Insecticide resistance in field populations of Asian citrus psyllid in Florida

Tiwari, Siddharth; Mann, Rajinder S.; Rogers, Michael E.; Stelinski, Lukasz L.

doi:10.1002/ps.2181

Cited by 308 publications

(335 citation statements)

References 36 publications

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“…A psyllid colony was maintained in the same greenhouse using the same cultivar. All psyllids originated from a long-term colony that has been used in previous research (18,45). The colony used in these tests required periodic infusions of psyllids from the original colony, but at least 1 week elapsed between colony augmentation and the removal of psyllids for experiments.…”

Section: Diaphorina Citri Coloniesmentioning

confidence: 99%

A Plant Bacterial Pathogen Manipulates Its Insect Vector's Energy Metabolism

Killiny

Hijaz

Ebert

et al. 2017

Appl Environ Microbiol

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Insect-transmitted plant-pathogenic bacteria may alter their vectors' fitness, survival, behavior, and metabolism. Because these pathogens interact with their vectors on the cellular and organismal levels, potential changes at the biochemical level might occur. "Candidatus Liberibacter asiaticus" (CLas) is transmitted in a persistent, circulative, and propagative manner. The genome of CLas revealed the presence of an ATP translocase that mediates the uptake of ATP and other nucleotides from medium to achieve its biological processes, such as growth and multiplication. Here, we showed that the levels of ATP and many other nucleotides were significantly higher in CLas-infected than healthy psyllids. Gene expression analysis showed upregulation for ATP synthase subunits, while ATPase enzyme activity showed a decrease in ATPase activity. These results indicated that CLas stimulated Diaphorina citri to produce more ATP and many other energetic nucleotides, while it may inhibit their consumption by the insect. As a result of ATP accumulation, the adenylated energy charge (AEC) increased and the AMP/ATP and ADP/ATP ratios decreased in CLas-infected D. citri psyllids. Survival analysis confirmed a shorter life span for CLas-infected D. citri psyllids. In addition, electropenetrography showed a significant reduction in total nonprobing time, salivation time, and time from the last E2 (phloem ingestion) to the end of recording, indicating that CLas-infected psyllids were at a higher hunger level and they tended to forage more often. This increased feeding activity reflects the CLas-induced energetic stress. In conclusion, CLas alters the energy metabolism of its psyllid vector, D. citri, in order to secure its need for energetic nucleotides.IMPORTANCE Insect transmission of plant-pathogenic bacteria involves propagation and circulation of the bacteria within their vectors. The transmission process is complex and requires specific interactions at the molecular and biochemical levels. The growth of the plant-pathogenic bacteria in the hemolymph of their vectors indicated that the hemolymph contains all the necessary nutrients for their growth. In addition to nutrients, "Candidatus Liberibacter asiaticus" (CLas) can take up energetic nucleotides, such as ATP, from its vector, Diaphorina citri, using ATP translocase. In this study, we found that the CLas pathogen manipulates the energy metabolism of its insect vector. The accumulation of ATP in CLas-infected D. citri psyllids indicated that CLas induces ATP production to fulfill its need for this energetic compound. As a result of ATP accumulation, a shorter life span and altered feeding behavior were observed. These findings increase our knowledge of insect transmission of the persistent-circulative-propagative type of plant pathogens vectored by insects.KEYWORDS huanglongbing, Diaphorina citri, "Candidatus Liberibacter asiaticus," energy metabolism, ATP, adenylated energy charge, HPLC, electric penetration graph, electropenetrography

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Section: Diaphorina Citri Coloniesmentioning

confidence: 99%

A Plant Bacterial Pathogen Manipulates Its Insect Vector's Energy Metabolism

Killiny

Hijaz

Ebert

et al. 2017

Appl Environ Microbiol

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“…Overall, the insecticide treatments did not reduce HLB spread compared to the untreated controls. Indeed, the insecticides commonly used for the control of the psyllid were not as effective as expected (Ichinose et al 2010), and even induced insecticide resistance in field populations of D. citri in Florida (Tiwari et al 2011). For each of the treatments, the Ct values of Las varied over time but generally decreased from November 2008 to October 2011 ( Fig.…”

Section: Discussionmentioning

confidence: 96%

“…Many different insecticides are available for managing the Asian citrus psyllid, and insecticides are rotated to limit the development of resistance in the psyllids. Nevertheless, insecticide resistance, in particular to imidacloprid, has already developed in field populations of D. citri in Florida (Tiwari et al 2011), and negative side-effects on the parasitoid Tamarixia radiata, introduced into Florida for biological control of the psyllid, has also been observed (Hall and Nguyen 2010). Moreover, secondary pest outbreaks of various citrus scales and mealy bugs can be a real threat resulting from intensive insecticide use for psyllid control (Wakgari and Giliomee 2003).…”

Section: Introductionmentioning

confidence: 97%

Relation between plant nutrition, hormones, insecticide applications, bacterial endophytes, and Candidatus Liberibacter Ct values in citrus trees infected with Huanglongbing

et al. 2013

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Intensive insecticide and nutrient management have been attempted worldwide to reduce citrus huanglongbing (HLB) symptom development and yield loss. However, effects of insecticide and nutrient applications on HLB have been poorly understood. Leaf nutrients, jasmonic and salicylic acid contents, cycle threshold (Ct) values of Ca. Liberibacter asiaticus (Las), and community structure of endophytic α-proteobacteria were evaluated after insecticide treatment, 'nutrition' treatment (including systemic resistance inducing agents), or both in comparison with a control in a two-factor field experiment in 2008-2012. Leaf N, Mn, Zn and B significantly increased whilst Cu decreased after nutrient applications. Salicylic acid significantly increased in old leaves treated with insecticides, nutrients or both, and in young leaves treated with nutrients only. The jasmonic acid concentration was highest after the nutrition treatment in both old and young leaves. Ct values of Las and leaf area and weight significantly increased after long-term nutrient applications in 2011 and/or 2012. Redundancy analysis of the endophytic α-proteobacteria community structure indicated that the communities were mainly separated according to nutrient applications, which were positively associated with Ct values of Las and Ca, Mn, Zn, B, Mg, and Fe contents in leaf samples collected in 2012. Thus, effects of insecticides on HLB were significant in the early 2-year period whilst nutrients had significant effects on Las content and leaf size and weight after at least 3 years of application.

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“…Since detection of HLB in Florida, control of D. citri with synthetic, broad-spectrum insecticides has become prevalent and many growers spray monthly. Evidence for resistance to neonicotinoids, pyrethroids, and organophosphates has emerged in some Florida ACP populations (Tiwari et al, 2011).…”

Section: Introductionmentioning

confidence: 99%