Incidence of Huanglongbing-Associated ‘CandidatusLiberibacter Asiaticus’ inDiaphorina citri(Hemiptera: Psyllidae) Collected from Plants for Sale in Florida

Abstract

We question widely held assumptions about the origins of huanglongbing (HLB) and the genus Citrus [Rutaceae: Aurantioideae: Aurantieae] and propose alternative hypotheses. In doing so, we comment on recent changes in the systematics of the family Rutaceae, particularly the subfamily Aurantioideae.The widely accepted assumptions are that the genus Citrus originated in China and that HLB originated, in Citrus, in the same region. We present evidence that suggests: that Citrus evolved in Australasia (where HLB and its vectors do not occur naturally); and that 'Candidatus Liberibacter' forms known to infect Citrus and other Rutaceae originated in Africa in association with the African citrus psyllid, Trioza erytreae (del Guercio) [Hemiptera: Sternorrhyncha: Triozidae] and one or more species of Vepris [Rutaceae: Rutoideae].Other evidence suggests that the 'Ca. Liberibacter' forms that cause HLB spread from Africa to India in infected citrus budwood or plants, then from India to Guangdong in China (directly or indirectly) about 1930, then from Guangdong to Taiwan, the Philippines, Indonesia, Malaysia after 1945, and subsequently more widely to other countries.Ours view that HLB did not originate in China is supported by published literature and other documents that have not been cited in major reviews of HLB and its vectors, particularly the Asiatic citrus psyllid, Diaphorina citri Kuwayama [Hemiptera: Sternorrhyncha: Psyllidae].Recent hypothesis about the origins of 'Ca. Liberibacter' in Gondwana 100-300 million years ago, and the possible role of parasitic plants in natural spread of the bacteria, are considered. Our views are continually being revised as new information, including historical records, becomes available.

Huanglongbing: An overview of a complex pathosystem ravaging the world's citrus

“…Psyllids have been tested for Liberibacter species for a long time (Bové et al ), but psyllid testing was done only to confirm presence of the bacteria in the vectors. Manjunath et al () were the first to use psyllid testing to look at large‐scale epidemiological questions and as a result, a lot has been learned about the distribution and movement of HLB in Florida (Halbert et al ; Halbert et al ). Las could be found in psyllids months before symptoms appeared on infected plants.…”

“…Finally, testing psyllids has proven valuable in assessing the status of plants for sale (Halbert et al ). Psyllids testing positive for HLB were found an average of 9 months prior to the discovery of positive‐testing symptomatic plants in retail venues.…”

“…In 2008, about halfway through the sampling period, new regulations were enacted by DPI that required regular monthly inspections and enclosed structures for all phases of citrus propagation (but not retail sales). As a result, the percentage of psyllid samples from citrus propagation facilities dropped dramatically in 2008 and remained low in the final year of the project (Halbert et al ). The new transmission mechanism described in Lee et al () explains the high numbers of positive psyllids in retail environments.…”

“…Human‐assisted movement occurs via plants for sale (Halbert et al ) and transportation, especially movement of unprocessed fruit (Halbert et al ). The rapid spread in Florida probably cannot be accounted for by natural spread of infected psyllids alone.…”

Detection of Citrus Huanglongbing-Associated ‘Candidatus Liberibacter asiaticus’ in Citrus and Diaphorina citri in Pakistan, Seasonal Variability, and Implications for Disease Management

“…The recent rapid spread of HLB in Brazil and Florida (18,28,54) and its impact on these two major citrus industries in a short span of time has led to increased concern among growers, regulators, and researchers. An analysis of the situation in Pakistan may be useful in understanding the dynamics of citrus HLB in a situation where citrus, the psyllid vector, and the pathogen may have coexisted for more than a century.…”