The Threat of Cadang-Cadang Disease

19931 MARAMOROSCH:CADANG-CADANG t87

Principes,37(4), 1993, pp. r87-r96

The Threat of Cadang-CadangDisease

Kenr Menerr,roRoscH Department ofEntomology, Cook College, New Jersey Agricuhural Experiment Station, Rutgers-The State Uniuersity, Neu Brunswick, Nl 08903

"milk") ABSTRACT (coconut and the palms provide the only shade and building material. of cadang-cadang disease In 1975 the viroid cause Cadang-cadang disease occurs and of coconut and other palms became established in the Philippines and Guam. The suspected occurrence of spreads currently.on Luzon and a number this disease on other Pacific inlands requires confir- of other Philippine islands, as well as on mation. Replanting with the early maturing Mawa Cuam. The diseasehas been suspected on cultivar, widely advocated in the Philippines, merely a few other Pacific islands recently. provides a temporary but inadequate remedy because this cultivar is susceptible to viroid infection. The HistoricalBackground spread of the disease could be controlled by proper "dying-dying," extension work, requiring the thorough decontami- Cadang-cadang means nation of tools used by plantation workers. Concen- or slowly dying in Bicolano, the language trated sodium carbonate solution can degrade RNA viroids, remaining stable and retaining its RNA- spoken in southeastern Luzon. The first destroying activity under tropical conditions. An well-documented outbreak of the disease extensive testing program for resistance to cadang- was noticed on San Miguel Island off Luzon Such a long-term program will cadang is imperative. in 1928. By 1933 nearly 257o of the require proper funding, commitment, trained person- nel and quarantined importation of coconut cultivars coconut palms had died there and the plan- from all parts of the world. tation owners approached Prof. Gerardo Ocfemia, a U.S. trained plant pathologist Cadang-cadang disease of palms, the and head of the Plant Pathology Depart- most devastating viroid disease known, is ment at the College of Agriculture in Los always fatal. In the Philippines, where the Banos. to helo control the disease. Since disease has killed more than 30 million no fungi or bacteria were found associated coconut palms, currently 1,000,000 palms with dying palms, Ocfemia (1937) con- succumb every year. The Philippines are cluded that the disease was infectious and the world's largest producer of coconuts most likely caused by a virus. Shortly and half of the country"s export income is thereafter the disease reached the main- derived from copra, the dried coconut meat land of Luzon Island. Before the Japanese from which coconut oil is extracted. This invasion in I 94 I , nearly half of the original oil provides the main source of fat in the 250,000 coconut palms on San Miguel had diet of the local population. Elsewhere died and the disease appeared in several coconut oil is used in soaps. margarines. provinces in the Bicol area of Luzon, as synthetic rubber, cosmetics and moistur- well as on some nearby islands. During izing compounds. Coconut palms also pro- World War II no further research was vide lumber, while leaves are used for carried out, but after the war the Philip- thatching, brooms, baskets and hats. The pine Government obtained active help from husk fiber is transformed into mats and the United States, through the Interna- carpets, and ropes are made from the yarn. tional Cooperation Administration (ICA). On many Pacific atolls the only potable By that time cadang-cadang was devas- liquid is provided by the coconut water tating plantations in the provinces of Albay, 188 PRINCIPES lVoL. 37

Sorsogon,Camarines Sur, and Camarines found as causative agents of other plant Norte, as well as on the islands of Samar, diseases(Romaine and Horst 1974; Yan Masbate,and Catanduanes.On SanMiguel Dorst and Peters 1974; Diener 1979, 90% of the palms were dead and the 1987). In 1975, Randles provided evi- remaining onesdied soonafterwards. Else- dence for the association of two RNA spe- where on Luzon the disease incidence cies with cadang-cadang disease. The ranged from IOTI ta 60To. ICA assigned establishment of the viroid etiology was Dr. Donald De Leon, an entomologistwho followed by intensive studies on the epi- had earnedhis Ph.D, at CornellUniversity demiology of the disease and rate of spread in 1933 and specializedin insect trans- as well as on certain measures to control missionof virusesand taxonomy.to study cadang-cadang. Surprisingly, by 1992 the the diseasein the Philippines(De Leon and diseasehas not yet entered the main coco- Bigornia1953). In 1953 the ICA abruptly nut growing areas in Laguna province' Its cancelledthe technicalassistance program spread in some areas appears to be very for cadang-cadangand perman€ntly aban- slow, yet in parts of Camarines Sur, where donedit under the pressureof U'S. soy- the incidence in 1956 was only 37o, some bean and corn oil producers' lobby. The areas are now heavily affected and up to Philippine Government turned for help to 70% of the palms are dying. the United Nations' Food and Agriculture Organization (FAO). During the following Symptomatology four decades,experts were sent by FAO to the Philippinesto study the devastating The cadang-cadang disease cannot be diseaseand to determineits cause,manner diagnosed authoritatively by symptoma- of spread,and possiblemeans of control. tology, but in an endemic area symptoms Indian,U.S., Australian, Cerman, and Ital- can assist in the detection of affected palms. ian experts were assistedby Philippine sci- On young leaves the earliest symptoms entistsfrom the Bureau of Plant Industry. are tiny, circular, translucent spots on the By 1960 the diseasereached Bondoc veins. On mature leaves the number and Peninsulain QuezonProvince, only a short size of the spots increases so as to impart distance from the solid stand of coconut a characteristic chlorotic pattern of the palmsof Laguna Province (Maramorosch spots (Fig. l). On the lower surface of I 96 I Lessthan 100 palmsof the original mature coconut leaves appear irregular ). "water-soaked quarter million on San Miguel were still spots." Mature coconut standing and slowly dying. Strip surveys leaves display yellow streaks as a result of indicated that more than a million trees enlargement and fusion of adjacent spots. becameinfected every year (Maramorosch The veins and veinlets become cleared in 1964). a very characteristic, although not very Until i967 plant pathologistsdid not pronounced, way. The basal portion of the know of the existence of autonomously petiole of a healthy tree differs strongly replicating low-molecular-weightRNA from those of a diseased one, because the speciesthat could infect and damageplants. stipules of diseasedtrees remain attached In 1967 Diener and Raymer ( I 967) found to the base of the petiole, giving it a winged that potato spindle tuber diseaseis caused appearance. Nuts are produced only dur- by a free RNA. The following year Diener ing the early stages of the disease, but they (1968) demonstratedthat this RNA is sen- are smaller, rounded at the base or mis- sitive to ribonuclease.In I97l Diener shaped and scarified with brown streaks "viroid'n coinedthe name as a genericterm (Fig. 2). Nut bearing of diseasedtrees can for pathogenicnucleic acids of low molec- stop within 18 months, but occasionally ular weight. Viroids were subsequently the period is extended to 4-5 years. A r9931 MARAMOROSCH:CADANG-CADANG 189 comparison of healthy and diseased inflo- Epidemiology rescences shows an abundance of female florets (buttons) on the healthy and fewer The mode of spread of cadang-cadang on the diseased,that is reduced in size and has not been well elucidated. An aerial retains a characteristic upward position of vector has been suspected, but none ever its branches (Fis. 3). found or incriminated. Viroids that cause The fronds of diseased palms gradually potato spindle tuber, chrysanthemum stunt, assume an erect position in the crown (Fig. hop stunt, citrus exocortis, and other viroid 4), dry up, die, and drop off. This results diseasesare mechanically transmissible and in a gradual reduction in the total number do not require vectors to infect susceptible of fronds until a small, yellowish-green or plants (Diener 1979). Man is the actual yellow tuft is left at the apex of the trunk. vector in those diseases. Experimentally, Finally, the bud dies, falls off, and leaves the cadang-cadang viroids have been the crownless trunk standing. A plantation transmitted to coconut and other palms in this stage looks like a field of telephone mechanically (Randles 1985). There is no poles (Fig. 5). doubt that mechanical transmission could Coconut oalms seldom become diseased be responsiblefor the spread of the disease before flowering. In rare cases the disease under natural conditions. The fact that strikes before flowering sets in. The prog- young palms that have not yet commenced ress of the disease is slow, with a five to bearing nuts are very seldom infected might ten year interval between the appearance support this assumption. On the other hand, of first symptoms and the death of younger pollen transmission or long incubation peri- trees. In older palms this period may extend ods would also fit this observation. How- to l5-lB years. ever, pollen transmission could in no way The proper recognition of typical symp- explain the very rare infection of palms toms of the disease helps in field diagnosis before flowers are formed. Pollen trans- but it requires long practice and experience mission could hardly be responsible for the and cannot prove accurately cadang- very slow, perhaps not more than 500 cadang etiology. In an epidemic area, meters, spread of the disease in certain symptomatology is still adequate for rec- areas, while in others cadang-cadang ognizing the disease. However, the symp- seemed to have been able to jump from toms may differ slightly, depending on the island to island. coconut variety and other factors. While The mechanical transmission hvoothe- the progressionof symptoms is constant sis seems supported by observations'made in the Philippines, observations in Guam, by me on Luzon Island (Maramorosch where the disease is called tinangaja, 1987 a, b, 1992). A consistent correlation revealed slightly different nut symptoms was found between the destruction of coco- there (Weston 1918, Maramorosch 196I, nut palms owned by Bicolanos and the lack Boccardo et al. 198I, Boccardo I985). of infection on plantations owned by Taga- The outbreak of cadang-cadang on Guam logs. This correlation, at first, appeared to preceded the appearance of the diseaseon be absurd. However, if we accept that San Miguel Island by more than 20 years viroids are primarily or exclusively trans- (Weston I9I8). No recovery has ever been mitted mechanically by man, the observed observed and the disease is always fatal. correlation can easily be explained. Most Therefore cadang-cadang presents one of likely the cadang-cadang viroids are being the most serious threats to coconut palms carried from infected to healthy palms by not only in the Philippines but also to some tools, called bolos, the machetes used by Pacific islands, and, if not controlled, to plantation workers. Steps are first cut at all of southeast Asia. the base of a palm to facilitate climbing. PRINCIPES lVoL. 37 r e93l MARAMOROSCH:CADANG-CADANG

Afterwards, the same knives are used in the crowns to dislodge the nuts. In addition, flower sap is often being collected for "tuba," the sugary sap that ferments and provides a cheap alcoholic beverage in the Philippines. For tuba collection, crowns of several palms are usually linked with bam- boo planks so workers can move from palm to palm high up in the crowns, without descending each time. This practice easily explains why clumps of diseasedpalms often occur at considerable distance from other diseased palms. If a worker uses his bolo on an infected palm, the cadang-cadang viroid can be transmitted to the next palm when steps are cut into the base, when nuts are being collected, or when the inflo- rescences are being tapped for tuba. Bico- lano plantation owners prefer to hire Bico- lano workers, while Tagalog owners prefer mainly Tagalogs for work in their plantations. Workers employed decades ago on San Miguel island were Bicolanos from 4. Left:healthy coconut palm. Right: diseased palm with erectfronds and leafletsreduced in size. Tabaco, the first locality where subsequently the disease appeared on Luzon Island. The link with Bicolano language seemsto make senseon Luzon, but it does responsible, the localization of the disease not pertain to Guam. There the disease in a very small pocket area in Quezon was actually noticed earlier than in the Province, at the locality of Mulaney, could Philippines (Weston l9l8) and it spread not be explained. This small pocket is sur- all over the island in later years (Boccardo rounded by healthy plantations. Neither l98s). can the hypothesis of pollen transmission It is generally accepted that all viroid be sustained the disease would have diseases are of recent, twentieth-century moved out of Mulaney town since 1958 origin (Diener I979). Despite the fact that if the causative viroids were pollen-borne, all viroids of plants can be transmitted wind-borne, or carried by insects. The mechanically, attempts to find other means mechanical transmission by contaminated of transmission are often being made. machetes of plantation workers remains Attempts to find an insect vector of cadang- the most plausible explanation for cadang- cadang viroids have been continued until caoang. now, even though this seems a complete Cadang-cadang viroids have a narrow waste of time and funds. If an insect were host range, limited to the palm family. No

l. Portions of diseased leaflets in transmitted light, with progressive appearance of spots. 2. Left: healthy female inflorescence with an abundance of buttons. Right: inflorescence from diseased palm, lacking buttons and reduced in size. 3. Left: scarified small nuts from cadang-cadang diseased coconut palm. Right: healthy nuts. PRINCIPES [Vor. 37

5. Coconut plantation on Luzon island, totally destroyed by cadang-cadangdisease' herbaceous hosts are known to be suscep- southeast Asia. In the Philippine Republic, tible. In addition to coconut, Cocos nucife- with its population increasing very fast, ro, several other members of the palm the loss of so many million coconut palms family, growing in the Bicol provinces, were is catastrophic. found to exhibit symptoms similar to cadang-cadang(Maramorosch I96l). The Etiology African oil palm, Elaeis quineensis Jacq., the Anahau (Areca catechu Linn.), the Randles (i975) discovered two viroid- Bunga de China(Adonidia merrilli Becc.), like ribonucleic acid species, associated with and the pugahan fish tail palm (Caryota cadang-cadang affected coconut palms. cumingii Lodd.) have all been found to This finding determined the viroid etiology display the yellow mottle symptoms, oli- of cadang-cadang. Consequently, viroid vaceous spots, decline in fruit production association of tinangaja-affected palms on followed by sterility, brittle leaves, stunt- Guam was also demonstrated (Boccardo et ing, and a general slow decline and death, al. l98l, Boccardo l9B5). characteristic of cadang-cadang. When coconut seedlings were inocu- It is reasonable to assume that cadang- lated with crude nucleic acid extracts by cadang disease is of fairly recent origin in high power injection and by razor slashing coconut palms. Its ability to spread from (Randles et al. 1979), typical cadang- plantation to plantation and from one island cadang symptoms apPeared in the to another, demonstrated clearly in its mechanically inoculated seedlings. Nucleic progress during the past decades, makes acid probes (Randlesand Hatta 1979) were cadang-cadang a dangerous potential threat used in hybridization assays, permitting the to all the islands of the Philippine Republic analysis of the kinetics and comparison of and to other coconut growing areas o[ percentage homology. This method defi- 19931 MARAMOROSCH:CADANG-CADANG r93

nitely identified the presence of cadang- the appearance of symptoms that would cadang viroids in the African oil palm and permit the identification and removal of the buri palm, as well as the Manila palm diseased trees. grown in the Philippines. It also confirmed At oresent. eradication can be carried that tinangaja, the coconut palm disease out much earlier. It was hooed that this of Guam, was cadang-cadang because early eradication would prevent lurther homologous ccRNA was detected there as spread of the devastating disease. How- well (Boccardo et al. l98t). The viroid ever, it has not been proven that the nature of cadang-cadang disease was fur- infected and as yet symptomless trees were ther confirmed by using highly purified unable to contaminate the tools of plan- RNA and demonstrating that it was infec- tation workers. In fact, eradication has not tious and reproduced the disease in been able to prevent further spread of mechanically inoculated palm seedlings. cadang-cadangand diseasecontinues lo Nucleic acid hybridization probes are now appear in places where all infected trees being used in the Philippines to detect were cut and removed. infected coconut palms long before they There is another possibility to control show symptoms of the disease-perhaps cadang-cadang. Viroids form mild strains two years before visual symptoms appear. that barely affect plants but protect them This allows removal of trees before they from infection by a virulent strain (Fernow could become a potential source of infec- 1967, Niblett et al. l97B). If a mild strain tion to neighboring palms. ofthe cadang-cadang viroid could be found in nature or developed artificially, such Control strain could be introduced into healthy seedlings to protect the palms from the Sound and successfulslralesies to con- killer form. Long-term tests will be required trol cadang-cadangshould make use not to implement this approach. only of the available manpower in the Phil- The decontamination of bolos used by ippines but also of facilities of international coconut workers could provide a simple organizations.Simple, reliable and cost effi- control measure, by dipping the knives into cient measures of control will require long- a solution of concentrated sodium carbon- term and costly efforts. ate solution (NarCOr). This solution would Replanting has been suggested as early degrade the contaminating RNA viroids as the 1950s, because the disease spreads and retain its stability and its RNA-degrad- comparatively slowly and kills slowly, so ing ability in the tropical environment. that copra production can be maintained Although this suggestion has been made in affected areas by new plantings. The repeatedly (Maramorosch 1,987b, 1992), use of early maturing varieties, such as it has yet to be implemented. Mawa, permitted coconut production to Hopefully, cadang-cadang will be cur- continue on Luzon Island despite consid- tailed eventually by a combination of con- erable losses. Unfortunately, Mawa palms trol measures-selection of tolerant or are not resistent to cadang-cadang infec- resistant cultivars, introduction of mild tion and they die just as do later maturing strains for cross-protection, and decontam- parms. ination of tools. Usually eradication is recommended as a standard procedure to prevent the spread Discussionand Conclusions of a plant disease. Eradication has failed to control cadang-cadang,probably because Cadang-cadang, like all other viroid dis- of the long period between the actual con- eases,originated in the twentieth century. traction of the cadang-cadang viroids and Where did it come from? A possiblesource t94 PRINCIPES [Vor 37 of the viroid could have been an orna- was reported by Ocfemia from San Miguel mental plant introduced to Guam, and later Island in 1930 and thus natural selection to San Miguel Island around the turn of may have started quite early. I consider the century. Perhaps Spanish boats, sailing the assumptionas incorrect and the tests from Acapulco to Guam, carried such a as ill-conceived for the following reasons. plant on board? Cadang-cadang was Ocfemia, a native of Guinobatan,used to already well established on Guam when spendhis yearly vacations and holidays in Prof. Weston described the disease in that locality in Bicol. A very well trained 1917, and it appearedon San Miguel Island plant pathologist and a keen observer, he a decade later, but since the incubation never sawa cadang-cadangdiseased palm period and slow progress of the disease are in or around Guinobatan, as he told me now well established, the first contacts of when he visited Rockefeller University in coconut palms with the infectious viroids the late 1950s. If the diseasehad existed must have preceded the observed destruc- in Albay earlier, resulting in the survival tion by several years. No plant quarantine of resistant palms, the subsequentsevere existed then and even today quarantine is outbreaks could hardly be explained. comparatively lax in tropical countries. Attempts to import a Iarge number of Cadang-cadang is unquestionably an coconut varieties from other parts of the extremely serious palm disease that has world were initiated by me and were also caused huge devastation and great eco- attempted by the late F. O. Holmes 30 nomic losses.If we look at the problem as years ago in the hope that a resistant vari- "local," a Philippine disease, the present ety would be found. Shipmentswere made economic and political instability in that possibleby a joint effort of several people country makes any suggested solutions and financial support obtained from the highly problematic. The rapid and constant Franklin Baker Company.When sackswith population growth in the islands is hardly seed nuts arrived by air in Manila, they "accidentally" "forgot- conducive to long-term breeding for dis- were destroyedor ease resistance, the best practical solution. ten" while in the customs area of the air- Preventing the spread by decontamination port. At present only local varieties are of machetes has been suggested but not being tested.The Mawa variety, ownedby Replanting gives temporary a former closefriend of PresidentMarcos, implicated. "coconut relief only. The disease, endemic in certain the king" Eduardo Cojuangco, parts of the Philippines and Guam, appar- was hailed as the best solution to the ently has been noted on a few remote cadang-cadangproblem. It grows faster Pacific islands recently. Besides, cadang- than the tall varieties but is susceptibleto cadang is not limited to coconut palms. In the disease.Instead of dependingon such the Philippines other palms have been temporary remedies, an effort should be diagnosed-first only by symptomatology madeto plant both local and imported vari- and later by viroid analysis-to be infected eties in isolation, on San Miguel Island, by cadang-cadang viroids. Therefore the wherethe diseasehas never ceasedto exist problem is not, and must not be, considered and where seedlingscould be mechanically as of local imPortance onlY. inoculated. Even if such tests were per- Large trials have been initiated in Albay formed and a resistant variety found, the Province to find whether natural selection resultswould benefit the Philippinesin 20- for resistance would reveal a resistant 50 years at the earliest.Who could, and coconut population among native palms. would be willing, to finance such a long- This attempt has been based on the term effort? assumption that cadang-cadang disease There seems to be no question that may have existed in Bicol Iong before it cadang-cadang,similarly to all other viroid r9931 MARAMOROSCH:CADANG.CADANG I95

diseases, is of recent, twentieth-century Il,lpsnrer. 198I. Tinangaja and bristle top, origin. Human activities have contributed coconut diseasesof uncertain etiology in Guam, and their relationship to cadang-cadangdisease to the origin of viroids in cultivated plants of coconut in the Philippines. Phytopathology, but they might have existed earlier in a 7I:1104-1107. latent state in as yet unknown natural hosts Dt LsoN. D. exo A. E. BrcoRNrA. 1953. Coconut in which they cause no symptoms. Through cadang-cadangdisease in the Philippines and human activities, such as grafting, han- experimental control program. U.S. Operations Missionto the Philippines.U.S. Embassy,Manilla, dling or cutting, viroids have been trans- IZ pp. mitted to susceptible cultivated plants. We DIEnrR, T. O. 1968. Potato spindletuber virus: can expect that new viroids will continue jn sitz sensitivity of the infectious agent to ribo- to appear unexpectedly, just as did those nuclease.Phytopathology 58: I048. 197I. A plant virus with propertiesof a known today which all appeared in the free ribonucleic acid: potato spindle tuber virus. twentieth century (Diener I9B7). 1z:K. Maramoroschand E. Kurstak (eds.).Com- The discovery of viroids has opened new parative virology. Academic Press, New York, vistas in plant pathology as well as in med- pp.433-478. icine and molecular biology, becoming the 1979. Viroids and viroid diseases.Wiley- Interscience,New York. 252 pp. first RNA pathogens whose molecular 1987. The viroids. Plenum Press,New structure became completely known. Even York. 344 pp. though the natural mode of transmission - eno W. B. RAYMER. 1967. Potatosoindle and possible natural reservoirs of cadang- tuber virus: a plant virus with propertiesof a free nucleic acid. Science158: 378 38I. cadang and other viroids are still an enigma, FtnNow, K. H. 1967. Tomato as a test plant for they are among the most thoroughly detecting mild strains of potato spindle tuber understood host-pathogen systems. virus. Phytopathology57: 1347-1352. In terms of dollars lost in copra pro- Hnrr, A., D. B. YouNc, e.NoG. D. BrRNrE. 1916. duction, the cadang-cadang disease rep- Synthesis of DNAs complementary to human ribosomal RNAs polyadenylated. in uitro. resents the most important viroid disease Biochim. Biophys. Acta 442: 37-49. known today and one of the most devas- Maneuonoscg, K. 1961. Report to the Govern. tating diseasesof plants anywhere. Efforts ment of the Philippines on the cadang-cadang to curtail the disease have not yet been diseaseof coconut. FAO ETAP Bull. 133. 26 successfuland cadang-cadang continues to PP. 1964. A survey of coconut diseasesof post a serious threat to the economy of unknown etiology. Food and Agriculture Orga- the Philippine islands and to other tropical nization,Rome 1964. 38 pp. areas of the world. 1985. Control of viroid diseases.1z; K. Maramorosch and J. J. McKelvey (eds.). Sub- Acknowledgments viral Pathogensof Plants and Animals: Viroids and Prions. Academic Press, New York, pp. The author'swork wassupported by the 151-162. Food and Agriculture Organization, the I987a. The cadang-cadangdisease of United Nations Development Fund, and coconutpalms. Rev. Trop. Plant Pathol. 4: 109- 126. the New Agricultural Experiment Jersey 1987b. The curseofcadang-cadang. Nat. Station,Publication No. D-08420-L5-92, Hist. 96: 2O 22. supportedby State funds. 1992. The cadang-cadangviroid disease of plants. 1z; K. Maramorosch (ed.). Viroids and LrrcneruRs Crrsl satellites:molecular parasites at the frontier of life. CRC Press,Boca Raton, pp. 125 I39. BocceRlo, G. 1985. Viroid etiology of tinangaja Nrnrrrr, C. L., E. DrcKSoN,K. H. FsnNow, R. K. and its relationship with cadang-cadangdisease HoRSr, AND N. M. Ze.rruN. 1978. Cross of coconut. In; K. Maramorosch and J. J. protectionamong four viroids. Virology 9I: I98- McKelvey (eds.). Subviral pathogens of plants 203. and animals:viroids and prions. Academic Press, OCFEMIA,G. O. 1937. The probable nature of New York, pp. 75 99. cadang-cadangdisease of coconut.Philipp. Agric. R. G. Bnevrn, J. W. Rexlrrs, aNo J. S. 26: 338-340. 37 196 PRINCIPES [VoL.

palm, insensitivity of the diseaseto anti' Renorns, J. W. 1975. Association of two ribo- nut and 67: L27I-I216' nucleic acid specieswith cadang-cadangdisease biotics. Phytopathology K. HoRSr. 1974. Evidence of coconutpalm. Phytopathology65: 163-167 ' Rou.rtNn.C. P. eNl R. chrysanthemum 1985. Coconut cadang-cadangviroid' 12" suggestinga viroid etiology for Proc. Am. Phytopathol' K. Maramorosch and J. J. McKelvey (eds')' chiorotic mottle disease. Subviral pathogensof plants and animals:viroids Soc. 1: 143. WEATHERS.1968. Exo- and prions.Academic Press, New York, pp' 39- Snu,rNcrr, J. S. eNo L. G. association of infectivity 74. cortis virus of citrus: 36:326- e.No T. Herre. 19?9. Circularity of the with nucleic acid properties. Virology ribonucleic acidsassociated with cadang' cadang 324. PETERS.1974. Some disease.Virology 96: 47 -53. VAN DoRsr, H. J. M. ANDD. fruit' a viroid- AND P. PALUKAITIS. 1979. In oitro syn' biological observations on pale Neth. Plant Pathol' thesis and characterizationof DNA complemen- incitJ diseaseof cucmber. J. tary to cadang-cadangassociated RNA. J' Gen' 80: 85-96. Report on the plant Virol.43: 649-662. WESTON,W. H., JR. 1918. Agr' Exp' Stn' G. Boccenlo, M. L. RETUERMI' ,lNl E. diseasesituation in Guam. Guam S. RILLo. 1979. Transmission of the RNA Rep. l9l7: 45-62. speciesassociated with cadang-cadangof coco'

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