Shifting the Balance: Heat Stress Challenges the Symbiotic Interactions of the Asian Citrus Psyllid,<i>Diaphorina citri</i>(Hemiptera, Liviidae)

Dossi, Fábio Cleisto Alda; Silva, Edney Pereira da; Cônsoli, Fernando L.

doi:10.1086/699755

Cited by 6 publications

(4 citation statements)

References 64 publications

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“…This has been reported from aphids, where the microbial symbiont, Serratia symbiotica, lyses when exposed to heat stress (39 • C for 4 h), which is correlated with increased levels of thermoprotective metabolites, for example sorbitol, in the aphid host (Burke et al, 2010). Comparably, bacterial symbionts in the Asian citrus psyllid (Diaphorina citri) degrade during heat stress due to increased lysosomal activity, which provides nutrients to the surviving symbionts and host (Dossi et al, 2018). Busck et al (2022) estimated that for every host cell there are 1-2 bacterial cells in S. dumicola, and such a bacterial load could potentially influence the host metabolome upon cell lysis and supply the spider host with metabolites aiding its temperature response.…”

Section: Discussionmentioning

confidence: 76%

Metabolite Profiling of the Social Spider Stegodyphus dumicola Along a Climate Gradient

Sandfeld

Malmos²,

Nielsen³

et al. 2022

Front. Ecol. Evol.

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Animals experience climatic variation in their natural habitats, which may lead to variation in phenotypic responses among populations through local adaptation or phenotypic plasticity. In ectotherm arthropods, the expression of thermoprotective metabolites such as free amino acids, sugars, and polyols, in response to temperature stress, may facilitate temperature tolerance by regulating cellular homeostasis. If populations experience differences in temperatures, individuals may exhibit population-specific metabolite profiles through differential accumulation of metabolites that facilitate thermal tolerance. Such thermoprotective metabolites may originate from the animals themselves or from their associated microbiome, and hence microbial symbionts may contribute to shape the thermal niche of their host. The social spider Stegodyphus dumicola has extremely low genetic diversity, yet it occupies a relatively broad temperature range occurring across multiple climate zones in Southern Africa. We investigated whether the metabolome, including thermoprotective metabolites, differs between populations, and whether population genetic structure or the spider microbiome may explain potential differences. To address these questions, we assessed metabolite profiles, phylogenetic relationships, and microbiomes in three natural populations along a temperature gradient. The spider microbiomes in three genetically distinct populations of S. dumicola showed no significant population-specific pattern, and none of its dominating genera (Borrelia, Diplorickettsia, and Mycoplasma) are known to facilitate thermal tolerance in hosts. These results do not support a role of the microbiome in shaping the thermal niche of S. dumicola. Metabolite profiles of the three spider populations were significantly different. The variation was driven by multiple metabolites that can be linked to temperature stress (e.g., lactate, succinate, or xanthine) and thermal tolerance (e.g., polyols, trehalose, or glycerol): these metabolites had higher relative abundance in spiders from the hottest geographic region. These distinct metabolite profiles are consistent with a potential role of the metabolome in temperature response.

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Section: Discussionmentioning

confidence: 76%

Metabolite Profiling of the Social Spider Stegodyphus dumicola Along a Climate Gradient

Sandfeld

Malmos²,

Nielsen³

et al. 2022

Front. Ecol. Evol.

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“…The nutritional quality of the plants will change, as will the relative proportion of defensive compounds in plants under elevated CO 2 [98,99]. Metabolic rates will change under elevated temperatures and the balance of endosymbionts may also change [100,101,102,103]. These factors will all impact vector and pathogen biology, as each component of the system struggles to find a new level of homeostasis.…”

Section: Environmental Changementioning

confidence: 99%

The Probing Behavior Component of Disease Transmission in Insect-Transmitted Bacterial Plant Pathogens

Ebert

2019

Insects

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Insects can be effective vectors of plant diseases and this may result in billions of dollars in lost agricultural productivity. New, emerging or introduced diseases will continue to cause extensive damage in afflicted areas. Understanding how the vector acquires the pathogen and inoculates new hosts is critical in developing effective management strategies. Management may be an insecticide applied to kill the vector or a host plant resistance mechanism to make the host plant less suitable for the vector. In either case, the tactic must act before the insect performs the key behavior(s) resulting in either acquisition or transmission. This requires knowledge of the timing of behaviors the insect uses to probe the plant and commence ingestion. These behaviors are visualized using electropenetrography (EPG), wherein the plant and insect become part of an electrical circuit. With the tools to define specific steps in the probing process, we can understand the timing of acquisition and inoculation. With that understanding comes the potential for more relevant testing of management strategies, through insecticides or host plant resistance. The primary example will be Candidatus Liberibacter asiaticus transmitted by Diaphorina citri Kuwayama in the citrus agroecosystem, with additional examples used as appropriate.

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“…[22][23][24][25][26] These endosymbionts not only occupy the psyllid's body cavity but also interact with the HLB pathogen and the host plant, creating a complex network of associations. [27][28][29][30][31][32][33][34][35] These differential responses of psyllids from varying tree ages emphasize the intricate interplay between host-symbiont interactions and the physiological attributes of psyllids at different developmental stages. The underlying mechanisms driving this discrepancy warrant further investigation, as they may hold critical implications for our understanding of vector biology and HLB transmission dynamics.…”

Section: Introductionmentioning

confidence: 99%

“…Candidatus Carsonella ruddii, a primary endosymbiont, and Wolbachia, a secondary endosymbiont, have been identified in psyllid populations 22‐26 . These endosymbionts not only occupy the psyllid's body cavity but also interact with the HLB pathogen and the host plant, creating a complex network of associations 27‐35 . These differential responses of psyllids from varying tree ages emphasize the intricate interplay between host–symbiont interactions and the physiological attributes of psyllids at different developmental stages.…”

Section: Introductionmentioning

confidence: 99%

Effect of tree height and spraying methods on Diaphorina citri kuwayama endosymbionts in the context of Huanglongbing disease management in citrus orchards

Hussain,

Zhong,

Tao

et al. 2023

Pest Management Science

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BACKGROUNDHuanglongbing (caused by Candidatus Liberibacter asiaticus) is the most damaging disease of citrus around the world. This study investigated the effects of citrus tree age on Diaphorina citri Kuwayama mortality, endosymbiont responses, and Huanglongbing distribution.RESULTSThe results reveal that the age of citrus trees plays a significant role in psyllid mortality. Notably, four‐year‐old plants exhibited higher psyllid mortality (31.50%) compared to thirteen‐year‐old trees (9.10% and 0.09%, respectively). Our findings also revealed that psyllids from both 4 and 13‐year‐old citrus trees carried Candidatus Carsonella ruddii species and Wolbachia, the primary and secondary endosymbionts, respectively. Surprisingly, infection rates of these endosymbionts remained consistent across different age groups, as confirmed by qPCR analysis. Furthermore, our study highlights the significance of tree height as a proxy for tree age in influencing Huanglongbing occurrence. Specifically, 4‐year‐old trees subjected to the US‐SMART mechanical sprayer for citrus psyllid control demonstrated effective disease management compared to 13‐year‐old trees treated with handheld gun sprayers. Additionally, the investigation explored the impact of tree height on HLB distribution. In four‐year‐old trees, no significant correlation between HLB disease and tree height was observed, potentially due to effective spray coverage. However, in thirteen‐year‐old trees, a negative correlation between tree height and HLB disease was evident.CONCLUSIONThis research provides valuable insights into the complex interaction between citrus tree age, psyllid endosymbionts responses, and HLB distribution. These results emphasize effective HLB management strategies, especially in orchards with diverse tree age populations, ultimately contributing to the long‐term sustainability of citrus cultivation.This article is protected by copyright. All rights reserved.

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Shifting the Balance: Heat Stress Challenges the Symbiotic Interactions of the Asian Citrus Psyllid,Diaphorina citri(Hemiptera, Liviidae)

Cited by 6 publications

References 64 publications

Metabolite Profiling of the Social Spider Stegodyphus dumicola Along a Climate Gradient

Metabolite Profiling of the Social Spider Stegodyphus dumicola Along a Climate Gradient

The Probing Behavior Component of Disease Transmission in Insect-Transmitted Bacterial Plant Pathogens

Effect of tree height and spraying methods on Diaphorina citri kuwayama endosymbionts in the context of Huanglongbing disease management in citrus orchards

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