BIOLOGY, HISTORY AND WORLD STATUS OF HUANGLONGBING
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Biology, history and world status of huanglongbing (Hermosillo, Sonora. México 2008)
BIOLOGY, HISTORY AND WORLD STATUS OF HUANGLONGBING
John V. da Graça
Texas A & M University-Kingsville, Citrus Center, Weslaco TX 78596, USA
Keywords: greening – citrus –candidatus Liberibacter – psyllids
ABSTRACT
Citrus Huanglongbing (HLB), or greening disease, is considered to be one of the most serious diseases of citrus,
having been responsible for the loss of tens of millions of trees. It is caused by phloem-limited bacteria of the
genus Candidatus Liberibacter which are transmitted by citrus psyllids. The first record of HLB-like symptoms
came from India in the 18th century. Prior to this, the pathogens were probably present in native rutaceous plants,
and as citrus trees were planted in new areas, psyllids may have transmitted the disease to them. HLB was
noticed by citrus farmers in southern China in the late 19th century; infected citrus may have been transported to
China from India by sea. In South Africa, greening was first reported in the 1920s, and may also have originated
from native rutaceous trees. Several non-citrus rutaceous plants are known to be hosts of liberibacter (eg.
Murraya paniculata/exotica, Clausena lansium, Atalantia (Severinia) buxifolia, Toddalia lanceolata, Limonia
acidissma). The Asian form is caused by Ca. L. asiaticus, a temperature-tolerant species which is transmitted
naturally by Diaphorina citri. In Asia, it is now found from southern Japan and Indonesia in the east, westwards to
Pakistan, as well as in Saudi Arabia, Mauritius, Reunion and most recently in Papua New Guinea. African HLB,
which is naturally transmitted by a temperature-sensitive psyllid Trioza erytreae, now occurs at higher cooler
elevations throughout eastern and southern Africa, and in Yemen and the Indian Ocean islands. Although D. citri
has been present in Brazil for many years, HLB was only confirmed there in 2004. Most trees have been found to
be infected by a previously unknown liberibacter, now named Ca. L. americanus, but a small number carry Ca. L.
asiaticus which is now increasing in incidence, suggesting that the environment is more suited to the temperature-
tolerant Asian form. While the Asian species was probably imported from Asia, it is not yet known where Ca. L.
americanus originated. D. citri has spread beyond Brazil to other countries in the Americas, and was found in
Florida in 1998. Asian HLB was confirmed there in 2005, but the extent of the disease suggests it had been
present for some years. Cuba reported the detection of Asian HLB in 2007. The likelihood of the spread of HLB to
places which already have psyllids (eg. Argentina, Mexico, Texas, Costa Rica, various Caribbean nations) is high,
and nearby regions which are currently psyllid-free (eg. California, Australia) are also at risk. The picture is
complicated by the reason report of phytoplasma-associated HLB-like symptoms in Brazil, recalling the
descriptions of Australian citrus dieback which resembles HLB.
BIOLOGÍA, HISTORIA Y SITUACIÓN MUNDIAL DEL HUANGLONGBING
Palabras claves: enverdecimiento – candidatus Liberibacter – psilidos
RESUMEN
La enfermedad Huanglongbing de los cítricos (HLB) o enverdecimiento, está considerada a ser una de las
enfermedades mas serias de los cítricos. Ha sido la responsable de la pérdida de diez millones de árboles. Es
causada por la bacteria limitada al floema del género Candidatus Liberibacter que es transmitida por el psilido
asiático de los cítricos. El primer reporte de síntomas de HLB se dió en la India en el siglo 18. Antes de esto, el
patógeno estaba probablemente presente en plantas nativas de rutaceaes y cuando los cítricos se plantaron en
áreas nuevas, los psilidos pudieron haber transmitido la enfermedad a ellos. HLB fué reportado por citricultores
del sureste de China a finales del siglo 19; los cítricos infectados pudieron haber sido transportados a China desde
la India por mar. En Africa del Sur (Suráfrica) el enverdecimiento fué reportado por primera vez en los años 20’s y
pudo también haber sido originado de árboles nativos de rutaceaes. Algunas plantas Rutaceaes no cítricas son
conocidas por ser hospederas de liberibacter (eg. Murraya paniculata/exotica, Clausena lansium, Atalantia
(Severinia) buxifolia, Toddalia lanceolata, Limonia acidissma). La forma asiática es causada por Ca. L. asiaticus,
una especie tolerante a la temperatura, la cual es trasmitida naturalmente por Diaphorina citri. En Asia, Esta se ha
encontrado ahora en el Sureste de Japón y en el este de Indonesia, en el paso oeste de Pakistán, así como
también en Arabia Saudita, Mauritania y más recientemente en Papua Nueva Guinea. El HLB en Africa es
I Taller Internacional sobre Huanglongbing de los cítricos (Candidatus Liberibacter 1
spp) y el psílido asiático de los cítricos (Diaphorina citri)Biology, history and world status of huanglongbing (Hermosillo, Sonora. México 2008)
naturalmente transmitido por un psilido sensible a la temperatura Trioza erytreae. Este ocurre actualmente en
elevaciones altas con temperaturas frescas desde el este y sur de Africa, en Yemen hasta las islas del Océano
Índico. Aunque D. citri ha estado presente en Brasil desde hace algunos años, HLB fue confirmado en el 2004. La
mayoría de los árboles se han encontrado infectados por un liberibacter desconocido anteriormente y ahora
llamado Ca. L. americanus, y muy pocos poseen Ca. L. asiaticus el cual ahora está incrementando su incidencia.
Ello sugiere que el medio ambiente es más adecuado para la forma asiática tolerante a la temperatura. Aunque las
especies Asiáticas fueron probablemente importadas de Asia, no se sabe aún donde se originó Ca. L. americanus.
D. citri se ha dispersado desde Brasil a otros países de América y se encontró en Florida en 1988. HLB Asiática
fué confirmada hasta el 2005, pero lo extenso de la enfermedad sugiere que ésta ha estado presente desde hace
algunos años. Cuba reportó la presencia HLB asiática en el 2007. La probabilidad de dispersión de HLB a lugares
donde se tiene la presencia de psilidos (p. ej. Argentina, México, Texas, Costa Rica, varios países del Caribe) es
alta y en la regiones cercanas que actualmente están libres del psilido (p. ej. California y Australia) están también
en riesgo. El panorama es complicado por las razones reportadas de fitoplasmas asociados a los síntomas de HLB
en Brasil que ha provocado la revisión de los síntomas de la muerte regresiva de los cítricos en Australia la cual se
parece a HLB.
INTRODUCTION
During the 18th and early 19th centuries, Phytophthora was the most destructive pathogen of citrus
(Fawcett, 1936). Then after the 1930’s, Citrus tristeza virus became the most destructive pathogen of
citrus, causing the death of over 100 million trees on sour orange rootstock worldwide (Román et al.,
2004), and additional losses through stem pitting disease. Citrus huanglongbing (HLB), or greening, is
now poised to challenge tristeza for this unenviable distinction. Before the introduction of HLB into the
western hemisphere sometime in the decade before 2004, it was estimated that it had been
responsible for the loss of over 60 million trees (Aubert, 1993), but with current losses in Brazil and
Florida, the present destruction total will have increased greatly, and more losses are anticipated as
the disease threatens new areas.
Currently, three species of bacteria belonging to the Candidatus Liberibacter genus have been
identified as causal agents of HLB, and transmission by two species of citrus psyllids have been
identified. Many efforts have been made over the years to unravel the complex interaction of hosts,
pathogen, vectors and climate, and it is clear that much more still needs to be done.
HISTORY
The first puzzle surrounding HLB is where did it come from? Citrus has been grown as an agricultural
crop for over 4,000 years in China while India is considered to be second in citricultural antiquity
(Burke, 1967), yet there was no record of any disease resembling this disease until 260 years ago.
Perhaps the pathogens were absent from these countries, and were only introduced in more recent
times, or they were present in wild rutaceous plants, and only infected citrus as commercial citriculture
expanded. In India, garden citriculture flourished for centuries, with a modern commercial industry
only being developed in the last century or two.
In South Africa, citrus was first planted in the Western Cape in the 17th century (Burke, 1967), but
greening was not observed until the early part of the 20th century after citriculture expanded into the
northern parts of the country (Oberholzer et al., 1965). As in Asia, the African pathogen was possibly
present in indigenous rutaceous trees, and was introduced into the newly established citrus orchards
by the insect vector.
It appears that the first description of HLB may have been recorded in the central provinces of India as
“dieback” in the middle of the 18th century (Capoor, 1963). Its incidence at the time may have been
limited in extent, but during the 18th century it was recorded in Assam, and by 1912 was a severe
2 I Taller Internacional sobre Huanglongbing de los cítricos (Candidatus Liberibacter
spp) y el psílido asiático de los cítricos (Diaphorina citri)Biology, history and world status of huanglongbing (Hermosillo, Sonora. México 2008)
problem in Bombay province. Although Capoor (1963) opined that Citrus tristeza virus was probably
the cause, Raychaudhuri et al. (1969) showed that dieback was the same as greening.
HLB was observed in southern China in the late 19th century in Guangdong Province (Zhao, 1981), and
later spread to other areas; by 1935 it had become a severe problem (Lin, 1956). It has been
suggested that the disease may have been brought to China from India along the sea trade routes
(Beattie et al., 2005). During the first half of the 20th century, the disease was recorded in many Asian
countries, including Taiwan (Ôtake, 1980), Philippines (Lee, 1921) and Indonesia (Aubert et al., 1985).
This suggests that infected plant material may have been taken to several areas either directly from
India or from China, and that further dissemination then occurred through infected propagation
material and insect transmission.
But where did HLB come from before the 18th century? Beattie et al. (2005) first suggested that
common ancestors of the causal bacteria and the insect vectors may have co-existed in the Gondwana
land mass which later separated, resulting in the evolution of the African and Asian species of both
pathogen and vector. Then they revised this hypothesis, and suggested that HLB has an African origin,
and was introduced to India by Portuguese 300-500 years ago (Beattie et al., 2006). This has been
rejected by Teixeira et al. (2008a) who have calculated that the three known species of HLB bacteria
separated millions of years ago.
BIOLOGY
Current evidence indicates that HLB is caused by at least three species of a so far non-culturable
bacterial genus, Candidatus Liberibacter. These are phloem-limited bacteria, with very thin cell walls
allowing them to pass through the narrow sieve pores. The Ca. genus belongs to the α subdivision of
the class Protobacteria. The Asian form of the disease is associated with Ca. L. asiaticus, which exists
as several strains. It is heat tolerant, and is able to survive at temperatures above 30C for extended
periods. The African form is cause by Ca. L. africanus, which is suppressed by high temperatures; a
closely related sub species, Ca. L. africanus subsp. capensis, has been discovered in an indigenous
rutaceous tree, the Cape chestnut (Calodendrum capense). In Brazil, HLB is associated with two
liberibacter; most infected trees carry a previously unknown species which has been called Ca. L.
americanus, with a few samples testing positive for Ca. L. asiaticus (Teixeira et al., 2005a). The new
species appears to have similar temperature sensitivity to that of Ca. L. africanus, and recent reports
indicate that the incidence of the Asian form is increasing (Coletta-Filho et al., 2008). The discovery of
a new species raises the questions on origins again – is it an indigenous South American species which
spread from a local rutaceous tree to citrus, or was it introduced along with the Asian species? The
insect vector was present in Brazil for many decades before HLB was detected (Lima, 1942), and no
indigenous HLB host has been identified, but Ca. L. americanus has not been reported elsewhere. The
increasing incidence of Ca. L. asiaticus suggest the americanus species is not a good competitor, and
may exist elsewhere at very low incidence.
The vector of HLB in Asian and the Americas is the Asian citrus psyllid, Diaphorina citri, while African
HLB is transmitted in nature by another psyllid species, Trioza erytreae. These two species share the
temperature preferences of the bacteria they transmit naturally, but both have been shown
experimentally to transmit other species (Lallemand et al., 1986; Massonie et al., 1976). Psyllids can
acquire liberibacter as both adults and third to fifth instar nymphs (Capoor et al., 1974). Reports on
acquisition times, latent periods and transmission times vary widely; these were all conducted before
sensitive molecular detection methods were available, and the research needs to be repeated. The
question of transovarial passage also needs to be clearly answered. The fact that large numbers of
liberibacter can be observed in psyllids by electron microscopy (Moll & Martin, 1973), it is assumed
that it multiplies in the insect.
I Taller Internacional sobre Huanglongbing de los cítricos (Candidatus Liberibacter 3
spp) y el psílido asiático de los cítricos (Diaphorina citri)Biology, history and world status of huanglongbing (Hermosillo, Sonora. México 2008)
In addition to psyllid transmission, HLB can be experimentally transmitted by grafting and by dodder,
and there is evidence that a low number of seedlings derived from infected trees carry liberibacter (M.
Irey, pers. comm.).
The symptoms of HLB are similar irrespective of the causal liberibacter species. The most characteristic
symptom is the foliar blotchy mottle. The first gross symptom often seen is the yellow shoot, the
leaves of which are mottled. Leaves can also be thicker, with enlarged corky veins, and zinc-like
deficiency can develop. Leaf drop and twig dieback follow. Excessive fruit drop occurs, and remaining
fruit are often lop-sided, remain green at the stylar end, contain aborted seed and discolored vascular
bundles, and can have a bitter taste. The Asian form has been reported to cause the death of young
trees (Gottwald et al., 2007).
In the History section above, the possibility of HLB originating from indigenous trees was raised. Initial
attempts to infect a range of such species via infective psyllids was unsuccessful (van Vuuren & da
Graça, unpublished data). Diagnosis technology was limited at that time to symptomology, electron
microscopy and fluorescent marker detection, which were all negative. Subsequently a number of
rutaceous hosts have been identified using molecular detection assays. These include Toddalia
lanceolata (Vepris undulata) for African HLB (Korsten et al., 1996), Severinia (Atalantia) buxifolia (Su
et al., 1995; Deng et al., 2008), Limonia acidissima, Clausena lanceum (wampee)(Deng et al., 2007a)
and Murraya spp. (orange jasmine) (Deng et al., 2007b). No symptoms were reported for T.
lanceolata, but the others all were reported to show foliar symptoms.
WORLD SITUATION
During the 20th century up to the 1980s, Asian HLB spread through much of the citriculture regions of
south and southeast Asia, so that disease became endemic from Pakistan in the west through to
southern Japan and Indonesia/Philippines in the east (da Graça, 1991). It also appeared in the Arabian
peninsula (Bové & Garnier, 1984). It is difficult to know when the disease entered each country and
from where it came, but the result is that HLB has become endemic over a wide area in Asia. More
recently, HLB has moved into neighboring countries such as Timor Leste and Papua New Guinea
(Weinert et al., 2004.). Neighboring countries, such as Iran where D. citri already exists (Bové et al.,
2000), and Australia where psyllids appeared once in the 1920s and were eradicated (Bellis et al.,
2005), are now at very high risk.
African HLB now exists throughout southern Africa, and through East Africa to the Red Sea and in the
highlands of Yemen. The first reports of the disease were from South Africa, but this does not
necessarily mean it originated there. It is known, however, the budwood was sent from South Africa to
several pre-independence anglophone countries, resulting in high CTV incidence compared to
francophone areas (Mendel, 1968) – however the apparent absence of HLB in West Africa, does not
support this, and one should consider the possibility that Ca. L. africanus was already present in East
Africa in indigenous rutaceous species prior to the introduction of citrus.
The discovery of HLB in Brazil in 2004 (Anon., 2004), followed just a year later but its discovery in
Florida (Halbert, 2005), raised the alert level significantly. The entire citriculture areas of the Americas,
and eventually the Mediterranean, were now alerted to the reality of HLB. The African psyllid has been
recorded on the island of Madeira (Jagoueix et al., 1996), dangerously close to the citrus areas of
Portugal, Spain and Morocco. A new twist was the discovery that most of the Brazilian trees were
infected with a previously unknown species, Ca. L. americanus (Teixeira et al., 2005b). D. citri has
been in Brazil for many decades, without any sign of HLB. It later began to appear in other countries,
and spread to the north especially, into Venezuela, the Caribbean islands, Central America, Mexico,
Florida and Texas (Halbert & Manjunath, 2004). In Brazil it is possible that HLB was introduced in
relatively recent times, perhaps in the 1990s. In Florida, the extent of HLB discovered soon after the
4 I Taller Internacional sobre Huanglongbing de los cítricos (Candidatus Liberibacter
spp) y el psílido asiático de los cítricos (Diaphorina citri)Biology, history and world status of huanglongbing (Hermosillo, Sonora. México 2008)
first find was confirmed, showed that the disease had been disseminated probably by a combination of
human movement of plants, and by psyllids (these being aided by humans moving infested potted
plants). The psyllid had arrived by 1998 (Knapp et al., 1998), but perhaps HLB was already there.
The confirmation of HLB in Florida prompted action in other states. In Texas, where D. citri was
discovered in 2001 (French et al., 2001), immediately began surveys to determine the extent of psyllid
spread, and whether HLB could be detected (da Graça et al., 2007). Arizona and California, where
psyllids are not yet established, have also began to make preparations, conducting surveys, and
drawing up an action plan. The USA and Mexico are also collaborating closely in several areas, such as
in training surveyors and setting up diagnostic facilities.
The latest news is that Asian HLB has been discovered in Cuba (L. Batista, pers. comm.). One could
speculate that infected psyllids from Florida crossed the short distance to Cuba, and infected trees
there. This brings HLB closer to Mexico and its neighbors. The spread of psyllids and HLB is not yet
over, and it is hard to see other regions not acquiring both. Nevertheless, proactive steps can be taken
to minimize the risks and perhaps slow down outbreaks.
Could there be other pathogens causing HLB-like diseases? Recently trees with blotchy mottle were
found in Brazil which were negative for liberibacters, but were infected with a phytoplasma (Teixeira et
al., 2008b). Some years ago, phytoplasmas were associated with Australian citrus dieback, the
symptoms of which were similar to HLB (Broadbent et al., 1976). The symptoms of stubborn, caused
by Spiroplasma citri, while not identical to HLB, do bear some resemblances (Bové & Garnier, 2000).
Perhaps all these phloem limited prokaryotes cause similar disruptions in host cell metabolism resulting
in a common range of symptoms. Clearly, one has to be open minded regarding causal organisms
when one encounters trees with HLB-like symptoms.
It appears that HLB is now well placed to take over the role of the most serious citrus disease
worldwide. Its potential to seriously damage citriculture is not to be taken lightly.
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I Taller Internacional sobre Huanglongbing de los cítricos (Candidatus Liberibacter 7
spp) y el psílido asiático de los cítricos (Diaphorina citri)You can also read
