Plant Disease Publications
Extension, College of Agriculture & Life Sciences, The University of
Diseases of Citrus in Arizona
Publication adapted by
Mary Olsen, Plant Pathology Specialist
Mike Matheron, Research Scientist, Plant Pathology
Mike McClure, Professor, Plant Pathology
Zhongguo Xiong, Associate Professor, Plant Pathology
Based on material originally written by Richard Hine, Plant Pathologist
(retired), Mike Matheron, and Lowell True, Agricultural Agent
Photographs by Richard Hine
- Parastic Diseases
- Virus Diseases
- Virus or Virus-Like Diseases
- Mycoplasma Diseases
- Nematode Diseases
- Nonparasitic Diseases
Citrus, a crop of international importance, is indigenous to
areas in southeast Asia. In Arizona, oranges were first planted commercially
in central Arizona in the late 1800s. Today, commercial production is
centered in several warm and low-frost-risk areas of central and southwestern
Arizona. A great number of citrus varieties are also widely planted
in home gardens. Many diseases of citrus have been described world wide
and have colorful and descriptive names such as: blue mold, green mold,
gray mold, pink mold, pink nose, brown rot, black spot, black rot, black
pit, yellow vein, yellow spot, rubbery wood, lumpy rind, curly leaf,
corky bark, slow decline, spreading decline, and stubborn. Other names
are rooted in the many international languages of citrus such as: Italian
(impietratura and mal secco), Portuguese (tristeza), or Greek and Latin
(cachexia, psorosis, exocortis, xyloporo-sis, cristacortis, and leprosis).
Fortunately, most of the more serious, widespread diseases do not occur
or are of little importance in Arizona. There are, however, a few diseases
of sufficient importance to discuss in this bulletin. They include several
diseases caused by fungi: foot rot gummosis (Phytophthora root
rot) caused by the soil occurring fungi Phytophthora parasitica
and P. citrophthora, Hendersonula branch wilt (caused
by the fungus Hendersonula toruloidea), Brown heartwood rot of
lemons caused by a species of Antrodia and Coniophora,
and black rot of fruit, caused by Alternaria alternata. Catastrophic
bacterial diseases that have plagued more humid and rainy production
areas, such as Florida, do not occur in the desert environments of Arizona.
Figure 1. Non-specific symptoms in citrus
of general tree decline with tip die back and sparse foilage. This condition
could be caused by several factors including Phytophthora crown and
root rot, citrus nematode, or nutrient deficiencies or excesses. (Yuma,
Of the more than 30 virus and virus-like diseases that have been
described world wide, only Tristeza, Psorosis and a mycoplasma disease,
Stub-born, are presently known to occur in Arizona. Tristeza and Stubborn
disease have been extensive-ly studied in Arizona and in other citrus
areas of the world. These studies have increased our knowledge of the
basic biology of these two very different pathogenic micro-organisms
including vector transmission, strains, alternate hosts, effects on
host plants and new methods of diagnosis and detection.
In 1956, research in Arizona
identified Tristeza virus in Meyer lemon, and Psorosis, a virus-like
disease, in several old line citrus varieties including Marsh grapefruit,
Valen-cia orange, and Washing-ton navel. These two diseases were probably
introduced into Arizona in infected budwood and planting material prior
to 1930. Stubborn disease was first identified in Arizona in 1965.
One of the most important
diseases found in citrus in Arizona is caused by the citrus nematode
(Tylenchulus semipenetrans). This disease has become more widespread
and important because present control options are limited.
Many serious and widespread
diseases in citrus grown in Arizona are nonparasitic in nature. These
diseases are not the result of infection by living microorganisms but
are caused by factors such as: excessive sun and heat, excesses of certain
elements including boron or lithium, excess soil salts, mineral deficiencies,
water stress, freeze injury, hail, lightning, and genetic disorders.
Two excellent publications that discuss diseases of citrus are: Compendium
of Citrus Diseases and Citrus Health Management, both published by the
American Phytopathological Society and Integrated Pest Management for
Citrus, published by the University of California (publication 3303).
Phytophthora foot rot (Phytophthora gummosis)
Figure 2. Seedling death (damping-off) in a
citrus nursery caused by Phytophthora parasitica. (Weslaco, TX)
Phytophthora foot rot or gummosis of citrus in Arizona is caused
by two soil microorganisms, Phytophthora parasitica and P.
citrophthora. This disease is relatively common in citrus groves
in the Salt River Valley and Yuma areas. Loss of individual trees in
home gardens occurs in all of southern Arizona. Disease incidence is
especially high in trees established with the graft union at or below
the soil surface, exposing susceptible scion tissue to the two pathogens.
Severe losses also can occur in groves subjected to flood irrigation
if trees are planted on susceptible rootstocks.
Figure 3. Typical gummy
lesions caused by Phytophtora parasitica in citrus bark. (Yuma, AZ)
Symptoms: The most diagnostic symptoms of Phytophthora
foot rot are found at or below the soil level. Longitu-dinal cracking
of bark, accompanied by profuse gum-ming, usually is positive evidence
of infection. Soil removal around affected trees reveals bark that is
watersoaked, slimy, reddish-brown, or in late stages, black. Diseased
bark may be easily removed if fungal activity is recent. Advanced stages
of infection will result in yellow, sparse foliage. Trees may later
collapse and die due to the girdling action of the fungal infection.
Figure 4: Bark removed
from sample shown in previous photograph. Note the dark tissue where
P. parasitica is active. (Yuma, AZ)
Fruit infections, although not common in southern Arizona, may occur
during or shortly after warm rainy periods during summer and fall. These
infections are caused by motile spores being splashed onto fruit. This
stage of the disease is called brown rot, since the diseased areas on
the fruit are brown in color. Active growth of trunk lesions occurs
during May and June, declines somewhat during the hot summer months
of July and August, then resumes during September and October.
Disease cycle: Both P. citrophthora and P.
parasitica are soil-borne fungi. They complete their life cycles
in the soil. In our dry desert conditions infection by these two pathogens
occurs, for all practical purposes, only on roots and lower bark tissue
at the crown of the tree. In humid, wet areas of the world, however,
these fungi have the capacity to infect fruit and upper trunk tissue.
Recent surveys have determined that P. parasitica is the more
common of the two species, in soils in the lower elevation, higher temperature
areas of Yuma County. This may be due to the fact that P. parasitica
has a higher optimum temperature for growth (85o-90o F) than P.
citrophthora (75o-80o F). However, both species are commonly found
in central Arizona. These species have been recovered from soil and
infected plant tissue in over 85 percent of 60 different citrus plantings
in Maricopa and Yuma counties. Both of these fungi produce motile, swimming
zoospores when soils are saturated from irrigation or rainfall. These
spores are attracted to root tips. After attachment they germinate and
infect cortical root tissue. Infected feeder root cortical tissue becomes
rotted and dark in appearance.
Figure 5. A close-up
of a rootstock susceptible to P. parasitica and a resistant scion. Note
the line of demarcation between resistant tissue (previous photo) and
the susceptible discolored tissue (next photo). (Weslaco, TX)
Physical removal of this decayed tissue (by rubbing between your fingers)
reveals the whitish, central root tissue. This is a simple diagnostic
technique that can be used in the field. Proof that a Phytophthora
sp. is the cause of the decay requires the isolation and identification
of the fungus on Phytophthora specific media in the laboratory.
Both species produce survival structures in decayed root tissue that
permits indefinite survival in soil. Studies in Arizona have shown that
isolates of P. parasitica from noncitrus hosts (tomato, for example)
are not pathogenic to citrus. Interestingly, in contrast, isolates of
P. parasitica from citrus are highly pathogenic to tomato.
Control: Most citrus trees are budded on to a rootstock.
Most of these rootstocks are more resistant to Phytophthora diseases
than the scions (tops), so it is necessary to keep the bud union at
least four to six inches above the soil line at planting. In general,
water should not be allowed to stand around the crown of citrus during
irrigation. This is particularly true when rootstocks susceptible to
Phytophthora disease, such as some selections of rough lemon
or sweet orange, are used. Moderately resistant rootstocks include Citrus
macrophylla, Cleopatra mandarin, and Troyer citrange. Over irrigation
that causes soil saturation is detrimental to normal feeder root development
even in the absence of Phytophthora. It is important to dig a
planting hole as deep as necessary to obtain good drainage. Caliche
layers, commonly found in our low rainfall, alkaline soils, should be
opened up to allow water drainage and unrestricted root development.
Figure 6. Typical symptoms
of an active lesion caused by P. parasitica. Note the dark, discolored
infected tissue that extends into the light-colored disease-free trunk
tissue (Cagayan, Philippines)
Control of Phytophthora diseases in citrus has been enhanced
by the availability of highly active, systemic fungicides specific for
control of Phytophthora. These chemicals are applied to the soil
and the crown and trunk areas of affected trees. Studies in Arizona
indicated that isolates of P. parasitica and P. citrophthora
pathogenic to citrus do not occur naturally in Arizona soils. This
fact suggests that these fungi were most likely introduced into Arizona
on imported planting material prior to our present inspection and certification
Hendersonula Branch Wilt
This disease, also known as sooty canker or limb wilt, is caused by
the fungus, Hendersonula toruloidea, a wound pathogen that invades
citrus bark that has been damaged by freezing injury, sunburn, or mechanical
injury but does not infect uninjured bark tissue. This fungus has a
wide host range and causes disease in many plants unrelated to citrus.
Figure 7. Symptoms of
sooty canker caused by Hendersonula toruloidea. (Phoenix, AZ)
Symptoms: The most common symptom of sooty canker is
the sooty, black growth that develops beneath bark tissue. This black
canker is due to the presence of masses of black, fungal spores that
appear under the bark and on the surface of the canker. Because the
fungus grows into and kills sapwood, the leaves on branches with cankers
wilt, turn brown, and die. Branches die back to the cankered area. Scattered
branches are usually affected. Most cankers develop on unshaded trunks
or limbs that face toward the sun. Sunburned trunks and limbs are highly
susceptible to infection.
Biology of the pathogen: In Arizona, the fungus produces
only conidia and thus has a very simple life cycle. The small conidia,
produced in black, powdery masses under bark, are easily wind disseminated.
These spores, which arise from segmented hyphae, are carried to damaged
bark tissue where they germinate and initiate infection. The mycelium
grows into living tissue. Infected sapwood is stained gray to black
Control: Sooty canker can be controlled when infections
are confined to limbs and upper branches. Smaller infected branches
should be removed when symptoms appear. Since sunburned bark is the
primary infection site, large limbs should be pruned only when trees
Figure 8. A close up
of the sooty canker trunk lesion shown in previous photograph
When removing infected limbs, cut back to at least one foot below the
canker. The cut area and pruning tools should be treated with a solution
of one part household bleach and nine parts water. Pruning wounds should
be painted with a copper fungicide to prevent infection. Reapply the
copper compound to the wound each spring to insure adequate protection
against infection. Control becomes increasingly difficult as the disease
progresses into the scaffold branches and is virtually impossible once
the main trunk is infected.
Tree vigor should be maintained through proper fertilization and deep
watering on a regular schedule. Severe pruning of larger branches and
limbs of trees should be avoided. Whitewash, applied to exposed lower
trunk areas, will reduce the possibilities of infection. This material
reflects radiation and reduces bark temperature.
Heartwood Rot of Lemons
Two different wood rot fungi recently have been shown to cause decay
and death of branches of lemon trees in the Yuma area. The fungi, Antrodia
sinuosa and Coniophora eremophila, initially invade branch
tissue though wounds resulting from fractured or partially broken limbs.
These wounds usually result from tractor damage, heavy fruit load and
wind damage. The aerially dispersed spores of the fungi are deposited
in these wounds, where subsequent colonization of wood tissue and development
of wood decay in living heartwood occur. These infections result in
death of branches above the infection site.
Figure 9. A broken branch
in lemon caused by infection by a wood decay fungus Coniophora. (Yuma,
Symptoms: The first obvious symptom is death of a lemon
tree branch. These branches are often partially broken from the tree.
The fractured infected wood is light brown in color. No evidence of
fungal growth is observed on wood infected with Coniophora, whereas
white fungal mycelium can be observed within the brown decayed wood
infected with Antrodia. As the wood rot spreads, limbs continue
to break from the tree until all that remains is a decayed stump.
Biology of the pathogens: Antrodia and Coniophora both produce aerially dispersed spores. Coniophora has not
been found sporulating on infected lemon wood, so infected wood in lemon
plantings is not producing spores that could infect other lemon trees.
On the other hand, Antrodia has been observed sporulating on
lemon wood, so that additional infections could arise from spores produced
from decayed lemon wood.
Control: Broken or dying branches should be removed with
a flush, clean cut close to the main branch to minimize development
of wood rot at wound sites. If the wood rot decay is caused by Antrodia,
removal of wood debris will eliminate this potential source of spores
and minimize the threat of new infections. Maintaining tree vigor with
adequate irrigation and proper fertilization should promote wound healing
and minimize development of wood rot. No fungicides currently available
for use on citrus will control this disease.
Dry Root Rot
Dry root rot of citrus occurs sporadically, attacking trees that usually
are weakened by some other factor. The most susceptible rootstocks include
citranges, citrumelo, Citrus macrophylla, rough lemon and Cleopatra
mandarin. The general symptoms of dry root rot resemble those caused
by Phytophthora and other pathogens that damage roots or girdle
the trunk, such as reduced vigor, leaves dull green in color, restricted
new growth and twig dieback. If root damage is severe, leaves may suddenly
wilt and dry on the tree during summer and early autumn.
Symptoms: Examination of infected trees usually reveals
a dry decay of fibrous roots, larger roots and trunk at or below the
soil surface. The wood below the bark is not decayed but may be stained
a dark color. A soil-borne plant pathogenic fungus, Fusarium solani,
can be recovered from infected root tissue. Dry root rot may advance
and develop for years with a slight wilt under dry conditions being
the only symptom. However, once enough root tissue has been destroyed,
leaves on infected trees may suddenly wilt and turn yellow; at this
stage the tree may die with the leaves still attached. In addition to
direct destruction of root tissue, the symptoms of Fusarium dry root
rot are caused by inhibition of water transport in root tissue and production
of toxins by the pathogen.
Biology of the pathogen: Fusarium solani is a common
soil and root-inhabiting fungus which is associated with the roots,
stem and bark of healthy as well as diseased citrus trees. The transformation
of the fungus into a pathogen is correlated with stress factors, such
as root damage caused by Phytophthora, over-watering, under-watering,
poor soil drainage, excess fertilizer, heat stress and root injury due
to plowing, herbicides or nematodes.
Control: Since stress factors like those listed above
can trigger disease development, prevention of these stress factors
can minimize the occurrence and severity of dry root rot. To date, control
of Fusarium dry root rot with fungicides has not been successful.
and Green Fruit Molds
Blue and green mold are common postharvest diseases of citrus. All
types of citrus fruit are susceptible to these two mold diseases.
Symptoms: The initial symptom of blue and green mold
is the appearance of a soft, watery and slightly discolored spot from
1/4 to 1/2 inch in diameter. This spot enlarges to 1 to 2 inches in
diameter after 1 to 1.5 days at 75EF. White mycelium appears on the
surface, and when the growing fungus is about 1 inch in diameter, blue
or olive green spores are produced. The entire fruit surface is rapidly
covered with the blue or olive green spores, which are easily spread
if the fruit is handled or exposed to air currents.
Biology of the pathogens: The fungus that causes blue
mold is Penicillium italicum, whereas the pathogen causing green
mold is Penicillium digitatum. Spores of the fungi are produced
in chains in massive quantities on infected fruit. The fungi survive
in the orchard as spores. Infection occurs by airborne spores entering
the fruit rind through injuries. The infection and sporulation cycle
can occur many times during the season in the packinghouse. Blue and
green mold develop most rapidly at around 75EF; on the other hand, rot
is virtually stopped at a temperature of 34EF.
Control: Careful picking, handling, packing and storage
of fruit minimizes injuries to the fruit rind and the risk of blue or
green mold development. Sanitary packinghouse practices, including the
use of disinfectants such as chlorine or other materials, help reduce
the concentration of fungal spores capable of causing infection. Post-harvest
application of selected fungicides can help delay the development of
blue and green mold, especially in combination with immediate cooling
of fruit after packing.
Alternaria fruit rot, also called Black rot, is a fungal disease
caused by Alternaria alternata. The disease occurs occasionally
in lemons and navel oranges in Arizona. It was first described in the
late 1890s from California. The fungus occurs throughout the citrus
growing areas of the world. Alternaria attacks only citrus fruit.
Alternaria rot is primarily a problem in storage, but it sometimes
occurs in the orchard where it can cause premature fruit drop. In other
parts of the world the disease has been reported on citrus fruit other
than navels and lemons. Alternaria fruit rot is most important
in areas where citrus is processed for juice because of juice contamination
by masses of black fungal mycelium found in the interior of the infected
Figure 10. Tear stain,
caused by drops of water carrying spores of Alternaria alternata. (Phoenix,
Symptoms: Fruit infected with Altrnaria may turn
light in color several weeks before the color break in healthy fruits.
Some infected fruit may prematurely drop while others may remain on
Infected fruit may appear normal. The simple method of diagnosis is
to cut the fruit in half, exposing the stylar or "blossom" end and the
central cavity. Diseased fruit have a brown to blackish discoloration
at the "blossom" end. The discoloration and decay may be restricted
to the "blossom" end or it may extend deep into the central cavity.
Observations of infected tissue in the laboratory reveals the presence
of Alternaria. Fungal spores are unique in appearance. There
may be little or no external evidence of infection. In lemons the disease
is most common during storage. In Arizona, splitting, caused by environmental
factors, often predispose navel oranges to infection by Alternaria.
Large navel fruit may split and drop in the fall during hot, dry weather.
The incidence of splitting is higher in sunburned fruit, and in trees
stressed by drought and frost injury.
Figure 11. A mummy-like,
black fruit infected by a wood decay fungus, Coniophora. (Yuma, AZ)
Biology: Alternaria alternata is an active saprophyte.
The fungus grows on dead citrus tissue during wet weather. Airborne
conidia are produced during these periods. These spores germinate and
the fungus establishes itself in the button or stylar end of the fruit.
Entrance into the fruit is facilitated when splits or growth cracks
occur. The fungus grows into the central core of the fruit and causes
a black decay. Alternaria produces large numbers of conidia in
infected fruit. The fruit may dry and become black and mummy-like in
appearance. This fruit becomes one of the survival mechanisms for the
Control: Proper fertilization and irrigation will reduce
the incidence of this disease. There are no chemicals that are presently
recommended for control.
Rio Grande Gummosis
This name has been given to a gumming disease of mature citrus, particularly
grapefruit, thought to be caused by several fungi, but no particular
pathogen has been identified.
Symptoms: Symptoms begin as narrow cracks in the bark
of limbs and trunk in which a yellow, water soluble exudate accumulates.
Gum formation on the trunk or branches and gum exudation from blisters
on the trunk continues and forms gum pockets under the bark. The advancing
margin of infection is orange to pink. Once sapwood is exposed, wood
decay may begin. In later stages of disease, heart rot may also be prevalent.
Control: Several factors have been identified as contributing
to disease including freeze damage, poor drainage, and salt accumulation.
Weakened and injured trees seem to be predisposed the disease. There
is no control other than cultural practices that keep trees in vigorous
condition. Good pruning practices that remove freeze damaged wood and
encourage fast healing are the best way to prevent disease.
Citrus Tristeza Virus
Introduction: Citrus Tristeza Virus (CTV) is one of the
most destructive of the many viruses that affect citrus. The virus pathogen
has been responsible for the death and debilitation of millions of citrus
trees in Argentina, Brazil, South Africa, and other areas. Observations
in the late 1800s and early 1900s of declining sweet orange trees on
sour orange rootstocks led scientists to conclude that tree failure
was due to an incompatibility between certain scion varieties and sour
orange roots. In 1946, American and Brazilian plant pathologists reported
that tree failure was caused by a virus disease. The Brazilians demonstrated
that an aphid, Toxoptera citricidus, was a vector of the virus.
The Brazilians named the disease "tristeza," a Portuguese word meaning
sadness, an appropriate name for a virus disease that had killed 18
million trees in Argentina and 10 million trees in Brazil. The virus
was identified in California in the late 1940s. Severe losses occurred
in Southern California in a number of citrus varieties that were budded
to sour orange rootstocks. Studies in California demonstrated the existence
of several variants or strains of CTV. These strains varied in severity,
vector specificity, and host range. It was proven that several distinct
diseases (Tristeza, Stem-pitting, Seeding-yellows, and Lime dieback)
were caused by strains of CTV. In Arizona, CTV was first identified
in 1956 in Meyer lemon. Later surveys discovered the virus in mature
trees of Clementine mandarin, Dancy tangerine, and Marsh white grapefruit
at both the Yuma and Tempe University of Arizona Citrus Experiment Stations.
Figure 12. Advanced symptoms
caused by the Citrus Tristeza virus in sweet orange on sour orange rootstock.
Symptoms: Symptoms of CTV in citrus are extremely variable
and depend on the isolate of the virus, host, environment, and scion/rootstock
relationships. Common symptoms include reduced fruit size, leaf vein-clearing,
yellowing and cupping of leaves, and stem pitting. Infection of sweet
orange, mandarin, or grapefruit trees on sour orange rootstock causes
necrosis in the phloem of the sour orange rootstock just below the bud
union. This girdling causes eventual decline and death of the infected
Present Situation in Arizona: To understand the present
situation of CTV in Arizona, it is necessary to discuss certain biological
properties of this virus. CTV is not transmissible by seed or mechanical
means. The virus is disseminated only in infected bud wood, planting
material and by several species of aphids. The most efficient vector,
Toxoptera citricidus (the tropical citrus aphid) does not occur
in North America. This species, prevalent in South America, played a
key role in the early epidemics of CTV. The cotton aphid, Aphis gossypii,
is a vector of certain strains of CTV in California, but not in Arizona.
There is no evidence that aphids are involved in the spread of CTV in
Arizona. The introduction of T. citricidus into Arizona or California,
however, would present a peril to trees on sour orange rootstock. CTV
has not been detected in citrus grown in the Salt River Valley of Central
Arizona even though citrus in this area is grown predominately on sour
orange rootstock. All citrus trees in the certification program have
been recently tested for the presence of CTV by use of an ELISA serological
test. The results were 100 percent negative on mother block trees at
the Yuma station. The fact that CTV is not presently a factor in commercial
or back yard plantings of citrus on sour orange roots is due to a number
of factors: the Arizona Citrus Certification Program, initiated over
25 years ago, has been effective in preventing the introduction of diseased
bud wood and planting material into Arizona; the cotton aphid (A.
gossypii), which occasionally feeds on citrus in Arizona, apparently
does not transmit the strains of CTV that occur in Arizona; old line
citrus varieties carrying the virus have been eradicated; and quarantine
regulations on imported citrus have been effective.
Virus or Virus-like Diseases
Psorosis is an occasional problem in old citrus plantings in Arizona.
The disease, which occurs primarily in orange and grapefruit trees,
is characterized primarily by the scaling and flaking of the bark on
the scion cultivar. Because of these symptoms, the disease is sometimes
referred to as scaly bark. Symptoms do not occur until the tree is usually
over ten years in age. First symptoms of scaly bark consist of small
flecks of gum on the trunk and main branches. These areas become dry
and scaly. As they enlarge, the tree becomes stressed and less productive.
Twig and limb death may occur.
Causal agent: The cause of bark scaling in citrus has
frustrated plant pathologists since symptoms were first observed in
Florida and California in the late 1890s. Initially, in the 1930s, bark
scaling in citrus was named Psorosis. In the late 1970s, a number of
graft-transmittable diseases that caused bark scaling were lumped together
and referred to as Psorosis. They included Psorosis A, Psorosis B, citrus
ringspot, concave gum, cristacortis, and impietratura. The causal agent
of these diseases was listed as virus or virus-like. The first of these
diseases to be identified as caused by a virus was the citrus ringspot
disease. The causal virus was named the Citrus Ringspot Virus (CRV).
In the 1990s plant pathologists from Argentina, South Africa, Spain,
and the U.S. identified a virus, Citrus-psorosis-associated Virus (CPsAV)
as a probable cause of certain strains of Psorosis. All of the Psorosis
diseases, including the two caused by viruses, are disseminated only
by infected bud wood. No vectors of these diseases have been identified.
The strains of Psorosis that occur in Arizona have not been studied.
Control: These diseases have been controlled by eradication
and effective citrus certification programs in Arizona and California.
The disease is not common in Arizona.
Stubborn disease is a major disease of citrus in North Africa and in
the middle-eastern and Mediterranean citrus areas including Israel,
Egypt, and Turkey. In North America the disease is known to occur only
in the hot, dry citrus areas of Arizona and California. For unknown
reasons, the disease has not been found in citrus in Florida or Texas.
Prior to the 1970s, it was thought the disease was caused by a virus.
In the early 1970s, however, research in several areas determined the
disease was caused by a unique mycoplasma-like organism that was named
Spiroplasma citri. Presently, Stubborn is an important disease
in Arizona and California. In Arizona, Stubborn disease is especially
prevalent in Washington Navel trees but may occur in Valencias, Sweets,
Figure 13. Symptoms of
Stubborn disease in citrus fruit. Note the small malformed fruit (right)
taken from a diseased tree in coparision with a healthy fruit (left).
Symptoms: The disease may appear at any time during the
life of the tree, and severity and symptoms vary from year to year.
Symptoms consist of stunted growth; misshapen, flat-topped trees; proliferation
of shoot development resulting in witches'-brooms; twig die-back; small,
stiff, upright foliage showing marked Zn or Mn deficiency-like symptoms;
occasional diffuse yellow and green mottling of leaves; small leaves
sharply pointed, cupped, and having marginal chlorosis; fruit malformed,
"acorn shaped" with rind thick at stem end and thin at stylar end; many
aborted seeds found in seedy varieties; progressively decreasing yields
of small fruits having insipid flavor; "off-season" bloom. In some instances,
only part of the tree shows these described symptoms. Stubborn disease
does not normally cause death in citrus. Stunting is most common in
trees that are infected when young. Symptoms are accentuated during
Field diagnosis of Stubborn is difficult because many of the variable
symptoms caused by stubborn may also be the result of freezing damage,
insect infestations, wind, and improper irrigation or nutritional factors.
Several laboratory tests are currently available for diagnosis. They
include serological techniques (including ELISA) and indexing.
Situation in Arizona: The causal organism of Stubborn,
Spiroplasma citri, has been isolated from ten different cultivars
of citrus in Arizona. Some naturally infected plants other than citrus
include: wild turnip, Brassica sp; London rocket, Sisymbrium
irio; Zinnia sp.; Marigold, Tagetes spp.; Viola
sp.; periwinkle, Vinca rosa; onion, Allium cepa; squash,
Cucurbita pepo; plantago and Malva sp. Two leafhoppers,
Circulifer tenellus and Scaphytopius nitridus are vectors
of the disease in the southwestern United States. Recent studies demonstrated
that Spiroplasma citri reproduces in the sugarbeet leafhopper
C. tenellus. The cells of Spiroplasma citri are injected into
plants via salivary secretion during leafhopper feeding.
Figure 14. A photomicrograph showing typical filamentous growth in Spiroplasm citri on a laboratory medium.
Causal agent: Spiroplasma citri is one of the few mycoplasma-like
organisms that can be grown in laboratory media. The cells of the organism
are wall-free, filamentous, motile or spiral-shaped. The organism can
be cultured from infected tissue. Isolates from infected citrus in Arizona
have been obtained by passing the sap of leaves, bark, and seed through
small microbiological filters into specific media. Amazingly, S.
citri, which was though to be restricted to the southwestern United
States, was identified in the early 1980s as the cause of brittle root
of horseradish in Illinois and Maryland. This fact has prompted a reevaluation
of the potential threat of this organism to non-citrus crops in areas
far removed from the southwestern United States.
Control: Nursery trees should be propagated from Stubborn-free
budwood. Infected trees should be removed from the orchard and replaced
with healthy replants.
The Citrus Nematode
More than 40 nematode species have been described worldwide on citrus.
In Arizona, however, only one species, the citrus nematode, Tylenchulus
semipenetrans, is important and damaging. This nematode has become
of increasing importance since the withdrawal of the soil fumigant,
DBCP, which was previously used as a post plant fumigant for control.
The citrus nematode was first found infecting citrus in California in
1912. The nematode was described from Arizona in 1926. Today, the citrus
nematode has been reported in all citrus producing regions of the world.
Surveys made in the United States indicate that infestations of citrus
areas range from approximately 50 to 60 percent in California and Florida
to 90 percent in Texas and Arizona.
Symptoms: Symptom development depends on overall tree
vigor. Infected trees growing under optimum conditions may appear healthy
for many years. For this reason, the disease is often referred to as
"slow-decline." Heavily infected root systems eventually cause a reduction
in yield and quality of fruit. Trees in early stages of decline, however,
may have relatively vigorous root systems. Above ground symptoms of
nematode damage are non-specific. Root feeding and subsequent damage
reduces the overall vigor of infected trees. Symptoms include leaf yellowing,
sparse foliage, small, non-uniform fruit, and defoliated upper branches.
Dieback is particularly noticeable in the upper portion of trees. Affected
trees appear similar to stress conditions caused by Phytophthora
root rot, poor nutrition, and inadequate irrigation. Tree decline,
which depends upon care of the grove and overall tree vigor, may not
occur for three to five years after heavy infection. Infected roots
may appear coarse and dirty. Female nematodes are found in small groups
on the root surface. Soil adheres to the gelatinous matrix in which
eggs are embedded. Positive identification requires the extraction of
the nematodes from soil samples taken in the feeder root zone between
the trunk and the drip line of the tree. The nematodes may also be identified
microscopically on infected roots in the laboratory.
Biology: The citrus nematode, an obligate parasite, reproduces
only on living roots of host plants. Early researchers in Arizona proved
that populations of nematodes in roots were highest in the early stages
of tree decline and lowest in roots of declining trees. They found that
nematode populations and root systems were almost in equilibrium. Low
nematode populations in dead or dying root systems allowed new root
development. New root development resulted in increased nematode populations.
This repeating cycle, however, eventually resulted in tree decline.
Four races or biotypes of the citrus nematode have been described worldwide.
A "citrus" biotype has been described from populations of the nematode
from Arizona. This biotype reproduces on Citrus spp. and on the
hybrids "Carrizo" and "Troyer" citrange as well as on grape, olive,
Control: No chemicals are presently recommended for post-plant
control of the citrus nematode.
In general, citrus trees do not have to be fertilized heavily, but
regular applications of nitrogen in one form or another are needed.
Usually nitrogen is the only major nutrient required. Potassium and
phosphorous generally are adequate in central Arizona soils, but all
soils require nitrogen. On the Yuma Mesa, citrus has responded to phosphate
Nitrogen deficiency, showing up as yellow-green leaves, normally develops
over a period of two or four years on unfertilized trees but can be
quickly corrected with proper fertilization.
Pale green leaves are normal in two situations. A heavy drop of old
leaves normally occurs in March and April. Before leaf drop, nitrogen
is removed from these leaves and migrates to new leaves, leaving old
leaves pale green. Leaves on shoots produced on grapefruit during the
summer and fall normally turn yellow in the winter, but regain their
green color in the spring.
In southern Arizona, a mature grapefruit tree in good, healthy condition
will need an annual application of one pound of actual nitrogen each
year. Oranges and other mature citrus will require two pounds. Apply
half of this in February and the remainder as a split application in
May/August. Manure may be applied periodically in the fall, but should
be supplemented with commercial fertilizer in the spring.
On the sandy Yuma Mesa soils, an annual application of two to three
pounds of actual nitrogen is needed for mature trees.
Nitrogen can be supplied to the soil in the form of animal manures,
commercially prepared chemical fertilizers or a combination of the two.
Commercial fertilizers are generally preferred because research indicates
that excessive use of animal manure may induce iron chlorosis in citrus
and increase salts.
Micronutrient deficiencies: The most common micronutrients
that are deficient for normal citrus growth in Arizona are iron, zinc,
and manganese. These elements are normally not needed before trees are
three to five years old. Diagnosis of specific micronutrient deficiencies
is dependant on the location of the symptoms on the tree, the pattern
of leaf discoloration, and tissue analysis.
Iron: Iron chlorosis (yellow-white leaves with green
veins) is common in Arizona because iron is less available for root
uptake in our alkaline soils. Symptoms normally appear on young, rapidly
growing leaves. Mild symptoms may disappear with aging of leaves. The
entire young leaf appears yellow-green with exception of the tissue
surrounding leaf veins which remain green.
Leaves may turn almost white with green tissue remaining only around
the leaf veins. Lime induced iron chlorosis is a common nonparasitic
disease in many plants grown in Arizona, including citrus. The disease
is more common in home plantings than in commercial groves because ornamentals
and lawns are often planted near citrus in back yard plantings. These
nearby plants need frequent irrigation. Iron chlorosis in citrus is
exacerbated by overwatering. Shallow-rooted ornamentals that require
frequent watering should not be planted in tree basins. Grapefruit trees
normally turn yellow during the winter months but re-green as new leaves
appear in the spring. Do not apply iron to correct this "winter chlorosis"
To correct iron chlorosis chemically, treat trees with iron sulfate
or an iron chelate compound. Place iron sulfate in a shallow circular
trench around the tree trunk or broadcast it around the entire tree
basin from the trunk to outside the drip line, and apply four to six
inches of water. An average-size tree requires 20 to 30 pounds of iron
sulfate. When using iron chelate, apply according to label directions
to the tree basin area and irrigate thoroughly.
Trees do not respond to chelate applications in winter but will respond
well from April through September.
Zinc: Zinc is a common deficiency in Arizona. The symptoms
appear, as with iron deficiency, on recently expanded, young leaves.
A "mottle-leaf" pattern occurs in leaf tissue. Yellowing develops in
areas between the leaf veins. Severe deficiency causes small leaves
and short internodes. Defoliation and dieback may occur in stressed
trees. Zinc deficiency is more of a problem on sandy soils or where
manure has been frequently applied. Optimum leaf concentration is 25-100
ppm (parts per million) Zinc. Deficiencies may be corrected by foliar
or soil applications of zinc salts or zinc chelates.
Manganese: Deficiency symptoms also occur on young leaves.
Symptoms overlap with those of iron deficiency. If leaf tissue concentration
of manganese is below 25 ppm a foliar application of manganese sulfate
may be helpful. Soil applications of manganese sulfate in our alkaline
soils are less effective than foliar applications.
Water stress: Water use in citrus is highest during June,
July, and August and lowest from November through March. In central
Arizona research on water consumption in mature citrus indicates that
daily moisture use is less than 0.1 inch per day from November through
March but increases to a peak of 0.23 inches per day in July. It was
also determined in these studies that approximately 85 percent of the
water used in mature navel oranges in central Arizona was from the upper
three feet of the soil profile. Thus, water loss from the soil under
a large mature tree 16 to 20 feet tall is about six inches in July and
one inch in January. Average sandy-loam soils that hold about four inches
of water require irrigation at about 20-day intervals in July. Coarser
soils (sandy) require more frequent irrigation. Time each irrigation
by the condition of the tree or trees rather than by the calendar. A
slight wilting of leaves indicates that a tree does not have enough
water and irrigation is needed. New leaves show the first sign of water
Symptoms of inadequate soil moisture depend on the period of stress.
Early symptoms consist of leaf rolling. Long droughts may cause defoliation
and dieback. In Arizona, hot dry winds may accentuate moisture stress
and cause leaves to dry up on the tree. In young leaves, chlorosis may
occur on the leaf blade between the midrib and the leaf margins. These
chlorotic (yellowish) areas may later turn gray to light brown. This
condition is referred to as "mesophyll collapse." Damage to surface
roots by disking or ploughing during water stress situations may accentuate
this symptom. High daytime temperatures and dry winds may cause heavy
leaf drying in October and November. Grapefruit trees seem most susceptible
to this type of injury. In severe cases, small twigs may crack, gum
and die. Adequate water during these hot windy periods is the only practical
method of reducing injury.
Figure 15. Frost damage in lemon. (Yuma, AZ)
Freezing damage: Freezing can damage both tree and fruit
of all citrus varieties, but some are more sensitive than others. Limes
and lemons are the most tender, oranges, and grapefruit are of intermediate
hardiness, and mandarins are the most hardy. Older orange and grapefruit
trees are quite tolerant to cold, and seldom need to be protected. The
fruit is usually damaged when temperatures fall below 26 ° F for
a period of several hours.
In the desert areas of Arizona, nighttime temperatures can drop below
freezing from mid-November to late March, most often in January. In
most areas of southern Arizona where citrus is grown, some type of frost
protection is necessary from November through March during the first
two or three years. Palm fronds give effective protection, but corn
stalks also work well. Protect the trunk and main branches of young
trees, leaving one-third of the leafy area exposed to sunlight and air,
by placing and tying four to six fronds or 12 to 15 corn or sorghum
stalks around the tree.
Young trees can be successfully protected from frost by running water
under the tree during below-freezing hours, covering them with a large
cardboard box, placing a burlap bag over the tree, or covering with
cloth. Do not use plastic unless you build a frame to keep the plastic
away from tree foliage. Plastic does not hold in much heat compared
to other materials. Remove heavy cloth coverings after each frost period.
Burlap may be left in place for the entire winter. Hanging a light bulb
in the branches on cold nights provides additional heat.
If a tree is frozen, do not prune frozen parts until new growth emerges
in spring. After new growth begins, the exact portions killed by frost
can be more clearly seen and pruned off.
Figure 16. Sunburn damage on citrus fruit. (Phoenix, AZ)
Sunburn: Temperatures above 110 ° F usually burn
some leaves and fruit and may damage any exposed bark on young or old
trees. Protect any exposed bark areas with tree wraps or white, water-base
When lower branches or tops of old trees have been pruned, exposed
bark usually is sunburned and may be killed. Fungus infection may follow
and destroy larger areas. Such trees must be protected by painting trunks
and scaffold limbs with whitewash or any white, water-base paint. Heavy
paper tree protectors or cardboard should be applied to young trees
Leaf and Fruit Drop: Two conditions, leaf drop and fruit
drop, are poorly understood problems in citrus. Leaf drop appears to
be a normal phenomenon. Citrus, an evergreen tree, sheds leaves gradually
throughout the year. Replacement of leaves occurs naturally. Leaf drop
is heaviest during the spring months but occurs to some extent all year.
Fruit drop may also be a normal physiological event.
Only a small percentage of the blossoms on a tree develop into fruit.
Although most of these drop soon after petal fall, some fruit will drop
in later May and June.
In most years, this June drop allows crop thinning. If it did not happen,
the tree would break down under the load and fruit would be small and
The amount of June drop depends on variety. Seedless oranges have greater
drop than ones with many seeds; tangerines with many seeds have a small
amount of drop. Cross-pollination of Tangelo and Tangerine varieties
causes many more seeds to develop and thus reduces the drop.
With Valencia oranges and grapefruit, a heavy crop of mature fruit
reduces the food supply to the young fruit and this increases the drop.
In some years, high temperatures in May help induce heavy drop. Maintaining
an even watering schedule and adequate nutrient level for tree use will
minimize small fruit drop in most varieties.
Toxicity of salts: Salinity is measured and reported
in terms of EC (electrical conductivity) of a soil-saturation extract
(ECe) or water (ECw). Citrus is moderately salt tolerant provided that
levels of boron or lithium are not toxic.
The units of ECe measurement are mhos per centimeter (mhos/cm). A soil
analysis report will usually contain a column for ECe x 103, the electrical
conductivity of a saturation extract of the soil multiplied by 1000
and reported as mmhos/cm. The soil sample should be taken in the root
zone. Water analysis will report ECw x 103. It is interesting to compare
the sensitivity of citrus to some of the major crops grown in Arizona.
Citrus is sensitive to soil salinity at ECe values in excess of 1.8.
This sensitivity is similar to other crops grown in Arizona such as
potatoes, corn, peppers, lettuce, grapes, almonds, and plums.
The threshold for salt damage in citrus is an ECe of 1.8 (approximately
1152 ppm total salts). At ECe 3.0 (approximately 1920 ppm salts) there
is approximately a 20 percent reduction in yield. Symptoms of salt injury
consist of irregular brown necrotic (dead) areas along the leaf margins
and near the leaf tip. Defoliation, dieback, and fruit drop and yield
reductions occur in acute cases. Excessive fertilization may cause these
symptoms. Heavy irrigation may reduce salt concentrations. Most commonly
these problems occur in backyard situations where frequent, light irrigations
and soil water evaporation move salts into the upper root zone.
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Document located http://ag.arizona.edu/pubs/diseases/az1154/
Publication revised April 2000
Publication adapted by Mary Olsen, Plant Pathology
Mike Matheron, Research Scientist, Plant Pathology,
Mike McClure, Professor, Plant Pathology,
Zhongguo Xiong, Associate Professor, Plant Pathology
Based on material originally written by Richard Hine, Plant Pathologist
(retired), Mike Matheron, and Lowell True, Agricultural Agent
Photographs by Richard Hine
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