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Datasheet

Candidatus Liberibacter asiaticus
(citrus greening)

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Datasheet

Candidatus Liberibacter asiaticus (citrus greening)

Summary

  • Last modified
  • 09 June 2022
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Candidatus Liberibacter asiaticus
  • Preferred Common Name
  • citrus greening
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Proteobacteria
  •     Class: Alphaproteobacteria
  •       Order: Rhizobiales
  •         Family: Phyllobacteriaceae
  • Summary of Invasiveness
  • The Asian form of huanglongbing is considered very invasive due to the cryptic nature of the pathogen, ‘Candidatus Liberibacter asiaticus’, and its ability to be transported either in infected plant material or infective psyllids. ‘Ca...

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Pictures

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PictureTitleCaptionCopyright
Candidatus Liberibacter asiaticus (Asian greening); blotchy mottle, showing early symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); blotchy mottle, showing early symptoms.
Copyright©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); blotchy mottle, showing early symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); blotchy mottle, showing early symptoms.©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); leaf symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); leaf symptoms.
Copyright©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); leaf symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); leaf symptoms.©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); blotchy mottle, showing early symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); blotchy mottle, showing early symptoms.
Copyright©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); blotchy mottle, showing early symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); blotchy mottle, showing early symptoms.©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); advanced symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); advanced symptoms.
Copyright©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); advanced symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); advanced symptoms.©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); advanced symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); advanced symptoms.
Copyright©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); advanced symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); advanced symptoms.©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); devastated orchard.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); devastated orchard.
Copyright©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); devastated orchard.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); devastated orchard.©Matthew Weinert/AQIS
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2013.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2013.
Copyright©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2013.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2013.©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2016.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2016.
Copyright©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2016.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2016.©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2016.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2016.
Copyright©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2016.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms. April 2016.©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
Copyright©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
Copyright©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
Copyright©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
Copyright©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
TitleSymptoms
CaptionCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
Copyright©Nian Wang (Citrus Research and Education Center)
Candidatus Liberibacter asiaticus (Asian greening); HLB symptoms.
SymptomsCandidatus Liberibacter asiaticus (Asian greening); HLB symptoms.©Nian Wang (Citrus Research and Education Center)

Identity

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Preferred Scientific Name

  • Candidatus Liberibacter asiaticus Jagoueix et al.

Preferred Common Name

  • citrus greening

Other Scientific Names

  • Ca. Liberibacter asiaticus
  • Ca. Liberobacter asiaticum
  • Ca. Liberobacter asiaticus
  • Candidatus Liberobacter asiaticum Jagoueix et al.
  • Candidatus Liberobacter asiaticus
  • Liberibacter asiaticus Jagoueix et al.
  • Liberobacter asiaticum Monique Garnier
  • Liberobacter asiaticus

International Common Names

  • English: Asian greening; blotchy mottle disease of citrus; citrus huanglongbing; decline of citrus; greening; huang long bin; huanglongbing; leaf mottling of citrus; vein phloem degeneration of citrus; yellow branch disease; yellow branch of citrus; yellow shoot; yellow shoot of citrus
  • Spanish: enverdecimiento de los cítricos
  • French: greening des agrumes; virescence des agrumes
  • Chinese: huang shao (yellow shoot) disease; likubin; yellow dragon

Local Common Names

  • India: citrus dieback
  • Indonesia: citrus vein phloem regeneration (CVPD)
  • Philippines: blotchy mottle; mottle leaf disease
  • South Africa: yellow branch disease
  • Taiwan: likubin

EPPO Code

  • LIBEAS ('Candidatus Liberibacter asiaticus')

Summary of Invasiveness

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The Asian form of huanglongbing is considered very invasive due to the cryptic nature of the pathogen, ‘Candidatus Liberibacter asiaticus’, and its ability to be transported either in infected plant material or infective psyllids. ‘Ca. L. asiaticus’ was first reported in Asia, the origin of citrus species. It has spread to most citrus-producing countries including top citrus producers Brazil, China and the USA, but has not spread to countries in the Mediterranean region and Australia. Yield losses due to this disease have been estimated to be between 30 and 100%, depending on disease status, environmental factors, management approaches, varieties and the age of the trees during inoculation. History has shown that the appearance of the vector in a country will almost guarantee the appearance of the disease in the future, e.g. in Brazil and USA. The species and its vector are on several alert lists including the EPPO A1 List of Regulated Quarantine Plant Pests.

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Proteobacteria
  •         Class: Alphaproteobacteria
  •             Order: Rhizobiales
  •                 Family: Phyllobacteriaceae
  •                     Genus: Candidatus Liberibacter
  •                         Species: Candidatus Liberibacter asiaticus

Notes on Taxonomy and Nomenclature

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Candidatus Liberibacter asiaticus’ is a Gram-negative bacterium that belong to the family Rhizobiaceae (Class: Alphaproteobacteria). It was originally named as ‘Candidatus Liberobacter asiaticum’ (Jagoueix et al., 1997), but changed to ‘Candidatus Liberibacter asiaticus’ later (Garnier et al., 2000). In addition to ‘Ca. L. asiaticus’, ‘Ca. L. africanus’ and ‘Ca. L. americanus’ infect citrus to cause huanglongbing (HLB). ‘Ca. Liberibacter spp.’ also include ‘Ca. L. solanacearum’ (syn. ‘Ca. L. psyllaurous’) causing diseases on many solanaceous plants and on carrot, celery, parsley and parsnip, ‘Ca. L. europaeus’ infecting Scotch broom, ‘Ca. L. crescens’ and ‘Ca. L. brunswickensis’ (Jagoueix et al., 1994; 1997; Texeira et al., 2005b; Hansen et al., 2008; Liefting et al., 2008; Raddadi et al., 2011; Leonard et al., 2012; Thompson et al., 2013; Morris et al., 2017).

Description

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Ca. L. asiaticus’ is restricted to the sieve tube elements of the phloem vessels. However, ‘Ca. L. asiaticus’ was also observed in nucleated non-sieve element cells although the identity of these Ca. L. asiaticus-containing nucleated cells remain unknown (Achor et al., 2020). Electron microscopy studies reveal that ‘Ca. L. asiaticus’ possesses the characteristic double membrane cell envelope of Gram-negative bacteria (Garnier et al., 1984; Texeira et al., 2005a). Thin-section EM examination reveals pleiomorphic round and elongated bacilliform-like shapes. The length of the bacteria ranges from 594.6 to 1368.2 nm. The diameter of bacilliform cells range from 0.14 to 0.26 µm, whereas round bacterial cells have a diameter of 0.30 to 0.99 µm (Hilf et al., 2013). Similar particles are observed in the haemolymph and salivary glands of the two insect vectors.

Distribution

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Of the ‘Ca. Liberibacter’ species that cause huanglongbing, the Asian form is the most widespread. It has spread to most citrus-producing countries including top citrus producers Brazil, China and the USA, but has not spread to countries in the Mediterranean region and Australia. ‘Ca. L. asiaticus’ was reported in Ethiopia (Saponari et al., 2010) and Kenya (Ajene et al., 2020). In addition, Diaphorina citri was reported in Kenya (Rwomushana et al., 2017), Tanzania (Ajene et al., 2020) and Nigeria (Oke et al., 2020). ‘Ca. L. asiaticus’ was also detected in field populations of Trioza erytreae in the Ethiopian highlands (Rasowo et al., 2019). ‘Ca. L. asiaticus’ was also reported in Tanzania (Shimwela et al., 2016) and Uganda (Kalyebi et al., 2015), which was disapproved by Roberts and colleagues as probable misidentifications that were reclassified as ‘Ca. L. africanus subsp. clausenae’ (Roberts et al., 2017). ‘Ca. L. asiaticus’ is not present in the Mediterranean region, but is present in neighbouring countries including Iran (Faghihi et al., 2009) and Saudi Arabia (Bové, 2006). T. erytreae has now spread in Spain and Portugal.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 12 May 2022
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

EgyptAbsent, Invalid presence record(s)
EthiopiaPresent
KenyaPresent, Few occurrencesFirst report.
MauritiusPresent, LocalizedIntroducedInvasive
RéunionPresent, LocalizedIntroducedInvasive
TanzaniaAbsent, Invalid presence record(s)
UgandaAbsent, Invalid presence record(s)

Asia

BangladeshPresent
BhutanPresent
IndonesiaPresent
-BorneoPresent
-Irian JayaPresentIntroducedInvasive
-JavaPresent
-Lesser Sunda IslandsPresent, Widespread
-SulawesiPresent
-SumatraPresent
CambodiaPresent
ChinaPresent
-FujianPresent
-GuangdongPresent
-GuangxiPresent
-GuizhouPresent
-HainanPresent
-HunanPresent
-JiangxiPresent
-SichuanPresent
-YunnanPresent
-ZhejiangPresent
Hong KongPresent, Few occurrences
IndiaPresent, Widespread
-Andhra PradeshPresent
-Arunachal PradeshPresent
-AssamPresent
-BiharPresent
-DelhiPresent
-GujaratPresent
-HaryanaPresent
-Himachal PradeshPresent
-Jammu and KashmirPresent
-KarnatakaPresent
-KeralaPresent
-Madhya PradeshPresent
-MaharashtraPresent
-ManipurPresent
-MeghalayaPresent
-MizoramPresent
-NagalandPresent
-OdishaPresent
-PunjabPresent
-RajasthanPresent
-SikkimPresent
-Tamil NaduPresent
-TripuraPresent
-Uttar PradeshPresent
-UttarakhandPresent
-West BengalPresent
IranPresent, Localized
JapanPresent, Localized
-KyushuPresent, Localized
-Ryukyu IslandsPresent
LaosPresent
MalaysiaPresent, Localized
-Peninsular MalaysiaPresent
-SarawakPresent
MyanmarPresent
NepalPresent, WidespreadIntroducedInvasive
OmanPresent, Localized
PakistanPresent
PhilippinesPresent, Widespread
Saudi ArabiaPresent
Sri LankaPresent
SyriaAbsent, Invalid presence record(s)
TaiwanPresent, Widespread
ThailandPresent
VietnamPresent, Localized
YemenPresent, Localized

Europe

BelgiumAbsent
NetherlandsAbsent, Confirmed absent by survey
PortugalAbsent, Confirmed absent by survey
SloveniaAbsent
SpainAbsent, Confirmed absent by survey

North America

BarbadosPresent, Localized
BelizePresent, Localized
Costa RicaPresent, Localized
CubaPresent, Widespread
DominicaPresent, Few occurrences
Dominican RepublicPresent, Localized
El SalvadorPresent, Localized
GuadeloupePresent2012
GuatemalaPresent
HondurasPresent
JamaicaPresent, Widespread
MartiniquePresent2013
MexicoPresent, Localized
NicaraguaPresent, Few occurrences
PanamaPresent, Localized
Puerto RicoPresent, Widespread
Trinidad and TobagoPresent, Localized
U.S. Virgin IslandsPresentOriginal citation: NAPPO (2010)
United StatesPresent, Localized
-AlabamaPresent, Few occurrences
-CaliforniaPresent, LocalizedPresent: subject to official control
-FloridaPresent, Widespread
-GeorgiaPresent, Few occurrences
-LouisianaPresent, Localized
-South CarolinaPresent, Few occurrences
-TexasPresent, Localized

Oceania

Cook IslandsAbsent, Confirmed absent by survey
FijiAbsent, Confirmed absent by survey
Papua New GuineaPresent, Localized
SamoaAbsent, Confirmed absent by survey
Timor-LestePresentIntroducedInvasive
TongaAbsent, Confirmed absent by survey

South America

ArgentinaPresent, Localized
BrazilPresent
-BahiaPresent, Few occurrences
-Minas GeraisPresent
-ParanaPresent, Widespread
-Sao PauloPresent
ChileAbsent, Confirmed absent by survey
ColombiaPresent, Few occurrences
French GuianaPresent, Localized
ParaguayPresent, Localized
VenezuelaPresent, Localized

History of Introduction and Spread

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Ca. L. asiaticus’ is widely present in citrus-producing regions in Asia, including Bangladesh (confirmed in 2016) (Tipu et al., 2017), Bhutan (confirmed in 2002) (Ahlawat et al., 2003), Cambodia, China, East Timor (detected in 2000) (Weinert et al., 2004), India, Indonesia, Iran (detected in 2009) (Faghihi et al., 2009), Japan, Laos, Malaysia, Myanmar, Nepal, Oman, Pakistan, Philippines, Papua New Guinea (confirmed in 2002) (Weinert et al., 2004), Saudi Arabia, Sri Lanka, Syria, Thailand, Vietnam and Yemen. ‘Ca. L. asiaticus’ was introduced into the Americas in 2000s and is now present in South America (Argentina (confirmed in 2012) (Badaracco et al., 2017), Brazil (in 2004) (Coletta-Filho et al., 2004), Colombia (in 2015) (Olvera-Vargas et al., 2020), Paraguay (in 2013) (EPPO, 2013) and Venezuela (in 2017) (Marys et al., 2020)), North America (USA (in 2005) and Mexico (in 2009)), and Central America and the Caribbean (Barbados (IPPC, 2014), Belize (in 2009) (Manjunath et al., 2010), Costa Rica, Cuba (in 2009) (Martinez et al., 2009), Costa Rica (in 2011) (Molina-Bravo et al., 2015), Dominica (in 2012) (EPPO, 2012), Dominican Republic (in 2008) (Matos et al., 2009), El Salvador, French West Indies (Guadeloupe (in 2012), Martinique (in 2013)) (Cellier et al., 2014), Guatemala, Honduras (in 2010), Jamaica, Nicaragua (in 2010), Panama (in 2017) (EPPO, 2017), Puerto Rico, and Trinidad and Tobago (in 2017)). ‘Ca. L. asiaticus’ has also spread to Africa (Ethiopia (in 2009) (Saponari et al., 2010), Mauritius, Réunion and Kenya (in 2017-2018) (Ajene et al., 2020)) and Oceania (Papua New Guinea in 2000 (Weinert et al., 2004)).

Risk of Introduction

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Currently, Australia and the Mediterranean Basin are the two major citrus-producing regions that are free of HLB. However, African citrus psyllid (Trioza erytreae) has been reported in Spain and Portugal even though HLB pathogens have not been found in either country (Cocuzza et al., 2017). Human-mediated spread is an important trajectory for ‘Ca. L. asiaticus’ spreading. Human activities such as movement of fruit and/or plant material are suggested to be necessary for long distance dispersion of Diaphorina citri and spread of ‘Ca. L. asiaticus’. Citrus materials (e.g. budwood, grafted trees, seedlings) as well as ornamental rutaceous species (e.g. Murraya) have been suggested to be critical for introduction of HLB pathogens and psyllid vectors (Duran-Vila et al., 2014). Additionally, hurricanes or storms have been suggested to play important roles in long distance dispersal of Asian citrus psyllids (Gottwald, 2010; Wang et al., 2017).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial ManagedProtected agriculture (e.g. glasshouse production) Present, no further details Harmful (pest or invasive)
Terrestrial ManagedManaged forests, plantations and orchards Secondary/tolerated habitat Harmful (pest or invasive)
Terrestrial ManagedManaged grasslands (grazing systems) Secondary/tolerated habitat Harmful (pest or invasive)

Hosts/Species Affected

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Most commercial citrus varieties (with few exceptions, such as Sugar Belle) are susceptible to HLB, owing to their limited genetic diversity (Wu et al., 2018; Deng et al., 2019). However, multiple citrus relatives, such as Microcitrus australis, M. warburgiana, M. papuana, Eremocitrus glauca and Swinglea glutinosa, have shown tolerance/resistance against HLB (Cifuentes-Arenas et al., 2019; Alves et al., 2021). Poncirus trifoliata was initially classified as partially resistant (Folimonova et al., 2009; Ramadugu et al., 2016) but has recently been considered as a possible source of genetic resistance to Diaphorina citri rather than to ‘Ca. L. asiaticus’ (Alves et al., 2021). Murraya paniculata and S. glutinosa are considered as short-term transient hosts of ‘Ca. L. asiaticus’ (Cifuentes-Arenas et al., 2019) and their infection is just transient and after a few months, plants become Ca. L. asiaticus-free.

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
Atalantia buxifoliaRutaceaeOther
Catharanthus roseus (Madagascar periwinkle)ApocynaceaeOther
CitrusRutaceaeMain
Citrus amblycarpaUnknown
Citrus aurantiifolia (lime)RutaceaeOther
Doe et al. (2003), Li et al. (2009), Matos et al. (2009)
Citrus aurantium (sour orange)RutaceaeOther
Citrus hystrix (mauritius bitter orange)RutaceaeUnknown
Citrus jambhiri (rough lemon)RutaceaeOther
Citrus latifolia (tahiti lime)RutaceaeOther
Li et al. (2009), Cellier et al. (2014)
Citrus limettioides (palestine sweet lime)RutaceaeUnknown
Citrus limon (lemon)RutaceaeOther
Li et al. (2009), Shimwela et al. (2016)
Citrus limonia (mandarin lime)RutaceaeUnknown
Dung et al. (2009), Badaracco et al. (2017)
Citrus macropteraRutaceaeOther
Citrus maxima (pummelo)RutaceaeOther
Citrus medica (citron)RutaceaeOther
Doe et al. (2003), Deng et al. (2008b)
Citrus paradisiOther
Citrus reticulata (mandarin)RutaceaeMain
Doe et al. (2003), Cellier et al. (2014)
Citrus sinensis (sweet orange)RutaceaeMain
Duan et al. (2008), Li et al. (2009), Cellier et al. (2014), Shimwela et al. (2016), Badaracco et al. (2017)
Clausena indicaRutaceaeOther
Clausena lansium (wampi)RutaceaeOther
Cleome rutidosperma (fringed spiderflower)CapparaceaeWild host
Limonia acidissima (elephant apple)RutaceaeOther
Pisonia aculeataNyctaginaceaeWild host
Solanum lycopersicum (tomato)SolanaceaeUnknown
Trichostigma octandrumPhytolaccaceaeWild host
Triphasia trifolia (limeberry)RutaceaeOther

Growth Stages

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Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

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The first symptom of huanglongbing is usually the appearance of a yellow shoot on a tree (hence the name huanglongbing, which literally means ‘yellow dragon disease’). Meanwhile, root decline follows. In early stages of symptom development, the blotchy mottle symptom, yellow shoots and hardened leaves are common. With disease progress, secondary symptoms such as zinc or manganese deficiency, corky veins, upright small leaves, twig dieback and thin canopy become more obvious. With disease progression, the fruits are often small, lopsided, can have a sour or bitter taste and are poorly coloured (hence the origin of the name greening). They often contain aborted seeds. Similar fruit symptoms are also observed with Citrus tristeza virus (CTV) infection. The lifespan of infected trees is shortened.

List of Symptoms/Signs

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SignLife StagesType
Fruit / abnormal patterns
Fruit / abnormal shape
Fruit / premature drop
Fruit / reduced size
Growing point / dieback
Growing point / discoloration
Growing point / dwarfing; stunting
Leaves / abnormal colours
Leaves / abnormal forms
Leaves / abnormal patterns
Leaves / yellowed or dead
Whole plant / discoloration
Whole plant / dwarfing
Whole plant / early senescence
Whole plant / plant dead; dieback

Biology and Ecology

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Ca. L. spp.’ have undergone reductive evolution. The genome sizes of ‘Ca. Liberibacter spp.’ range from c.1.2 Mbp to 1.5 Mbp (Leonard et al., 2012; Thapa et al., 2020). The genome sizes for ‘Ca. L. asiaticus’, ‘Ca. L. americanus’ and ‘Ca. L. africanus’ are approximately 1.23 Mb (Duan et al., 2009), 1.18 Mb (Wulff et al., 2014) and 1.19 Mb (Lin et al., 2015), respectively.

Notes on Natural Enemies

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The vector Diaphorina citri is parasitized by Tamarixia radiata in Africa, Réunion, Mauritius and Guadeloupe and by Diaphorencyrtus aligarhensis in Florida, USA. T. radiata and D. aligarhensis were reported to attack D. citri in Punjab, Pakistan (Khan et al., 2014). The two natural enemies were later used in California, USA, to control D. citri (Hoddle, 2012). In addition, four coccinellids (Coleoptera: Coccinellidae), one syrphid (Diptera: Syrphidae), two parasitoids (Hymenoptera) and two spiders (Araneae) were determined as natural enemies of D. citri in Iran (Rakhshani and Saeedifar, 2013).

Means of Movement and Dispersal

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In the 1960s, citrus HLB was shown to be transmitted by two insects: the African citrus psyllid, Trioza erytreae, in Africa (Mcclean and Oberholzer, 1965) and the Asian citrus psyllid, Diaphorina citri, in Asia (Capoor et al., 1967). Experimentally, both species of psyllid have been shown to transmit both ‘Ca. L. asiaticus’ and ‘Ca. L. africanus’ (Massonie et al., 1976Lallemand et al., 1986). The bacteria are transmitted by psyllids as they feed. ‘Ca. L. asiaticus’ and ‘Ca. L. americanus’ are transmitted by the adults of the citrus psyllid D. citri (Bové, 2006). Transmission of ‘Ca. L. asiaticus’ by D. citri is propagative and circulative. Psyllid nymphs are more efficient in ‘Ca. L. asiaticus’ acquisition than adults, and adult D. citri acquiring ‘Ca. L. asiaticus’ as nymphs are more efficient in transmission than adults that acquired ‘Ca. L. asiaticus’ as adults (Pelz-Stelinski et al., 2010). Vertical transmission (transovarial) allows ‘Ca. L. asiaticus’ to be transmitted from female D. citri to their offspring in low amounts (Kelley and Pelz-Stelinski, 2019). In addition, ‘Ca. L. asiaticus’ can be sexually transmitted from infected male D. citri to uninfected females at a low rate (<4%) during mating (Mann et al., 2011).

Ca. L. asiaticus’ can be transmitted by plant materials via grafting. ‘Ca. L. asiaticus’ is present in leaf, root, stem, flower, fruit, trunk and seed coat, in which phloem tissues are present, of citrus plants. It can also infect many ornamental rutaceous species (e.g. Murraya spp.), even though the detailed locations in those plants remain to be characterized.

Seedborne Aspects

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Ca. L. asiaticus’ is present in seed coats, but not in endosperm and embryo (Tatineni et al., 2008; Hilf et al., 2013). Despite its presence in seed coats, it was reported that ‘Ca. L. asiaticus’ cannot be transmitted through infected citrus seed (Hartung et al., 2010).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
HorticultureDeliberate by locals Yes
Industrial purposesFruit industries that decide to establish their own orchards from imported cuttings Yes
Live food or feed tradeCountry markets at border points Yes Yes
Nursery tradeDeliberate introductions within countries Yes
Off-site preservation Genetic resource conservation within and between collaborating countries Yes Yes
People sharing resourcesDeliberate between friends and family Yes
ResearchResearch organisations Yes
SmugglingTourists Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
GermplasmResearch Yes
Land vehicles Yes
Plants or parts of plants Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Fruits (inc. pods) Yes Pest or symptoms usually invisible
Leaves Yes Pest or symptoms usually invisible
Seedlings/Micropropagated plants Yes Pest or symptoms usually invisible
Stems (above ground)/Shoots/Trunks/Branches Yes Pest or symptoms usually invisible
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
True seeds (inc. grain)

Vectors and Intermediate Hosts

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VectorSourceReferenceGroupDistribution
Diaphorina citriCABI/EPPO (2012)Insect

Impact

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Huanglongbing has been regarded as one of the most important threats to global commercial and sustainable citrus production (Garnier et al., 2000Duan et al., 2009; ANR, 2010; Ammar et al., 2011; Islam et al., 2012). It is estimated that globally more than 60 million trees had been destroyed by the disease by the early 1990s (Aubert, 1993). In West Java alone it was estimated that from 1960 onwards no less than 3 million trees were destroyed by Huanglongbing, and the destruction is still taking place (Tirtawadja, 1980). In Asia, approximately 100 million infected citrus trees have been destroyed by this disease, and 1 million trees were eliminated in Brazil in 2004 (Gottwald et al., 2007Duan et al., 2009).

Economic Impact

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Citrus HLB is the most detrimental citrus disease worldwide. It causes billions of dollars annual economic losses worldwide. HLB was first reported in Florida, USA, in 2005 and is the major contributor for the decrease of citrus production in Florida. Compared to the pre-HLB era, citrus production in Florida in 2019 has decreased by 74% (Singerman and Rogers, 2020). Since 2004, HLB has eliminated 54.2 million citrus trees in Brazil. In China, approximately 51.61 million citrus trees were removed in the Gannan citrus-producing region of China alone (Yuan et al., 2021). HLB has significantly increased production costs (Singerman and Rogers, 2020).

Risk and Impact Factors

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Invasiveness
  • Invasive in its native range
  • Has a broad native range
  • Abundant in its native range
  • Highly adaptable to different environments
  • Is a habitat generalist
  • Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
  • Benefits from human association (i.e. it is a human commensal)
  • Reproduces asexually
  • Has high genetic variability
Impact outcomes
  • Damaged ecosystem services
  • Host damage
  • Increases vulnerability to invasions
  • Loss of medicinal resources
  • Negatively impacts agriculture
  • Negatively impacts livelihoods
  • Reduced native biodiversity
  • Threat to/ loss of endangered species
  • Threat to/ loss of native species
  • Negatively impacts trade/international relations

Diagnosis

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A diagnostic protocol for ‘Ca. L. africanus’, ‘Ca. L. americanus’ and ‘Ca. L. asiaticus’, and for their detection in their psyllid vectors Diaphorina citri and Trioza erytreae has been published by EPPO (2014). The protocol involves detection based on the disease symptoms and molecular tests (PCR), and reporting and documentation.

Here diagnosis of HLB via detection of ‘Ca. L. asiaticus’, ‘Ca. L. africanus’ and ‘Ca. L. americanus’ based on PCR and quantitative PCR are briefly described.

Ca. L. asiaticus’ and ‘Ca. L. africanus’ can be identified by PCR-amplification of their 16S rDNA followed by restriction enzyme (XbaI) analysis of the amplified DNA (Jagoueix et al., 1996). Currently, quantitative TaqMan PCR using 16S rDNA-based TaqMan primer-probe sets specific to ‘Ca. L. asiaticus’, ‘Ca. L. africanus’ and ‘Ca. L. americanus’ is commonly used for regulatory purposes (Li et al., 2006). In addition, TaqMan qPCR targeting ribosomal protein genes as well as SYBR Green qPCR targeting different ‘Ca. L. asiaticus’ sequences have been reported and used (Wang et al., 2006; Kogenaru et al., 2014). Quantitative reverse transcriptional PCR (qRT-PCR) targeting 16S rRNA has been shown to be ten times more sensitive than qPCR targeting 16S rDNA (Kim and Wang, 2009).

Detection and Inspection

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Huanglongbing is easy to recognize due to its characteristic blotchy mottle symptoms on leaves. Yellow shoots are also obvious. Both blotchy mottling and yellowing symptoms are early symptoms for detection and inspection of HLB. However, other citrus disorders might generate similar symptoms (see Symptoms). For confirmation purposes, quantitative PCR or PCR is required by the regulatory agencies (Li et al., 2006).

Similarities to Other Species/Conditions

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Disease symptoms are almost identical to, and can be confused with, those of the other strains of Liberibacter causing huanglongbing. Mixed infections of two of the strains have been reported (Coletta-Filho et al., 2005). Leaf symptoms also resemble nutrient deficiencies, particularly deficiencies of zinc, calcium and nitrogen. But those symptoms are usually secondary symptoms and appear much later than blotchy mottling and yellowing.

Blotchy mottle is the most characteristic symptom of huanglongbing but is not specific to it. Stubborn disease (Spiroplasma citri), severe forms of Citrus tristeza virus (CTV), species of Phytophthora, waterlogging and the use of marcots can produce similar blotchy mottle patterns. Symptoms of zinc deficiency are also associated with the early stages of citrus blight (a disease of unconfirmed aetiology). However, ‘Ca. L. asiaticus’ does not induce the xylem dysfunction and wilting observed in blighted trees.

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

In areas where HLB is not present, effective quarantine measures are essential to prevent the introduction of ‘Ca. L. asiaticus’, or the vector. Furthermore, the possibility exists that the vector could be introduced 'naturally' or through alternative hosts such as Murraya spp. This poses a potential threat because the adult Diaphorina citri can transmit the disease, which can persist in the vector for up to 3 months (Graca and Korsten, 2004). When only the insect vector is present while ‘Ca. L. asiaticus’ is absent, biological control of psyllids is commonly used. In the absence of hyperparasitic wasps, the parasitic wasp Tamarixia radiata significantly reduced populations of D. citri, the vector of HLB, on the Indian Ocean island of Réunion, leaving a strongly limited population of the vector (Aubert and Quilici, 1984).

For citrus-producing areas with low HLB incidence, region-wide comprehensive implementation of roguing infected trees, tree replacement and insecticide applications has been reported to successfully control citrus HLB (Yuan et al., 2021).

For citrus-producing areas where HLB is endemic, treating HLB-diseased trees with horticultural approaches such as optimized application of macronutrients (N, P and K) and micronutrients (e.g. B, Cu, Fe, Mn, Mo, Ni, Se and Zn), growth hormones and psyllid management has shown effect to mitigate the impact of HLB. In addition, growing citrus trees inside screened containments has been shown to be economically viable in HLB endemic citrus-producing regions.

References

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27/03/13 Updated by:

Esther Arengo, National Agricultural Research Laboratories, Uganda

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