Diseases of Citrus Fruit in Plant Pathology

1. Diseases of Citrus and their
management
Dr. ADITI SHARMA
Assistant Professor, Plant Pathology

2. Fungal Diseases
Disease Pathogen
Anthracnose = wither-tip
Glomerella cingulata
Colletotrichum gloeosporioides [anamorph]
Black mold rot Aspergillus niger
Black root rot Thielaviopsis basicola
Black rot Alternaria citri
Black spot
Guignardia citricarpa
Phyllosticta citricarpa [anamorph]
Blue mold Penicillium italicum
Botrytis blossom and twig blight,
gummosis
Botrytis cinerea
Brown rot (fruit) Phytophthora spp
Phytophthora foot rot, gummosis
and root rot
Phytophthora citrophthora
Phytophthora hibernalis
Phytophthora nicotianae var. parasitica
= Phytophthora parasitica
Phytophthora palmivora
Phytophthora syringae

3. Fungal Diseases
Disease Pathogen
Pink disease
Erythricium salmonicolor
= Corticium salmonicolor
Powdery mildew
Oidium tingitaninum
= Acrosporium tingitaninum
Rhizopus rot Rhizopus stolonifer
Scab
Elsinoë fawcettii
Sphaceloma fawcettii [anamorph]
Sclerotinia twig blight, fruit rot and
root rot
Sclerotinia sclerotiorum
Twig blight Rhytidhysteron rufulum
White root rot
Rosellinia sp.
Rosellinia necatrix
Dematophora necatrix [anamorph]
Rosellinia subiculata

4. Bacterial Diseases
Disease Pathogen
Bacterial spot Xanthomonas euvesicatoria pv. citrumelo
Black pit (fruit) Pseudomonas syringae
Blast Pseudomonas syringae
Citrus canker Xanthomonas citri pv. citri
Citrus variegated chlorosis Xylella fastidiosa
Huanglongbing = citrus greening
Candidatus Liberibacter asiaticus
Candidatus L. africanus
Viral Diseases
Tristeza = decline and stem pitting,
seedling yellows
genus Closterovirus, Citrus tristeza virus (CTV)
Psorosis Citrus psorosis virus (CPsV)
Citrus yellow mosaic genus Badnavirus
Crinkly leaf
Crinkly leaf virus (strain of Citrus variegation
virus)
Viroid Diseases
Exocortis Citrus exocortis viroid (CEVd) Pospiviroidae

5. Nematode Diseases
Disease Pathogen
Dagger nematode Xiphinema spp.
Lesion nematode
Pratylenchus spp.
Pratylenchus brachyurus
Pratylenchus coffeae
Pratylenchus vulnus
Needle nematode Longidorus spp.
Root-knot nematode Meloidogyne spp.
Phytoplasmal and Spiroplasmal Diseases
Stubborn Spiroplasma citri (spread by leafhoppers)
Witches’ broom of lime Phytoplasma

6. Gummosis- Phytophthora citrophthora, P. parasitica,
P.palmivora
Symptoms and Signs
• An early symptom of Phytophthora gummosis is sap oozing
from small cracks in the infected bark, giving the tree a
bleeding appearance.
• The gumming may be washed off during heavy rain. The
bark stays firm, dries and eventually cracks and sloughs
off.
• Lesions spread around the circumference of the trunk,
slowly girdling the tree.
• Decline may occur rapidly within a year, especially under
conditions favourable for disease development, or may
occur over several years.

7. Sap oozing from small cracks in the
infected bark
Bleeding appearance

8. Drying and eventually cracking on the Bark

9. Pathogen
Aseptate mycelia, zoospore are the asexual spores produced in the sporangium
where as oospores are sexual spores or resting/dormant spores borne in oogonium
PSI: Dormant mycelia and oospores present in infected debris and soil.
SSI: Zoospore spread through soil and irrigation water.
Kingdom:Chromista
Phylum:Oomycota
Order:Peronosporales
Family:Peronosporaceae
Genus:Phytophthora
Favorable conditions
Prolonged contact of trunk with water as in flood irrigation; water logged areas and
heavy soils.
Etiology

10. Disease cycle and epidemology
There are 3 stages
1) Asexual stage: Zoospores borne in sporangium
2) Sexual stage: Oospores borne in Oogonium
3) Vegetative stage: Mycelia with haustoria
 Oospores are sexual spores and also the resting spores present in infected debris for a longer
period (6-8 months). When conditions become favourable, these oospores germinate by
producing germ tube, and tip of the germ tube swells to form sporangium.
 Initially sporangium is a multinucleated structure in which each nucleus starts forming
zoospore wall. Once these zoospores mature, they start moving randomly, burst open the
sporangium wall and become air borne.
 Air borne zoospores move to a certain distance, then they loose their flagella and form a thin
circular structure which is the encystment of sporongium
 Haustoria are intercellular where as mycelia intracellular. Under advance conditions like
temperature rise and low humidity, the pathogen goes for the sexual reproduction, in which
male reproductive organ is the Antheridium and female reproductive organ is oogonium.
 Oogonium is circular in nature, eunucleated, sometimes 1 or 4 celled. Antheredium , is
tubular and multinucleated. Once the union of two gametangia takes place, it is followed by
Plasmogamy, karyogamy, mitosis and meiosis.
• Epidemiology
Cool weather, temperature 18-220C, 90-95% RH, high soil moisture, PH 6.0-7.0

12. Management
• Management focuses on preventing conditions favorable for infection
and disease development.
• Injuries to crown roots or base of stem during cultural operations
should be avoided.
• If lesion has girdled less than ½ the girth, remove the diseased bark
with a knife along with ½” of uninvaded bark.
• Budding onto sour orange (C. aurantium), is known to be highly
resistant to Phytophthora
• All scion cultivars are susceptible to infection under the right
environmental conditions.
• Preventive measures like selection of proper site with adequate
drainage, use of resistant rootstocks and avoiding contact of water
with the tree trunk by adopting ring method of irrigation are effective.
• Alternatively the disease portions are scraped-out with a sharp knife
and the cut surface is disinfected with Mercuric chloride (0.1%) or
Potassium permanganate solution (1%) using a swab of cotton.
Cultural Control
• Plant trees high enough so that the first lateral roots are just covered
with soil.
• Correcting any soil or water problems is essential for a recovery.

13. • Remove the dark, diseased bark and a buffer strip of healthy, light
brown to greenish bark around the margins of the infection.
• Allow the exposed area to dry out. Scrape the diseased bark lightly to
find the perimeter of the lesion and then use a propane torch to burn
the lesion and a margin of 1 inch (2.5 cm) around it. Recheck
frequently for a few months and repeat if necessary.
• Late stages of Phytophthora gummosis are distinct, but early
symptoms are often difficult to recognize. Yet early detection and
prompt management actions are essential for saving a tree.
• If 50% or more of a trunk or crown region on a mature tree is girdled,
it may be more economical to replace the tree than to try to control the
infection.
• Painting 1 m of the stem above the ground level with Bordeaux helps
in controlling the disease. Also spraying and drenching with a combi-
fungicide such as Metalaxyl (8%) + Mancozeb (64%) @ 2.75 g/l or
Fosetyl -Al 80% WP (2.5 g/l) is effective in controlling the disease.
• Bordeaux paste 1.0 percent amended with mustard oil was most
effective.

14. Scab/Verucosis : Elsinoe fawcetti
• Anamorph: Sphaceloma fawcettii Jenk.
Citrus scab is only a serious problem on some varieties.
It is severe on rootstock seedlings of rough lemon, sour orange, Rangpur lime, and Carrizo
citrange, and scions of Murcott tangor, Temple tangor, and other tangerine hybrids.
Grapefruit, sweet oranges and acid lime highly resistant.
Symptoms
Attacks leaves, twigs and fruits of mandarin.
On the leaves the disease starts as small pale orange coloured spots.
The leaf tissue is distorted to firm hollow conical growths with the lesion at the apex.
The crest of these growth becomes covered with scabby corky tissue colour at first but
later becomes dark olive with age.
Lesions most common on undersurface of leaf. They penetrate leaf and are later visible on
both sides.
Infected areas run together and cover large area.
Leaves wrinkled, distorted and stunted.
On twigs similar lesions are produced.
They form corky outgrowths. On fruits irregular scaby spots or caked masses produced.
Cream colour in young fruits; dark olive grey in old fruits.
Fruits attacked when young become misshapen with prominent warty projections. They
drop prematurely.

15. Close-up of scabby areas at the tip of conical
formations on leaf

16. Common citrus scab on sour orange
leaf. Note the scabby areas at the tip
of the conical formations.
Symptoms on leaf

17. • Kingdom:Fungi
• Division:Ascomycota
• Class:Dothideomycetes
• Order:Myriangiales
• Family:Elsinoaceae
• Genus:Elsinoë
Elsinoe fawcetti

19. Epidemiology:
 Severe in rainy seasons
 Conidia are produced on the surface of scab pustules.
 These spores spread to new susceptible tissue.
 There are two kinds of spores, clear oval shaped and colored
spindle shaped (found in Florida and Brazil).
 The clear oval shaped type are spread by splashing rain and
perish as soon as they dry, while the spindle-shaped form
remain viable for a short time and are dispersed by wind for
short distances.
Management
 The diseased leaves, twigs and fruits should be collected and
destroyed.
 Spraying of Bordeaux mixture or Blitox (0.3%) is quite effective
 Spray Carbendazim 0.1%

20. Powdery mildew: Acrisporium tingitanium, Oidium citri and O.
tingitaninum
• Fungal disease that causes leaf and shoot distortion, premature leaf
and fruit drop, and twig and branch dieback.
• Severe infection can significantly reduce tree productivity, fruit
quality and yield.
• The disease can also be a major problem in citrus nurseries.
• It has been reported to cause serious damage to mandarins,
particularly nursery stock, in Asia.
• The disease is common in parts of Asia where it is prevalent in
shady, poorly ventilated orchards.
• There have also been reports from Uganda, Israel, Central and South
America and the United States (California).
• All citrus cultivars can be affected, though some cultivars appear
more susceptible than others.
• In India, the citrus varieties that are most susceptible are mandarins,
sweet oranges and tangerines.

21. Symptoms
Whitish powdery growth appears on young
leaves & twigs. In infected leaves get distorted
and defoliated in severe conditions.
Infected twigs exhibit characteristic die back
symptom.
Young fruits are also covered by whitish
powdery mass of the fungus and drop
prematurely resulting in poor yield.

22. Early symptoms of citrus powdery
mildew on leaves
Symptoms of powdery mildew on leaves
Young citrus fruit covered with
powdery spores

23. • Kingdom:Fungi
• Division:Ascomycota
• Class:Leotiomycetes
• Order:Erysiphales
• Family:Erysiphaceae
• Genus:Oidium
• Species:O. tingitaninum

24. Etiology and Spread
 Comparatively cool and moist fields are prone to
disease development.
 Damp mornings with only few hours of sunshine
favours onset of the disease.
 The fungus is an ectoparasite and absorbs food
material from the epidermal cells of leaf through
haustoria.
 It is a wind- borne disease. Septate mycelia, barrel
shaped conidia borne in chains, ectophytic, sub
epiderml haustoria, external mycelia.
 PSI: Dormant mycelia.
 SSI: Air borne barrel shaped conidia.

25. Life cycle
 Dormant mycelia present in the infected parts
germinate and produce oidia during congenial
conditions.
 On maturity, barrel shaped conidia are released, which
are air borne and find a host.
 Infection takes through sub- epidermal haustoria and
plant starts producing powdery growth comprising of
oidea.
 Oidia is an asexual fruiting body of the powdery
mildew and barrel shaped conidia are borne in chains
on oidiophores.
 They release and land on their respective host through
air.
 Infection process continues asexually

26. Control :
 Powdery mildew can be controlled easily by spraying
Wettable Sulphur (1.5kg/200 litres of water).
 Sulphur dusting (20kg/hectare) in the morning hours
controls the disease effectively.
 Systemic fungicides like Bayleton (1g/litre of water) or
Calaxin (3-4 ml/10 litres of water) or Benomyl (5g/10 litres
of water) offer better and prolonged control of the disease.

27. Citrus Canker: Xanthomonas axonopodis pv. citri
• Citrus canker is a serious bacterial disease of commercial
varieties of citrus, and relatives.
• The disease affects the leaves, twigs and fruit causing the
leaves to drop and fruit to fall to the ground before it
ripens.
• Citrus canker has resulted in heavy economic losses to
citrus industries across the globe, due to damage to trees,
reduced fruit production and access to export markets and
increased cost of management.
• Outbreaks of this disease have previously been eradicated
from Queensland and the Northern Territory of Australia at
great cost to industry and growers. The last detection was
in Emerald in May 2005 and Australia was declared free of
citrus canker in 2009

28.  Xanthomonas citri subsp. citri causes warty, rust-brown spots (cankers) that
form on the leaves, twigs and shoots.
 The cankers on leaves are rough to touch on both upper and lower surfaces
and are surrounded by a distinctive bright yellow halo.
 Scabby cankers also appear on the fruit.
 Citrus canker is most severe in hot, wet areas. Strong winds and rain help it to
spread from tree to tree.
 The canker lesions ooze bacterium when wet and these can be spread by rain
splash or overhead irrigation systems over short distances.
 Citrus canker can spread quickly over long distances on infected citrus fruits
and leaves, people and equipment.
 Crusty, tan spots on citrus leaves, fruit or twigs, leaf spots with a yellow halo.

29. Hamlin' orange leaf with watersoaking
symptom surrounding canker lesions.
Canker lesions on
pummelo leaf
Canker lesions on ‘Valencia’ orange showing
chlorotic halo

30. Canker induced defoliation
Citrus canker is mostly a leaf-spotting and fruit rind-blemishing
disease, but when conditions are highly favorable for infection,
infections cause defoliation, shoot dieback, and fruit drop
Canker infected fruit, foliage, and
stems

31. Fruit and Stem Lesions:
 Citrus canker lesions on fruit and stems extend to 1 mm
in depth, and are superficially similar to those on leaves.
 On fruit, the lesions can vary in size because the rind is
susceptible for a longer time than for leaves and more than
one infection cycle can occur.
 Infection of fruit may cause premature fruit drop but if the
fruit remain on the tree until maturity such fruit have
reduced fresh fruit marketability.
 Usually the internal quality of fruit is not affected, but
occasionally individual lesions penetrate the rind deeply
enough to expose the interior of the fruit to secondary
infection by decay organisms.
 On stems, lesions can remain viable for several seasons.
 Thus, stem lesions can support long-term survival of the
bacteria

32. • Pathogen: The bacterium Xanthomonas axonopodis pv. citri is a rod-
shaped, gram-negative, and has a single polar flagellum. Colonies on
laboratory media are usually yellow due to ‘xanthomonadin’ pigment
production.
• When glucose or other sugars are added to the culture medium,
colonies become very mucoid due to the production of an
exopolysaccharide slime.
• A semi-selective medium can be prepared by adding an antibiotic,
kasugamycin, which inhibits many contaminants but not
xanthomonads.
• The maximum and optimum temperature ranges for growth are to
39°C (95 to 102°F) and 28 to 30°C (82 to 86°F), respectively.
Xanthomonas axonopodis pv. citri colony on nutrient agar
showing yellow xanthomonadin pigment production and general
mucoid appearance

33.  Canker-infected leaves and twigs serve as the source of
inoculum to spread the disease from season to season.
 However, the cankered leaves drop early and bacteria perish
rapidly in the soil.
 Primary source of inoculum: infected plant and soil
 Secondary source of inoculum: Bacterial cells spread through
Irrigation water, agricultural implements, pruning shears etc.
Epidemiology
Prevalence of 20°-35°C temperature, high humidity
and the presence of moisture on the host surface
favour the disease.
Etiology

34. Life cycle
The bacterium enters the host
through stomata or wounds.
It multiplies in the intercellular
space, dissolves the middle lamella
and get established in the cortex
region.
Canker pustules develop an exude
bacteria in the form of gummy
substance.
They are freely disseminated,
chiefly by wind.
Citrus leaf-minor helps
dissemination and infection of citrus
canker.
Leaves affected by minor
and canker get distorted and drop
early.
The injury in the leaf epidermis
made by the burrowings of leaf-
minor serve as an easy opening to
the canker bacterium and
the canker lesions appear through
out the leaf in zig zag manner.

35. Management
 Quarantine: If area is disease free, restrict the entry of planting
material from infected to healthy area.
 Eradication: Once introduced into an area, elimination of inoculum
by removal and destruction of infected and exposed trees is the most
accepted form of eradication.
 Cultural: Infected leaves, stem, fruit etc should be removed and
burnt. Bordeaux paste should be applied at the cut end portions of
stem.
 Hot water treatment of root stocks at 50°C for 10-15 minutes.
 Biological: Pseudomonas fluorescens suspension can be sprayed as
biological control agent.
 Chemicals:1% Bordeaux mixture or
 0.3%Copper Oxychloride or 500 ppm Streptocycline should be
sprayed on the plant.

36. Citrus Tristeza Virus
Common Name: Citrus quick decline virus, grapefruit stem pitting; tristeza
Scientific Name: Citrus tristeza virus, Citrus tristeza closterovirus. The abbreviation is
CTV. The word "tristeza" is from Portuguese meaning "sadness”
Distribution : Worldwide. Africa, Asia, North, South and Central America, Caribbean, Europe,
Oceania. CTV is common in orchards in Southeast Asia, southern Africa, India, Japan, South
America, North America (Florida and California) and Oceania. It is recorded from Australia,
Cook Islands, Fiji, French Polynesia, Niue, Northern Mariana Islands, Papua New Guinea,
Samoa, Tonga, Wallis & Futuna.
Hosts : Citrus species and hybrids
Impact
• CTV is the most economically important disease of citrus worldwide, and responsible for
enormous losses.
• Damage is worse for sweet orange, mandarin and grapefruit when grafted on to sour orange
rootstocks.
• It is estimated that in Brazil and Argentina, 16 million citrus trees on sour orange rootstocks
were killed by CTV after the introduction of the citrus brown aphid that spreads the virus.
• Major epidemics have also occurred in Peru and Venezuela, as well as in California and
Florida.
• Citrus is commonly grafted onto sour orange, and there may be some 200 million trees still
vulnerable to CTV worldwide

37.  Citrus tristeza virus (CTV) is a phloem-limited virus whose natural host
range is restricted to citrus and related species.
 Although the virus has killed millions of trees, almost destroying whole
industries, and continually limits production in many citrus growing
areas, most isolates are mild or symptomless in most of their host range.
 There is little understanding of how the virus causes severe disease in
some citrus and none in others.
 Movement and distribution of CTV differs considerably from that of
well-studied viruses of herbaceous plants where movement occurs
largely through adjacent cells.
 In contrast, CTV systemically infects plants mainly by long-distance
movement with only limited cell-to-cell movement. The virus is
transported through sieve elements and occasionally enters an adjacent
companion or phloem parenchyma cell where virus replication occurs.
 In some plants this is followed by cell-to-cell movement into only a
small cluster of adjacent cells, while in others there is no cell-to-cell
movement.
 Different proportions of cells adjacent to sieve elements become infected
in different plant species.

38. Symptoms & Life Cycle
• CTV is spread by aphids; those that are most important are Toxoptera
citricida (brown citrus aphid), Toxoptera aurantii (black citrus aphid), Aphis
gossypii (cotton or melon aphid) and Aphis spiraecola (green citrus aphid).
• Among the four, the brown citrus aphid is the most efficient, as it can spread
strains that cause stem pitting that the others cannot.
• The aphids acquire the virus as they feed on the sap of infected plants; this
takes 30-60 minutes.
• The ability to transmit is lost within 24-48 hours.
• There are many strains; some show no symptoms, while others are
extremely serious and result in death. Symptoms are divided into three
types: (i) slow and quick decline; and (ii) stem pitting, and (iii) seedling
yellows:
• Decline (slow or quick) occurs when scions are budded onto sour orange
rootstocks and become infected with certain strains.
• CTV causes death of the phloem below the graft union so that carbohydrates
from the leaves cannot reach the roots, and nutrients and water from the
roots cannot reach the leaves.
• Trees with slow decline show small leaves, yellowing, especially of the
veins , leaf fall, twig dieback and small fruit; those with quick decline wilt
and die in a few weeks. The inside of bark flaps cut at the graft junction may
show pits known as "honeycombing".

39. Stem Pitting
Electron microscopy of Citrus Tristeza virus

40. • Stem pitting is also caused by some CTV strains, regardless of
the rootstock used.
• Grooves and pits occur in the wood of the trunk and branches.
• Gum may be present, too. There are strains that cause stem
pitting on grapefruit, sweet orange and lime.
• Trees with stem pitting grow poorly, fruit is smaller than
normal and, consequently, yields are lower.
• Seedling yellows of, e.g., sour orange and lemon occur in the
nursery. Leaves become yellow and the branches die back.
• Symptoms of CTV become more obvious in the hotter
summer months when water needs are greater and cannot be
met by poor root systems.
• Usually, aphids disperse only a few kilometres, either by
flight or on the wind. However, long-distance spread of
aphids is possible by tropical storms and cyclones.
• Long-distance spread also occurs with the movement of
nursery plants infected with CTV, or infested with CTV-
infected aphids.

41. Leaf showing vein-clearing symptoms
typical of infection from Citrus
tristeza virus
Yellowing of leaves, general dieback and
decline of orange trees affected by Citrus
tristeza virus.

42. Yellow patterns on the leaves and branch
dieback on orange caused by Citrus
tristeza virus

43. Detection & Inspection
• Bark flaps cut across the graft union show small holes
(honeycombing) on the inside face of the bark flap from the
rootstock side of the union.
• Quick decline trees may only have a yellow-brown stain at the
bud union, without honeycombing.
• There are three methods of detection used:
Biological indicator. Buds are taken from diseased trees and
grafted onto Mexican lime (West Indian lime) used as an
indicator plant.
The test can take up to 15 months for results to be seen, but
usually symptoms occur within 2-6 months.
ELISA - Enzyme Linked Immunosorbant assay:
 Antisera is available that detects most strains that cause
decline on sour orange, and also strains that cause stem-
pitting.
 PCR - polymerase chain reaction. Useful for stem-pitting
strains.

44. Management
QUARANTINE
There are many strains of CTV and they are not found in all
countries; this is particularly so for stem-pitting strains.
 Where possible, introductions should be made as seed and,
if vegetative propation is needed, it should be treated to
remove possible virus infections, and then tested to make
sure the treatments have been successful.
 Certification schemes are used to control CTV. Nurseries,
whether private or public, provide plants that have been
established from bud wood-source trees that have been
screened for viruses, and grafted onto tolerant rootstocks.
CULTURAL METHODS
• Use only certified, virus-free budwood, grafted onto resistant
rootstocks.
• Replace individual diseased trees (or the entire blocks) if they have
reached uneconomical levels with certified trees on tolerant
rootstocks.

45. RESISTANT VARIETIES
Only trees on sour orange rootstock are affected by tristeza decline.
• Sweet orange is usually more affected than grapefruit, whereas
lemons on sour orange rootstock are not affected by tristeza decline.
• Poncirus trifoliata (trifoliate orange) is commonly used as a
rootstock for citrus decline. Other CTV-tolerant root stocks are
Rangpur lime, rough lemon and sweet orange.
• As for scions, tangerines are generally tolerant of stem-pitting
strains, and so are most varieties of mandarin, including Satsuma.
However, there are severe strains that cause stem pitting, stunting,
poor quality fruit, even on tolerant rootstocks. There are no CTV-
tolerant limes.
CHEMICAL CONTROL
Chemical control of aphids is not likely to stop the spread of CTV;
this is because spread of the virus is fast, and occurs before the
insecticide kills the aphid.
• However, chemical control of aphids may be beneficial in nurseries,
and also to protect trees used as sources of budwood.

46. Citrus greening Huanglongbing (Asian)
Candidatus Liberibacter asiaticus
 Citrus Greening (Candidatus Liberibacter asiaticus) is one of the
most serious citrus plant diseases in the world.
 It is also known as Huanglongbing (HLB) or yellow dragon disease.
 Once a tree is infected, there is no cure.
 While the disease poses no threat to humans or animals, it has
devastated millions of acres of citrus crops throughout the United
States and abroad.
 Citrus greening is spread by a disease-infected insect, the Asian citrus
psyllid (Diaphorina citri Kuwayama or ACP), and has put the future of
America's citrus at risk.
 Infected trees produce fruits that are green, misshapen and bitter,
unsuitable for sale as fresh fruit or for juice. Most infected trees die
within a few year

47. Signs and Symptoms:
 Visible psyllids or waxy psyllid droppings
 Lopsided, bitter, hard fruit with small, dark aborted seeds
 Fruit that remains green even when ripe
 Asymmetrical blotchy mottling of leaves
 Yellow shoots
 Twig dieback
 Stunted, sparsely foliated trees that may bloom off season
Aetiology:
• Candidatus Liberibacter asiaticus (Asian
form), Candidatus Liberibacter africanus (African form),
and Candidatus Liberibacter americanus (South American
form).
• The three pathogens can only be distinguished by molecular
tests. The abbreviation is HLB. The name “Huanglongbing"
means "yellow shoot disease".

48. Hosts
• All species and varieties of citrus are affected, such as orange,
grapefruit, mandarin, tangelo, kumquat, lemon, lime, pomelo,
trifoliate orange and tangelo. Mock orange or orange jasmine
(Murraya paniculata), and the curry tree (Bergera koenigii) are also
hosts.
Symptoms & Life Cycle
• The damage is done by a bacterium, Candidatus Liberibacter species.
Spread is by the Asian psyllid, Diaphorina citri, or in Africa by Trioza
erytreae.
• HLB causes a yellowing of leaves, and this can be confused with nutritional
deficiencies, especially lack of zinc.
• However, there are two important differences. First, early symptoms of HLB
yellowing often appear on a single shoot or branch, and then spreads
randomly in the tree canopy over several years.
• This is in contrast to nutritional deficiencies which usually occur uniformly
throughout the canopy.
• Secondly, HLB leaves show what is called "blotchy mottle". The patches of
yellow (i) cross the veins and (ii) are lop-sided, i.e., are often more on one
side of the leaf then the other, and (iii) are most obvious on newly hardened
leaves, and fade with age. Leaves with nutritional deficiency, zinc for
instance, show a general yellowing throughout the leaf .

49. • These symptoms are followed by premature leaf drop, twig dieback, decay
of feeder and lateral roots, decline in vigour and, ultimately, death of the
entire tree. Affected trees have stunted growth, bear multiple off-season
flowers (most of which fall down), and produce small, irregularly-shaped
fruit with thick pale peel that remains green at the bottom (hence the other
name of "greening" for the disease). Fruit from these trees tastes bitter.
• Spread of the disease is by psyllids which become infected by the HLB
bacterium as they feed. Both adults and nymphs spread the disease
throughout a life of 1-2 months. Long distance spread occurs by the
movement of infected citrus planting material infested with psyllids.
Movement of other host plants, such as orange jasmine (Murraya
paniculata) and curry leaf (Bergera koenigii) also poses a risk of
introducing HLB and psyllids to new areas, as happened in Florida.
• Tropical storms and cyclones could also spread the psyllid, and may explain
the occurrence of the psyllid in Samoa.
• The two HLB strains, African and Asian, differ in their sensitivity to
temperature. The African strain is heat sensitive with no symptoms
developing above 25-30°C; it occurs at elevations above 600-1000 m in
Kenya, Madagascar, South Africa, and Yemen. By contrast, the Asiatic strain
is heat tolerant occurring at low elevations in hot climates (symptoms
occur above 30°C).

50. Oranges showing signs of Citrus
greening disease.
The "blotchy mottle" symptom of
huanglongbing, yellow patches that are not the
same size and position on both sides of the leaf.

51. Patches of yellow on a leaf showing the
"blotchy mottle" symptom of
huanglongbing; Note that the patches
are uneven, there are more on one side
of the leaf than the other
Late stage symptoms of huanglongbing:
yellowing of most of the leaves, loss of leaves
in the canopy and the start of dieback. Note
that some of the fruit have green patches,
hence the name of the disease "greening".

52. Fruit, affected by huanglongbing, cut
in two to show the dark coloured
seeds; the development of these seeds
has aborted due to the disease.
Management
Quarantine
There is no known cure for HLB, and the only way to protect citrus is to
prevent introduction and spread of the disease in the first place.
If the quarantine barrier is breached, then it is necessary to control
the psyllid, and to destroy infected trees.
If countries wish to import citrus germplasm, it should be under strict
conditions following the FAO/IBPGR Technical Guidelines for the Safe
Movement of Citrus Germplasm. Advanced techniques using PCR (polymerase
chain reaction) are now part of indexing procedures.

53. NATURAL ENEMIES
The nymphs are killed by parasitic wasps and predators including
ladybeetles - larvae and adults - syrphid fly larvae, and pirate bugs.
In California, the eulophid wasp, Tamarixia radiata, has been
imported from the Punjab of Pakistan and released. Introduction
of Tamarixia radiata has to be done with care, as there are
hyperparasites that attack it.
CULTURALCONTROL
 Citrus should be monitored for huanglongbing and psyllids. It should
be done to confirm that they are not present, or if they are present
whether they are spreading.
 It is usual for the psyllid to be found first, and then 1-2 years latter the
disease appears. An IPM program against this disease requires (i)
disease-free nursery plants, (ii) monitoring, and (iii) removal of
infected trees (i.e., those with symptoms).
 Plants supplied by commercial or government nurseries have been
tested for huanglongbing bacteria and important viruses.
 The use of certified healthy trees is important in the management of
the disease.
 It is also important that as part of the certified healthy tree program
the nursery stocks are grown under psyllid-proof screenhouses.

54. • If diseased trees are found they should be removed, and burnt, but before
removal they should be sprayed with the chemicals listed below to prevent
spread of the psyllids.
• Do not allow ornamental plants that are hosts of huanglongbing and psyllid,
for instance, orange jasmine (Murraya paniculata) and curry leaf (Bergera
koenigii), to be moved from areas where the disease and/or insects occur.
• It is important to monitor citrus for disease symptoms and for the presence
of the psyllid.
• Monitoring should be done by farmers (preferably monthly if in a disease
area, otherwise every 3 months), and also by quarantine authorities using
yellow sticky traps placed in the tree canopy.
• Citrus growers should be trained how to do this. Early detection of the
disease and the psyllid is very important.
CHEMICAL CONTROL
Spray trees with a pyrethroid (e.g., lambda-cyhalothrin) insecticide to kill
the adults and nymphs. Malathion can also be used.
• Spray the ground around trees with a systemic product (e.g., imidacloprid)
so that it is taken up by the roots to kill nymphs in the folds of leaves in the
canopy. Note, do not use imidacloprid when trees are flowering as it is toxic
to bees.
• As an alternative to synthetic products, use "soft" insecticides, e.g.,
horticultural spray oil, neem or insecticidal soap.
• These treatments give protection for 9-12 months.