Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

Circular 1131 December 1993

Citrus Viruses and Virus-Like Diseases1

J.J. Ferguson and S.M. Garnsey2

IMPORTANCE sheath of protein and an inner core of nucleic acid, the genetic messenger material found in all living Virus and virus like diseases have a major impact organisms. Plant viruses differ in shape and size but on production world-wide and often become the are generally either threadlike or spherical. They dominant yield-limiting factor in grove management. range in size from 1/12,000 to 1/1,250,000 inch and The most obvious impact of these diseases is their are considerably smaller than other plant pathogens. lethal effect on specific hosts. Tristeza alone has Although viruses are agents of disease, as are destroyed approximately 50 million trees in the past bacteria, fungi and nematodes, and can transmit 40-50 years. A less obvious but economically genetic information, they cannot grow or reproduce important effect is the variety of non-lethal, subtle by themselves outside the host plant as can most responses that reduce tree size, tree vigor and fruit living organisms. Viruses can replicate only inside yield. In many cases, growers suffer significant losses suitable host cells by converting the reproductive from virus diseases without recognizing the nature of machinery of the host cell to reproduce the these diseases. Finally, citrus virus and virus-like components of the virus. Viroids are even smaller and diseases may restrict the grower’s choice of scions and contain only nucleic acid without any protein coat. rootstocks that can be grown profitably in certain areas. For example, tristeza-sensitive cultivars must Hosts often be avoided in areas where severe forms of the virus are prevalent, even though all other factors A multitude of living organisms, from would predict profitable use of these cultivars. single-celled plants or animals to large trees and mammals, can be attacked by viruses. Some viruses NATURE OF VIRUSES attack man and other animals and cause diseases such as influenza, polio, rabies, smallpox and warts. Other Structure viruses cause plant galls, flower break, stunting and decline. Still other viruses attack microorganisms such Viruses are extremely small, infectious particles. as bacteria and fungi. Over a thousand viruses are Plant viruses are composed of an outer protective known and more than half of these viruses cause plant diseases.

1. This document is Circular 1131, a series of the Horticultural Sciences Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida.Publication date: December 1993. 2. J.J. Ferguson, Associate Professor, Citrus Specialist, Department of Fruit Crops, Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL 32611; S.M. Garnsey, Citrus Virologist, USDA, Agricultural Research Service, 2120 Camden Road, Orlando, FL 32803. The use of trade names in this publication is solely for the purpose of providing specific information. It is not a guarantee or warranty of the products named, and does not signify that they are approved to the exclusion of others of suitable composition.

The Institute of Food and Agricultural Sciences is an equal opportunity/affirmative action employer authorized to provide research, educational information and other services only to individuals and institutions that function without regard to race, color, sex, age, handicap, or national origin. For information on obtaining other extension publications, contact your county Cooperative Extension Service office. Florida Cooperative Extension Service / Institute of Food and Agricultural Sciences / University of Florida / Christine Taylor Stephens, Dean Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

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Symptoms spread mainly by propagation such as much of the psorosis complex, exocortis and xyloporosis. Plant viruses can cause a variety of disease symptoms, most of which result from systemic Insects are significant vectors of several important infection (infection spread throughout the plant). virus and virus-like pathogens of citrus. Although Stunting and reduction in yield are probably the most tristeza is spread by several species of aphids, the common effects of viral diseases of plants but specific most effective aphid vector of tristeza, Toxoptera foliage, fruit, wood and bark symptoms also occur. citricida, the brown citrus aphid, has not yet occurred in Florida, but has been recently discovered These symptoms include mosaics, yellowing and throughout the Caribbean. Three major virus-like ringspots. A mosaic pattern consists of light-green, diseases (stubborn, greening and citrus variegated yellow or white areas mixed with the normal green chlorosis) are caused by specialized types of bacteria color of leaves. Depending on the intensity of and are spread by several different leafhoppers and 2 infection or the particular pattern of discoloration, species of citrus psyllids (insects the size of mosaics can be described as mottling, streaking, vein planthoppers). clearing, vein banding, chlorosis and spotting. Yellowing refers to a uniform discoloration or IDENTIFICATION AND DETECTION chlorosis of foliage without any spotting patterns. Ringspot is a distinctive pattern of a brown, The classic means of identifying virus and virus- red-brown or yellow border surrounding a green like infections in citrus is based on identification of center. symptoms in the field or by inoculating citrus indicator plants (herbaceous and woody plants that Transmission are sensitive to a particular virus). Herbaceous indicator plants have been used 1) to identify some Plant viruses can be spread in various ways, mechanically transmitted viruses and 2) to detect including propagation (budding and grafting), unsuspected latent infections (infection without the contaminated plant sap, seed or pollen, insects, mites, development of visible symptoms) not revealed by nematodes, certain fungi and parasitic plants tests using citrus indicator plants. Reliable herbaceous (dodder). The principal means of transmission of indicator plants have been found for exocortis, but citrus viruses are infected propagative material, not for tristeza, xyloporosis and most forms of insects and contaminated tools. psorosis.

The primary purpose of budwood certification Although improvement in the use of citrus programs has been to prevent the spread of viruses by indicator plants has been made, plant procedures still infected budwood and contaminated seed. Despite require extensive periods of time, good plant material various quarantines against the movement of and facilities, and skilled personnel. Interpretation of potentially diseased plant material, including results for mild strains (virus strains that cause only budwood, man has frequently moved citrus viruses mild symptoms) and for mixed infections (infection of long distances and established them in new a plant by more than one virus at the same time) may production areas. Seed transmission of psorosis has depend on temperature, plant vigor and the been observed in Troyer , Carrizo citrange experience of the observer. and trifoliate . No other citrus viruses are known to be transmitted through seed. Pollen Considerable progress has been made in transmission of citrus viruses has not been developing serological detection procedures for citrus demonstrated. viruses. Serology refers to the use of a portion of animal blood, the serum, in procedures that are used Inoculation of healthy plants with sap from to identify viruses. The first step in the serology infected plants (mechanical transmission) is important procedure is to inoculate animals, usually rabbits or in the field spread of pathogens, such as citrus mice, with purified virus. The virus acts as an antigen exocortis viroid which can be easily spread as a or foreign substance that stimulates the immune contaminant on pruning and cutting tools. The use of system of the animal to produce specific antibodies virus-free budwood and budwood certification that react only with the virus injected. These programs are highly effective for controlling viruses antibodies are collected from the serum portion of the animal’s blood and are used in various laboratory Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

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tests to identify viruses. One such assay referred to as of seedling yellows is that it indicates the presence of ELISA (Enzyme Linked Immunosorbant Assay), has severe strains of tristeza. been used around the world to test millions of citrus trees for tristeza. Serology procedures are available Symptoms for three citrus viruses which occur in Florida (tristeza, citrus variegation, and citrus leaf rugose Decline viruses). Field diagnosis of tristeza can be based on CONTROL observation of the following symptoms: 1) tristeza decline, associated primarily with trees on sour orange Control strategies for plant viruses include 1) or rootstocks, 2) affected trees lack avoidance or exclusion of the disease, 2) the use of feeder roots and do not maintain normal amounts of certified budwood, 3) eradication or suppression, 4) starch in roots, 3) declining trees frequently, but not the use of tolerant or resistant cultivars, 5) cross always, show honeycombing and thickening of the protection, and 6) cultural practices that reduce inner bark just below the bud union. infection. The success of each of these control strategies depends on a number of factors, including Tree decline usually results from reduction of the knowledge of the causal agent of the disease, feeder root system or necrosis of the phloem tissue symptoms and mode of dissemination. near the bud union. Decline symptoms can be associated with a number of diseases including foot MAJOR VIRUSES AND VIRUS-LIKE rot and root rot, nematode diseases like spreading DISEASES decline and slow decline, blight, a number of viruses, and root weevil and water damage. In tristeza decline, Tristeza the phloem (conducting tissue located inside the bark through which sugars produced in the leaves by Significance photosynthesis are moved to roots) is affected, thus girdling the tree. This girdling is associated with leaf (CTV), the most destructive chlorosis and wilting, heavy fruit set, starch depletion virus disease of citrus, has caused disastrous losses in in the root system and destruction of feeder roots. many citrus-producing areas worldwide. "Tristeza," Without feeder roots the tree wilts, producing quick which means sadness or melancholy in Spanish, decline symptoms. actually refers to several disease symptoms, many of which occur in Florida. Strains of tristeza exist which Trees declining from tristeza usually have reduced differ in the symptoms they produce. starch levels in their root systems. Starch can be detected by dipping cut ends of roots in an iodine The tristeza symptom most familiar to Florida potassium iodide mixture. Roots turn blue-black when growers is a quick decline of orange, and starch is abundant but the roots of a tristeza-affected mandarin trees on sour orange rootstock. CTV can sour orange tree usually do not stain. However, since also cause stem pitting in limes, some sweet oranges, declining trees affected by other diseases like blight grapefruit and in some root stocks like Citrus often have low root starch levels, this procedure is not macrophylla. Severe stem pitting, which can be very an infallible test for tristeza. damaging, is present in major citrus growing areas such as Brazil, South Africa, Australia and Asia. Trees with "quick decline" may die rapidly, with Severe stem pitting due to tristeza is not present in the progression of symptoms from leaf wilting to tree Florida but would cause severe problems in the future death occurring within several weeks. Such trees may if introduced. Severe strains of tristeza may cause also fruit heavily because of starch accumulation seedling yellows, a leaf chlorosis and stunting of sour above the budunion. A yellow or brown stain may orange, , grapefruit, and seedlings. The occur on the inner face of the bark, just below the leaves on affected plants are small and yellow and budunion. growth usually ceases after the first few leaves are formed. Seedling yellows is an experimental reaction In Florida, trees commonly decline over a period that occurs in laboratory indicator plants and is of several years. Trees that decline slowly usually usually not encountered in the field. The significance develop honeycombing symptoms (a massing of numerous small pinholes on the inside of the bark Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

Citrus Viruses and Virus-Like Diseases Page 4 just below the budunion). In addition, the inner bark in the field and newly propagated nursery trees would of affected trees on sour orange rootstock often become infected eventually in any case. thickens just below the budunion. When budwood infected with severe isolates of citrus tristeza virus is A 1980 survey indicated that about 90% of the propagated on sour orange rootstock, young trees registered budwood sources of sweet orange grow weakly, often set fruit prematurely, are chlorotic propagated on sour orange were infected with and may remain stunted and unthrifty. tristeza. Many of these trees presumably carry mild strains, but since most nurseries have propagated their Stem Pitting budwood sources on tristeza-tolerant rootstocks the severity or virulence of the strain cannot be Stem pitting, a condition associated with tristeza determined from the condition of the tree from which and several other citrus virus diseases, consists of the budwood was taken. depressions in the outer wood with corresponding pegs or projections on the inner face of the bark. This Recent observations clearly show that some pitting can be seen by peeling the bark off small budwood source trees are, in fact, infected with severe twigs. Tristeza-induced stem pitting can vary strains that produce stunted trees on sour orange according to virus strain and host. rootstock. Budwood from trees infected with severe strains produce vigorous, normal trees on In severe cases of stem pitting, the trunk and tristeza-tolerant stocks. However, these trees only scaffold limbs have a gnarled or rope like in serve to increase the reservoir of severe tristeza appearance. Citrus macrophylla seedlings frequently strains that can be spread by aphids to adjacent show moderate stem pitting from Florida strains of plantings of trees on sour orange rootstock. tristeza. Severe strains of tristeza may cause stem pitting in sweet orange cultivars regardless of Three species of aphids (Toxoptera aurantii, the rootstock. black citrus aphid, Aphis gossypii, the melon aphid, and Aphis spiraecola, the spirea aphid) can vector Affected trees are usually stunted or have a more tristeza in Florida. Fortunately, the most effective compact growth habit than normal trees. Sweet vector, Toxoptera citricida, the brown citrus aphid, is orange stem pitting strains of tristeza occur in Brazil, not yet present. Peru, Japan and California. However, no severe stem pitting strains have been reported in Florida. Different strains of tristeza can be spread by different aphids at different rates. Aphid spread of Plants Affected citrus tristeza virus is also affected by environmental conditions and by the host itself. Some host cultivars With few exceptions, most citrus cultivars can apparently are better tristeza sources and some are become infected with citrus tristeza virus (CTV), but better receptor plants than others. In general natural many (mandarins, sweet oranges, and spread is more rapid in orange and grapefruit than in ) often do not show obvious symptoms). other citrus. Others (lime, lemon, grapefruit, citron and Citrus macrophylla) show symptoms of varying intensity. Control and some trifoliate orange hybrids such as Carrizo citrange are resistant to tristeza Tristeza Resistant Rootstocks infection. That is, the virus does not multiply in these plants even when they are grafted with CTV-infected Several conditions affect control strategies for scion material. citrus tristeza virus (CTV) in Florida: 1) the virus is already widespread and most budwood sources are Transmission infected, 2) CTV is naturally spread by aphids from the large inoculum source already present. The Tristeza is spread in Florida by propagation and grower is faced with the choice of either accepting the by aphids. By 1968, extensive natural spread of risks of tristeza and planting trees on sour orange tristeza by aphids forced the Budwood Registration rootstock or of choosing another rootstock with other Program to abandon hopes of maintaining the Citrus inherent disease susceptibilities and horticultural Budwood Foundation Grove as virus-free. Valuable characteristics. scion sources could not be maintained free of tristeza Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

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Tristeza-tolerant or resistant rootstocks are new horticultural selections from overseas is always a available, and tristeza decline can be avoided by using temptation and cannot be entirely prevented by rough lemon, , Rangpur lime, regulations. Growers should therefore strongly Cleopatra mandarin, Carrizo citrange, trifoliate support agricultural quarantines and inspections at orange, sweet orange or Swingle (see Table ports of entry. 1). These alternatives generally have other drawbacks such as susceptibility to blight, foot rot or cold. New Mild Strain Cross Protection hybrid rootstocks are being developed continuously, but their value cannot be determined without years of Mild strain cross protection, whereby the mild field testing. For the moment, the grower must strain is deliberately introduced into a tree and evaluate all risks carefully and choose the rootstock prevents the subsequent expression of severe strains that poses the fewest risks for his own situation. which are inoculated later, has been proposed as a control strategy for tristeza. Healthy-looking trees on The tristeza situation in Florida will not improve sour orange carrying mild strains of tristeza may, in and growers should not use sour orange without fact, have a natural cross protection already. The considering the long term risks. If sour orange protective ability of naturally occurring mild strains in rootstock is used, it should not be propagated with Florida has not been proven although many tests are budwood containing a severe isolate of CTV. At in progress. Preliminary experimental data suggest present this can best be done by ascertaining that the caution in that some mild isolates do not protect well budwood source has previously performed well on against aphid reinfection with severe quick-decline sour orange and by observing that the young budlings isolates. Mild strain cross protection is used on a grow off well in the nursery and in young plantings. commercial basis in Brazil to protect against the stem Beware of budwood sources that perform markedly pitting effects of citrus tristeza virus (CTV) in Pera less well on sour orange than on Cleopatra grafted on CTV-tolerant rootstocks, primarily or Carrizo citrange rootstock. Rangpur lime. Only very limited field data for cross protection in trees on sour orange rootstock are Screening available from Florida, California and Australia. Mild strain cross protection may eventually be used to help The Budwood Registration Program is screening deter CTV decline effects on sour orange but it will some of the most heavily used registered scion trees not be a complete long term solution. and information on the specific citrus tristeza virus (CTV) content of individual source trees should soon Long Term Approaches be available. Since biological screening tests are slow and difficult to conduct on a large scale, means to A long term approach to tristeza control is to rapidly screen trees for strain severity remains a high develop resistant scion cultivars and citrus tristeza research priority. virus (CTV) tolerant sour orange types. The resistance found in trifoliate orange can be It is important to all growers that the reservoir of transferred by hybridization and preliminary results severe CTV isolates not be increased needlessly by suggest that development of CTV resistant scion propagation. Yet with the current production of over cultivars with acceptable fruit quality is possible. 14 million budded nursery trees per year, the Unfortunately, incorporating the needed horticultural potential is obvious. properties will be more difficult than incorporating CTV resistance. Growers who choose tristeza tolerant or resistant stocks are less likely to be concerned than those who Another approach is to reduce natural spread by choose sour orange. aphid vectors, either by direct control of the vector at critical periods or by developing cultivars that are Quarantine efforts should be maintained and repellent to aphids. increased to prevent entry of more severe CTV strains from overseas and from other citrus producing areas and to prevent entry of the brown citrus aphid which is the most efficient vector. Smuggling of prize Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

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Table 1. Susceptibility to Tristeza Decline. veins. Leaf flecking arranged in an oak leaf pattern centered on the midrib is associated with concave Rootstock Susceptibility gum form of psorosis. Leaf patterns fade as leaves mature and usually are not visible in fully mature Carrizo Citrange not susceptible leaves. Citrus macrophylla more susceptible Psorosis B leaf symptoms consist of flecking and Citrus volkameriana not susceptible chlorotic blotch patterns, often with some ringspot Cleopatra Mandarin not susceptible patterns that can persist in mature leaves. Fruit may show partial or complete rings of sunken tissue on the Milam not susceptible rind. The undersurface of mature leaves may also Rangpur Lime not susceptible show brown swellings that resemble greasy spot. Since Rough Lemon not susceptible meticulous inspection is required to find leaf symptoms even on known infected trees, leaf flecking Sour Orange very susceptible is generally not considered to be a good field Sweet Orange not susceptible diagnostic symptom.

Swingle Citrumelo not susceptible Bark Symptoms Trifoliate Orange not susceptible In Florida, psorosis A bark scaling usually develops approximately 6 years after the appearance of leaf symptoms. Scaling begins in isolated areas of Psorosis the trunk or main limbs and consists of the separation from the bark of small, dry irregular flakes 0.2-0.3 Significance mm (1/127-1/84 inch) thick. Scaling involves more and more of the bark until the affected area encircles the Psorosis, a complex of diseases that is distributed entire trunk, severely affecting tree health, yield and worldwide, can affect most citrus cultivars. The causal susceptibility to freeze injury. Scales remain attached agent of psorosis has not yet been identified, but it is at the edge of the lesion and curl outward like a assumed to be a virus or a group of viruses. The shingle. Conducting tissue just inside the bark forms of psorosis that occur in Florida are psorosis A, becomes impregnated with brown gum. When lesions psorosis B, blind pocket and concave gum. There is become advanced, normal transfer of nutrients is some evidence that the psorosis B strain may be impeded by the gum formation and the portion of the identical to some strains of citrus ringspot virus. tree above the lesion declines. The curling of the bark to produce an awning-like effect and the exudation of Psorosis had been well controlled by the Budwood minor quantities of gum help to distinguish psorosis Registration Program but can still be found in older A from scaling induced by other causes. In psorosis B, plantings in many areas. scaling and wood symptoms are similar to psorosis A except that they develop more extensively. Recently, interest in psorosis B or ringspot has increased because natural spread occurs by unknown Blind pocket psorosis is characterized by means in Argentina, Texas, and, in one case, in steep-sided, narrow, channel-like parallel depressions Florida. Tree decline from natural psorosis infections running lengthwise in the trunk. A form known as is currently a major problem in Argentina and is eruptive blind pocket psorosis is further characterized regarded as a potential threat in Florida and Texas. by scaling of the bark and the flow of gum. Neither type of psorosis occurs frequently in Florida, but they Leaf and Fruit Symptoms are mentioned here because blind pocket psorosis is sometimes confused with folds that normally occur in All forms of psorosis can cause flecking symptoms cultivars such as , and trifoliate in young leaves but these symptoms normally are seen orange. Concave gum psorosis causes somewhat only in early spring in the field and even then only on similar symptoms, but the depressions are less severe. some leaves. Leaf symptoms characteristic of psorosis Limbs may be flattened somewhat to create an A consist of a flecking pattern arranged in faint bands "ax-handle" effect. In contrast to normal depressions, 1/4-1 mm wide (1/101 - 1/25 inch) along the leaf Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

Citrus Viruses and Virus-Like Diseases Page 7 gum impregnations are found in the wood with Control concave gum and blind pocket forms of psorosis. Florida growers who purchase registered trees Plants Affected should have no psorosis problems. The observation of natural spread of a form of psorosis (ringspot) in Most cultivars develop leaf symptoms, but bark Argentina and, to a lesser extent, in Texas, is scaling and tree decline occur primarily on sweet triggering some additional research on psorosis. At orange, grapefruit and some mandarins. Even least one case of natural spread has been observed cultivars which do not express distinct symptoms experimentally in Florida but it apparently remains generally can be infected by the virus. Budunion uncommon. Growers who are replanting in areas effects have not been described, but different heavily infested with psorosis should watch for reactions can be seen readily in some scion-rootstock evidence of natural infection in young trees and combinations (see Table 2). For example, when sweet contact their Extension office immediately if orange scions are grafted on sour orange rootstock, symptoms are observed. bark scaling is confined to sweet orange. Exocortis Transmission Significance All strains of psorosis are transmitted by infected budwood. No vectors are known but they are was originally considered to be suspected in some locations. Experimental, caused by a virus, but is now known to be caused by mechanical transmission of some strains has been a viroid; a small, infectious, self-replicating nucleic demonstrated, but mechanical spread in the field has acid molecule without a coat protein. Viroids are not been reported. Seed transmission of psorosis extremely small and, even when highly magnified with occurs in Carrizo and Troyer and in special techniques, are difficult to visualize with an trifoliate orange. electron microscope. Since the viroid molecule has a special configuration, it is stable to heat and to other Table 2. Susceptibility to Psorosis. treatments which inactivate viruses.

Rootstock Susceptibility The primary economic effect of citrus exocortis viroid (CEV) is dwarfing of trees grafted on Carrizo Citrange not susceptible susceptible rootstock. Scaling of the rootstock bark Citrus macrophylla not susceptible may also occur. The effects are rarely lethal and the degree of stunting varies with the strain of CEV. Citrus volkameriana not susceptible Major damage from exocortis has not occurred in Cleopatra Mandarin not susceptible Florida because exocortis-free budwood sources were developed before exocortis-sensitive rootstocks were Milam not susceptible used extensively, and the possibilities for spread on Rangpur Lime not susceptible contaminated tools were recognized. Rough Lemon not susceptible Strains of exocortis vary greatly in severity. Mild Sour Orange not susceptible forms of exocortis have been used to produce dwarfed Sweet Orange susceptible citrus trees for high-density plantings. While this approach to tree dwarfing is promising, it may have Swingle Citrumelo not susceptible limited application in Florida where Trifoliate Orange not susceptible exocortis-sensitive stocks (trifoliate orange, Carrizo citrange, Rangpur lime and sweet lime) are also susceptible to blight. Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

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Symptoms and grapefruit are less susceptible to mechanical inoculation than sweet orange. If a tree is The most obvious field symptoms of exocortis are large enough to hedge and top, then exocortis bark scaling on the rootstock and general stunting of infection should not be a problem even to trees on the tree. Bark scaling usually begins when trees are sensitive rootstocks. Some eventual reduction in from three to eight years old. Infection by severe growth could occur if mature trees were infected but strains becomes apparent more quickly than infection these trees should continue to be productive. by mild ones. The first symptoms are shallow, longitudinal splits in the bark below the budunion. In Accidental contamination of budwood source time, splitting occurs over the entire rootstock and trees, nursery trees or young tree plantings via strips of bark begin to scale off. In contrast to some budding or pruning equipment can be a very serious other diseases, the bark tissue underneath the scales problem and must be avoided. Growers should remains alive. purchase trees propagated from exocortis-free budwood and should protect young trees against Severe strains of exocortis can stunt trees badly, contamination. especially those on trifoliate orange rootstock. Fruit quality is normally not affected. Yield reduction is For example, Carrizo citrange has been frequently generally associated with reduced canopy size. A rapid used as a replant rootstock in mature grove sites and indexing method is available for exocortis which can easily be contaminated during normal grove utilizes the viroid-stimulated leaf distortion and operations. stunting of citron and several herbaceous plants. Another rapid indexing procedure which Disease Control involves purifying citrus exocortic viroid from infected tissue and subjecting it to laboratory analysis has Since exocortis can be spread through recently been developed. propagation of infected budwood and via contaminated budding or pruning tools, budwood Plants Affected certification coupled with decontamination of cutting tools constitutes the primary control strategy. Two Trifoliate orange, Carrizo and Troyer citrange and disinfectants that have been found effective against Rangpur and sweet lime are important commercial the viroid are an aqueous solution containing 2% rootstocks susceptible to scaling; however, cultivars sodium hydroxide plus 2% formalin or a freshly made which do not express distinct symptoms generally 5 - 10% solution of common household bleach. allow replication of the viroid. Budunion effects have not been described, but different host reactions can be seen readily in some scion-rootstock combinations. For example, when sweet orange scions are grafted on trifoliate orange rootstock bark scaling is confined to the trifoliate orange tissue of the trunk.

Transmission

Exocortis can be spread by budding and grafting and as a contaminant on pruning equipment. The Budwood Registration Program has largely eliminated the spread of exocortis through the use of registered nursery stock, but exocortis-infected citrus is still produced from nonregistered sources in Florida. Trees with tolerant scion-rootstock combinations will not show any obvious symptoms (see Table 3). Hedging equipment can probably spread the viroid, but the extent of the spread depends upon the number of trees that are infected, the cultivars that are infected and the cultivars that will be inoculated. Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

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Table 3. Susceptibility to Exocortis Viroid. symptoms become well developed, a flat cut about halfway into the bark will reveal gum pockets of Rootstock Susceptibility varying size. Symptoms usually take 18-48 months to develop in highly susceptible cultivars such as Orlando Carrizo Citrange more susceptible tangelo and Citrus macrophylla and longer in less Citrus macrophylla not susceptible sensitive cultivars. Satsumas may not show symptoms for 8 years or more. Indexing is usually done by Citrus volkameriana not susceptible inoculating an indicator side graft of Parson’s Special Cleopatra Mandarin not susceptible mandarin on a vigorous rootstock such as rough lemon, or by grafting the test plant on Orlando Milam not susceptible tangelo or Ellendale mandarin seedlings. Rangpur Lime more susceptible

Rough Lemon not susceptible Plants Affected Sour Orange not susceptible Xyloporosis can affect most tangelos, some Sweet Orange not susceptible mandarins, many mandarin hybrids, sweet lime and Citrus macrophylla. Rough lemon may also show mild Swingle Citrumelo not susceptible symptoms. It is especially severe on Citrus macrophylla Trifoliate Orange very susceptible and Orlando tangelo. Oranges, grapefruit, , acid limes, some mandarins, trifoliate orange and its hybrids are among those hosts which can be infected, but usually don’t show obvious symptoms (see Table Xyloporosis/Cachexia 4).

Significance Transmission

Xyloporosis/Cachexia has generally been Like exocortis, xyloporosis can be transmitted by considered a virus disease but recent evidence infected budwood and contaminated cutting tools. A suggests it is caused by a viroid. Xyloporosis is surplus of white grapefruit has led some growers to common in old-line trees and is a continuing problem top work old-line trees with other cultivars that are in where growers have top worked old-line trees with greater demand. Top working involves grafting or cultivars such as mandarin hybrids that are sensitive budding a new scion cultivar onto an existing to xyloporosis. Xyloporosis-free budwood for nearly rootstock-scion combination. The new scion material all cultivars is available, but in an attempt to cut costs, is set in the main scaffold branches after the tree has growers sometimes pay dearly for using unregistered been pruned severely or is set directly in the trunk budwood. following removal of the entire top of the tree. When mandarin hybrids are propagated this way, they can Symptoms become infected by the xyloporosis pathogen that was present but not expressed in the white grapefruit Xyloporosis was originally described in sweet lime scion. Conversely, if Orlando tangelos are top worked, and cachexia was described in Orlando tangelo, but they may also become infected unless virus-free the diseases are apparently identical. Fovea is a budwood is used for top working. similar disease in Murcotts. Xyloporosis can cause stunting, chlorotic foliage and decline symptoms that Control can be similar to those caused by other agents. The definitive symptoms of xyloporosis are stem pitting Control of xyloporosis can be achieved by using and gum impregnation of the bark in sensitive registered budwood and by decontamination of cultivars. Pitting and gum development usually begin cutting tools. Two disinfectants that have been found near the budunion, but may spread to the effective are an aqueous solution containing 2% xyloporosis-sensitive portion of the tree. The pits and sodium hydroxide plus 2% formalin or a freshly made corresponding pegs are not as angular as those found 5-10% solution of household bleach. Top-working in tristeza-affected trees and may result in a generally sensitive cultivars should be avoided when xyloporosis bumpy surface on both wood and bark faces. Pegs on could be present in the rootstock or scion. the bark face usually contain gum. Once these Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

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Table 4. Susceptibility to Xyloporosis. serological techniques are available and the Enzyme Linked ImmunoSorbant Assay procedure can be used Rootstock Susceptibility for rapid detection of CVV. Use of registered budwood should prevent problems with CVV in new Carrizo Citrange not susceptible plantings. Citrus macropyylla very susceptible Citrus Leaf Rugose Virus Citrus volkameriana not susceptible

Cleopatra Mandarin not susceptible Citrus leaf rugose virus (CLRV) is related to citrus variegation virus. CLRV was discovered by Milam not susceptible chance in an old variety planting near Eustis, Florida Rangpur Lime susceptible and is thought to be spread naturally, possibly through pollen. Subsequent indexing showed it to be Rough Lemon susceptible present in a number of cultivars, including early Sour Orange not susceptible introductions from California and several seedlings Sweet Orange not susceptible trees. Serological techniques are now available for the detection of CLRV. Swingle Citrumelo not susceptible

Trifoliate Orange not susceptible CLRV causes minor leaf flecking in lemons, some puckering in leaves of Mexican lime and a severe stunting in young grapefruit seedlings. It infects a large number of other cultivars without producing MINOR VIRUS DISEASES obvious symptoms. This disease is not yet widespread and has not been found in registered budwood The current absence of extensive natural spread sources. As with citrus variegation virus, the best and the use of disease free registered nursery stock control strategy for CLRV is to avoid the disease by currently seems effective in containing the following using only registered budwood sources. diseases. Several of these diseases could be extremely damaging if they become widespread. Growers should Citrus Ringspot Virus be aware of these diseases and their destructive potential. The spread of citrus ringspot virus (CRSV) presents a classic illustration of the importation and Citrus Variegation Virus spread of a virus disease on infected nursery stock. CRSV was first isolated in Florida from a young Star Citrus variegation virus (CVV) has been found in Ruby grapefruit tree that had been smuggled from all major citrus producing regions, including Florida. Texas into Florida. Budwood cut from infected trees Once considered a form of psorosis, CVV and the was used in a commercial nursery, further spreading closely related crinkly leaf virus are now known to be the disease. distinct pathogens. CVV can be readily transmitted mechanically to non-citrus hosts. Although some natural spread of ringspot has occurred in Texas, there is no good evidence of Several different isolates of CVV have been found natural spread in Florida. The Texas strain of CRSV in different locations in Florida. CVV can produce and subsequently discovered Florida strains produce variegated leaf symptoms in , lemons and similar symptoms but the viruses have not yet been grapefruit, and milder symptoms in many other hosts, fully characterized. The relationship of the naturally including sweet orange. Striking leaf and fruit spread form of psorosis in Argentina to CRSV strains symptoms often appear in grapefruit after a severe in Florida also needs clarification. The persistent winter, but the trees may subsequently grow normally observations of natural spread of this disease are with few visible symptoms. ominous because CSRV strains appear capable of causing severe damage to mature trees. At present, Normally, CVV can be detected in Etrog citron the best control policy is to use registered budwood indicator plants while indexing for exocortis, but a and to be vigilant against natural spread of the recently discovered mild isolate produced very weak disease. symptoms in this indicator plant. Fortunately, good Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

Citrus Viruses and Virus-Like Diseases Page 11

Strains of psorosis B commonly produce The best control strategy is to reduce the number symptoms similar to those produced by CRSV. These of TL-CSV infected trees. All new plantings of Meyer psorosis strains are mechanically transmissible to lemon should be from virus-free sources. Other herbaceous indicator plants, producing leaf lesions in cultivars should never be grafted on old-line Meyer these herbaceous plants and typical leaf ringspot lemon or on grafted to other cultivars. symptoms in grapefruit seedlings. Numerous sources of the psorosis B strain have been found in old trees Algerian Navel Orange Virus in Florida that exhibit bark-scaling symptoms. This virus was discovered in a navel orange Tatterleaf-Citrange Stunt Virus cultivar imported many years ago from Algeria when that cultivar was screened for virus diseases using In Japan and the United States, tatterleaf-citrange herbaceous indicator plants. This virus produces stunt virus (TL-CSV) has been recovered from citrus symptoms in several herbaceous indicator plants but originally imported from China. Although it is of it has not yet produced symptoms in any of the limited distribution and natural spread has not been seedling citrus cultivars tested thus far. Host range reported in the US or Japan, it is of interest because tests on grafted trees have yet to be done. of the devastating scion-rootstock incompatibility it causes in inoculated mandarin and sweet orange trees At this point there is no indication of a disease on trifoliate orange or citrange rootstocks. The virus problem associated with this virus but its presence is widespread in Meyer lemon trees in Florida. Meyer indicates that all the viruses affecting citrus have not lemon as well as orange, mandarin and grapefruit can yet been discovered. Some of these viruses may not be symptomless carriers. The virus can be detected by become apparent until a sensitive host is infected. graft inoculation to Rusk citrange or Citrus excelsa plants, or by mechanical inoculation to beans. Archival copy: for current recommendations see http://edis.ifas.ufl.edu or your local extension office.

Citrus Viruses and Virus-Like Diseases Page 12

Milam Stem Pitting

In the mid-1970’s, a severe stem pitting condition was observed in some Milam lemon seed-source trees. Definite but less severe pitting was also observed in several mandarin hybrids, including Robinson, Lee and Page. The symptoms were very similar to those caused by tristeza, but tristeza was not found in all of the pitted trees. Milam trees with stem-pitting were top worked to different cultivars to determine if it would severely affect other cultivars. No striking symptoms occurred in any of the eight cultivars tested, including and Marsh grapefruit. Transmission tests have been inconclusive. Pitting has not been produced on small, container grown plants in the glasshouse or screenhouse. Pitting is generally confined to the trunk and major scaffold limbs on affected trees in the field and does not extend below ground on Milam seedlings. This pitting does not appear to affect tree vigor and has not yet become a problem. Growers, however, should be aware of this situation and propagate Milam, Page, Lee and Robinson from sources free of obvious stem-pitting.