Impact of different temperatures on survival and energy metabolism in the Asian citrus psyllid, Diaphorina citri Kuwayama

El-Shesheny, Rabeh; Hijaz, Faraj; El-Hawary, Ibrahim; Mesbah, I. I.; Killiny, Nabil

doi:10.1016/j.cbpa.2015.11.013

Cited by 28 publications

(21 citation statements)

References 38 publications

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“…Interestingly, our recent study also showed that the AEC of D. citri was negatively correlated with adult psyllid survival (23). In agreement with our results, AEC was also negatively correlated with the survival of other species.…”

Section: Resultssupporting

confidence: 92%

“…The effects of CLas infection on psyllid genes, including ATP synthase ␣-and ␤-subunits mitochondrion-like (ATP synthase A and B), V-type proton ATPase catalytic subunit A (V-ATPase-V1a), the transitional endoplasmic reticulum ATPase (TER94), nucleotide diphosphate kinase (NDPK), and AMP-activated protein kinase ␣-subunit (AMPK-A) genes in D. citri adults, were evaluated using RT-qPCR as described by El-Shesheny et al (23). The actin gene was used as a reference (endogenous gene) for comparing the relative levels of gene expression among treatments (46).…”

Section: Diaphorina Citri Coloniesmentioning

confidence: 99%

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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: Resultssupporting

confidence: 92%

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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“…In addition to the 18 and 22°C treatments, the individuals that developed at 32°C showed a reduced propensity for flight than those developed at 27°C, indicating that high temperatures can also reduce the flight propensity of the insect. It is well known that temperatures of 30–45°C drastically reduce the survival of D. citri (El‐Shesheny, Hijaz, El‐Hawary, Mesbah, & Killiny, ), reaching a life cycle viability next to 7% from 32°C (Nava et al., ). Deleterious effect of high temperatures may explain the lower propensity of the insect for flight at 32°C.…”

Section: Discussionmentioning

confidence: 99%

Environmental conditions for Diaphorina citri Kuwayama (Hemiptera: Liviidae) take‐off

Tomaseto¹,

Miranda

Moral³

et al. 2017

J Applied Entomology

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Environmental factors that influence flight activity of Diaphorina citri Kuwayama (Hemiptera: Liviidae) may have implications for Huanglongbing spread and management. In this work, four studies were conducted to evaluate the effect of environmental conditions on D. citri take‐off. In the first, insects were transferred to sweet orange seedlings and confined inside an acrylic cage to verify the take‐off periodicity and the effect of environmental factors on this process. In the second, take‐off temperature threshold was estimated by recording the number of insects that initiated flight from a platform when subjected to gradual temperature increases from 15 to 39°C. In the other studies, we evaluated the effect of different photoperiods and temperature regimes (third study) and of constant temperatures (fourth study) on the propensity for D. citri flight. Insects were confined in clear plastic bottle cages with tubes of 50 ml placed on the cab, to collect emerged adults that initiated flights. Results showed that a small portion of the tested population (maximum 10%) tends to take off from plants and this behaviour is more prevalent in the afternoon (14:00–16:00 h), coinciding with daytimes of lower humidity and higher thermal amplitude. Adults that were submitted to lower temperatures (18°C) and short light periods (10 h) showed less propensity to flight. In contrast, at constant 27°C, the insects were more prone to flight, and this result was confirmed when individuals were submitted to increases in temperature, indicating that 27.14°C is the take‐off temperature threshold of D. citri. Results show that temperature plays an important role in the flight activity of D. citri and suggest that control measures of the insect may be more effective in the morning and in temperatures below 27°C, when the probability to take off from a host is lower.

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“…Firstly, about 20-30 adults were released in a 35 3 40 3 30 mm clip cage on orange jasmine leaves. Different orange jasmine plants with the 1-day-old adult psyllids were placed in incubators seperately (Sanyo, MLR-370H) at 5, 10, 27, 35 and 408C (Hussain et al, 2017), but with the same RH of 75 6 5% and under 14 h light (L):10 h dark (D) photoperiod for 24 h. Previous reports (Gomez-Torres et al, 2012;El-Shesheny et al, 2016) and our observations indicated that 278C is in the range of suitable temperatures for psyllid species, so it was used as a control in this experiment.…”

Section: Different Temperature Treatments On Psyllidsmentioning

confidence: 99%

Effects of different temperature regimes on survival of Diaphorina citri and its endosymbiotic bacterial communities

Hussain

Akutse

Keppanan

et al. 2017

Environmental Microbiology

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The Asian citrus psyllid, Diaphorina citri, is a major pest of citrus and vector of citrus greening (huanglongbing) in Asian. In our field-collected psyllid samples, we discovered that Fuzhou (China) and Faisalabad (Pakistan), populations harbored an obligate primary endosymbiont Candidatus Carsonella (gen. nov.) with a single species, Candidatus Carsonella ruddii (sp. nov.) and a secondary endosymbiont, Wolbachia surface proteins (WSP) which are intracellular endosymbionts residing in the bacteriomes. Responses of these symbionts to different temperatures were examined and their host survival assessed. Diagnostic PCR assays showed that the endosymbionts infection rates were not significantly reduced in both D. citri populations after 24 h exposure to cold or heat treatments. Although quantitative PCR assays showed significant reduction of WSP relative densities at 40°C for 24 h, a substantial decrease occurred as the exposure duration increased beyond 3 days. Under the same temperature regimes, Ca. C. ruddii density was initially less affected during the first exposure day, but rapidly reduced at 3-5 days compared to WSP. However, the mortality of the psyllids increased rapidly as exposure time to heat treatment increased. The responses of the two symbionts to unfavorable temperature regimes highlight the complex host-symbionts interactions between D. citri and its associated endosymbionts.

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Impact of different temperatures on survival and energy metabolism in the Asian citrus psyllid, Diaphorina citri Kuwayama

Cited by 28 publications

References 38 publications

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

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

Environmental conditions for Diaphorina citri Kuwayama (Hemiptera: Liviidae) take‐off

Effects of different temperature regimes on survival of Diaphorina citri and its endosymbiotic bacterial communities

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