Gaghexia, a Bud-Transmitted Disease and the Manifestation of Phloem Symptoms in Certain Varieties of Citrus, Citrus Relatives and Hybrids

CHILDS: CACHEXIA 47 group but slightly more than the mandarin 3. Grant, T. J., Costa, A. S., and Moreira, S. Studies of tristeza disease of citrus in Brazil. III. Further group. results on the behavior of citrus varieties as rootstocks, scions and seedlings when inoculated with tristeza virus. The results of examination of the pummelo, Proc. Fia. State Hort. Soc. (1949). 62: 72-79. 1950. trifoliate hybrid, lemon, and lime groups 4. Grant, T. J., and Costa, A. S. A mild strain of the tristeza virus of citrus. Phytopath. 41: 114-122. strongly suggest that minor differences in 1951. 5. Grant, T. J., Costa, A. S., and Moreira, S. hybrid plant reactions can have an important Studies of tristeza disease of citrus in Brazil. V. effect on the presence and degree of pitting. Further information on the reactions of grapefruits, limes, lemons, and trifoliate hybrids to tristeza. Calif. Tristeza-inoculated plants of the sour Citrog. 36 (8) 310,311, 324-326, 328, 329. 1951 6. McClean, A. P. D. Virus infections of citrus in orange group would seem to have no or very South Africa. Farming in South Africa. 25: (293) 262, little tendency to show pitting. 25: (294) 289. 1950. 7. Oberholzer, P. C. J., Mathews, I., and Stimie. S. F. The decline of grapefruit trees in South Africa. A LITERATURE CITED preliminary report on the so-called stem pitting. Union 1. Costa, A. S., Grant, T. J., and Moreira, S. In- of South Africa Sci. Bull. 297. (1949). vestigacoes sobre a tristeza dos citrus. II. Conceitos e 8. Wallace, J. M., and Drake, R. J. Newly dis dados sobre a rcacao das plantas citricas a tristeza. covered symptoms of quick-decline and related diseases. Bragantia 9: 59-80. 1949. Citrus Leaves. 31: (2) 8, 9, 30. 1951. 2. Costa, A. S., Grant, T. J., and Moreira, S. A 9. Knorr, L. C, E. P. Ducharme and A. Banfi. The possible relationship between tristeza and the stem occurrence and effects of "stem pitting" in Argentina pitting disease of grapefruit in Africa. Calif. Citrog. grapefruit groves. Citrus Magazine 13: (14), 32-36, 85 (12) : 504, 526-528. 1950. 1951.

GAGHEXIA, A BUD-TRANSMITTED DISEASE AND THE MANIFESTATION OF PHLOEM SYMPTOMS IN CERTAIN VARIETIES OF CITRUS, CITRUS RELATIVES AND HYBRIDS

J. F. L. CHILDS Symptoms of the Disease

Bureau of Plant Industry, Soils and Agri The symptoms described here refer spe cifically to the Orlando tangelo. On other cultural Engineering varieties and species of citrus the symptoms United States Department of Agriculture may or may not be as sharply defined. Orlando Phloem discoloration:—Discoloration of the innerbark, br phloem, through gum impreg Introduction nation is a characteristic and diagnostic symp Cachexia, derived from two Greek words, tom of cachexia. In order to observe gum im kakos (bad) and hexis (condition), refers to pregnated phloem tissues, it is necessary to the symptoms of malnutrition and wasting cut away the outer bark at the bud union characteristic of affected citrus trees of those boundary. Discoloration commences just above varieties that are highly susceptible to, or that the bud union and in the early stages may readily express symptoms of, the disease of consist of no more than a series of small that name. The trouble was first brought brown spots along the scion-rootstock boun to our attention in 1945 when affected Or dary, but in five or six year old trees the lando tangelo trees were found near Clear- phloem may be discolored 18 inches or more water, Florida (2). A few plantings of this above the union. Discoloration has not been variety are free of the disease, but in others observed below the union when the rootstock (sometimes on the same property) 1 to 60 is Rough lemon, Cleopatro mandarin, Rusk percent of the trees may be diseased. That Citrange, grapefruit,or sweet orange, but certain trees are diseased may become notice when the rootstock is Orlando tangelo phloem able within two years from planting, because discoloration also appears below the union. of their lack of vigor, chlorotic foliage, and Wood-pitting:—When the bark of a diseased other symptoms. If no symptoms have ap Orlando tangelo is peeled off at the bud union peared by the time a tree is five years of age the exposed wood is found to be indented or (from planting date) it seems to remain free pitted in a very characteristic manner. The of cachexia indefinitely, indicating that the inner (cambial) surface of the removed bark disease is seldom spread from tree to tree is marked by lumps and projections that coin in a grove. cide with and fit into the depressions in the 48 FLORIDA STATE HORTICULTURAL SOCIETY, 1951

wood. Below the union, the wood and the A number of Rough lemon rooted grape inner surface of the bark of Rough lemon fruit trees that had been topworked to Orlan and other symptomless rootstocks are smooth do tangelo were found in 1949. Although the and normal to all appearances. buds were from healthy trees, most of the Bark-cankers:—The occurrence of bark Orlando scions showed symptoms of cachexia. cankers on the Orlando tangelo above the bud In 1950 buds from sprouts on the grapefruit union and occasionally on the branches may interstocks were inserted in one lot of healthy constitute a more conspicuous symptom than Orlando tangelo budded trees. phloem discoloration or wood pitting, from the The 90 Orlando tangelo seedlings were bud grower's standpoint. Bark cankers, like ded in 1947 as follows: 30 with diseased Or phloem symptoms and wood pitting, do not lando buds, 30 with healthy Orlando buds, develop below the union when the rootstock is and 30 were left as unbudded checks. None of Rough lemon, Cleopatra mandarin, or other the Orlando stocks were cut back. symptomless variety. In some respects the In February 1951 the first phloem discolo bark cankers resemble bark lesions caused ration was found and immediately all trees in by the foot rot fungus Phytophthora citron- the experiment were examined for that symp phthora, but all attempts to culture Phyto- tom. In the three lots of diseased Orlando pthora from the advancing margin of these buds on Rough lemon root, 40 of the 54 scions cankers have been unsuccessful (2). that survived, or 74.1 percent, expressed Stunting and chlorosis:—Affected trees are phloem symptoms (3). Each diseased tree usually severely stunted and often severely represents an instance of cachexia transmis defoliated. Frequently, the leaves are chloro- sion from a separate source. Seventy-one tic, especially along the midrib. These are healthy Orlando tangelo buds on Rough lemon typical starvation symptoms such as occur rootstock survived and none of the trees from when a tree is ringed or girdled and indicate these buds showed phloem symptoms (3). that the flow of nutrients has been impeded in Here also each tree represents a bud from a some manner. An application of fertilizer separate tree source. may stimulate a flush of new green leaves In that portion of the experiment in which on diseased trees but these leaves soon be Orlando tangelo seedlings were used as root- come chlorotic. stocks, 27 of the buds from diseased parent trees survived and 25 (92.6%) showed phloem Bud Transmission Studies symptoms at the bud union. The discoloration It is often possible to recognize the phloem appeared equally marked on the Orlando scion symptoms of cachexia the first year after above the union and on the Orlando stock Orlando tangelo trees are set out; so it below it. In the case of the healthy Orlando seemed possible that the trees may have been tangelo buds on Orlando rootstocks none of infected when they were set out, possibly the 28 surviving scions showed phloem dis through the buds. An experiment to test coloration, and none of the unbudded seedlings sources of budwood was started in 1947 (2) showed symptoms. This indicates that ca in which Rough lemon seedlings, 210 in num chexia can be transferred from tree to tree ber, and 90 Orlando tangelo seedlings were through the budwood and also shows the im set out for use as rootstocks in lots of thirty portance of selecting budwood from cachexia- each. free trees for propagation purposes. Buds from several sources were inserted in Unfortunately very few of the grapefruit the Rough lemon seedlings as follows: (a) buds that had been inserted in the Rough Buds from Orlando tangelo trees affected with lemon stocks below healthy Orlando scions cachexia disease, as determined by presence survived, because of the unusually hot weather of discolored phloem, were inserted in three at the time of budding. However, 7.7 percent lots of seedlings. (b) Buds from healthy of the Orlando scions expressed phloem symp Orlando tangelo trees, as determined by the toms of cachexia within the short period of absence of phloem discoloration and generally two years. The grapefruit interstocks were vigorous appearance, were inserted in four lots the presumed source of the disease in this of seedlings. All the Rough lemon stocks were instance but even if they were not, the evi cut back to the bud in the spring of 1948. dence indicates that grapefruit trees can CHILDS: CACHEXIA 49 harbor the disease and could therefore become TABLE 1. symptomless carriers. PHLOEM SYMPTOMS OF CACHEXIA (XYLOPORO- SIS) IN 59 VARIETIES OF CITRUS, CITRUS RELA TIVE, AND HYBRIDS AS ROOTSTOCKS Phloem Symptoms In Certain Varieties of Citrus and Citrus Relatives Rootstock Number Number with Group and variety examined symptoms Although originally not intended to be part of the research on cachexia disease, extensive Sour orange (Citrus aurantium) 29 0 Sour No. 2 (laboratory) 25 0 citrus rootstock experiments set up by the Oklawaha 29 0 U. S. Dept. of Agriculture in 1948 in Florida Bergamia 29 0 Sauvage 27 0 and Texas have yielded important information Bittersweet 25 0 Natsu Milkan 6 0 on the expression of cachexia symptoms by Sweet orange (C. sinensis) varieties other than Orlando tangelo and on Florida sweet seedling 21 0 Hamlin 27 0 symptomless carriers. These plantings con Grapefruit (C. paradisi) Duncan 27 0 sisted of seedlings of a number of citrus varie Leonardy 27 1* ties and a few citrus relatives budded with Pummelo and shaddock (C. grandis) Almoen 12 0 two standard varieties of sweet orange (Va Ogami 10 0 Siamese 24 0 lencia and Pope Summer) in Florida and one Thong Dee 27 0 variety of grapefruit (Red Blush) in Texas. Cuban shaddock 27 0 Lemon (C. limon) hybrid Although an effort was made to secure psoro- Iran 11 0 Rough 27 0 sis-free buds of Red Blush grapefruit, it was Lime (C. aurantifolia) hybrid subsequently discovered on the basis of leaf Kalpi 31 0 Rangpur 25 0 symptoms that some of the bud sources were Mandarin (C. reticulata) Cleopatra 25 0 diseased. In March 1951 E, O. Olson reported Dancy 25 0 in a private communication to the author Sunki 28 0 King 25 0 that rootstocks of Orlando tangelo and Temple Owari 2 0 orange in the Texas planting showed the Swatow 21 2 Clementine 27 8 phloem discoloration and wood pitting symp Ponkan 7 1 Poncirus trifoliata toms of cachexia. Upon examination of the Small flowered 25 0 other stocks in the experiment he found eleven Large flowered 6 0 Kumquat other citrus varieties and hybrids with cache Nagami (Fortunella margarita) 12 6 Tangelo (C. paradisi x C. reticulata}1 xia symptoms (9). Sampson 29 0 As a result of the information from Texas, Watt 31 0 Webber 2 0 three rootstock plantings in Florida were ex Williams 29 2 Suwannee 24 5 amined in June 1951 and the results are pre Orlando 32 23 sented in table 1. It is evident that the buds Sunshine 30 15 Pina 28 3 used in these rootstock trials were not all in Thornton 23 4 Yalaha 25 7 fected with cachexia from the fact that but Minneola 27 4 72 percent of the Orlando tangelo stocks and Seminole 8 8 Wekiwa 13 9 but 50 percent of the Sunshine tangelo stocks Citrange (P. trifoliata x C. sinensis) Savage 4 0 were affected (table 1). Hence some of the Saunders 4 0 rootstocks replicated only a few times may C-1425 8 0 Morton 21 0 have escaped inoculation. Rustic 7 0 Citrumelo (P. trifoliata x C. paradisi) However, in most instances sufficient rep C-4475 25 0 licates of a variety and sufficient varieties of C-4561 6 0 Citranpror ((P. trifoliata x C. sinensis) x C. sinensis) a species or hybrid were examined to give C-42681 8 0 a clear picture of symptom expression. It Citransrequat ((P. trifoliata x C. sinensis) x Fortunella) C-48032 10 0 can be seen that three of the eight mandarin Limpquat (Fortunella japonica x C. aurantifolia) Lakeland 31 23 varieties showed phloem discoloration as did Tavares 16 2 the one kumquat variety. Symptoms were also Tanp-or ^C. reticulata x C. sinensis) C-653 31 0 expressed in the mandarin hybrids such as Umatilla 21 1 Temple 21 2 tangelos and tangors and in the kumquat T.empum (C. limon x C. grardis) fi 0 hybrids such as Calamondin and limequat. Calamondin (C. retiiulata x Fortunella * 25 1 The two varieties of sweet orange and the two varieties of grapefruit did not show cache- ♦It *s suspected that the infected rootstock was not Leonardy, 50 FLORIDA STATE HORTICULTURAL SOCIETY, 1951 xia symptoms although sweet orange and diseases (6). Our studies on symptom ex grapefruit have been found to carry the di pression suggest that certain mandarins are sease. Nor were symptoms found on the six injured by cachexia as is indicated by gum varieties of sour orange, five varieties of impregnation of the phloem tissues and other pummelo, two varieties (probably hybrids) symptoms; but these same mandarins were of lemon, or the two varieties of Poncirus found by Grant, Costa and Moreira (5) to be trifoliata. The hybrids in which both parents extremely tolerant of the tristeza virus. Also, are symptomless such as citrange, citrumelo, cachexia infected sweet orange buds from citrangor did not show phloem discoloration. two sources in Florida and grapefruit buds The one citrangequat in the test expressed no from one source in Texas (3) grew vigorously symptoms but other citrangequats might re on six different sour orange rootstocks, this act differently. is certainly contrary to the observed re The rootstock experiments in Florida and action of tristeza-inf ected citrus trees of these Texas (9) give further evidence that sweet varieties on sour orange stock (1, 5, 11). orange and grapefruit trees can harbor and Summary and Conclusions transmit cachexia through buds from trees Cachexia has been transmitted many times that show no phloem discoloration or wood under controlled conditions by means of buds pitting symptoms. taken from trees with typical symptoms of Relation to Other Diseases the disease. At the same time and under the Xyloporosis \—The symptoms described for same cultural conditions trees propagated xyloporosis disease of sweet lime rootstocks in from budwood of healthy trees did not show Palestine (10) and Brazil (8) are strikingly symptoms. Seedling Orlando tangelo trees similar if not identical with those of cachexia were inoculated with cachexia by means of (2) in Florida. Attempts to obtain specimens budwood from diseased trees but, growing for comparison from the Palestine area were in close proximity, unbudded Orlando seedlings unsuccessful, but through the kindness of A. and those budded with healthy buds remained S. Costa specimens of Bahia Navel orange on healthy, indicating no natural spread from Lima da Persia (sweet lime) affected with tree to tree within the experiment. xyloporosis were obtained from Brazil. These The rootstock experiments in Florida and specimens, preserved in alcohol-acetic acid- in Texas showed that cachexia may cause formaldehyde solution, showed the typical pit gum impregnation and discoloration of the ting of the cambial surface and the typical phloem, characteristic of cachexia, in varie annular deposits of gum, visible on the ex ties other than the Orlando tangelo. These posed surfaces of radial sections of the varieties are principally the mandarins and sweet lime wood, as described by Reichert and kumquats and hybrids of either of these. Perlberger (10). After careful study it was Evidence is presented that (sweet orange concluded that the symptoms of xyloporosis and grapefruit) two species of citrus that on sweet lime exactly duplicate in all respects do not express phloem symptoms may harbor the symptoms of cachexia on Orlando tangelo cachexia, becoming in effect symptomless car (3). riers of the casual agent of the disease. Bud Tristeza:—On the basis of wood-pitting ding from such trees onto seedlings of varie symptoms McClean (7) suggested that xylo ties that readily express symptoms, such as porosis on sweet lime may be related to the the Orlando tangelo, has shown the casual aphid-transmitted, wood-pitting virus disease agent of cachexia to be present in symptom of grapefruit in South Africa and that this less varieties. Establishment of known sources last disease is the same as tristeza in South of healthy budwood would appear to be one America. Costa, Grant, and Moreira (4) of the important means of control of this showed that, on the basis of insect transmis disease. sion and the expression of leaf symptoms, A comparison of the described symptoms tristeza and the aphid-transmitted, wood-pit and examination of wood specimens of both ting disease of grapefruit are the same or diseases indicate that cachexia and xypo- closely related, but they pointed out that, on porosis are the same disease. the basis of differential host reactions, tris A comparison of the host relationships of teza and xyloporosis are separate and distinct cachexia (xyloporosis) and tristeza presents STEWART AND LEONARD: MOLYBDENUM DEFICIENCY 51 additional evidence that they are separate and of tristeza disease of citrus in Brazil. Proc. Fla. State Hort. Soc. 62: 72-79. 1949. distinct diseases. 6. Grant, T. J., A. S. Costa and S. Moreira. Tris teza disease of citrus in Brazil. Calif. Citrograph. 36: 310. 1951. LITERATURE CITED 7. McClean, A. P. D. Virus infections of citrus in South Africa. Farming in. So. Africa 25: 1-9, Sept, 1. Bennett, C. W., and A. S. Costa. Tristeza disease 1950. of citrus. Jour. Agr. Res. 78: 207-237. 1949. 8. Moreira, Sylvio. Xyloporosis. Hadar 11: 234-237. 2. Childs, J. F. L. The cachexia disease of Orlando 1938. tangelo. Plant Dis. Reporter 34: 295-298. 1950. 9. Olson, E. O. Investigations of citrus rootstock 3. Childs, J. F. L., The cachexia disease of citrus, diseases in Texas. Proc. Rio Grande Valley Hort. Inst. its transmission and relation to xyloporosis and to 1952 (In press). tristeza. (Ms. submitted to Phytopathology). 10. Reichert, I., and J. Perlberger. Xyloporosis. the 4. Costa, A. S., T. J. Grant and S. Moreira. On a new citrus disease, Agr. Exp. Sta. Rehoboth, Palestine possible relation between Tristeza and the Stem-pitting Bui. 12, 49 pp. 1934. disease of grapefruit in Africa. Calif. Citrograph 35: 11. Wallace, J. M. Recent developments in studies 504. 1950. of quick decline and related diseases. Phytopath, 41: 5. Grant, T. J., A. S. Costa and S. Moreira. Studies 785-793. 1951.

MOLYBDENUM DEFICIENCY IN CITRUS

Ivan Stewart and Q, D. Leonard amounts of molybdates were applied to trees as soil treatments and as nutritional Florida Citrus Experiment Station sprays. No response to the soil treatments Lake Alfred has been observed after two months. Moly bdenum sprays, however, caused yellow spot Preliminary investigations indicate that leaves to become green within three to four molybdenum deficiency is widespread in Flor weeks after the application was made. Some ida citrus. The symptom caused by this de response was obtained from a concentration ficiency is the well known yellow spot illus as low as one gram of sodium molybdate in trated in Fig. 1. This disease occurs chiefly in 100 gallons of dilute lime sulfur spray, when Florida and was first described by Floyd (1) 10 gallons was applied to each tree. This in 1908. Since then, numerous attempts have amounts to only 0.1 gram per tree. Complete been made to determine its cause. The de greening of yellow spot leaves was obtained ficiency appears first as water-soaked areas by spraying or injecting 1 gram of sodium in leaves in the early spring, and then de molybdate in one gallon of water per tree. velops into large interveinal yellow spots The lowest satisfactory amounts found have with gumming on the lower leaf surface late been one ounce of sodium molybdate or am in the summer. In extreme cases, yellow monium molybdate in 100 gallons of water, spot may cause complete defoliation of the applied at the rate of 10 gallons per tree. trees. Repeated studies (3) failed to demon Increasing rates up to 8 ounces per 100 gal strate that it was due to an infectious fungus, lons did not give marked improvement over bacterium, or virus. Yellow spot has been re the 1 ounce per 100 gallon treatments. Stu ported on practically all kinds of citrus but dies made with plants other than citrus in trees on grapefruit rootstock appear to be dicate that large amounts of molybdenum are the most susceptible. The disease has been required to produce toxicity to the plant itself. associated with acid soils and acid producing The amount of molybdenum actually needed fertilizers such as ammonium sulfate. by the tree is very small. Greenhouse studies Studies on other plants have indicated that (5) have indicated that molybdenum defi molybdenum deficiency occurs chiefly on acid ciency shows up in citrus when there is be soils. By the use of radioactive molybdenum tween .01 and .02 p.p.m. molybdenum in the (4) it has been shown that this element tends dry leaves. Chemical analyses of yellow spot to concentrate between the leaf veins in nor leaves and of leaves from healthy trees grow mal leaves; hence, in deficient leaves it would ing near by, have indicated that the moly be expected that a breakdown would occur in bdenum content was below .05 p.p.m. in both the interveinal tissue first. In order to de cases. The water soluble molybdenum as de termine whether yellow spot of citrus was re termined on soil taken from around yellow lated to molybdenum deficiency, various spot trees and that from healthy trees in the same area indicated it to be below .005 p.p.m. Florida Agricultural Experiment Station Journal Series No. 39. Methods now in use for molybdenum analysis