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UF/IFAS Citrus Research and Education Center

UF/IFAS Citrus Research and Education Center

Citrus Greening

Huanglongbing (HLB; citrus greening) is thought to be caused by the bacterium, Candidatus Liberibacter asiaticus. HLB has seriously affected citrus production in a number of countries in Asia, Africa, the Indian subcontinent and the Arabian Peninsula, and was discovered in July 2004 in Brazil. Wherever the disease has appeared, citrus production has been compromised with the loss of millions of trees. HLB has not been reported in Australia or in the Mediterranean Basin. In August 2005, the disease was found in the south Florida region of Homestead and Florida City. Since that time, HLB has been found in commercial and residential sites in all counties with commercial citrus.

The early symptoms of HLB on leaves are vein yellowing and an asymmetrical chlorosis referred to as “blotchy mottle.” The blotchy mottle symptom is the most diagnostic symptom of the disease, especially on sweet orange. Leaves may be small and upright with a variety of chlorotic patterns that often resemble mineral deficiencies such as those of zinc, iron, and manganese. Some leaves may be totally devoid of green or with only green islands. The blotchy mottle symptom also may be confused with other diseases or damage such as severe forms of citrus tristeza virus (CTV), Phytophthora root rot, water logging, citrus blight, leafminer tunnels or stubborn, a disease that is not known to be present in Florida. Root systems of infected trees are often poorly developed and new root growth may be suppressed. Early symptoms of yellowing may appear on a single shoot or branch. The yellowing usually spreads throughout the tree over a year, especially on young trees, and affected trees may show twig dieback, causing the productivity to decline within a few years. Fruit are often few in number, small, may be lopsided with a curved central core, and fail to color properly, remaining green at the stylar end. Many fruit drop prematurely from afflicted trees. A yellow stain may be present just beneath the peduncle (stem) on a cut fruit. The affected fruit often contain aborted seeds and have a salty bitter taste.

  • History

    Greening or Huanglongbing (HLB) Worldwide

    Information and photos were obtained from the Journal of Plant Pathology, 2006, Huanglongbing: A Destructive, Newly-Emerging, Century-Old Diesease of Citrus by J.M. Bové

    1919: First reported in southern China

    1921: First report of disease in the Philippines, but it was thought to be related to zinc deficiency.

    1928: A disease under the names, yellow shoot or greening depending on region, was observed in South Africa

    1937: The first description of HLB in South Africa was assumed to be mineral toxicity

    1941-1955: Most extensive work on greening in southern China was conducted

    Greening or Huanglongbing (HLB) Worldwide

    Areas visited in Southern China and Taiwan by Lin Kung Hsiang in between 1941 and 1955. Red dots represent where HLB was found and blue dots represent areas where it was unclear whether HLB was present.

    1956: Lin Kung Hsiang (researcher from China) concluded that greening is a graft transmissible infectious disease, not related to physiological disorders (e.g. nutrient deficiencies, water logging, etc.) or soil borne diseases (e.g. phytophthora, etc.)

    Lin Kung Hsiang

    1960's: HLB first appeared in Thailand

    1965: Researchers in South Africa demonstrated HLB was transmissible by graft inoculation and by the African citrus psyllid, Trioza erytreae

    1966: Philippine and Indian researchers recognized the similiarities between the 'mottle leaf' or 'citrus dieback' disease and HLB in China and Taiwan and 'greening' in South Africa

    1967: Philippine researchers demonstrated 'mottle leaf' or 'citrus dieback' could be transmitted by the Asian citrus psyllid, Diaphorina citri

    1995: The offical name of the disease became huanglongbing (HLB) at the International Organization of Citrus Virologists (IOCV) at the 13th conference of the Organization in
    Fuzhou (Fujiam, China)

    1998: Asian citrus psyllid arrived in Florida

    2004: The disease was confirmed to be in Brazil

    2005: The disease was confirmed to be in Florida

    Florida History

    2005

    August -Citrus greening was first confirmed in south Miami-Dade county

    October 25 - Four counties confirmed positive (Dade, Broward, Palm Beach, Hendry) Map

    September 16 - Federal order issued to restrict the interstate movement of all citrus greening
    and Asian citrus psyllid host plant material from Florida's quarantined areas

    2006

    October 2006 map

    March 14 - Regulations for citrus nurseries were established

    May 3 - The September federal order was revised

    June 16 - Twelve counties confirmed positive (Monroe, Collier, Lee, Martin, St. Lucie, Highlands, DeSoto, Manatee) Map

    2007

    October 2007 HLB map

    January 26 - Fourteen counties confirmed positive (Brevard, Hillsborough) Map

    April 30 - Twenty counties confirmed positive (Orange, Sarasota, Volusia, Okeechobee, Glades, Charlotte) Map

    May 31 - Twenty-two counties confirmed positive (Osceola, Seminole) Map

    July 27 - Twenty-five counties confirmed positive (Hardee, Marion, Indian River) 

    August 24 - Twenty-six counties confirmed positive (Polk) Map

    October 30 - Federal order revised

    October 31 - Twenty-eight counties confirmed positive (St. Johns, Pasco) Map

    November 2 - A third Federal order was issued due to the spread of greening and the Asian citrus psyllid

    November 30 - Two new counties, Lake and Hernando, confirmed with citrus greening Map

    December - Federal order issued was revised to include all counties with a confirmed positive greening find

    2008

    January 2008 HLB Map

    January 11 - Federal order issued to quarantine the entire state of Florida

    June 24 - Thirty-one counties confirmed positive (Pinellas) Map

    August 7 - Thirty-two counties confirmed positive (Sumter) Map

    2009

    February 16 - Thirty-three counties confirmed positive (Putnam) Map

  • Transmission and Spread

    The Asian Citrus Psyllid transmits the greening bacterium. The psyllid was first found in Florida in June 1998.

    Psyllid eggs are 0.3 mm long, elongated and almond-shaped. The newly laid eggs are pale in color, then become yellow and turn to an orange color as the time approaches for hatching

    Nymphs are 0.25 to 1.7 mm and yellowish orange. Larger nymphs can be seen with the naked eye usually found on the young flush. The nymphs are sessile and move slowly if disrupted. They secrete sticky waxy secretions similar to honeydew produced by aphids which causes sooty mold.

    The adults are 3 to 4 mm long. They have a brown mottled body and feed at a 30 degree angle. They can usually be found on the underside of leaves and move quickly.

    ACP Damage
    Psyllid feeding damage (Deformation)
    Click to enlarge


    Transmission and Spread HLB

    The disease can also be spread by grafting, but not all buds from an infected tree carry the greening bacterium

    Citrus Huanglongbing: The Pathogen and Its Impact

    Citrus Huanglongbing: Understanding the Vector-Pathogen Interaction for Disease Management

    English Tap Sampling for Asian Citrus Psyllids (ACP)

    Spainsh Tap Sampling for Asian Citrus Psyllids (ACP)

  • Alternate Hosts

    Alternate hosts plants of the Asian citrus psyllid are Murraya paniculata (orange jasmine), Severinia buxifolia (box orange) and other plants in the Rutaceae family.

    Asian citrus psyllid

    Additional Information about Alternate Hosts

    Plant Characteristics of Severinia buxifolia

    Plant Characteristics of Murraya paniculata

  • Nutrient Deficiencies Compared to Citrus Greening

    Citrus greening symptoms can easily be mistaken for a nutrient deficiency. Nutrient deficiencies are often symmetrical on each side of the vein whereas, citrus greening is asymmetrical. Below are the symptoms of each the seventeen nutrients needed by citrus trees.

    Nitrogen Deficiency

    Nitrogen Deficiency

    • Occurs on older leaves first then toward the younger leaves
    • Light yellowish to green leaves. Mature leaves slowly bleach to a mottled irregular green and yellow pattern, become entirely yellow and then are shed
    • Fruit peel is pale and smooth

    Phosphorus Deficiency

    Phosphorus Deficiency

    • Occurs on older leaves first
    • Leaves are small and narrow with purplish or bronze discoloration
    • Fruit drops before normal harvesting time, hollow core and thicker peel

    Potassium Deficiency

    Potassium Deficiency

    • Occurs on older leaves first
    • Yellowing of the tips and margins and gets broader
    • Smaller fruit size

    Calcium Deficiency

    • Occurs on mature leaves with young leaves appearing normal
    • Leaves lose color along the leaf margins and between the main veins
    • Fruit is undersized and misshapen

    Magnesium Deficiency

    Magnesium Deficiency

    • Occurs on mature leaves with young leaves appearing normal
    • Inverted green V-shape surrounded by yellowing
    • Fruit yield and quality is reduced; seedy varieties are more Magnesium
    • Deficiency severely affected by a magnesium deficiency than seedless varieties

    Sulfur Deficiency

    Sulfur Deficiency

    • Occurs on new growth
    • Pale green to yellow in color
    • Fruit peel is pale and smooth

    Iron Deficiency

    Iron Deficiency

    • Occurs on young leaves
    • Green veins with the leaf appearing light yellowish to white in color
    • Small fruit

    Zinc Deficiency

    Zinc Deficiency

    • Occurs first on new growth and remains on leaf as it matures
    • Reduced leaf size, narrow leaves, yellow mottled on green background
    • Decreased overall fruit yield

    Manganese Deficiency

    Manganese Deficiency

    • Occurs on young leaves
    • Dark green veins with a lighter green background
    • Small, soft fruit

    Boron Deficiency

    Boron Deficiency

    • Occurs on younger leaves first
    • Leaves show small water-soaked spots
    • Fruit becomes hard and dry

    Copper Deficiency

    Copper Deficiency

    • Occurs on new growth first
    • Leaves are uniform in color, long-willow looking leaves, bushy appearance, dieback
    • Fruit splitting, gumming

    Molybdenum Deficiency

    Molybdenum Deficiency

    • Occurs on mature leaves first
    • Interveinal chlorotic spots in early summer
    • Under severe conditions, fruit has large irregular brown
      spots surrounded with yellow discoloration

    Nickel Deficiency

    • No one has ever seen a nickel deficiency soil-grown plant 

    Chlorine Deficiency

    • No one has ever seen a chlorine deficiency soil-grown plant

  • Management
    • You should manage your grove as if you already have greening
    • It is an integrated approach of the use of disease free nursery stock, reduction of the inoculum by frequent disease surveys, removal of symptomatic trees and suppression of the Asian citrus psyllid

    Antibacterial Management

    • Suggested Antibacterial Product Use Pattern for Huanglongbing (HLB; citrus greening) Management PDF
    • Crisis Declaration PDF

    Propagation

    • Use of clean bud wood and certified healthy trees
    • Only purchase trees from a certified nursery

    Tree Removal

    • Only way to ensure infected trees will not serve as a source inoculum
    • Pruning of symptomic branches will NOT be successful

    Scouting 

    Frequency

    • Four times a year is recommended
    • If you currently have greening in your grove or close by, scouting more than four times a year is recommended
    • Symptoms are most easily seen September through March
    • During the spring flush, scouting becomes more difficult and scouts should look further into the tree canopy

    Methods

    • Tractor or pickup mounted platform
        - Use a mounted platform for taller trees
    • ATV's
        - Medium sized trees can be scouted from an ATV
    • Walking
        - Young trees can be scouted by walking
    • Tractor or pickup mounted platform

    scouting methods

     Diagram on a suggested scouting movement within a grove

    Grove Survey

    Grove Conditions

    • Scouting is more difficult in an unkept grove
    • Nutritional deficiencies can cause greening symptoms to blend and go unnoticed
    • Excessive weeds and unmanaged row middles cause scouts to watch where they are walking more than scouting
    • Tree size

    Flagging

    • Several colored flagging tapes are available
    • Choose a tape that will only be used for greening and cannot be confused with other colored flagging tape

    Flagging tape

    • If a suspect tree is found, flag the suspected branch and write on the flagging tape the inspector's name and date

    • Mark the end of the row and the number of suspect trees in that row

    Safety Concerns

    • Grove conditions
    • Chemical spray applications
    • Weather
    • Potential for slips and falls

    Additional Resources

    Asian Citrus Psyllid Management

    • Some biological control of the psyllid is available but the amount of psyllid control provided by introduced parasitoids has been insufficient to slow disease spread

    • Area wide spay programs through citrus health management areas (CHMA)

    • Speed sprayer, low volume and aerial are application methods available

    Grower Experience

    Host Plants

    • If possible, remove host plants, Murraya paniculata (orange jasmine) and Severinia buxifolia (box orange) from around a commercial citrus grove

      Photo Credit: Steve Futch, Ph.D.
  • Links

    UF/IFAS Publications

    Current

    Archived

    *All documents are in PDF format
    • An Iodine-Based Starch Test to Assist in Selecting Leaves for HLB Testing PDF
    • Biology and Management of the Asian Citrus Psyllid, Diaphorina citri Kuwayama, in Florida Citrus PDF
    • Citrus Greening and Citrus Tree Planting in Florida PDF
    • Dooryard Citrus Production: Citrus Greening Disease PDF
    • Dooryard Citrus Production: The Value of the Florida Citrus Industry to Florida Residents PDF
    • Economic Evaluation of Citrus Greening Management and Control Strategies PDF
    • Economic Impacts of the Florida Citrus Industry in 2007-08 PDF
    • Economic Impacts of Citrus Greening (HLB) in Florida, 2006/07–2010/11 PDF
    • GPS Accuracy for Tree Scouting and Other Horticultural Uses PDF
    • IFAS Guidance for Huanglongbing (Greening) Management PDF
    • The Dynamics and Implications of Recent Increases in Citrus Production Costs PDF
    • The Incidence of Greening and Canker Infection in Florida Citrus Groves from September 2007 through August 2008 PDF

    UF/IFAS Identification Tools

    UF/IFAS Brochures

    Citrus Greening Articles and Websites

  • Regulations

    Citrus Growers and Caretakers

    • Must sign a compliance agreement and submit a business plan

    • Required to decontaminate upon exiting a grove

    • Decontamination upon entering a grove is optional

    • Only fruit being shipped to the European Union Markets are required to have pre-harvest inspections

    • Only purchase trees from a certified nursery

    • https://www.fdacs.gov/Agriculture-Industry/Pests-and-Diseases/Plant-Pests-and-Diseases/Citrus-Health-Response-Program

    Citrus Harvesters

    Citrus Harvesters

    • Must sign a compliance agreement and submit a business plan

    • http://forms.freshfromflorida.com/08359.pdf

    Citrus Processors

    • Must sign a compliance agreement and submit a business plan

    • The business plan must determine the company procedures for decontamination

    • http://forms.freshfromflorida.com/08356.pdf

    Citrus Packers

    • Must sign a compliance agreement with the USDA

    • https://www.fdacs.gov/Agriculture-Industry/Pests-and-Diseases/Plant-Pests-and-Diseases/Citrus-Health-Response-Program

    Citrus Nursersies

    • As of January 1, 2007 all citrus nursery propagations must occur in enclosed greenhouses

    • As of January 1, 2007 all citrus nursery propagations must occur in enclosed greenhouses

    • New nursery sites must be one mile from citrus groves. Existing sites can remain, but must build their nursery structure to comply with all other regulations

    • All budwood must be grown in structures meeting the rule requirements, tested annually for pathogens, registered with the Florida Division of Plant Industry and originated from screened budwood sources

    • Nurseries must be inspected every thirty days

    • All new nursery sites and structures must be approved by Florida Division of Plant Industry

    • As of January 11, 2008, all plants and plant parts, including but not limited to nursery stock, cuttings, budwood, and seed (excluding fruit), of Citrus spp., Murraya spp., etc may not be moved between states from areas quarantined due to citrus greening

    Citrus Nursersies

    • https://www.fdacs.gov/Divisions-Offices/Plant-Industry/Office-Locations/Plant-Inspector-Directory/Commercial-Citrus-Nursery-Inspector-Directory
    For more information on Florida citrus regulations, please contact the Division of Plant Industry 863-298-3000

  • Pathogen

    • Candidatus Liberibacter spp. are phloem-limited plant pathogenic bacteria.The phloem system of the plant transports sugars, which are the food source of the plant, bidirectionally through the plant. The phloem system of the plants transports the products of photosynthesis (sugars) from sources of photosynthetic activity (leaves) in the plant to sinks (flowers, fruits, roots, seeds).

    • Psyllids are the main means of transmission to plants. An infected psyllid feeds on a healthy tree and injects the bacterium into the phloem. Once a tree is infected with the bacterium, there is no known cure for the disease. This in part is because the bacterium is inside the vascular system of the plant (systemic) and is therefore very difficult to access.

    • The bacterium is Gram-negative. Part of the evidence used to show that the bacterium is Gram-negative was the fact there were two membranes (figure 2), outer and cytoplasmic, and a thin peptidoglycan layer in between the cell walls seen in electron micrographs.

    • At this time, greening has not been cultured, but ongoing research shows promise this will be accomplished. Once the bacterium has been isolated in pure culture plant pathologists will be able to complete Koch's postulates (pathogenicity tests). Completetion of Koch's postulates will allow plant pathologists to definitively say Ca. Liberibacter sp. causes the symptoms of HLB.

    Electron micrograph of Ca. Liberibacter cells in a sieve tube of sweet orange leaf in Saudi Arabia The peptidoglycane layer of the Gram negative cell wall can be visualized (PG) in between the inner membrane cytoplasmic membrane (CM) and the outer cell wall membrance (OM).  
    Figure 1. Electron micrograph of Ca. Liberibacter cells in a sieve tube of sweet orange leaf in Saudi Arabia Figure 2. The peptidoglycane layer of the Gram negative cell wall can be visualized (PG) in between the inner membrane cytoplasmic membrane (CM) and the outer cell wall membrance (OM).  


    Photo Credit: Huanglongbing: A Destructive, Newly-Emerging, Century-Old Disease of Citrus, J.M. Bové

    Various Species of Ca. Liberibacter

    FORM
    VECTOR
    HEAT TOLERANCE
    Asian
    Diaphorina citri (psyllid)*
    heat tolerant
    African
    Trioza erytreaae (psyllid)*
    heat-sensitive
    American
    Diaphorina citri ( psyllid)
    heat tolerant

    *It has been shown experimentally that the two psyllids can transmit both the Asian and African forms, but the preferential vector is shown above.

    Various Names of HLB (Huanglongbing) throughout the World

    HLB became the official name because it was the first recorded in the literature.

    • South Africa: greening
    • Philippines: mottle leaf
    • India: dieback
    • Indonesia: vein phloem degeneration
    • China: Huanglongbing (yellow shoot or yellow branch disease)
    • Taiwan: likubin
  • Symptoms
    • Symptoms can be found year round, but are most easily seen from September through March
    • The disease affects all parts of the tree canopy -  leaves, twigs and fruit

    • As the disease progresses, it will cause the whole tree to decline

      Leaf Symptoms

    • Leaf symptoms include blotchy mottle, yellow veins, vein corking or green islands
    • Yellow veins, vein corking or green islands are not diagnostic alone
    • Blotchy mottle is the best diagnostic leaf symptom of greening
    • Blotchy mottle: a random pattern of  yellowing (chlorosis) on leaves that is not the same on the right and left sides of the leaf
    • Yellow veins can be confused with other diseases (e.g. foot rot) or damage (e.g. broken or girdled limb)

      Leaf Symptoms

      Pen Test for Leaves

    • A simple procedure to determine if symptoms are the same on both halves of a leaf
    • Draw two circles on opposite halves of the leaf
    • Is the pattern the same in both circles?
    • Different patterns indicate potential greening if other problems have been ruled out

    Nutrient

    Nutrient Deficiency

    Greening

    Greening

    		  

    Fruit Symptoms

    • Fruit external appearance may be lopsided, misshapen or small green fruit
    • The fruit would taste salty and bitter
    • The internal appearance may have aborted seeds, yellow stain beneath the calyx button and/or a curved central core

    Tree Appearance

    • Yellow shoots
    • Twig dieback
    • Stunting
    • Off-season bloom
    • Overall tree decline

    Tree appearance

  • Diagnostics

    Testing Sites

    Field Test

    • The iodine-based starch test is used to aid in the selection of leaves for PCR testing
    • Greening infected trees and various other citrus diseases show an increased level of starch accumulation
    • By using an iodine and water solution, it can be applied to a leaf to exhibit starch levels
    • This does NOT verify a positive greening infected tree
    • An Iodine-Based Starch Test to Assist in Selecting Leaves for HLB Testing
  • Photo Gallery
    ...
  • Contacts
    Megan Dewdney, Ph.D. 
    Plant Pathologist Extension Specialist
    863-956-8651
    mmdewdney@ufl.edu    		 Lauren Diepenbrock, Ph.D.  
    Entomology
    863-956-8801
    ldiepenbrock@ufl.edu
    Lukasz Stelinski, Ph.D. 
    Entomology and Nematology
    863-956-1151 
    stelinski@ufl.edu    		 Jamie Burrow
    Extension Program Manager 
    863-956-8648
    jdyates@ufl.edu
    Tripti Vashisth
    Horticultural Sciences and Citrus Extension Specialist
    863-956-4631
    tvashisth@ufl.edu    		 Chris Oswalt
    Multi-County Citrus Extension Agent
    Polk and Hillsborough Counties
    863-519-8677 
    wcoswalt@ifas.ufl.edu
    Ajia Paolillo
    Multi-County Citrus Extension Agent
    DeSoto, Desoto, Hardee, Manatee
    863-993-4846 
    ajiacunningham@ufl.edu    		 Mongi Zekri, Ph.D.
    Multi-County Citrus Extension Agent
    Hendry, Glades, Lee, Charlotte and Collier Counties
    863-674-4092
    maz@ifas.ufl.edu
    Lourdes Pérez Cordero 
    Citrus Extension Agent
    Highlands County
    863-402-6540
    lperezcordero@ufl.edu    		 Amir Rezazadeh 
    Multi-County Citrus Extension Agent
    St. Lucie, Indian River
    772-462-1628
    amir2558@ufl.edu
    Matt Smith
    Citrus Extension Agent
    Sumter - Central
    352-569-6862
    smith197@ufl.edu    		 Danielle Sprague
    Citrus Extension Agent
    Jefferson
    850-342-0187
    dsprague@ufl.edu
    Brandon White
    Multi-County Citrus Extension Agent
    Orange, Lake
    352-343-2729
    brandon1.white@ufl.edu