Psyllid Vectors: From Genetics to Pest Integrated Management

A topical collection in Insects (ISSN 2075-4450). This collection belongs to the section "Insect Pest and Vector Management".

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Editor

Citrus Research and Education Center, Department of Plant Pathology, University of Florida, Lake Alfred, FL 33850, USA
Interests: vector biology; plant pathogen-vector interactions; RNA interference
Special Issues, Collections and Topics in MDPI journals

Topical Collection Information

Dear Colleagues,

Psyllids are plant sap-sucking insects that transmit many plant bacterial pathogens in a persistent propagative and circulative manner. Two groups of bacteria are transmitted by psyllids: members of the genus Candidatus Liberibacter, including Ca. L. asiaticus, the causal agent of Huanglongbing, currently the most destructive disease in citrus, and Ca. L. solanacearum, the causal agent of Zebra chip in tomato and potato; and mollicutes, though there is only one group of phytoplasmas, the 16SrX or apple proliferation group, whose members are transmitted by psyllids. The psyllid vector species of these phytoplasmas are also closely related and all belong to the genus Cacopsylla.

As crops infected with these bacteria cannot be cured, and resistant plant material is not yet available to growers, preventive control measures such as vector control are of paramount importance to limit the spread of these diseases. Thus, detailed knowledge about the genetics, biology, and ecology of the vector species as well as knowledge about the transmission parameters is crucial. This Topical Collection will focus on psyllid–plant–pathogen interactions, including psyllid genetics and biology, factors affecting transmission, and new approaches to psyllid control, blocking transmission and decreasing the dispersal of plant bacterial diseases.

Dr. Nabil Killiny
Collection Editor

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Keywords

  • psyllid
  • vectors
  • pest integrated management
  • molecular interactions
  • Candidatus Liberibacter
  • phytoplasma

Published Papers (8 papers)

2024

Jump to: 2023, 2022, 2021

15 pages, 1190 KiB  
Article
Optimal dsRNA Concentration for RNA Interference in Asian Citrus Psyllid
by Esmaeil Saberi, Mosharrof Mondal, Jorge R. Paredes-Montero, Kiran Nawaz, Judith K. Brown and Jawwad A. Qureshi
Insects 2024, 15(1), 58; https://doi.org/10.3390/insects15010058 - 12 Jan 2024
Viewed by 1075
Abstract
The Asian citrus psyllid (ACP) is a citrus pest and insect vector of “Candidatus Liberibacter asiaticus”, the causal agent of citrus greening disease. Double-stranded RNA (dsRNA) biopesticides that trigger RNA interference (RNAi) offer an alternative to traditional insecticides. Standardized laboratory screening of [...] Read more.
The Asian citrus psyllid (ACP) is a citrus pest and insect vector of “Candidatus Liberibacter asiaticus”, the causal agent of citrus greening disease. Double-stranded RNA (dsRNA) biopesticides that trigger RNA interference (RNAi) offer an alternative to traditional insecticides. Standardized laboratory screening of dsRNA requires establishing the minimal effective concentration(s) that result in effective RNAi “penetrance” and trigger RNAi, resulting in one or more measurable phenotypes, herein, significant gene knockdown and the potential for mortality. In this study, knockdown was evaluated for a range of dsRNA concentrations of three ACP candidate genes, clathrin heavy chain (CHC), vacuolar ATPase subunit A (vATPase-A), and sucrose non-fermenting protein 7 (Snf7). Gene knockdown was quantified for ACP teneral adults and 3rd instar nymphs allowed a 48 h ingestion-access period (IAP) on 10, 50,100, 200, and 500 ng/µL dsRNA dissolved in 20% sucrose followed by a 5-day post-IAP on orange jasmine shoots. Significant gene knockdown (p < 0.05) in ACP third instar nymphs and adults ranged from 12–34% and 18–39%, 5 days post-IAP on dsRNA at 10–500 and 100–500 ng/µL, respectively. The threshold concentration beyond which no significant gene knockdown and adult mortality was observed post-48 h IAP and 10-day IAP, respectively, was determined as 200 ng/µL, a concentration indicative of optimal RNAi penetrance. Full article
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2023

Jump to: 2024, 2022, 2021

11 pages, 1033 KiB  
Article
Identifying the Gut Virome of Diaphorina citri from Florida Groves
by Chun-Yi Lin, Ozgur Batuman and Amit Levy
Insects 2023, 14(2), 166; https://doi.org/10.3390/insects14020166 - 08 Feb 2023
Cited by 1 | Viewed by 1602
Abstract
Asian citrus psyllid (Diaphorina citri) transmits the bacterial pathogen Candidatus Liberibacter asiaticus (CLas), the putative causative agent of citrus Huanglongbing disease (HLB). Insect-specific viruses can act against insects as their natural enemies, and recently, several D. citri-associated viruses [...] Read more.
Asian citrus psyllid (Diaphorina citri) transmits the bacterial pathogen Candidatus Liberibacter asiaticus (CLas), the putative causative agent of citrus Huanglongbing disease (HLB). Insect-specific viruses can act against insects as their natural enemies, and recently, several D. citri-associated viruses were discovered. The insect gut plays an important role as not only a pool for diverse microbes but also as a physical barrier to prevent the spread of pathogens such as CLas. However, there is little evidence of the presence of D. citri-associated viruses in the gut and of the interaction between them and CLas. Here, we dissected psyllid guts collected from five growing regions in Florida, and the gut virome was analyzed by high throughput sequencing. Four insect viruses, including D. citri-associated C virus (DcACV), D. citri densovirus (DcDV), D. citri reovirus (DcRV), and D. citri flavi-like virus (DcFLV), were identified, and their presence in the gut, including an additional D. citri cimodo-like virus (DcCLV), were confirmed with PCR-based assays. Microscopic analysis showed that DcFLV infection leads to morphological abnormalities in the nuclear structure in the infected psyllid gut cells. The complex and diverse composition of microbiota in the psyllid gut suggests a possible interaction and dynamics between CLas and the D. citri-associated viruses. Our study identified various D. citri-associated viruses that localized in the psyllid gut and provided more information that helps to evaluate the potential vectors for manipulating CLas in the psyllid gut. Full article
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2022

Jump to: 2024, 2023, 2021

24 pages, 5363 KiB  
Article
In Silico Characterization and Gene Expression Analysis of Toll Signaling Pathway-Related Genes in Diaphorina citri
by Mahnaz Rashidi and Nabil Killiny
Insects 2022, 13(9), 783; https://doi.org/10.3390/insects13090783 - 29 Aug 2022
Cited by 1 | Viewed by 1685
Abstract
The Asian citrus psyllid, Diaphorina citri is the main vector of citrus greening disease, also known as Huanglongbing (HLB). Currently, mitigating HLB depends on the control of D. citri using insecticides. To design innovative control strategies, we should investigate various biological aspects of [...] Read more.
The Asian citrus psyllid, Diaphorina citri is the main vector of citrus greening disease, also known as Huanglongbing (HLB). Currently, mitigating HLB depends on the control of D. citri using insecticides. To design innovative control strategies, we should investigate various biological aspects of D. citri at the molecular level. Herein we explored the Toll signaling system-related proteins in D. citri using in silico analyzes. Additionally, the transcripts of the identified genes were determined in all life stages from eggs to adults. Our findings reveal that D. citri genome possesses Toll signaling pathway-related genes similar to the insect model, Drosophila melanogaster, with slight differences. These genes include cact, TI, Myd88, Dif/DI, pll, tub, and spz encoding Cactus, Toll, Myeloid differentiation factor 88, Dorsal related immunity factor/Dorsal, Pelle, Tube, and Spaetzle, respectively. Unlike D. melanogaster, in D. citri Dorsal, immunity factor and Dorsal are the same protein. In addition, in D. citri, Pelle protein possesses a kinase domain, which is absent in Pelle of D. melanogaster. Gene expression analysis showed the transcript for cact, TI, Myd88, pll, tub, and spz are maximum in adults, suggesting the immunity increases with maturity. Instead, Dif/DI transcripts were maximal in eggs and adults and minimal in nymphal stages, indicating its role in embryonic development. The overall findings will help in designing pioneering control strategies of D. citri based on repressing its immunity by RNAi or CRISPR and combining that with biological control. Full article
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8 pages, 540 KiB  
Article
Effects of Acibenzolar-S-methyl on the Probing Behaviour and Mortality of Cacopsylla pyri on Pear Plants
by Stefano Civolani, Daniele Mirandola, Lorenzo Benetti, Luca Finetti, Marco Pezzi and Giovanni Bernacchia
Insects 2022, 13(6), 525; https://doi.org/10.3390/insects13060525 - 06 Jun 2022
Cited by 3 | Viewed by 1570
Abstract
European pear psylla, Cacopsylla pyri, is one of the worst pests of pear in Europe. We investigated whether acibenzolar-S-methyl (ASM) application on pear plants might affect the behaviour in C. pyri. The elicitor was applied on pear potted plants, and after [...] Read more.
European pear psylla, Cacopsylla pyri, is one of the worst pests of pear in Europe. We investigated whether acibenzolar-S-methyl (ASM) application on pear plants might affect the behaviour in C. pyri. The elicitor was applied on pear potted plants, and after 48 h, we confirmed the ASM-mediated induction of several Pathogenesis-Related protein (PR) coding genes. At the same time, an in-depth analysis was performed on the probing behaviour of adults and nymphs of C. pyri on ASM-treated pear plants by the EPG-DC system, as well as the assessment of young nymphs’ survival 7 days after the ASM application. The elicitor application weakly interfered with C. pyri nymphs probing behaviour and survival, while it did not affect adult stages. These data confirm previous observations obtained on C. pyricola and suggest that the elicitor does not represent a viable tool in the control of pear psylla species, especially if used alone, but it might be used in integrated management strategies focused on other plant pathogens such as Erwinia amylovora. Full article
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17 pages, 2846 KiB  
Article
The Development and Evaluation of Insect Traps for the Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Psyllidae), Vector of Citrus Huanglongbing
by James Snyder, Katrina L. Dickens, Susan E. Halbert, Stefanie Dowling, Dyrana Russell, Ruth Henderson, Eric Rohrig and Chandrika Ramadugu
Insects 2022, 13(3), 295; https://doi.org/10.3390/insects13030295 - 16 Mar 2022
Cited by 6 | Viewed by 6073
Abstract
Citrus huanglongbing (HLB) is a severe problem for citrus cultivation. The disease management programs benefit from improved field tools suitable for surveying the ACP vector (Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae)) and the associated pathogen. In the present study, we utilize [...] Read more.
Citrus huanglongbing (HLB) is a severe problem for citrus cultivation. The disease management programs benefit from improved field tools suitable for surveying the ACP vector (Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae)) and the associated pathogen. In the present study, we utilize three-dimensional (3D) printers and design tools to develop traps that can capture and preserve ACPs. Three novel, 3D-printed traps were designed and evaluated: stem trap, and cylinder traps 1 and 2. The traps and yellow sticky cards were deployed weekly for 8 months in 2 non-commercial citrus groves in Florida; in California, the traps were evaluated for 12 months in field cages and 4 citrus groves. The stem traps captured lower numbers of ACPs at all experimental sites compared to the cylinder traps. Capture rates in the cylinder traps were comparable to the sticky trap, making the device a viable tool for monitoring field ACPs. The two main advantages of using the reusable 3D traps over standard methods of ACP and HLB surveys include dynamic sampling that can be conducted year-round and the capture of ACPs that can be preserved and tested. Improved trapping may facilitate quick management decisions and mitigate HLB. Full article
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2021

Jump to: 2024, 2023, 2022

14 pages, 493 KiB  
Brief Report
The Chorion Proteome of Diaphorina citri, the Vector of Huanglongbing Disease in Citrus
by Yulica Santos-Ortega and Nabil Killiny
Insects 2021, 12(11), 959; https://doi.org/10.3390/insects12110959 - 21 Oct 2021
Viewed by 1848
Abstract
Nowadays, the Asian citrus psyllid, Diaphorina citri (Kuwayama) (Hemiptera: Liviidae) is considered the most devastating pest of citrus because it transmits “Candidatus Liberibacter asiaticus”, the putative causal agent of huanglongbing (HLB) or citrus greening. Controlling the vector is the main strategy used [...] Read more.
Nowadays, the Asian citrus psyllid, Diaphorina citri (Kuwayama) (Hemiptera: Liviidae) is considered the most devastating pest of citrus because it transmits “Candidatus Liberibacter asiaticus”, the putative causal agent of huanglongbing (HLB) or citrus greening. Controlling the vector is the main strategy used to mitigate HLB. Targeting D. citri at the very early stages of its development may offer an effective control strategy. Identifying chorion proteins will contribute to a better understanding of embryo development and egg hatching and thus could lead to valuable targets to better control psyllid populations. Herein, we analyze the chorion proteins of D. citri. Mass spectrometry-based bottom-up/shotgun proteomics and databases were queried to achieve protein identification. Fifty-one proteins were identified in D. citri chorion. The D. citri chorion proteins were divided into eight categories according to their biological or molecular function: i—enzymes (25%); ii—binding proteins (10%); iii—structural proteins (8%); iv—homeostasis-related proteins, mostly vitellogenins (8%); v—proteins related to gene expression (6%); vi—immune system proteins (6%); vii—other proteins (16%); and viii—uncharacterized proteins (21%). The composition of the chorion proteome suggested that the hatching rate could be reduced by silencing chorion-related genes. The proteomic analysis of D. citri chorion tissue allowed us to identify its proteins, providing promising new targets for D. citri control through RNA interference technology. Full article
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19 pages, 4011 KiB  
Article
Silencing of Aquaporin Homologue Accumulates Uric Acid and Decreases the Lifespan of the Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Liviidae)
by Yulica Santos-Ortega and Nabil Killiny
Insects 2021, 12(10), 931; https://doi.org/10.3390/insects12100931 - 13 Oct 2021
Cited by 3 | Viewed by 2266
Abstract
The Asian citrus psyllid, Diaphorina citri Kuwayama is devastating the citrus industry worldwide. It transmits ‘Candidatus Liberibacter asiaticus’, the pathogen of Huanglongbing in citrus. RNA interference is an excellent tool for functional genomics and for screening target genes for pest control. [...] Read more.
The Asian citrus psyllid, Diaphorina citri Kuwayama is devastating the citrus industry worldwide. It transmits ‘Candidatus Liberibacter asiaticus’, the pathogen of Huanglongbing in citrus. RNA interference is an excellent tool for functional genomics and for screening target genes for pest control. Herein, we silenced the aquaporin (AQP) gene (DcAQP) homologue in D. citri to study its functionality and whether it could be a good target for a control strategy. AQP is an integral membrane channel protein that aids in the rapid flux of water and other small solutes that move across the lipid membrane. In Hemiptera, it is well established that AQP plays important roles in adjusting to physiological challenges including (1) regulating osmotic stress between the gut lumen and hemolymph after imbibing large quantities of a low nitrogen, sugar-rich liquid diet; (2) avoiding or preventing dehydration and desiccation; and (3) surviving at elevated temperatures. The dsRNA-DcAQP was applied twice to nymphs of the 4th and 5th instars through a soaking technique. Silencing AQP caused a significant increase in nymph mortality. Emerged adults showed malformations and a shorter lifespan. Silencing DcAQP provoked alterations in some metabolites and increased the uric acid content in emerged adults. DcAQP could be a useful target to control D. citri. Full article
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12 pages, 1254 KiB  
Article
Crude Extracts and Alkaloids Derived from Ipomoea-Periglandula Symbiotic Association Cause Mortality of Asian Citrus Psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae)
by Xue-Dong Chen, Navneet Kaur, David R. Horton, W. Rodney Cooper, Jawwad A. Qureshi and Lukasz L. Stelinski
Insects 2021, 12(10), 929; https://doi.org/10.3390/insects12100929 - 12 Oct 2021
Cited by 3 | Viewed by 2440
Abstract
Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is an important economic pest of citrus crops because it vectors the causal pathogen of huanglongbing (HLB; aka citrus greening). Population suppression of D. citri with insecticides has been disproportionally relied on for HLB management [...] Read more.
Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is an important economic pest of citrus crops because it vectors the causal pathogen of huanglongbing (HLB; aka citrus greening). Population suppression of D. citri with insecticides has been disproportionally relied on for HLB management and a greater diversity of more sustainable tools is needed. Periglandula spp. is a fungal endosymbiont (family Clavicipitaceae) that forms a mutualistic relationship with members of plants in family Convolvulaceae. This association results in the production of ergot alkaloids that were previously documented as having psyllicidal properties. We investigated the mortality and behavior of D. citri exposed to crude extracts from morning glories in the plant family Convolvulaceae, as well as synthetic ergot alkaloids. Nymphs and adults were exposed to the crude plant extracts from Periglandula positive species of Convolvulaceae, as well as five synthetic ergot alkaloids. Treatments were prepared by exposing clippings of citrus to 100 ng/µL of crude extract from Periglandula-positive species of Ipomoea (I. imperati, I. leptophylla, I. pandurata and I. tricolor), and Turbina corymbosa, and from one Periglandula-negative species (I. alba) (100 ng/µL). Mortality of adult and nymphal D. citri was significantly higher than the control after exposure to extracts from I. tricolor and I. imperati. The synthetic ergot alkaloids, lysergol (10–100 ng/µL), ergonovine maleate (100 ng/µL), agroclavine (10–100 ng/µL), and ergosine (10–100 ng/µL) increased mortality of D. citri nymphs, while ergosine (100 ng/µL) and agroclavine (100 ng/µL) increased mortality of adults compared to water controls. Fewer D. citri adults settled on plants treated with crude extracts or synthetic ergot alkaloids than on water controls at 48 h after release. D. citri that fed on citrus leaves treated with 10 ng/μL solution of crude extract from the Periglandula-positive species Ipomoea (I. imperati, I. leptophylla, I. pandurata, I. tricolor), and Turbina corymbosa excreted significantly less honeydew compared with a negative water control and extract from Periglandula-negative species (I. alba). Our results indicate that crude extracts and ergot alkaloids exhibit toxic and sub-lethal effects on D. citri that could be useful for management of this pest. Full article
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