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The Effects of Virus and Viruslike Diseases on Citrus Production In -11- The Effects of Virus and Viruslike Diseaseson Citrus Productionin Florida S. M. Garnsey Summary Florida hasnot experiencedas much devastatinginjury from virus diseasesas many citrus-growingareas; however, tristeza, psorosis, exocortis, and xyloporosis have all been damaging. Tristela continues to be a major problem, but psorosis, xylopo- rosis, and exocortis are now controllable. Sewral other viruses have been described, but are not widely distributed. New dis- eases,including a stem-pitting disorder of 'Milam' (Citrus jambhiri Lush. hybrid?) and some tangerine hybrids (Citrus paradisi Macf. X Citrus reticulata Blanco), are appearing. Several viruses haw been discowred by inoculating herbaceous plants, but relationship of these viruses to specific diseaseshas not been established. Introduction of new citrus varieties, rapid shifts in rootstocks, and rapidly changing production practices will contribute to future problems. Vigorous researdt and regulatory programs will be needed in responseto existing and future problems. Introduction Strictlydefined, virus diseasesare causedby small, infectious nucleoproteins.Commonly, however, infectious citrus dis- easesnot obviouslycaused by fungi, bacteria,or nematodesare called "virus" diseases,although me identity of the causal agentis often unknown. This broaderdefinition will be retainedin this paperso that the necessarytopics can be covered. Emphasiswill be placedon diseaseeffects, not on propertiesof the causalagent. Somediseases that will be covered,haw beencalled virus diseases,but are now known to haveother causalagents. Examplesare exocortis, caused by a small, naked, infectious nucleicacid, pro~sionally calleda viroid or pathogene(41,42), and stubborn,which hasbeen associated with a mycoplasmalike organismmuch largerand more complex than a true virus (3, 11). Young tree decline(YTO) and sandhill decline(SH 0), which are very similar to the older and alsounsolved decline problem called blight (30),are cowred specific- ally by other authorsand will be treated only briefly in this paper. Regardle~ of nomenclature,virus and viruslike diseaseshave caused serious problems in most citrus-producingregions of the world. Thesediseases often limit the production of certaintypes of citrus in someareas. In addition, "latent" virus in- fectionscan causewidespread but lessobvious losses (43,44). For severalreasons, Florida hashad lessserious virus problemsthan most major citrus areas. In Florida, orangesand grapefruit (C.paradisi) havebeen grown mostly on rough lemon (C.jambhiri) and sour orange(C. aurantium L.) rootstocks. Exocortisand xyloporosis,although common in most mature plantings,do not causeobvious symptoms on thesetrees. Psor- osishas been under increasinglyeffective control for a number of yearsby budwoodregistration. Tristezavirus hasbecome widespread,but severeinjury to sour orange-rootedtrees has occurred only in localizedareas. Natural infection of grapefruit treesby tristeza hasbeen uncommon. Despitepast good fortune, concernabout citrus virus diseasesin Florida is increasing.Tristeza has spread rapidly into existingplantings on the eastcoast of Florida in recentyears, and evidenceof tristezadecline is increasingin this area. In spite of tristeza damage,sour orangeis beingwidely usedin new plantings. New virus or viruslike diseasesare appearing.Some, such as the new stem-pittingdisease in 'Milam' (a probably rough lemon hybrid) and in tangerinehybrids suchas 'Robinson', 'Page',and 'Lee' (C. reticulata XC. paradisi) (49), threatento be largeproblems in the future. Damageto rough lemon-rootedplantings in recentyears by YTD and SHD is causinga rapid shift to other rootstocks. The~ are largely untestedcommercially in Florida, and manyare susceptibleto exocortisand/or xyloporosis. New scion varieties,which may harbor unsuspectedsusceptibility to virus di~ases,are alsobeing propagated. Production practicescontinue to changerapidly in Florida. Many of thesechanges probably will not affect the citrus virus diseasesituation; but the effects of herbicides, permanent irrigation, hedging and topping, abscission agents, and mechanical harvesting devices are undetermined and may affect virus spread and diseasesymptoms. -78- This paper will review the variousvirus and viruslikediseases in Florida andwill discuss,where possible,the problemsthat lie ahead. Some discussion of the possible beneficial use of citrus viruses for cross protection and tree-size control will also be included. MajorViruses Tristeza. Tristeza remains a major threat to Florida citrus growers, in spite of its past failure to cause more widespread damageto sour orange-rooted trees. The presenceof tristeza in Florida was confirmed in 1951 (34), but it was un doubted- Iy introduced much earlier (20). Significant natural spread occurred first in central Florida, and then later in all major citrus areas in the State (5,34). It has just recently spread rapidly into existing plantings on the east coast and IMer interior (5). These plantings are largely on sour orange and were nearly free of tristeza until recently. The mostefficient vector of tristeza, Toxopteracitr;c;dus Kirk., hasnot ooenreported in Florida; but the 3 aphid vectors present(35) can causeconsiderable natural spread when inoculum is plentiful and vector populationsare high. The effect of tristeza on sour orange-rooted trees in Florida has been variable. Quick decline symptoms have been ob- served (Fig. 1), but a slower decline is more typical. Even more common are large numbers of tristeza-infected trees on sour orange that show no obvious signs of infection. The absence of symptoms is probably due to a predominance of mild strains of tristeza and mild climatic conditions. Florida isolatesof tristezaoften producemild vein-clearingand stem-pittingsymptoms in 'Mexican'lime (C.aurantifolia [Christm.] SNing.) indicators, but some isolates causesevere symptoms. Some isolates, especially from 'Meyer' lemon (C. limon [t.] Burm. f. hybrid), can causeseedling yellows in 'Eureka' lemon (C. limon) (20). Tristeza stem1Jitting in grape- fruit or sweet orange has been rare. Natural infection of grapefruit trees has been uncommon, but does occur and may be increasing (5). Tristeza decline in mature grapefruit trees on sour orange has recently been observed in central Florida. Fig.1. Tristezaquick decline symptoms in 'Valencia'tree on sourorange root. Treeis approximately20 yearsold. Phototaken an n3, at WinterGarden, Fla. .79. Tristezawill continue to be a problem in Florida citrus for a long time. The useof sour orangerootstocks is increasing, partly becauseof its VTO tolerance. Somelocally severedamage seems certain to continue as it hasin the past. The ex- tent of future damageprobably dependson the proportion of nM treesthat becomeinfected with severeand mild strains and whether treesinfected with mild strainswill resistsubsequent inoculation by severestrains (33,47). It is probable that there is somenatural cross-protectionat work in Florida, althoughthis is difficult to prove. There is considerablein- terest in deliberateuse of cross-protection,and this approachis beingstudied here. Onedifficulty with cross-protection testsin Florida is lack of rapid meansto subjectplants infectedwith mild strainsto natural challengeby severestrains to determinethe "protection" given by the variousmild strains. While naturalspread is occurring,young plants in the field do not all becomerapidly infectedand do not necessarilyget challengedby severeisolates. Some strainsof tristeza aretransmitted more readily than others in Israel(2). The relativetransmissibility of Florida strainsof tristeza hasnot beenstudied, but this factor could havean effect on the relativedistribution of different tris- tela strainsin new plantings. The largenumbers of uninfectedgrapefruit trees on sour orangein Florida appearvulnerable to further and more rapid spreadof tristezaisolates capable of causingdecline. Our grapefruittrees, regardless of stock, are alsovulnerable to severe stem-pittingforms of tristezathat exist in many parts of the world. Pitting hasbeen induced in experimentallyinoculated plants (24) and could be a problem if pitting strains becomewidespread. Reports of tristeza-related problems with citranges (poncirus trifoliata [L.] Raf. X C. sinensis Osbeck) and trifoliate orange(P. trifoliata) from other areas(8,36) suggestthat tristezawill be a continuing problmn in rootstock selection. However,no tristezaproblems have been reported to date on 'Carrizo' citrange-or trifoliate orange-rootedtrees in Florida. £xocortis. Citrusexocortis virus (CEV) is presentin most old-line Florida citrus trees. However,typical CEV symptoms, ar9 rare, becauseCEV-sensitiw rootstocks have been used sparingly until recently. The CEV isolatesfound in Florida vary widely in their effect on treesgrafted to trifoliate-orangerootstocks and on 'Etrog' citron (C. medica t.) indicators. Many CEV isolatescause severe tree stunting and bark scalingon trifoliate-orangerootstocks. Thesealso cause severe symptoms in citron indicators. Other isolatescause little stunting or scalingin treeson trifoliate orange,but causedefinite, although mild, symptomsin citron indicators. Intermediateforms are alsofound. There are indicationsfrom the budwood certification programindexing tests that symptomsof stunting and bark scaling in trifoliate orange-rooted trees are not always linked (G. D. Bridges, personal communication). Severescaling is not always accompanied by severestunting and, conversely, severestunting may occur with little
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