Foreign plant quarantines in-service training series

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Il Bacterium citri

United States Department of Agriculture April 1, 1940
Bureau of Entomology and Plant Quarantine

Foreign Plant Quarantines In-service Training Series. No. 2
(No. 1 is an introductory and explanatory number.)
Prepared by N. Rex Hunt

Name of disease Citrus canker, cancrosis.

Name of pathogens Bacterium citri (Hasse) Doidge
Syns. Pseud nonas itri Hasse
Bacterium oiTrrTHasse) Jehle
PFytmonas oitri (Hasse) Bergey et al

Hosts: Citrus spp. and numerous relatives. The citrus nursery stock
quarantine (No. 19) covers all plants belonging to the Sub-
family or Tribe Citratae. According to Dr. W. T. Swingle
B. oitri may attack any plant of the sub-tribe Citrinae,
3udg-ng by tests up to 1938. Swinglea flutinosa cankers
abundantly in the Philippine Islands. Plants of several
genera in the family Rutaceae and not in the sub-family
Citratae have been inoculated with positive results. (4, 5,
21a 17)
Part attacked: Leaves, twigs, larger branches, and fruit. Roots have
been inoculated successfully, but with difficulty. (8)

Place of origini Asia. Found on herbarium material of Citrus medical
collected in India (? 1827 1831) and on C. aurantifolia
collected in Java in 18142-1814. (6) ...

Country of first report: Organism described from U. S. in 1915 but
disease had been noted in Japan as far back as 1899. (10, 21)

First report from U. S.t Florida, Nov. 1912. Supposed to have been
introduced about 1911. (see (3))

Present distribution, Borneo, Ceylon, China, Dutch East Indies,
Formosa, Hawaii, India, Indo-China, Japan, Java, Malay States,
Mauritius, Mozambique (Portugese East Africa), New Guinea,
New Zealand, Northern Territory (Australia) Philippine Islands,
Seychelles, Siam. The disease was present in South Africa for
a time but was eradicated. Latest reports of the occurrence
of citrus canker in the United States are Alabama (1927),
Florida (1927), Georgia (1917), Louisiana (1959), Mississippi
a922), South Carolina (1916), and Texas (1938). The disease
is not present in the commercial citrus regions of Louisiana
and Texas and only a very few scattering infections have been
found in these states in recent years, hence eradication
should be established as completed before long. The disease
may have been eradicated from Northern Territory (Australia).
(it n. :1 18)







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Methods of spread: Air currents, beating rain, man, animals, insects,
etc. Drops of rain or dew on affected organs contain large
numbers of bacteria and the disease can be transferred
readily by physical or animal agencies from plant to plant.
Nursery stock, fruit or other plant parts serve to carry
the disease to new areas. The present distribution of the
disease shows its introduction into islands and other areas
near ports of call on trade routes radiating from its
original home, which may be taken to indicate spread with
the fruit. (_, 7)

Losses incurred: In Florida it was said to render infected grapefruit
trees worthless inside of two or three months. Owing to
its destructiveness and rapid spread, it was necessary to
eradicate the disease so quickly that it had no time to
demonstrate its power for sustained destructiveness under
Florida conditions and on less susceptible hosts under such
conditions. ()

Comparative losses: Where susceptible varieties are grown as in the
United States and the Union of South Africa it was necessary
to eliminate the disease or it would eliminate profitable
production with the citrus varieties being grown. Elsewhere,
as in Ceylon where the varieties grown are resistant and
conditions less favorable for the spread of the disease, it
is controlled by spraying, sanitation, and cultural practices
and losses are not severe. (7)

Control Methods: The cheapest control in some areas is accomplished
by eradication and strict quarantines. The most satisfactory
method of eradication is destruction of diseased trees and
burning of the soil surface with a blowtorch. In Ceylon
trees are sprayed every week in the rainy part of the
growing season and every two weeks the rest of the growing
season, diseased parts are removed and burned,and irrigation
is handled to stimulate the main growth when infection is
less likely to occur. These methods give reasonable control
in Ceylon. (1, 2, 5, 7, 20 21, 22)

Quarantine action: Quarantine No. 19, promulgated Dec. 10, 1914,
effective Jan. 1, 1915, prohibits the importation into the
United States of all citrus nursery stock, including buds,
scions, and seeds, from any part of the world. Effective
July 1, 1932, citrus seeds were transferred from this
quarantine to the less stringent restrictions of quarantine
1o. 37. The citrus fruit quarantine, No. 28 issued June 27,
1917, effective August 1, 1917, prohibited the importation








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of citrus fruits except oranges of the mandarin class
(satsuma oranges and tangerines) from a large part of the
orient and the Union of South Africa. The citrus fruits
permitted entry under quarantine No. 28 are subject to the
restrictions of the Fruit and Vegetable Quarantine No. 56
also and hence may be prohibited entry under its provisions.
(20)

Description: On leaves the disease becomes apparent as minute yollow-
brown, oily, translucent, raised spots, usually visible on
the lower surface first. As the spots grow and thicken the
lower surface becomes spongy and the upper surface also
becomes raised and either smooth or ruptured and spongy.
If growth is rapid the spongy growth appears white, if growth
is slow the surface is tan or brown. When the spot is
ruptured the margin is likely to become watery, glazed,
greasy appearing and often somewhat raised and yellowish
brown or green in color. The spot is surrounded by a halo
of chlorotic leaf tissue with a more or less irregular margin
which shades off quickly to the normal colored tissue. On
fruit the lesions are much the same as on leaves but usually
without the halo and in old stages with the margin likely to
be raised more sharply giving a more marked crater like
aspect.
After the lesions get old, on any part of the host, they
become corky looking and the tissue is hard. Margins are
likely to be irregular in whole or in part. The maximum size
of the lesions varies with the host and the part affected,
mostly ranging from an eighth to a third of an inch in diameter.
Other diseases, such as scab and leprosis, having raised
lesions do not have the glazed margin with an oily or greasy
appearance surrounding the eruption. While canker lesions do
not all have a crateriform appearance, there will usually be
some present showing this character and helping to distinguish
this disease. Melanose lesions may be raised but remain small
and smooth. However, it is difficult for specialists familiar
with the disease to determine it on intercepted fruit when
the lesions are few and not typically distinctive.
The damage done by citrus canker depends on host
susceptibility, weather and state of growth of the host.
Grapefruit, sweet oranges, limes, and some varieties of lemon
are very susceptible. Varieties of Citrus nobilis, including
tangerines, king, mandarin and satsuma oranges, are resistant
to canker. Three cultivated species of kumquat are highly
resistant while a wild species is very susceptible.







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Infected fruit may drop. If it matures the lesions
disfigure it. The disease may cause more or less defolia-
tion. Lesions may kill young growth. Cankers on older
wood may do relatively little direct damage but serve as
sources of inoculum during periods when spread is most
likely to occur.
The organism will withstand considerable periods of
drying. Abundant moisture is the most important factor in
the spread of the disease, infection taking place readily
under a temperature range between 20 and 50 C.
Abundance of moisture produces rapid growth which is
most susceptible and also helps to produce an abundance of
bacteria, helps to spread them and results in formation of
the film of moisture on the plant surface which is important
in enabling the organism to gain entrance without the
assistance of wounds.
The organism may persist for years in the soil according
to some workers but others believe it is killed out under
normal field conditions in a few months to a year or two at
the most. The length of time it persists seems to depend
on the relative antagonism of other organisms in the soil
as well as on the character of the soil and temperature and
moisture conditions. (5, 7, 8, 9, 10, 11, 12, 13, 1., 15,
16 1i7, i8, 19_, 20, 21, 22, --- -







-5-


Bibl biography:

(1) Berger, E. W., Stevens, H. E., and Stirling, Frank
19l14 Citrus canker II
History of Citrus canker, by E. W. Berger
Studies of Citrus canker, by H. E. Stevens
Eradication of Citrus canker, by Frank Sterling
Fla. Exp. Sta. Bu. No. 124, pp. 25-55, Oct. 1914
Brief account of occurrence in the United States of
citrus canker. Stevens' paper covers symptoms and uncompleted
studies including inoculations and effort to find the
pathogen, a fungus being mistakenly thought to be responsible
for canker. Spread found to be more rapid during rainy
weather. Any part of the tree seems to be susceptible at any
age. Eradication recommended. Stirling's paper discusses
failure of drastic pruning out and spraying treatment and
development of the forced flame burning of trees and soil in
order to eradicate the disease. "As I have said before, this
disease is by far the worst which has ever yet affected the
citrus industry. The leaves, twigs, and fruit become covered
with a cankerous growth. The fruit itself seems to be
especially susceptible to the disease, and drops soon after
becoming diseased. Canker is so deadly that when the tree
first becomes infected, in this territory, it is worthless
inside of two or three months."

(2) Bertus, L. S.
1951 Spraying against canker of Citrus. Trop. Agriculturist
76: 33557-9. 1951
In Ceylon citrus canker may be controlled by weekly
spraying with 1% solution of concentrated lime-sulphur or
fortnightly applications of a 2% solution, supplemented by
removal and burning of all affected leaves and twigs. It is
recommended that irrigation should be so managed as to get
maximum growth during the drier periods when infection of the
susceptible young leaves is less likely to occur.

(3) Doidge, Ethel M.
1916 The origin and cause of Citrus canker in South Africa.
U. of So. Afr. Dept. of Agric. Sci. Bul. No. 8, 20 pp. 1916.
Citrus trees imported from Florida during the 1905-6
season and planted in a government experimental orchard showed
scab-like spots on the fruit in 1908. The following summer
was wet and the disease spread with incredible rapidity.
Nursery stock was burned, other trees severely pruned and
sprayed five times. In 1910 pruning and spraying were
practiced again. The 1911 crop was free from disease but in
1916 the disease reappeared. In 1915 it was shown that
Pseudomonas citri Hasse was the cause of the disease.







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(NOTE: While it is stated that citrus canker was introduced into
South Africa from Florida in 1905, this does not accord with the
history of the disease in the United States. It seems more likely
that the disease was introduced into South Africa from the Orient
on some resistant host on which it escaped notice and spread to
the stock from Florida. However, this discrepancy has never been
cleared up apparently.)

(4) Doidge, E. M.
1929 Further Citrus Canker Studies. U. of So. Africa Dept.
Agr. Bu. 51, 51 pp. 1929.
Plants of the sub-tribe Citrineae are the most susceptible
usually but a number of genera of other sub-tribes were
successfully inoculated. Species of Toddalia and Xanthoxylon
are usually immune or highly resistant. Fagara (Xanthoxylon)
capensis and Clausena inaequalis were moderately susceptible
in inoculation tests.
The decline of Bacterium citri in the soil was found to
be much less rapid than indicated by Lee and Fulton. Experi-
ments in the field showed that the organism remained alive in
the soil and that trees planted in such soil two years or so
later developed canker the first year favorable for canker.
It is dangerous to replant infected sites even 4 to 6 years
after diseased trees aie destroyed.
Canker was carried 6 miles in flood water and infected
lemon trees.
Costs of canker inspection are given and the work
discussed.

(5) Elliott, Charlotte
1930 Manual of Bacterial Plant Pathogens. 349 PP. June, 1930.
Bacterium citri (Hasse) Doidge, description, synonymy,
symptoms, hosts, geographical distribution, and control are
given on pp. 112-13, literature is listed pp. 114-121

(6) Fawcett, H. S. and Jenkins, Anna E.
1933 Records of Citrus canker from herbarium specimens of the
genus Citrus in England and in the United States. Phytopath.
23t 820-8%4. 1933.
The earliest collections on which citrus canker was found
were on Citrus media from northwestern India believed to
have been collected 1827-1831 and on C. aurantifolia collected
in Java in 18l42-18%4.

(7) Fawcett, H. S.
1936 Citrus Diseases and Their Control (1st ed. in 1926, canker
covered pp. 212-222) 656 pp., 187 figs., some in color. 1936.
Pp. 237-249 Citrus canker is discussed, history, distribu-
tion, hosts, symptoms, organism, environment, and prevention.
Symptoms and how to distinguish canker from other diseases are
discussed in some detail.




-7-


(8) Fulton, H. R.
1920 Decline of Pseudomonas citri in the soil, Journ. Agr.
Res. 19: 207-223. June 1, 1920.
The decline of P. citri in soil kept under conditions
approximating those in the field was so rapid as to suggest
that agricultural soils probably can not long retain a
dangerous possibility of disseminating the citrus-canker
organism. The rapid decline of P. citri is thought to be
due to deterious effects of other organisms in the soil,
in part at least.

(9) Fulton, H. R. and Bowman, John J.
1929 Infection of Fruit of Citrus by Pseudomonas citri.
Journ. Ag. Res. 39, 403-L26. Sept. 15, 1929.
Inoculations on young fruits are much more likely to
be successful if wounds are fresh when inoculum is applied
and if oil glands are not punctured. Success is less
likely on large or small fruits than on medium sized fruits.
Stomatal infections are less frequent than infections at
visible injuries. The organism multiplies in lesions on
fruit of all sizes but does not increase but rather tends to
disappear quickly in orange and lemon fruits inoculated
after being picked at maturity. The organism seems to
persist longer in mature grapefruit. Tests of cankers induced
on young citrus fruits of orange, lemon, lime, and grapefruit
were all negative when tested eix or seven months later, after
the fruit had matured. However, viable canker bacteria have
been found in some of the tests of lesions on citrus fruits
intercepted at U. S. ports.
In inoculated fruit viable bacteria may be present without
forming a visible canker. Penicillium rot has a deleterious
effect on the canker organism.

(10) Hasse, Clara H.
1915 Pseudomonas citri, the cause of Citrus canker. Journ.
Agr. Res. 4: 97-10, pls. IX and X. Apr. 15, 1915.
Description of Pseudomonas citri Hasse and of its
isolation in pure culture, inoculations, structure of cankers.

(11) Hill, Gerald F.
1918 History of Citrus canker in Australia with a brief account
of the occurrence of the disease in the United States of
America and South Africa. North. Terr. Australia Bul. No. 18,
8 pp., 8 pl. Oct. 1918.
The part dealing with South Africa is based on Miss
Doidge's account in Sci. Bul. No. 8. A number of U. S.
authors are cited. Hill became interested in the disease in
Australia in 1912. After the cause of the disease was learned
in 1916, various quarantine and eradication measures were







-8-


undertaken. Details are given of the finding of citrus
canker in individual holdings, severity of the disease on
different hosts, the quarantine notice is given, and symptoms
of the disease as it occurs in Northern Australia are given.

(12) Hino, I.
1951 The behaviour of the Citrus canker organism in the soil
and in water. Studia Citrologica, Tanaka Citrus Exper. Stat.
4, 167-178. 1951 (English summary).
Canker organism remained viable several months in
inoculated garden soil and in pond water so it could overwinter
in the soil. The organism was found to thrive in relatively
dry highly alkaline soils. Soil protozoa, which destroy
bacteria including the canker organism, are not so active during
winter.

(13) Lee, H. A.
1918 Further data on the susceptibility of Rutaceous plants to
citrus canker. Journ. Agr. Res. 15t 661-666. Dec. 23, 1918.
This paper gives a tabulated summary of results of
inoculations on plants of Rutacea representing 24 species in
20 genera, 19 species being more or less susceptible.
Fortunella hindsii is suggested as possible original wild host.

(14) Lee, H. A.
1920 Behavior of the citrus-canker organism in the soil.
Journ. Agr. Res. 19: 189-206. June 1, 1920.
The canker organism was found to disappear very quickly in
normal soil under orchard conditions. When inoculated in
sterilized soil the organism increases and multiplies. "The
indication is that the normal soil organisms are antagonistic
in some way to the existence of P. citri in the soil."

(15) Lee, H. A.
1922 Relation of the age of Citrus tissues to the susceptibility
to Citrus canker. Philipp. Journ. of Science 20: 3531-3359, 4
pl., 1922.
Orange fruits of different types were tested and it was
found that young fruits were quite susceptible while older
fruits were slightly affected or immune. The period of suscept-
ibility for grapefruit was longer than for oranges. Washington
navels were virtually immune from stomatal infection after 85
days and wound infection after 110-120 days in one series of
observations. Leaves also lost susceptibility with age.

(16) Loucks, K. W.
1950 Some physiological studies of Phytomonas citri. Journ.
Agrio. Res. 41: 247-258. 1950.







-9-


Citrus canker organism died out after 13 iR'ys in
unsterilized Florida muck soils and after 6 days in unsterilized
sandy soils but persisted for 150 days or longer in both types
sterilized, inoculated, and kept at room temperature.

(17) Peltier, George L. and Frederich, William J.
1924 Further studies on the relative susceptibility to Citrus
canker of different species and hybrids of the genus Citrus,
including the wild relatives. Journ. Agr. Res. 28: 227-27'
Apr. 19, 1924.
All grapefruit plants and all of the sweet orange group are
susceptible to canker. All of the Citrus nobilis group show
resistance. A considerable number of genera, species, and
hybrids is listed and inoculation results noted.

(18) Peltier, G. L. and Frederich, W. J.
1926 Effects of weather on the world distribution and prevalence
of Citrus canker and Citrus scab. Journ. Agric. Res. 52: 147-
164, 1 map, 8 graphs. 1926.
Canker could develop in any citrus growing region but
should be most severe in areas with the longest periods of
temperature 80 F. or above. The precipitation curve is
important, a fairly long period of plentiful moisture produce 1,
tender susceptible growth and humidity conditions favorable
for infection.

(19) Stevens, H. E.
1915 citrus Canker III. Fla. Agr. Exp. Sta. bul. No. 128,
pp. 5-20. Nov. 1915.
Historical summary, symptoms, studies confirmir.g Pseudomonar,
citri Yasse as the pa-h-er arnd discussion f" tests showing that
P. c-tri lives for months in inoculated soil. Ten-reratures of
0 C7. or higher for c inu'es killed the citrus canker organism
in all cases.

(20) 3.0.-i.le, '. 7 lozin ... R. a E
1924 :Lrantiire prcceeure to safeguard the introduction of c+i -
plants: a system of aseptic plant propagation. U. S. Dept.
Agr., :ept. Circ. No. 299, pp. 1 15, figs. 1 13. Jan. 1924.
-.-i is a description and working plans of the special
greenhouses and equipment developed to make it possible for the
Department to obtain citrus breeding stock from foreign couintr-i
and be assured that no new diseases or insect pests were
introduced with such stock and permitted to escape.

(21) Tanaka, T.
1918 Citrus canker in Japan: a translation of the first
description of this disease, from the Japanese. "A new kind of







- 10 -


Pathogenic Microbe: being No. 8 of the organisms injurious to
citrus." From "Nippon to Mikan,* by Kumanosuke Abe, Pub. in
M. 37, v. (May, 1904), p. 162-165. Phytopath. 8: ,i53- ,.
Aug. 1918.
Citrus canker was found to affect 70 to 80% of the 70,000
to 80,000 Washington navel orange trees in nurseries of the
Meiji district of Japan in 1899. The disease attacked the new
vigorous growth, spreading rapidly. Trees were not killed but
the summer shoots were destroyed, causing a big loss to
nurserymen. No infections were found on nearby Satsuma orange
trees. The severity of the infection is more pronounced in
the wet years and spreads more rapidly at such times.
Diseased parts should be removed and burned at once.
Spraying with Bordeaux is recommended.
The organism was not isolated or described.

(22) Wolf, Frederick A.
1916 Citrus canker. Journ. Agr. Res. 6:69-99. 8 figs., pls.
VIII-XI. April 10, 1916.
A detailed account of studies of the organism in culture
and in the host, chemical changes in the host induced by the
pathogen, dissemination, control. A fungus found to occur in
the cankers caused by Pseudomonas citri is named Phoma social and
described. Complete eradication found to be the only effective
control measure.

(23) Wolf, F. A.
1916 Citrus Canker. Ala. Exp. Sta. bul. No. 190, pp. 91-100.
May, 1916.
The disease is discussed and illustrated, Pseudomonas
citri Hasse illustrated and cross-sections of diseased tissue
pictured. His tests indicated 65 C. temperature was required
to kill the organism under some conditions. New infections may
appear at any time during the growing season. Infections occur
on old leaves and twigs as well as new. Old diseased areas may
enlarge. Leaves are infected through stomata, which occur on
the lower surfaces of the leaves, but only when a film of
moisture is present. Infection also takes place. through wounds.
Eradication is only known method of checking citrus canker.






Bacterium aitri


Plato 1


Fig. 1--
Infected grapefruit.


Fig. 2-Infected twig of Citrus trifoliata, showing brokenn
membrane around lesions. (Magnified approxi-ately x3).


Fig. 3--Canker o.i _apefruit
leaves.


(From Florida Bulletin 128. Fig. 4a 5, and 3-.)


r- WMINIk -MENIMIN.- -











































































































































































































































. ... .. ... ..






Baoterium oitri


Plate 2


Fig. 1--Grapefruit leaf showing young Citrus cankers.
Fig. 2--Old Citrus canker on Satsuma leaves.
Fig. 3, 4* --Seedling grapefruit branches affected with Citrus canker.
Fig. 5--Severe banker infection of branches of Citrus trifoliata.


(From Jour. Agr. Res. 6t 69-100. Apr. 10, 1916. Plate VIII)






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