STUBBORN, GREENING, and RELATED DISEASES 141
Citrus Dieback in India- the Contribution of
Greening Virus
L. R. FRASER and DALJIT SINGH
DIEBACKDISEASE of citrus has caused increasing alarm to horticulturists
and growers in India since it was first observed over 20 years ago. It has
now been recorded in all citrus-growing areas of the country. As a result
of numerous investigations from many angles, it had come to be gener-
ally accepted that the disorder involved tristeza virus, zinc deficiency,
and some fungal parasites of twigs (1).
None of the above conditions can adequately explain the disease or its
spread. Tristeza is widespread in Indian citrus, but is not universal, and
is not invariably present in dieback-affected trees. Moreover, many of the
species affected in India are tolerant of tristeza in other countries. De-
ficiencies of zinc and other minor elements have been implicated on a
symptom basis, but application of zinc with or without other minor ele-
ments failed to cure the condition, although sometimes slight and tem-
porary improvement resulted. The fungi associated with dying-back
branches are well known as invaders of moribund or weakened tissues.
A study was made of citrus dieback disease in all major citrus areas
of India, during April, May, and June, 1966.
0bservations
As a result of the observations made, and a review of the experimental
work in progress at research institutions in several States (3), it is con-
cluded that dieback is caused by the virus responsible for greening dis-
ease of citrus in South Africa (3).
DISTRIBUTION AND MEANS OF SPREAD.-T~~ dieback disease was seen
in all citrus-growing districts in India, and almost all citrus appeared to
be infected. At present, all nurseries are taking budwood from infected
trees and much of the spread has been due to that practice. Insect trans-
mission is obviously taking place since seedling trees of all ages in private
plantations and in research institution orchards were infected. Infected
unbudded seedlings - only nine months old were seen in nursery seedbeds.
S Y M P T O M S . - S ~ ~ ~vary
~ O ~inS intensity with the variety. In sweet
orange [Citrus sinensis (L.) Osb.] the range of symptoms is exhibited
most clearly in young, vigorously growing trees. In trees which appear
to have been infected after reaching maturity, symptoms are less marked.
In spring-formed leaves, tissues along the main vein turn yellow after
142 PROCEEDINGS of the IOCV
leaves reach maturity, and chlorosis spreads over lateral veins and in-
volves much of the leaf in severe cases. Such leaves usually fall. Heavy
blossoming with poor setting of fruit may also be evident. Later growth
is less vigorous; many twigs are upright and produce smaller leaves.
The leaves develop patterns more or less resembling those of zinc and
iron deficiency; they may also exhibit round or angular yellowish
blotches or become entirely yellow. Frequently, small green spots occur
on chlorotic leaves.
Reduced vigor is associated with sparse foliage, dieback of branches,
and a steep decline in cropping. Final deterioration and death occur
through secondary invasion by wood-rotting fungi.
McClean and Oberholzer (3) noted that leaf symptoms of greening
are often restricted to one or several limbs in early stages of the disease.
This is also a striking symptom of the dieback disease in India and sug-
gests that to some degree the reaction of susceptible varieties to infection
is a hypersensitive one, and that the metabolic status of the host may be
important in determining virus multiplication and spread. Leaf symp-
toms are masked by high temperatures, and growth made at the hottest
time of the year is generally symptomless as noted by McClean and
Oberholzer (3) for greening disease.
Sudden wilting and death of some affected trees occurs during late
spring and early summer in several districts of central and southern
India. All gradations between this sudden collapse and the normal spring
sequence of symptom development were seen. Occasionally, young trees
showing the first symptoms of greening developed large vigorous leaves
with numerous small circular pale green spots of a ringspot type (Fig. 1 ) .
In species other than sweet orange, the general pattern of symptom
development is similar, although intensity of chlorosis, amount of die-
back, and degree of yield reduction is less in the more tolerant types.
Fruit symptoms
. . as described by McClean and Oberholzer were not
seen. A type of sunburning was common in the Mosambi and Sathgudi
sweet orange varieties, mandarins ( C . reticulata Blanco) , Meyer lemon
[ C . limon (L.) Burm. hyb.], and pummel0 [C. grandis (L.) Osb.]. Typi-
cally, a yellow patch with abrupt margin occurs on the exposed side of
the fruit, while the rest of the fruit remains conspicuously green. In sev-
eral tangelo varieties, and occasionally in mandarin, sweet orange, and
grapefruit, lopsided fruits with poorly developed seeds were observed,
but this is not a feature of the disease.
HOST RANGE AND REACTION.-All sweet orange - varieties grown
- are
highly susceptible and none show sufficient tolerance for commercial pur-
STUBBORN, GREENING, and RELATED DISEASES 143
poses. Sathgudi, when grown on Sathgudi stock, persists longer than
most others, but cropping eventually becomes uneconomic with this
variety also. No stock exerts a worthwhile ameliorative effect on the dis-
ease in sweet orange.
Mandarins vary in reaction with strain, locality, and stock. The seed-
ling varieties grown in hill areas (Kalimpong, Assam, Coorg, et cetera),
FIGURE1. A large vigorous leaf with small pale green spots of the ringspot type.
if affected at an advanced age, exhibit reduced cropping and vigor.
Finally, twig dieback occurs, and the trees gradually die from secondary
wood rots. Seedlings infected at an early age react more severely. Appar-
ently the yellowing of veins and adjacent tissue in mature leaves occurs
near the point of infection. Chlorotic leaf patterns develop in subsequent
growth, and considerable leaf fall results in sparse foliage. Dieback and
death ensue within a few years. Cleopatra-type mandarins appear to be
less severely affected.
144 PROCEEDINGS of the IOCV
Many strains of Rough lemon (C. jambhiri Lush.) exist in India and
most appear somewhat tolerant of the-disease, but in Assam, the Sohmyn-
dong strain is quite susceptible. The strains of Rough lemon in use as
stocks a t Coorg and at Nagpur show a useful degree of tolerance and
have the effect of prolonging productive life of the Coorg and Nagpur
mandarins, as compared with seedling mandarin trees.
Grapefruit (C. paradisi Macf.) appears almost as susceptible as sweet
orange, and tangelo (C. reticulata x C. paradisi) varieties appear ex-
tremely susceptible. On the other hand, lemons, Rangpur lime (C. reti-
culata var. austera hyb.) , sweet lime [C. aurantifolia (Christm.) Swing.],
and C. karna Raf. show considerable tolerance. Symptoms in sweet lime
and C. karnu Raf. were restricted to mild leaf blotching in young trees.
Moderate symptoms were shown by C. hystrix DC, Meyer lemon, C.
ichungelzsis Swing., citron (C. medica L.), and sour orange (C. auran-
tium L.). Mild symptoms were exhibited by Poncirus trifoliuta (L.)
Raf., C . maderaspatuna, C. assamensis, wild lemon, and C. latipes
(Swing.) Tann. Only one species, C. macroptera Montr., showed no
symptoms which could be related to greening.
AGEAT WHICH SYMPTOMS althoug although all budwood is now of
necessity taken from infected trees, generally less than 5 per cent of
young budded trees in commercial nurseries show visible evidence of
infection. Young commercial blocks of sweet orange varieties propagated
from infected sources usually grow well for four or five years. Major de-
velopment of symptoms occurs after the first crop of fruit and appears
first in only a few trees. However, by the time the block is seven to
eight years old, most or all of the trees show severe dieback. It is gener-
ally noted that when the virus is spreading through a virus-free planta-
tion, the first symptoms of dieback disease are seen following heavy
cropping. McClean and Oberholzer (3) have reported a variable per-
centage of transmission of greening and postulate uneven distribution
of the virus in the tree so that some buds do not carry it. Possibly, virus
multiplication is checked until the physiological state of the tree, coin-
cident with heavy cropping, favors its extension.
Literature Cited
1. CAPOOR, S. P. 1963. Decline of citrus trees in India. Bull. Nat. Inst. Sci. India
24.
2. FRASER, L. R. 1966. Citrus die-back in India. Report to the Department of Ex-
ternal Affairs, Canberra, Australia.
3. MCCLEAN, A. P. D., and OBERHOLZER, P. C. J. 1965. Greening disease of the
sweet orange. S. African J. Agr. Sci. 8: 253-276.
