Concave Gum - Blind Pocket

 

HISTORY, DISTRIBUTION AND IMPORTANCE

History. The history of concave gum - blind pocket is complicated, if not confusing, as it is mixed with that of several other citrus diseases: psorosis, crinkly leaf, infectious variegation, cristacortis and impietratura.

The name “psorosis” was selected by Swingle and Webber (1896) to describe a disease characterized by bark scaling lesions on trees of sweet orange and other varieties (CG-BP. 01). In addition to bark scaling, the disease was found by Fawcett (1933) to have also leaf symptoms, the so-called psorosis young-leaf flecking symptoms (CG-BP. 02). Two forms of psorosis were distinguished: “psorosis A”, the common form of the disease, and  “psorosis B”, a less common but more severe form, characterized by early bark lesions, mature-leaf symptoms  (CG-BP. 02), and twig dieback (Fawcett, 1932; Fawcett and Klotz, 1938). Next, it was shown by Fawcett and Cochran (1942): (i) that psorosis B could be produced by inoculating sweet orange seedlings with bark patches taken into a lesion of psorosis A (so-called “lesion bark”),  and (ii) that psorisis B was probably not caused by an agent different from that of psorosis A. Finally, Wallace (1957) demonstrated that sweet orange seedlings did not develop psorosis B upon inoculation with psorosis A lesion bark if they had been inoculated previously with Psorosis A non-lesion bark. In other words, inoculating a sweet orange seedling first with Psorosis A non-lesion bark, and next challenging them with lesion bark (challenge inoculation), will “cross-protect” the sweet orange seedling against the development of psorosis B symptoms. This cross-protection reaction became a powerful test to identify psorosis A and distinguish it from other disorders, which may show various leaf symptoms that could be mistaken for psorosis.

Fawcett was also involved in the first reports on concave gum (CG-BP. 03), blind pocket (CG-BP. 04) and crinkly leaf (CG-BP. 05). These diseases were first mentioned in 1926 (Fawcett and Lee, 1926), and further information was provided by Fawcett ten years later (Fawcett, 1936). He found that these three diseases had young-leaf symptoms very similar to the psorosis flecking symptoms, the ones he had reported in 1933 (Fawcett, 1933). Young leaves of Concave gum-affected trees not only had the psorosis young-leaf flecking, but also zonate or oak leaf pattern (CG-BP. 06).

Thus, psorosis young-leaf symptoms represented a common characteristic of psorosis A, concave gum, blind pocket and crinkly leaf. In addition, these symptoms could be transmitted by graft-inoculation. For these two reasons, concave gum, blind pocket and crinkly leaf were thought to be members of the “psorosis family” of diseases (Fawcett, 1939), all four diseases being caused by related strains of the same putative “virus” (viruses were the only type of infectious agents known in those days). Finally, in 1939, Fawcett and Klotz described a “psorosis-like” disorder of lemon, infectious variegation (CG-BP. 05), and suggested its relationship to crinkly leaf (Fawcett and Klotz, 1939), and so infectious variegation was added to the psorosis family of diseases. Descriptions of the various psorosis types and apparent evidence of their relationships were published in the years to follow (Klotz and Fawcett, 1941; Fawcett and Bitancourt, 1943). Even at the first International conference on citrus virus diseases in 1957 in Riverside, California, concave gum, blind pocket, crinkly leaf, and infectious variegation were still considered part of the psorosis group (Wallace, 1959).

Lilian Fraser in Australia was the first to challenge inclusion of crinkly leaf in the psorosis virus group (Fraser, 1961). No psorosis A young-leaf symptoms were produced by any of the many seedlings inoculated with bark from crinkly leaf-affected trees, provided that they were free of psorosis A. She suggested that the experiments in California, which led to linking crinkly leaf with psorosis, were conducted with citrus material carrying both psorosis A and crinkly leaf. Also, in early studies it was found that crinkly leaf and infectious variegation cross-protected sweet orange against psorosis A lesion inoculum. However, later work showed that cross-protection was also due to contamination of the crinkly leaf and infectious variegation sources with a psorosis A virus. In the case of crinkly leaf, the contaminating psorosis virus could be eliminated through seed- or mechanical-transmission, and the remaining crinkly leaf virus was found unable to induce the cross-protection reaction (Wallace, 1968). Similar results were also obtained with uncontaminated infectious variegation sources cleaned by mechanical transmission. Finally, Dauthy and Bové (1964, 1965, and 1968) purified crinkly leaf virus and infectious variegation virus and concluded that they were strains of the same virus. Similar conclusions were obtained by Majorana and Martelli (1968). It is known today that the agents of crinkly leaf, infectious variegation as well as leaf rugose are members of the ILAR virus group (Rana et al., 1974; Gonsalves and Garnsey, 1976). They are unrelated to the psorosis virus.   

The first suggestion that concave gum was unrelated to psorosis came from cross-protection experiments by Roistacher and Calavan (1965) who showed that a number of concave gum sources did not protect sweet orange seedlings against psarosis A lesion bark. Similar results were eventually obtained by Wallace (see Wallace, 1978). Cross-protection experiments with blind pocket sources gave rather confusing results. However, concave gum and blind pocket being diseases with very similar symptoms and characteristics, they were both removed from the psorosis group.

Vogel and Bové (1964, 1968, 1972), when studying cristacortis (CG-BP. 07), always observed psorosis young-leaf symptoms, not only flecking but also oak-leaf patterns (CG-BP. 08), on citrus plants infected either naturally or experimentally (by graft-inoculation) with the cristacortis pathogen. As oak-leaf patterns were thought to be characteristic of concave gum, and since many cristacortis sources showed or induced such leaf symptoms in inoculated navel sweet orange or Orlando tangelo seedlings, it was concluded, initially, that the young-leaf symptoms were caused by the concave gum agent, co-infecting the cristacortis sources (Vogel and Bové, 1972). However, sources of cristacortis free of concave gum could be identified on the basis of internal wood symptoms (Vogel and Bové, 1974). Indeed, the Concave gum agent induces gum deposits in certain annual growth rings in the wood. As the growth rings are concentric, the gum-stained layers have also a concentric appearance (CG-BP. 08). On the contrary, cristacortis induces radially oriented stem pits (CG-BP. 08). Furthermore, traces of previous, radially oriented pits remain buried in the wood (CG-BP. 29). Sources carrying both concave gum and cristacortis induce the concentric gum-stained layers as well as the radially oriented traces. On the basis of these criteria, sources of cristacortis free of the concave gum agent were identified, and these sources showed and induced young-leaf symptoms including oak-leaf patterns on inoculated citrus seedlings. These results showed that concave gum and cristacortis were different diseases, but both were associated with the same young-leaf symptoms (CG-BP. 06) (Vogel and Bové, 1974).

Impietratura was first described as “Samrah” by Reichert and Hellinger (1930) in Palestine.  The disease, under the name of “impietratura”, has long been known to Sicilian citrus growers, and is widely spread among Mediterranean countries (Ruggieri, 1955). Affected fruits are as hard as “stone”, hence the name “impietratura”, and contain pockets of gum in the albedo (CG-BP. 09). Ruggieri (1961) demonstrated that impietratura was transmissible by graft inoculation. Bar-Joseph and Loebenstein (1970) showed that budwood from infected trees induced flecking and oak-leaf pattern on citrus indicator seedlings, and these leaf symptoms could be used for indexing. However, in the absence of “pur” impietratura sources, the possibility could not be ruled out that the leaf symptoms were induced by some other agent, such as the concave gum agent, putatively present in all the impietratura trees examined.

Recent data have confirmed that there are no more reasons to include impietratura into a psorosis group, than there are to include concave gum-blind pocket and cristacortis. Indeed, the virus causing psorosis A has been identified and characterized in the 1990s as a bipartite, single stranded RNA ophiovirus (CpsV) (Martin et al., 2005) In particular, a 48kDa protein, probably the coat protein, is characteristic of CpsV-infected citrus. The 48kDa protein is absent from citrus infected not only with concave gum-blind pocket, but also cristacortis and impietratura, and thus these diseases are unrelated to psorosis, even though they are associated with “psorosis” young-leaf flecking symptoms (da Graça et al., 1991). At this moment, the agents responsible for the ”Oak-leaf pattern diseases” (concave gum-blind pocket, cristacortis, impietratura) have not been identified.

Distribution and importance. The disease is largely present in the Mediterranean region although it is now found worldwide. Injury develops slowly but may distort trunks and branches considerably (CG-BP. 03, 10, 11, 12, 13) and damage trees severely. Many spectacular cases were seen on old line mandarin and sweet orange trees in Corsica (Vogel, 1961).  Concave gum disease can be quite severe and very debilitating to young trees (D'Onghia et al., 1992). As the disease is not transmitted by insects or mechanically, it has disappeared from orchards started with citrus material certified free of graft-transmissible agents.

 

 

NAME   AND   SYNONYMS   OF   THE   DISEASE

Concave gum: named from (i) the broad concavities or depressions of various sizes on the trunk and limbs (CG-BP. 03, 10, 11, 12, 13),  (ii) the presence of gum beneath the concavities, in-between wood and bark (CG-BP. 14), and (iii) gum exudation through bark-cracks in the center or around the margins of the depression at certain seasons (CG-BP. 15). The disease was formerly called concave gum “psorosis”. It is however not related to psorosis (see history).

Blind pocket: named from pocket-like depressions, deeper and narrower than the concave gum depressions (CG-BP. 04, 16. 17) While concave gum depressions are “open”, with opposite margins relatively far apart, blind pocket depressions are “closed, with opposite margins almost touching each other (CG-BP. 18, 19). However, it is not always easy to distinguish between the two types of depressions, and depressions half way between concave gum depressions and blind pocket depressions do occur (CG-BP. 20). The agents of concave gum and blind pocket are graft-transmissible but have not yet been identified. On the basis of similar trunk and leaf symptoms (flecking and oak-leaf pattern) they are thought to be closely related and are considered here as one single disease: concave gum-blind pocket, one of the members of the ”oak-leaf pattern diseases”.

 Abbreviation: CG‑BP for Concave Gum ‑ Blind Pocket.

 

 

SYMPTOMATOLOGY

 

General aspect of affected field trees

Mild to severe stunting. Trunk and large limbs are gnarled and distorted, (making them most suitable for elegant lamp-stands of valuable citrus-wood). In Mediterranean countries where sour orange is still the major rootstock, trunk symptoms are characteristically only seen on the sensitive scion: mandarin (CG-BP. 03, 11), Clementine (CG-BP. 10), sweet orange, grapefruit, tangelo (CG-BP. 12, 13) but not on the tolerant sour orange stock (CG-BP. 12, 13). The same situation may occur with other tolerant rootstocks (lemon, P. trifoliata). Concavities developing on the scion trunk close to the bud union line may distort the sour orange tissues immediately below the bud union (CG-BP. 19).

 

Symptoms on trunk (on rootstock and/or scion), limbs and shoots

Concave gum: (i) Conspicuous broad concavities or depressions, 10-20 cm or more in length and half as wide (CG-BP. 03, 10, 19, 20), (ii) presence of gum between bark and wood at depressions (CG-BP. -/14), (iii) gum oozing through cracks in the bark (CG-BP. 15),  (iv) gummy, granulated tissue under the bark, cinnamon or russet in color, and (v) as seen on cross sections of small (CG-BP. 21) or large (CG-BP. 22) branches or limbs, some of the concentric growth rings in the wood may be stained with brownish gum-like material especially underneath depressions (CG-BP. 21, 22). The distorted, gnarled aspect of trunks and limbs affected by CG-BP is due to the development of numerous, partly overlapping depressions.

 Blind pocket : depressions are deeper, narrower, and more numerous than those of concave gum.  (CG-BP. 04, 16, 17, 18, 19, 20).

Often concave gum and blind pocket depressions occur together on the same tree (CG-BP. 11, 12, 18)

 

Symptoms on leaves 

Trees affected by CG-BP show (i) young-leaf flecking symptoms (CG-BP. 23), also seen on psorosis A-affected trees or inoculated seedlings, and (ii) young-leaves with oak leaf patterns (CG-BP. 23, 24). These young leaf symptoms are more generally observed in the spring and fall flushes of growth, when outside temperatures are still relatively mild. In the spring, the oak leaf pattern can be seen throughout the tree on almost all of the leaves in the young flush of growth. Symptoms on the young leaves gradually disappear as the leaves mature. Symptoms are seen most readily when the leaf is shaded (with one hand) from the direct sun and viewed against the light of the sky.

 

Symptoms on fruit

None

 

Histological symptoms

At the sites where depressions occur, wood development seems to be inhibited (Wallace, 1959, 1978). In the case of BP depressions, a smaller area of wood is affected, so that when growth continues on each side of the affected wood, the depression becomes very narrow. In the case of long-existing blind pocket depressions, the points of origin are deep within the wood (CG-BP. 18). At the point of origin, the cambial side of the invaginated bark has no peg formations fitting the narrow wood pocket. In the case of cristacortis, such pegs do occur and are characteristic. 

 

 

CAUSAL AGENT: DESCRIPTION AND PROPERTIES

The causal agent is readily transmitted by graft-inoculation. Its nature is unknown.

 

 

HOST RANGE

Thus far restricted to citrus spp. Non-rutaceous hosts are not known.

 

Sensitive species, varieties or combinations

Sweet orange (CG-BP. 04), mandarin (CG-BP. 03, 11), clementine (CG-BP 10), tangelo (CG-BP. 12, 13), grapefruit show the depressions characteristic of CG-BP. In Japan, severe symptoms of the disease occur on pumelo-like hyuganatsu (Citrus tamurana) (Ieki and Ito, 1996).

 During their early stages of life, infected trees may not show the depression symptoms. However, they may show the oak-leaf patterns common to CG-BP, cristacortis, and impietratura.

 

Symptomless species, varieties or combinations

Sour orange (CG-BP. 03, 12, 13), trifoliate orange and lemon do not show trunk and branch depressions and are considered symptomless carriers for these symptoms.

Sour orange, lemon, citron may show oak-leaf patterns, but no trunk or branch symptoms.

 

 

TRANSMISSION

 

Natural

Transmission is primarily by man through infected budwood. There is no evidence of vector transmission.

 

Experimental

The agent is readily transmitted by graft-inoculation of bark patches, buds or shoots. A high percentage of transmission is obtained.

Mechanical transmission: none reported.

Transmission of young-leaf symptoms was obtained in Corsica by placing pollen from a Parson Brown sweet orange tree infected with the agents of Concave gum (California strain 158-62) and exocortis under the bark of six tangelo seedlings. All six seedlings showed young-leaf symptoms ((flecking and oak-leaf pattern) within five years after pollen treatment. However, trunk or limb symptoms (concavities or depressions) had not appeared after eight years (Vogel and Bove, 1980). In the case of cristacortis, young-leaf symptoms (flecking and oak-leaf pattern) as well as stem pitting were obtained in five of six Orlando tangelo seedlings treated with pollen from an Orlando tangelo tree infected with cristacortis, concave gum and exocortis (Vogel and Bove, 1980). However no natural transmission of young-leaf symptoms and/or cristacortis symptoms has ever been observed in Corsica.

 

 

EPIDEMIOLOGY

     Not studied

 

 

DIAGNOSIS

 

Diagnostic field symptoms

     Broad concave depressions, narrow pocket-like depressions, intermediate depressions on trunk, main limbs, and branches (CG-BP. 19, 20). With tolerant rootstocks such as sour orange in many Mediterranean countries, depressions and distortions will only affect the scion trunk, not the sour orange rootstock. Photos CG-BP. 03, 04, 10, 11, 12, 13 show trunks highly characteristic of concave gum-blind pocket.

After having identified the depressions, look for young-leaf symptoms with oak-leaf pattern on spring and fall flushes of growth. For confirmation or in case of doubt, index for oak-leaf pattern (see below: biological indexing, leaf symptoms).

Field trees with oak-leaf pattern on young leaves, but without trunk, limb or branch symptoms, may be affected with any one of the three “oak-leaf pattern” diseases (CG-BP, cristacortis, and impietratura). Indexing on seedlings of sour orange, navel sweet orange, Orlando tangelo, and fruit-bearing grapefruit tree (CG-BP. 09) will give the results shown on the following table, and make it possible to identify the agent(s) involved.  This indexing might take several years. In many cases, identification of the agent(s) is not required, as leaf symptoms alone are sufficient to indicate that the candidate tree is infected.

 

	Trunk or branch symptoms on			Fruit symptoms on
	Sour orange seedling	Navel sweet orange seedling	Orlando tangelo seedling	Fruit-bearing grapefruit tree **
CG-BP	-*	Depressions, Gumming	Depressions, gumming
Cristacortis	Stem pitting	Stem pitting	Stem pitting
Impietratura**	-	-	-	Fruit with gum in albedo

* - : no symptoms.

** Fruit-bearing grapefruit trees are required only for impietratura indexing (CG-BP. 09).

 

 

Comparison with other diseases

Leaf symptoms

Young leaf symptoms of Psorosis-A are only of the “flecking” type. Young leaf symptoms of CG-BP, but also of cristacortis and impietratura, are of two types: flecking and the characteristic oak-leaf pattern (CG-BP. 06). However, the first symptoms to appear on the young emerging flush of seedlings of sweet orange, mandarin, or Dweet tangor, within 5 to 8 weeks after inoculation, is interveinal flecking (CG-BP. 39), and oak leaf patterns are usually not yet seen in this initial symptom. In the absence of branch or fruit symptoms, presence of oak-leaf pattern indicates infection with CG-BP, cristacortis or impietratura.

 

Symptoms on trunk and branches

Symptoms of cristacortis resemble those of CG-BP, but the depressions due to cristacortis (CG-BP. 07, 25, 27) are smaller than the concavities or pockets of CG-BP. With cristacortis, there are pegs on the inner side of the bark that go deep into corresponding pits in the wood (CG-BP. 07, 26, 27). No such pegs and pits develop with CG-BP. With CG-BP, gum deposits are seen in some of the concentric growth layers of the xylem (CG-BP. 21, 22, 28), while with cristacortis, radially oriented traces of old pits remain buried in the xylem (CG-BP. 28, 29, 30).

Stem pitting symptoms of cristacortis are frequently seen on sour orange rootstocks (CG-BP. 12, 25); symptoms of CG-BP are never seen on sour orange rootstocks (CG-BP. 03, 11, 13, 16). 

On varieties such as mandarin or tangelo, susceptible to cachexia, cristacortis and CG-BP, stem pitting symptoms of cristacortis (CG-BP. 31) or cachexia (CG-BP. 32) can be overimposed on the CG-BP depressions.

Concavities of Tarocco pit (Russo and Klotz, 1963), unlike those of concave gum, are often round, more numerous and exude a ground, corklike material (CG-BP. 33).

Deep pits associated with corresponding pegs on the cambial side of bark were observed on Rubidoux trifoliate orange rootstock infected with citrus bent leaf viroid (CBLVd) variant-1a (Roistacher et al, 1993). Similar symptoms were also seen in Corsica on Pomeroy trifoliate orange rootstocks in an extensive viroid assay involving various variants of CEVd, HSVd, CDVd, CBCVd, and variant 1a and 1b of CBLVd (Vernière et al., 2004). However, these symptoms were not the result of viroid infections as they were present in trees of all treatments, including the non-inoculated controls. Furthermore, the pits resemble more cristacortis pits than CG-BP depressions, since they have corresponding pegs on the cambial side of the bark.

Fingers marks (CG-BP. 34) have sometimes been associa­ted with CG-BP but they are not graft-transmissible.

 

Biological indexing

 

Indicator citrus seedlings

For oak-leaf patterns: mandarin, Dweet tangor or sweet orange seedlings, but citron and lemon will also show oak-leaf patterns.

For trunk and branch symptoms: Washington navel sweet orange and Orlando tangelo.

 

Symptoms

Sweet orange seedlings graft-inoculated with non-lesion bark from Psorosis-A-infected trees show “shock symptoms” (wilting, bending and decline of the first young shoots developing after inoculation and cutting back the index plant) (CG-BP. 40).  Shock symptoms do not occur after inoculation of bark from CG-BP infected trees.

Leaf symptoms. Very mild interveinal streaking or flecking is the very first symptom after graft-inoculation of the indicator seedlings (CG-BP. 39). Usually, oak-leaf patterns are best observed on the second flush of growth (CG-BP. 35, 36, 37); they appear in the expanding leaves, and are best before the expanded leaves harden; they disappear completely as the leaves mature and harden. If temperatures during indexing are too high, symptoms in sweet orange or Dweet tangor indicator seedlings are completely masked (CG-BP. 36). The recommended greenhouse temperatures are 24-27° C during the day and 18-21°C at night (Roistacher, 1991). Cool night conditions, especially in the spring and fall flush of growth, favor the development of oak leaf patterns.

Wood symptoms. On inoculated seedlings of Washington navel sweet orange and Orlando tangelo, CG-BP depressions (CG-BP. 38) develop earlier than on other citrus species, and characteristic wood symptoms of CG-BP [concentric gum-stained growth layers in the xylem  (CG-BP. 21)and gum oozing (CG-BP. 14)] often develop within two to three years, even before CG-BP depressions on the trunk and branches can be seen. The gum-stained layers frequently appear in shoots with very small diameters. On Orlando tangelo seedlings, the typical CG-BP depressions develop within six years, while cristacortis stem pitting is obtained within 3 years (Vogel and Bové, 1974).

 

 

CONTROL

 

Use budwood free of CG-BP. The agents associated with CG-BP and the other two oak-leaf pattern diseases, cristacortis and impietratura, are readily eliminated by shoot tip grafting (STG). After STG, indexing must confirm absence of the CG-BP agent in the shoot tip-borne material: leaves of indicator seedlings inoculated with shoot tip-borne material must remain free of oak-leaf patterns.

Thermotherapy (Calavan et al., 1972; Roistacher, 1977) can also be used to eliminate the agent of CG-BP.

 

 

SELECTED REFERENCES

 

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da Graça, J. V., R. F. Lee, P. Moreno, E. L. Civerolo, K. S. Derrick (1991). Comparison of citrus ringspot, psorosis, and other virus-like agents of citrus. Plant Dis. Reptr. 75: 613-616.

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Dauthy, D., J. M. Bové (1965). Experiments on mechanical transmission of citrus viruses. p. 250-253. In W. C. Price (ed.) Proc.3rd Conf. Intern. Organization Citrus Virol., Univ. Florida Press, Gainesville.

Dauthy, D., J. M. Bové (1968). Purification of crinkly-leaf virus. p. 255-263. In J. F. L. Childs (ed.) Proc.4th   Conf. Intern. Organization Citrus Virol., Univ. Florida Press, Gainesville..

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Fawcett H.S. and A.A.  Bitancourt (1943). Comparative symptomatology of psorosis varieties on citrus in California. Phytopathology 33: 837-864.

Fawcett, H. S., L. C. Cochran. (1942). Symptom expression in psorosis of citrus as related to kind of inoculum. (Abstr.) Phytopathology 32: 22.

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Fraser, L. (1961). Lemon crinkly leaf virus. p. 205-210. In W. C. Price (ed.) Proc. 2nd Conf. Intern. Organization Citrus Virol., Univ. Florida Press, Gainesville. 

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Prepared (1975) by L. J. Klotz

Department of Plant Pathology

University of California

Riverside, California 92502

(U.S.A.)

 

Revised April 2009 by C. N. Roistacher1 and J. M. Bové2

1 Department of Plant Pathology

University of California

Riverside, California 92502

(U.S.A.)

2 Laboratoire de Biologie Cellulaire and Moleculaire

I.N.R.A./ Université Victor Ségalen Bordeaux 2,

Centre INRA de Bordeaux,

71, Ave. E. Bourleau,

33883 Villenave d’Ornon,

(FRANCE)