweet orange, grapefruit, rootstock. Scrape lesions grafting, sap, mandarin, tangelo; and remove bad branches. ^ dodder only leaf symptoms + on most others Worldwide None yet found Budding, grafting, Sweet orange, lemon, Use disease-free budwood and natural root mandarin rootstocks. grafting -►Worldwide None yet found Seed (rarely), bud- Sweet orange, lemon, sour Use disease-free budwood and ding, grafting, orange rootstocks. natural root w grafting, sap Worldwide None yet found Budding, grafting, Lemon, sour orange Use disease-free budwood and kk sap rootstocks. Japan None yet found Budding, grafting, sap Satsuma mandarin Use disease-free budwood and rootstocks. ..Worldwide None yet found Budding, grafting, Sweet orange, mandarin, Use disease-free budwood and natural root lemon, lime, sour orange rootstocks. grafting California None known Budding and graft- ing Dweet tangor Use disease-free budwood and rootstocks. Nearly worldwide Toxoptera citri- Dodder, budding, Sweet orange, mandarin, Quarantine and eradication ► cidus, T. aur- grafting etc., on sour orange, for very limited infestations. antii, grapefruit, and some Control vectors. Use disease- Aphis gossypii, other rootstocks; lime free budwood and toler- A. spiraecola, ant rootstocks, such as tri- A. cracovora foliate, Troyer citrange, Dactynotus sweet orange, Rough lemon, jacae Rangpur lime, Cleopatra mandarin. Lemon trees on various stocks tolerant to tristeza may be damaged by seedling yellows. ~~Nearly worldwide T. citricidus Dodder, budding, Grapefruit, lemon, sour Same as above. A. gossypii grafting orange, citron * Known in Aden, T. citricidus Dodder, budding, Grapefruit, C. hassaku, Select for tolerance to stem Uruguay, grafting certain other varieties pitting. ^ Brazil, Argentina, Southern Africa, Australia, Japan Japan T. citricidus Budding, grafting C. hassaku, C. obovoidea, King mandarin Use disease-free budwood. (Control vectors?) U.S A., S. Africa, T. citricidus Budding, grafting, Sweet and sour orange, Avoid Rough lemon, C. volk- Australia, Peru, A. gossypii dodder Mexican lime, lemon, ameriana, and sour lime Japan Myzus Rough lemon, C. volk- rootstocks. Use disease-free persicae ameriana, etc. budwood in clean areas. [19] Continued Table Disease (common name) Literature* Symptoms Indexing plants fi- EXOCORTIS 1,4,23,24, 33, 53, 54, 56, 68, 69, 74, 80 Cracking and scaling of bark of trifoliates, citranges, and Rangpur lime; leaf and stem epinasty, cracking and callousing of underside of midveins, yellow blotches and cracks on shoots of some citrons; stunting of tree. Etrog citron (USDCS No. 60-13; Arizona 861) <* CACHEXIA- XYLOPOROSIS 15, 23, 24, 53, 55 Lens-shaped pits on trunk with or without gumming; pegs on inner bark surface. Orlando and Wekiwa tan- . gelos, Parsons Special mandarin, Palestine sweet and Kusaie limes. ** CRISTACORTIS 23,54 Pits in wood of trunk and branches; crested, gummy pegs on inner bark surface. Orlando tangelo, sour * orange IMPIETRATURA 20, 23, 24, 52 Hard, gummy deposits in rind, central core, and vascular bundles of fruit. Grapefruit YELLOW VEIN 16, 78 Bright yellow veins of leaves. Mexican lime, Rough lemon, Etrog citron USDCS 60-13 < LEAF CURL 53 Dieback of branches, curling of leaves like aphid injury; excessive flowering, only few small fruits; gum and grooves in wood. Caipira sweet orange TATTER LEAF 11, 17,23,24, 67, 77 Blotching and distortion of young leaves and twigs. C. excelsa « 4 CITRANGE STUNT 11, 17,23,24, 67, 77 Stunting; deep pits and grooves in wood; blotched, distorted leaves. Troyer, Carrizo, or Rusk citrange RINGSPOT 23 Yellowish rings with green islands on some leaves, sometimes vein clearing and stem lesions. -4 Grapefruit, lemon, Rough lemon, sweet orange ^_^, STUBBORN 9, 10, 14, 20, 21,22,23,24, 25, 29, 34, 35, 49, 50, 52, 53, 54,74 Trees stunted; low yield. Distorted, eccen- tric, or "acorn"-shaped fruits, sometimes stylar-end greening and blue albedo; seed abortion; stiff, upright, multiple twigs and buds; small chlorotic or mottled leaves; premature defoliation; dieback in severely affected trees. Sweet orange, tangelo 4 , GREENING 18, 19, 20, 23, 32,41, 43, 46, 52, 63, 66, 71 Similar to stubborn but usually with more chlorotic foliage and greening of fruit, dieback of branches; sometimes death of tree. Sweet orange, tangelo YELLOW SHOOT 43, 52, 54 General decline, yellowed or mottled leaves, premature defoliation, root decay, wilting, death of tree. See Greening and Stubborn } < 'See " Literature Cited," p. 39 [20] 1 (Cont.) Distribution Vector Other means of transmission Varieties attacked Control ' Worldwide Mechanically by cutting tools, fingers, and possibly by scratching and gnawing of animals Budding, grafting, dodder, sap Trifoliates, citranges, Rangpur lime, other mandarin limes, sweet limes, some lemons, citrons Use seed and budwood from disease-free sources; avoid susceptible rootstocks. Sterilize cutting tools to prevent spread to clean trees. Most citrus • "" regions None known Budding, grafting Sweet limes, mandarins, mandarin limes, tangelo Use seed and budwood from disease-free sources; avoid susceptible rootstocks. k Mediterranean ^ countries None known Budding, grafting Grapefruit, sweet and sour oranges, mandarin, tangelo Use disease-free budwood. Mediterranean ' countries None known Budding, grafting Grapefruit, oranges, man- darins, tangelos, lemon Use disease-free budwood. ». California (very limited) None known Budding, grafting Limequat, kumquat, Mexican lime, calamon- din, Orlando tangelo, Troyer citrange, lemon, citron Use disease-free budwood. Destroy infected trees. Brazil None known Budding, grafting Sweet orange, lemon, grapefruit, citron, shaddock, tangerine, sweet lime Use disease-free budwood. Destroy infected trees. ^ U.S.A. and probably in Meyer lemon in other countries None known Budding, grafting C. excelsa; Meyer lemons tested found to be symptomless carriers Use disease-free budwood. In Meyer lemon in U.S.A. and - probably in other countries None known Budding, grafting, sap Citranges, citremon, other trifoliate hybrids, trifoliates Use disease-free budwood. Destroy infected trees. 'U.S.A., Central America, Medi- H terranean area None known Budding, grafting, dodder Sweet orange, mandarin, lemon, grapefruit Use disease-free budwood. Destroy infected trees. Probably world- wide None yet found Budding, grafting Sweet orange, sour orange, grapefruit, mandarin, tangelo, lemon, lime, Rough lemon, citron, most other varieties regardless of root stock Use disease-free budwood. ^South Africa, India, Indo- nesia, Philip- ». pines, Taiwan, and probably most of S.E. Asia Trioza erytreae Diaphorina citri (citrus psyllidsl Budding, grafting Same as for stubborn Use disease-free budwood. (Control vectors?) ' China, Taiwan Diaphorina citri (?) Budding, grafting Tankan and Ponkan man- darins, sweet orange, C. grandis, calamondin, and various others Use disease-free budwood and rootstocks. [21] % %. Fig. 10. Exocortis: (above, left) on trifoliate rootstock; (above, right) yellow blotches on trifoliate branch; (below, left) epinasty effect on Etrog citron, an indicator plant. 42) . These insects transmitted vein ena- tion virus to Mexican lime seedlings from which, by graft-inoculation, the virus causing woody gall in Rough lemon seed- lings was transmitted, thus indicating the association of the two manifestations of this virus disease. Vein enation has been reported in South Africa, where it was shown to be transmitted by the aphid Toxoptera citricidiis (44). Woody gall is present in New South Wales, Australia, and is bud-graft transmissible. Since non- budded Rough lemon seedlings are af- fected in that area, an insect vector is assumed to be present and active. The economic importance of the disease has not yet been determined. EXOCORTIS Exocortis of trifoliate orange, citranges, Rangpur lime, sweet lime, and citron is caused by a virus and is characterized by vertical splits in the bark and by narrow, vertical, thin strips of partially loosened outer bark (4, 23, 53, 74) . Yel- low blotches often occur on young in- fected stems of these varieties (fig. 10). Troyer citrange is usually less severely affected than trifoliate orange. On some varieties of citron, exocortis causes epinasty, and cracking and darkening of veins and petioles of leaves. Orange, lemon, grapefruit, and other citrus trees on exocortis-sensitive rootstocks are slightly to greatly retarded in growth. Infected Eureka lemon on tolerant root- stocks is significantly retarded (74). The average yields of severely affected orange trees may be reduced as much as 40 per cent {23). Exocortis virus is present in most citrus areas and has increased in importance with the expanded use of exocortis-sensitive rootstocks. Exocortis virus is readily transmitted to healthy plants by budding knives (33) or other mechanical means and by hand (56) . It is also transmissible from citrus to citrus by dodder (80) . The virus is very stable, resistant to heat, and can persist on con- taminated surfaces for many days (1,69) . Exocortis virus separated from many of the host-cell contents can be inactivated by ribonuclease (68) . This finding, to- gether with the absence of typical virus particles in infectious preparations, led to the conclusion that this virus exists as a free ribonucleic acid (RNA) species in the host. There is some evidence for the existence of two infectious entities (69). Several factors were found impor- tant in the spread of the virus, including contaminated hands and tools of nursery- men and orchardists, which came into contact with phloem tissue in the bark; the fact that most citrus and many herbaceous plants can serve as donors of the virus; and the greater ease of trans- missions between related plants than be- tween unrelated ones (54) . For the detection of exocortis virus, a rapid indexing method is available which utilizes the virus-stimulated epi- nasty and stunting of Etrog citron selec- tions, U. S. Date and Citrus Station # 60-13 or Arizona 861 (24) (fig. 10) . Fluorescent chemical markers are useful in detecting exocortis virus in sensitive varieties (23). Gynura aurantiaca, G. sarmentosa, Petunia spp., and several other herbaceous plants exhibit pro- nounced epinasty, systemic mosaic, stunt- ing, and necrosis when inoculated with exocortis virus (80) . To control exocortis use virus-free, registered budwood and sanitary bud- ding, nursery, and field practices. Dis- infest tools between cuts into different plants by dipping in a 10 to 20 per cent solution of household bleach (5.25 per cent sodium hypochlorite in the concen- trated bleach) . To retard corrosion of the cutting edges, rinse in a solution-emulsion of 1 part vinegar, 2 parts water, and 2 teaspoons of an emulsifiable spray oil in each pint (56) . CACHEXIA Cachexia (xyloporosis) is a bud-trans- missible virus disease which attacks the stem bark and wood of several citrus species and varieties (24, 31, 51) . In this country the virus is frequently present in grapefruit and sweet orange without producing apparent symptoms, but it causes severe symptoms on Citrus macro- phylla and many varieties of mandarin, tangelo, sweet lime and their hybrids (6, 15, 23, 24, 53) . There is no evidence that the disease is carried through seed, and insect transmission has not yet been demonstrated. The wood shows elongated pits and the bark produces growth ridges that fit into the wood pits (fig. 11). Brown, gummy deposits form in the pits and bark phloem, and the stem wood may even- tually become brown. Bark scaling — which may not result only from ca- chexia- — secondary organisms, and vari- ous nutritional deficiencies complete the [23] s5 Fig. 1 1. Xyloporosis-cachexia: affected Wekiwa tangelo on Rough lemon rootstock. degeneration of the tree. While the dis- ease is uncommon in trees of young bud- lines, it is very important in Israel in trees of old budlines on Palestine sweet lime rootstocks, in which it produces a weakened, elastic wood (55), and it has recently appeared in some C. macro- phylla rooted lemon trees in California. Xyloporosis-affected trees in Israel are treated by inarching with sour orange. Many investigators are of the opinion that cachexia and xyloporosis are caused either by the same virus or strains of the same virus. Control is a matter of prevention ; that is, the use of tolerant scions and root- stocks or of budwood from indexed parent trees free of the virus. Indexing is done on susceptible indicator varieties, such as Orlando tangelo and Parsons Special mandarin, a method that often requires waiting two or more years for the development of typical symptoms (24). CRISTACORTIS Cristacortis is a severe, graft-transmis- sible disease causing stem pitting on sour orange (fig. 12), Tarocco orange, Or- lando tangelo, and some other varieties in several Mediterranean countries (23). Cristacortis resembles, but is apparently different from cachexia, and causes a very severe reaction in Orlando tangelo, which is a good indicator plant (54) . Since neither vector nor seed transmis- sion is known, prevention depends on the use of clean, indexed propagative ma- terials. IMPIETRATURA Impietratura, formerly believed to be Fig. 12. Cristacortis pitting in sour orange. 24] Fig. 13. Impietratura: gumming in navel orange peel. (Photographs by Henri Chapot.) caused by a water deficit, is now known to be graft-transmissible and is presumed to be caused by a virus (24, 52) . All of the commercial species of citrus are sus- ceptible, and the disease is widespread in the Mediterranean region (20, 23, 52) . The malady is characterized by small, more or less pear-shaped, hard fruits. The fruit has a hardened flavedo, and the rind generally has a few to many hard, gum-infiltrated protuberances (fig. 13) each surrounded by a yellowish halo. Many of the fruits on diseased trees fall off during the summer, the extent of loss being in direct proportion to severity of infection. The symptoms suggested boron deficiency as the cause, but analyses re- vealed adequate amounts of that element in the affected trees, and applications of boron compounds failed to correct or pre- vent the disease (20, 53). The growth from healthy orange and grapefruit buds that had been placed in impietratura-affected trees soon devel- oped typical symptoms of impietratura, and shield buds from diseased trees transmitted the pathogen to young, healthy grapefruit trees (20, 24) . Trans- missibility and incubation periods were highly variable. Sour orange and Avana mandarin are tolerant. Use of tolerant varieties and of pro- pagative material from disease-free trees is suggested as a control measure. YELLOW VEIN Yellow vein is a virus disease found on limequat, and is graft-transmissible to several rutaceous species, varieties, and hybrids, including West Indian lime, calamondin, Orlando tangelo, Troyer citrange, lemon, and kumquat (78). The striking symptom of the disease is the yellowing of the veins. The bright yellow color extends into the adjacent tissue and causes the veins to appear enlarged (fig. 14). The yellowing may extend down from a leaf petiole onto the young twig or stem. Certain citron, Red Rough lemon, and India lime selections are good in- dicators of yellow-vein virus (16, 78). Surveys thus far have indicated that the disease is not widespread, for it has been found in only four of many limequat trees in three California counties, and in one C. macrophylla seedling at Indio, California. LEAF CURL Leaf curl, reported only from Brazil, was shown to be transmissible by budding and grafting to several sweet orange varieties, Eureka lemon, sour orange, citron, grapefruit, and shaddock (53) . It appears to be caused by a virus entity distinct and different from the exocortis virus. The main symptoms are a curling and distortion of the leaves resembling that caused by a heavy aphid infestation; [25] x f$* .»*., m* Jk ' Fig. 14. Yellow vein of Mexican lime. abundant production of weak sprouts with gum in their wood vessels near their unions with branches; and channeling and pitting of the wood of the trunk and main branches. Indexing can be done in two to five months on sweet orange seedlings. The obvious control in Brazil was to eliminate the few trees found infected. TATTER LEAF and CITRANGE STUNT Mexican lime and Citrus excelsa seed- lings inoculated from Meyer lemon de- velop chlorotic blotches on their leaves, whereas the leaves of inoculated citrange and citremon plants become dwarfed, dis- torted, and strongly blotched, and the plants are stunted (figs. 15, 16). The ef- fects are obtained whether or not the [26] tristeza-seedling yellows virus complex is present in the Meyer lemon, and indi- cate the presence of another virus (or viruses) at first named tatter leaf virus (77). Additional studies revealed that the virus causing tatter leaf on Citrus excelsa is not the same as that which causes stunting of citrange (23). The latter virus was, therefore, designated as cit- range stunt virus and is believed to be the virus transmitted mechanically from Meyer lemon to various hosts and to cit- rus from herbaceous hosts (77, 23, 67). The citrange stunt virus was purified and characterized (67) . The tatter leaf virus is often lost during passage through C. excelsa or some other citrus hosts, and has not been transmitted mechanically, Fig. 15. Left: Tatter leaf of Citrus excelsa. (Photo by T. A. DeWolfe; leaves from J. M. Wallace.) Fig. 16. Below: Citrange stunt of Troyer citrange. (Specimen supplied by J. M. Wal- lace.) [27] whereas the citrange stunt virus appears to be retained indefinitely by many cit- rus and herbaceous hosts and is mechani- cally transmissible. Citrange stunt virus causes such severe stunting and distortion of citrange seed- lings that it could have considerable eco- nomic importance if it becomes wide- spread. It is assumed to cause a severe bud-union creasing, grooving, fluting, and stunting disease of Troyer citrange rootstock in trees inoculated with Meyer lemon buds (11, 23) . No vector is known for either the tatter leaf or the citrange stunt viruses. Although neither virus has been found in any uninoculated trees other than Meyer lemon, the citrange stunt virus occurs in some specialty trees that have Meyer lemon as one com- ponent. Indexing for tatter-leaf virus is done on Citrus excelsa seedlings. Citrange stunt virus may be indexed on Rusk, Troyer, or Carrizo citrange seedlings, but not on C. excelsa (17, 24). Cowpea is also an indicator plant for citrange stunt virus (24,67). CITRUS RINGSPOT Leaves of sweet orange seedlings inocu- lated with tissue from a lemon tree with psorosis developed not only typical psoro- sis flecking but also yellowish spotting of leaves that later changed to ring patterns and coalescing blotches as the center area of the spots remained green (23). Vein clearing, resembling that of tristeza at first, spread into adjacent areas of tissue, resulting in a feathery effect (fig. 17). The leaf patterns, together with a shock effect of the disease, which caused leaf drop, stem lesions, and death of parts, suggested certain effects of the rampant form of psorosis. However, sweet orange seedlings infected with ringspot virus were not protected from psorosis infec- tion, nor did infection with concave gum virus protect the seedlings against ring- Fig. 17. Ringspot of lemon. (Leaves supplied by J. M. Wallace.) [28] spot. Previous infection with psorosis or blind pocket viruses did, however, pro- tect against ringspot. While to date ringspot has only oc- casionally been observed on orchard trees in California and may be of little or no economic importance, the leaf symptoms have been seen on field trees in Florida and Central America. With present knowledge, use of disease-free propaga- tive material is the only recommendation for control. MYCOPLASMALIKE DISEASES STUBBORN DISEASE Stubborn disease materially reduces fruit bearing in commercial citrus varieties and especially in navel oranges (20, 29) . It is believed to be caused by myco- plasmalike bodies and not by a virus (34) . The little leaf disease of Israel ap- pears to be the same as stubborn (20) . The so-called "crazy top" of grapefruit trees with "acorn" or "pink nose" fruit, found in Arizona and California, is be- lieved to be the same disease (3) . Stubborn disease often retards growth considerably in trees infected when young, results in excessive abortion of seeds in many seedy varieties, and usually Fig. 18. Stubborn disease: (left, upper and lower) severe and moderate stunting; (lower right) healthy tree. Fig. 19. Stubborn disease: affected foliage and fruit of navel orange. causes bunchy, upright growth with leaves smaller than normal (14, 20) (figs. 18 to 22). On navel orange the symptoms, when pronounced, include a brushlike growth of twigs as a result of abnormal branching from multiple buds. The leaves tend to bend upward more on each side of the midrib than do those of healthy trees. Growth flushes are fre- quently out of phase with those on healthy trees, and the greatest amount of shoot growth on the diseased trees often occurs in the autumn. Foliage of some or all shoots tends to be inter- mittently abnormally mottled and chlo- rotic. When fruits are produced, many are smaller than normal and may be lopsided and occasionally acorn-shaped. The rind in affected portions, usually on the sides and distal half of the fruit, is thinner than the rind of healthy fruits (figs. 19 and 21). In severely affected fruits the pulp below the thin portions of [ Fig. 20. Stubborn disease: test with Madam Vinous sweet orange indexing plant, showing healthy seedling (largest), one mildly affected, one severely affected. Leaf symptom at right. Fig. 21. Stubborn disease: Valencia orange fruit showing lopsidedness (four fruits on left) and healthy fruit (right). the rind has a sour or bitter taste and disagreeable odor. The distal end of ma- turing fruits sometimes changes color from green to orange more slowly than does the button end, a reversal of the coloring process in normal fruits. The symptoms on the mature fruit are useful Fig. 22. Stubborn disease: (left) healthy Val- encia orange and seed; (right) diseased orange and aborted seed. in diagnosis. The fruit symptoms of stub- born have been reproduced by graft in- oculation of healthy trees and by grafting healthy fruits onto seedlings infected with the disease (35, 49). Occasionally the albedo of diseased fruit has a blue color. Several detailed descriptions of stubborn disease and its effects on cer- tain varieties have been published (9, 10,20,21,22,25,74). In many species and varieties, espe- cially navel orange, symptoms are highly variable, and several forms of the disease, possibly caused by different forms of the pathogen, are known. The stubborn pathogen is irregularly distributed in the tree, and certain branches of some stub- born trees are symptomless (20, 23, 49, 53). While symptoms on large trees de- velop slowly, small trees and indicator plants develop symptoms rapidly but may improve later (20, 53). The Madam Vinous variety of sweet orange and sev- eral others, Sexton tangelo, and some grapefruit varieties, grown at high tem- peratures, are suitable indicator plants for stubborn disease (24, 50) . Repeated experiments corroborate many previous observations by propa- [31] gators and growers that trees with stub- born symptoms, when topworked with carefully selected, healthy buds or scions, again produce the same symptoms after developing a new top. Stubborn disease is currently the greatest disease threat to production of sweet oranges and grapefruit in Califor- nia. Although no vector has been found, the disease has been spread into many trees, apparently by natural means, and has been so widely disseminated by propagation that it is now one of the most important citrus diseases in Cali- fornia, Arizona, Morocco, Israel, and some other Mediterranean countries, is present in Mexico and several South American countries, and may be world- wide. For prevention of the disease in future plantings, it is most important that nursery trees be propagated from trees free of the stubborn disease patho- gen. Examine parent trees very carefully, and cut budwood only from healthy trees and from branches that bear only normal fruits. Remove young stunted and stub- born-diseased trees and trees rendered unproductive by stubborn. Fig. 23. Greening disease: (top) in Taikat mandarin on Calamandarin rootstock (Philippines); (bottom) leaf symptoms of mandarin (Hong Kong). [32] *,V vv Fig. 24. Likubin or yellow shoot of mandarin near Hong Kong (left) and in Taiwan (right). GREENING DISEASE Greening disease is of major importance in South Africa, India, the Philippines, Indonesia, Thailand, Taiwan, and China. It is similar to stubborn disease in many ways, but has little or no tendency to cause brushlike growth or acorn-shaped fruit (20, 23, 32, 41, 53, 66) . Either af- fected branches or the entire tree is seasonally chlorotic with mottled leaves (fig. 23), and fruits are commonly of poor quality, retaining areas of green peel until maturity. Greening has been transmitted by the psyllid, Trioza ery- treae, in South Africa (46), and in India and some other areas by another psyllid, Diaphorina citri (13, 18, 19) . Greening has been the major factor in the devastation of orange orchards in some districts of South Africa, India, the Philippines (fig. 23), and Indonesia (20, 23, 71 ) . Mycoplasmalike bodies have been found associated with greening dis- ease (41) . "Yellow shoot" or "likubin," reported from China (43) and Taiwan (52), is evidently a form of greening or stub- born, despite its frequent association with tristeza virus (fig. 24). A fluores- cent chemical marker, often present in infected trees, has been useful for de- tection of greening disease (20, 23) . [33 DISEASES OF UNKNOWN CAUSE WITH VIRUSLIKE SYMPTOMS RUMPLE A serious abnormality of lemon fruits in Florida was first reported in 1958 under the name rumple (20, 40) . A disorder of Sicilian lemons, called wrinkle rind, and resembling rumple, was described in 1963 (59). It is now evident that the troubles in Sicily and Florida are simi- lar. The disease is also known to be present in Turkey, Cyprus, Lebanon, and Ethiopia. In Florida, rumple appears first in late summer as faint, chlorotic speckles on the rind surface, each spot covering an area including four or five oil glands. The oil glands first turn "greenish brown, then in order, tan, mahogany brown, and brownish black" ; finally they collapse (20) (fig. 25). In Sicily the breakdown appears to be initiated always near the end of the summer or beginning of autumn. Green lemons show the ef- fects during September, October, and November. After mid-December, or when a fruit starts its yellow coloring, it will not develop the trouble. When affected green lemons are placed in storage, the involved rind areas enlarge and new ones form, but losses from subsequent decay are not greater in rumpled than in nor- mal fruits. While the disease ruins lem- ons for the fresh-fruit market, they may be used for juice, rind oil, and other by-products (40) . The importance of rumple has been indicated by extensive surveys. Thirty- eight of 40 lemon varieties examined in Florida showed an average incidence of the disease ranging from 0.7 per cent in the Harvey selection to 37.8 per cent in the Edwards selection (20) . In Florida, the two varieties commonly grown in California — Lisbon and Eureka — had 8.8 and 8.4 per cent rumple, respectively. However, incidences of the malady in 1963 in some Florida orchards reached Fig. 25. Rumple: (left) primary stage; (right) secondary stage. (Photos by Dr. L. C. Knorr.) • • *(&\ ' inm^ [34] ill Fig. 26. Tarocco pit: (top left) surface view of affected Tarocco scion showing pits and ex- truded, corklike material; (top right) cambial surface with bark pulled back, exposing wood; (bottom left) longisection, showing depth of pits; (bottom right) small fruit from diseased tree and larger fruit from healthy tree. [35] 77 per cent. Incidences of 75 per cent have been reported in Turkish lemon plantings (20) . The Florida investigations into pos- sible causes of the trouble included studies on the effects of insects, mites, bacteria, water relations, heredity, fer- tilizers, and viruses. Much of the research was inconclusive, but several observa- tions appear significant. Large-sized fruits developed higher incidences of rumple than did small fruits. Trees with a low incidence of rumple continued the low incidence year after year, and trees with a high incidence continued to bear large numbers of affected fruits in suc- ceeding crops. This may suggest a con- nection with virus infection or the trees' genetic makeup. Trees receiving large amounts of nitrogen fertilizers had more rumpled fruits than did those given medium or low amounts. Trees with a low potassium content in their leaves showed high percentages of the disease. With the present lack of knowledge of the cause of rumple no recommendations can be offered beyond the careful selec- tion of budwood for propagation from disease-free trees, and judicious fertiliza- tion of the orchard. TAROCCO PIT On many Tarocco orange trees in the Lentini district of Sicily an unusual form of bark and wood disease, first noticed in 1962 and tentatively called Tarocco pit, has appeared (58) . The Tarocco scion near the bud union is most severely affected, showing large, distorted overgrowths and infoldings (fig. 26) . A circular hole, ranging in diameter from 1 mm to 2cm, is found in the center of each concavity. From these holes a material like ground cork is extruded. When the bark is removed, many of these circular holes, 2 to 8 mm in diameter, are found, that have not broken through to the external bark surface. At this stage of development they are filled with a soft, whitish, meristematic tissue which later darkens as it becomes infiltrated with gum, and still later, as the lesion breaks through to the outer bark sur- face, produces the ground corklike ma- terial. Buds from affected trees propagated on rootstocks of sour orange, Cleopatra mandarin, and Troyer citrange showed typical pits in the wood at the end of two to three years, but none had broken through the bark in that time. In common with ordinary concave gum disease, the young leaves of spring growth of Tarocco trees affected by Tarocco pit show typical oak-leaf pat- terns and some flecking. The autumn flush of growth shows less of the oak-leaf effect and more flecks. The flecks pro- duced in autumn are broader than those appearing in the spring. Cross-protection tests with psorosis have not been tried. It has been possible in some instances to trace the source of the affected bud- wood, in others not. Sweet orange seed- lings graft-inoculated with material from affected trees showed both oak-leaf pat- terns and flecking. Tests on Mexican lime seedlings showed no tristeza infec- tion. Palestine sweet lime seedlings budded in 1962 with buds from trees with Tarocco pit have not yet shown cachexia-xyloporosis symptoms. Affected trees are a third smaller than unaffected trees or trees affected by con- cave gum disease. Diseased trees have shorter internodes, smaller leaves, and more numerous and smaller fruits than do healthy trees, indicating the girdling effect of the trouble. The affected fruits have a more spongelike albedo, a much greater percentage of acid, and a lower solids-acid ratio than normal fruits. The ever increasing number of Tarocco orange trees found to be diseased points up the severity of the trouble on this orange variety. WOOD POCKET This disease, also called lignocortosis, affects certain varieties of lemon and [36 Pfe ^^ v.-- ; ■■> •' w V Hit 1 H* f ' M i JwS . .. ■&. JH Fig. 27A. Wood pocket of Lisbon lemon: (top) symptoms on leaf and fruit; (bottom) section through trunk showing symptoms in bark and wood. Fig. 27B. Limb of Lisbon lemon affected with wood pocket. [37] Non functioning phloem Functioning phloem Fig. 28. Lemon sieve-tube necrosis in radial section of bark. (Photo by H. Schneider.) lime. In California it occurs principally in the semidense Lisbon lemon (7). In Florida it is known also as blotch, and occurs mostly in Tahiti lime trees (39) . The first evidence of the disease is gen- erally a chimeralike variegation or blotching of the leaves (fig. 27A) . Fre- quently there is considerable chimeral striping of the fruit, especially of limes. The leaf color varies from only a slight loss of green to greenish-yellow to nearly pure yellow with diverse outlines. The disease apparently is a chimeral disorder which is seed- and bud-perpetuated but which is not transmissible by grafting. A short, narrow, irregular break in the bark of the trunk or limb is the first symptom on those parts (fig. 27B). The wood underneath discolors in definite re- gions even before this bark symptom ap- pears. This led to the name wood pocket or lignocortosis. Elongated areas of dead, fissured bark, 1 inch to several feet in length, form on one side of the branches or on portions of the trunk. Wood under- neath becomes irregularly discolored and darkly dotted in longitudinal view. Branches lose their leaves and die back gradually, or the leaves wilt suddenly as the branches die. LEMON SIEVE-TUBE NECROSIS Lemon sieve-tube necrosis (fig. 28) is probably the most important of the non- infectious diseases of lemons (52, 65). Eureka lemons and certain clones of other varieties are subject to the trouble; some clones are not, and do not develop it when budded with an affected clone. The older sieve tubes of three- or four- year-old trees die. During the next sev- eral years, more and more of these food- conducting vessels die, including even the youngest. Because elaborated food cannot then be transported to the roots, they starve and some die. Affected trees that had been making good growth suddenly decline and may die. In a vertical section through the phloem of lemon bark, af- fected sieve tubes appear as elongated, darkened areas under the microscope. Other significant disorders of unknown cause include: Crinkle scurf of Valencia orange (37) ; a seed-perpetuated dis- order of trifoliate orange resembling exocortis; sour orange rootstock necrosis (64), which develops when this stock is budded with Eureka lemon or with some Lisbon lemon clones; degeneration of bud union tissues when Eureka lemon is budded on trifoliate orange or Troyer citrange (79) . [38 LITERATURE CITED 1. Allen, R. M. 1968. Survival time of exocortis virus of citrus on contaminated knife blades. Plant Disease Reptr. 52: 935-39. 2. Bar-Joseph, M., G. Loebenstein, and J. Cohen 1970. Partial purification of virus-like particles associated with the citrus tristeza disease. Phytopathology 60: 75-78. 3. Batchelor, L. D., and H. J. Webber (eds.) 1948. The citrus industry, vol. 2. Berkeley: University of California Press, 1-933. 4. Benton, R. J., F. T. Bowman, L. Fraser, and R. G. Kebby 1949. Stunting and scaly butt of citrus associated with Poncirus trifoliata rootstock. Agr. Gaz. N. S. Wales 61: 521-26, 577-82, 641-45, 654. 5. Bitters, W. P., and E. R. Parker 1953. Quick decline of citrus as influenced by top-root relationships. Calif. Agr. Exp. Sta. Bui. 733, 35 pp. 6. Bove, J. M., and R. Vogel 1961, 1962, 1963. L'etat sanitaire des agrumes en Corse. Fruits 16: 137-42; 17: 163-69, 351- 56; 18: 53-59, 115-21, 185-87. 7. Calavan, E. C. 1957. Wood pocket disease of lemons and seedless limes. Calif. Citrograph 42: 265-68, 300-04. 8. Calavan, E. C, R. M. Burns, C. J. Barrett, D. W. Christiansen, and R. L. Blue 1968. Tristeza in lemon on Citrus macrophylla rootstock. Calif. Citrograph 53: 108, 119, 122. 9. Calavan, E. C, and J. B. Carpenter 1965. Stubborn disease retards growth, impairs quality, and decreases yield. Calif. Citro- graph 50: 86-87, 96, 98-99. 10. Calavan, E. C, and D. W. Christiansen 1966. Effects of stubborn disease on various varieties of citrus trees. Israel Jour. Botany 15: 121-32. 11. Calavan, E. C, D. W. Christiansen, and C. N. Roistacher 1963. Symptoms associated with tatter-leaf virus infection of Troyer citrange rootstocks. Plant Disease Reptr. 47: 971-75. 12. Calavan, E. C, R. M. Pratt, B. W. Lee, and J. P. Hill 1968. Tristeza related to decline of oranges on citrange rootstock. Calif. Citrograph 53: 75, 84-88, 90. 13. Capoor, S. P., D. G. Rao, and S. M. Viswanath 1967. Diaphorina citri Kuway, a vector of the greening disease of citrus in India. Indian Jour. Agr. Sci. 37: 572-76. 14. Carpenter, J. B., E. C. Calavan, and D. W. Christiansen 1965. Occurrence of excessive seed abortion in citrus fruits affected with stubborn disease. Plant Disease Reptr. 49: 668-72. 15. Carpenter, J. B., and J. R. Furr 1967. Susceptibility of Citrus macrophylla 'Alemow' to cachexia virus. Plant Disease Reptr. 51:525-27. 16. Carpenter, J. B., and L. G. Weathers 1968. Indicator plants of citrus yellow-vein virus. Phytopathology 58: 117-18. 17. Catara, A., and J. M. Wallace 1970. Identification of citrange stunt as the mechanically transmissible virus from Meyer lemons doubly infected with citrange stunt and tatter leaf viruses. Phytopathology 60: 737-38. 18. Catling, H. D. 1968. Distribution and biology of Diaphorina citri, the insect vector of leaf mottling (greening) disease of citrus. FAO Report No. TA2589. 14 pp. 19. 1970. Distribution of the psyllid vectors of citrus greening disease, with notes on the biology and bionomics of Diaphorina citri. FAO Plant Prot. Bui. 18: 8-15. 20. Chapman, H. D. (ed.) 1969. Proc. 1st Intern. Citrus Symp. 3: 1105-1838. Riverside: University of California. [39] 21. Chapot, H., J. Cassin, and M. Larue 1962. Nouvelles varietes d'agrumes atteintes par le stubborn. Al Awamia 4: 1-6. 22. Chapot, H., and V. L. Delucchi 1964. Maladies, troubles, et ravageurs des agrumes au Maroc. Institut National de la Re- cherche Agronomique, Rabat, 339 pp. 23. Childs, J. F. L. (ed.) 1968. Proc. 4th Conf. Intern. Organ. Citrus Virol. Gainesville: University of Florida Press, 404 pp. 24.— 1968. Indexing procedures for 15 virus diseases of citrus trees. Washington, D.C.: USDA Agric. Handbook 333, 96 pp. 25. Childs, J. F. L., and J. B. Carpenter 1960. Observations on stubborn and other diseases of citrus in Morocco in 1959. Plant Disease Reptr. 44: 920-27. 26. Desjardins, P. R., and J. M. Wallace 1966. Host reactions to citrus infectious variegation virus indicating wide diversity of virus strains. Phytopathology 56: 347-48. 27. Dickson, R. C, R. A. Flock, and Metta M. Johnson 1951. Insect transmission of citrus quick decline virus. Jour. Econ. Ent. 44: 172-76. 28. Fawcett, H. S. 1936. Citrus diseases and their control. New York and London: McGraw-Hill Book Co., 656 pp. 29. Fawcett, H. S., and L. J. Klotz 1948. Stubborn disease, one cause of nonbearing in navels, Valencias, and grapefruit. Calif. Agriculture 2 (8) : 4, 15. 30. Fernandez- Valiela, M. V. 1963. Principales enfermedades de virus de los citrus en la Republica Argentina. Delta de Parana Bol. de Div. 3: 3-37. 31. 1969. Introduccion a la fitopatologia. (3rd ed. ), vol. 1. Virus. Buenos Aires: Talleres Gra- ficas, 253-311. 32. Fraser, L., D. Singh, S. P. Capoor, and T. K. Nariani 1966. Greening virus, the likely cause of citrus dieback in India. FAO Plant Prot. Bui. 14: 127-30. 33. Garnsey, S. M., and J. W. Jones 1967. Mechanical transmission of exocortis virus with contaminated budding tools. Plant Disease Reptr. 51: 410-13. 34. Igwegbe, E. C. K., and E. C. Calavan 1970. Occurrence of mycoplasmalike bodies in phloem of stubborn-infected citrus seed- lings. Phytopathology 60: 1525-26. 35. Klotz, L. J. 1961. Color handbook of citrus diseases. Berkeley: University of California Division of Agri- cultural Sciences, 75 pp. 36. Klotz, L. J., and E. C. Calavan 1969. Gum diseases of citrus in California. Calif. Agr. Exp. Sta. Circ. 396 (2nd rev.) , 26 pp. 37. Knorr, L. C. 1953. Transmission trials with crinkle scurf of citrus. Plant Disease Reptr. 37: 503-07. 38. 1965. Serious diseases of citrus foreign to Florida. Florida Dept. Agr. Bui. 51. 59 pp. 39. Knorr, L. C, and J. F. L. Childs 1957. Occurrence of wood pocket (blotch) chimeric breakdown, and endoxerosis in Florida, with particular reference to the Tahiti lime. Proc. Fla. State Hort. Soc. 70: 75-81. 40. Knorr, L. C, R. W. Olsen, and J. W. Kesterson 1963. Rumple of lemons — its effect on fresh fruit, lemonade concentrate, and peel oil. Fla. State Hort. Soc. Proc. 76: 36-41. 41. Lafleche, D., and J. M. Bove 1970. Structures de type mycoplasme dans les feuilles d'orangers atteints de la maladie du "greening." Compte Rend. l'Acad. Sci. Ser. D. 270: 1915-17. 42. Laird, E. F., and L. G. Weathers 1961. Aphis gossypii, a vector of citrus vein-enation virus. Plant Disease Reptr. 45: 877. r 40 1 43. Lin, K. H. 1964. A preliminary study of the resistance of yellow shoot virus and citrus budwood tissue to heat. Acta Phytopath. Sin. (Peking) 7: 61-65. 44. McClean, A. P. D. 1954. Citrus vein-enation virus. S. African Jour. Sci. 50: 147-51. 45. 1960. Seedling yellows in South African citrus trees. S. Afr. Jour. Agr. Sci. 3: 259-79. 46. McClean, A. P. D., and P. C. J. Oberholzer 1965. Citrus psylla, a vector of the greening disease of sweet orange. S. African Jour. Agr. Sci. 8: 287-98. 47. Miyakawa, T., and H. Yamato 1969. Hassaku dwa^f disease in Tokushima. Bui. Tokushima Hort. Exp. Sta. No. 2: 1-13. 48. Norman, P. A., and T. J. Grant 1954. Transmission of tristeza virus by aphids in Florida. Proc. Florida Hort. Soc. 55: 89-92. 49. Olson, E. 0. 1969. Symptoms of stubborn disease in citrus and Poncirus fruit grafted onto virus-infected seedlings. Phytopathology 59: 168-72. 50. Olson, E. O., and B. Rogers 1969. Effects of temperature on expression and transmission of stubborn disease of citrus. Plant Disease Reptr. 53: 45-49. 51. Pratt, R. M. 1958. Florida guide to citrus insects, diseases, and nutritional disorders in color. Florida Agr. Exp. Sta. Gainesville, 181 pp. 52. Price, W. C. (ed.) 1961. Proc. 2nd Conf. Inter. Organ. Citrus Virol. Gainesville: University of Florida Press, 265 pp. 53. 1965. Proc. 3rd Conf. Inter. Organ. Citrus Virol. Gainesville: University of Florida Press, 319 pp. 54. 1972. Proc. 5th Conf. Inter. Organ. Citrus Virol. Gainesville: University of Florida Press. (In press) . 55. Reichert, I., and J. Perlberger 1934. Xyloporosis, the new citrus disease. Hadar 7: 163-67, 172, 193-202. 56. Roistacher, C. N., E. C. Calavan, and R. L. Blue 1969. Citrus exocortis virus — chemical inactivation on tools, tolerance to heat and separa- ration of isolates. Plant Disease Reptr. 53: 333-36. 57. Rossetti, V., and A. A. Salibe 1962. Prevalencia das doencas de virus dos citros no estado de Sao Paulo. Bragantia 21: 107-21. 58. Russo, F., and L. J. Klotz 1963. Tarocco pit. Calif. Citrograph 48: 221-22. 59. 1963. Wrinkle rind of lemons in Sicily. Calif. Citrograph 48: 264. 60. Sanchez- Arellano, L., and L. G. Weathers 1971. Enfermedades de los citricos. Santiago, Chile: S.A.G. Ministerio de Agricoltura. Bol. Tec. 45, 60 pp. 61. Sasaki, A. 1966. Studies on Hassaku dwarf. I. Detection of citrus viruses in a Hassaku tree severely alTected by Hassaku dwarf. Hiroshima Agr. Exp. Sta. Rept. 23: 39-47. 62. Scaramuzzi, G. 1965. Le malattie degli agrumi. Bologna: Officine Grafliche, Calderini. 167 pp. 63. Schneider, H. 1954. Anatomy of bark of bud union, trunk and roots of quick-decline-affected sweet orange trees on sour orange rootstock. Hilgardia 22 (16) : 567-601. 64.- 65. 1956. Decline of lemon trees on sour orange rootstock. Calif. Citrograph 41: 117-20. 1960. Sieve-tube necrosis in nucellar lemon trees. Calif. Citrograph 45: 208, 219-22. [41] 66. Schwarz, R. E. 1967. Results of a greening survey on sweet orange in the major citrus growing areas of the Republic of South Africa. S. African Jour. Agr. Sci. 10: 471-76. 67. Semancik, J. S., and L. G. Weathers 1965. Partial purification of a mechanically transmissible virus associated with tatter leaf of citrus. Phytopathology 55: 1354-58. 68. 1968. Exocortis virus of citrus: Association of infectivity with nucleic acid preparations. Virology 36: 326-28. 69. 1970. Properties of the infectious forms of exocortis virus of citrus. Phytopathology 60: 732-36. 70. Suit, R. F. 1949. Parasitic diseases of citrus in Florida. Fla. Agr. Exp. Sta. Bui. 463: 1-112. 71. Tirtawidjaja, S., T. Hadiwidjaja, and A. M. Lasheen 1965. Citrus vein-phloem degeneration virus, a possible cause of citrus chlorosis in Java. Proc. Amer. Soc. Hort. Sci. 86: 235-43. 72. Wallace, J. M. 1957. Tristeza and seedling yellows of citrus. Plant Disease Reptr. 41: 394-97. 73. 1957. Virus-strain interference in relation to symptoms of psorosis disease of citrus. Hil- gardia27 (8): 223-46. 74.- — (ed.) 1959. Citrus virus diseases. Proc. 1st Conf. Inter. Organ. Citrus Virol. Berkeley: Univer- sity of California, Division of Agricultural Sciences, 243 pp. 75. Wallace, J. M., and R. J. Drake 1953. A virus-induced vein enation in citrus. Citrus Leaves 33: 22, 24. 76. 1960. Woody galls of citrus associated with vein enation virus infection. Plant Disease Reptr. 44: 580-84. 77. 1963. New information on symptom effects and host range of citrus tatter leaf virus. Plant Disease Reptr. 47: 352-53. 78. Weathers, L. G. 1957. A vein-yellowing disease of citrus caused by a graft transmissible virus. Plant Disease Reptr. 41:741-42. 79. Weathers, L. G., E. C. Calavan, J. M. Wallace, and D. W. Christiansen 1955. A bud union and rootstock disorder of Troyer citrange with Eureka lemon tops. Plant Disease Reptr. 39: 665-69. 80. Weathers, L. G., F. C. Greer, Jr., and M. K. Harjung 1967. Transmission of exocortis virus of citrus to herbaceous hosts. Plant Disease Reptr. 51:868-71. 81. Yamada, S., and H. Tanaka 1969. Latent tristeza virus of Satsuma mandarin in Japan. Bui. Hort. Res. Sta. (Japan), Ser. B, No. 9, pp. 145-60. 82. Zanardi, D., G. Anneda, and B. Follesa 1967. Le virosi degli agrumi in Sardegna. Sardegna Assessorato Agricoltura e Foreste, 54 pp. Co-operative Extension work in Agriculture and Home Economics, College of Agriculture, University of California, and United States Department of Agriculture co-operating. Distributed in furtherance of the Acts of Congress of May 8, and June 30, 1914. George B. Alcorn, Director, California Agricultural Extension Service. 15m-l,'72(P8570)L.L. [42] his publication is one of many that are written, pro- duced, and distributed by the University of California Division of Agricultural Sciences. hey cover many subjects, from agronomy to zoology. They cover many crops, from alfalfa to zucchini. Some report new research findings . . . some tell "how to do it." Most are free . . . for some there is a charge. All are listed in a catalog that is issued annually. o get a copy of the catalog, visit the office of your local University of California Farm Advisor, or write to: Agricultural Publications University of California Berkeley, Calif. 94720