Mutualistic Relationships: Balancing metabolism and reproduction
The bacterium responsible for a disease that infects citrus plants across Asia facilitates its own proliferation by increasing the fecundity of its host insect.
- Department of Entomology, China Agricultural University, China
- Department of Entomology, Henan Agricultural University, China
Citrus huanglongbing – a disease known as ‘citrus cancer’ because of the devastating effect it can have on citrus plants – is caused by a bacterium called Candidatus Liberibacter asiaticus (CLas; Killiny, 2022). In Asia, this bacterium is primarily spread by a lice-like bug called Diaphorina citri. However, it is not possible to study CLas in the laboratory because efforts to culture it have been unsuccessful. Therefore, the most effective approach for preventing outbreaks of huanglongbing is to manage the population of D. citri (Wang et al., 2017).
Relationships between insects and plant pathogens – like that between D. citri and CLas – are common in the natural world, and many of these are mutually beneficial to both parties, though some are not (Eigenbrode et al., 2018). In a mutualistic or symbiotic relationship, the pathogen relies on the insect to help it spread from plant to plant, while infection by the pathogen can benefit the insect through an increase in fitness. To date, most research in this area has focused on relationships in which the pathogen is a virus (see, for example, Liu et al., 2014 on the spread of barley yellow dwarf virus by aphids, and Mao et al., 2019 on the spread of ice gall dwarf virus by leafhoppers), so less is known about mutualistic relationships involving bacteria.
Previous studies have revealed a mutualistic relationship in which CLas infection boosts the fitness of D. citri by increasing its ability to produce large numbers of offspring (fecundity), but the molecular dynamics driving this interaction were not fully understood (Pelz-Stelinski and Killiny, 2016; Ren et al., 2016). Now, in eLife, Yijing Cen, Xiaoge Nian and colleagues from South China Agricultural University, Shaoguan University, and Western Sydney University – including Jiayun Li as first author – report results that shed light on this interaction at the molecular level (Li et al., 2024).
Reproductive development in insects demands a significant energy supply (Yang et al., 2024), so exploring how CLas infection regulates and mobilizes energy metabolism in D. citri to improve fecundity is a promising avenue to explore. Insects store energy and fat as triglyceride and glycogen, and a process called AKH signaling (where AKH is short for adipokinetic hormone) has a crucial role in converting the former to diglyceride in order to release lipids, and the latter to trehalose to release energy (Arrese and Soulages, 2010).
First, Li et al. demonstrated that CLas infection significantly increases levels of triglyceride and glycogen, as well as lipid droplet size. These findings suggest that CLas-infected D. citri possess greater energy reserves and greater potential for energy mobilization, which may support the development of ovaries in females. Knocking down the gene for AKH (or its receptor) disrupted the mobilization of fat and this resulted in delayed ovary development, decreased egg production, and a reduction in the titer of CLas in the ovaries. These findings underscore the critical role of AKH and its receptor in managing the balance between energy metabolism and fecundity in D. citri.
To investigate how AKH signaling is regulated, Li et al. identified microRNAs that could potentially bind to AKH mRNA and prevent it being translated into protein. In vivo and in vitro experiments showed that a microRNA called miR-34 directly targets the 3’-untranslated region of the AKH receptor, therefore reducing the levels of this mRNA and the AKH receptor itself. Expression levels of miR-34 were lower in infected D. citri than in controls, suggesting that CLas may decrease levels of miR-34. Furthermore, treating infected D. citri with a synthetic microRNA that mimics the function of miR-34 led to outcomes similar to those observed when the gene for the AKH receptor was knocked down: delayed ovarian development, reduced egg production, and decreased levels of CLas in the ovaries (Figure 1). This finding represents the first instance of a host microRNA influencing AKH signaling to impact lipid metabolism and fecundity in infected D. citri. Additionally, the research points to an array of genes affected by the AKH signaling cascade, such as those associated with juvenile hormone signaling and two reproduction-related proteins called vitellogenin and vitellogenin receptor.
Figure 1
How infection by bacteria can modulate metabolism and increase reproduction in an insect.
When the lice-like insect D. citri is infected with CLas, the bacterium that causes huanglongbing in citrus plants, there is an increase in the production of adipokinetic hormone (AKH; pink circles; top) in the corpora cardiaca (yellow), which is part of the endocrine system of the insect. The AKH molecules bind to AKH receptors (pale pink barrel shapes), and the resulting increase in AKH receptor signaling leads to increased levels of triglyceride and increased numbers of lipid droplets (not shown). A microRNA called miR-34 usually inhibits AKH receptor signaling, but infection with CLas also results in the downregulation of miR-34. The increase in AKH receptor signaling caused by CLas infection increases the energy reserves available for reproduction, leading to increased fecundity for D. citri, which also aids the proliferation of CLas. CLas: Candidatus Liberibacter asiaticus.
The work of Li et al. in highlighting the role of AKH signaling in increasing the fecundity of D. citri that have been infected by CLas contributes to our understanding of the rapid spread of huanglongbing in the field. Future research should focus on elucidating the intricate interactions among endocrine signals such as hormones, neuropeptides and neurotransmitters, and their collective influence on the increased fecundity prompted by CLas infection. Undertaking these investigations will broaden our understanding of the complex relationships between plant pathogens and their insect vectors, and could potentially lead to new methods to control plant pathogen populations.
References
-
Insect fat body: energy, metabolism, and regulationAnnual Review of Entomology 55:207–225.https://doi.org/10.1146/annurev-ento-112408-085356
-
Insect-borne plant pathogens and their vectors: Ecology, evolution, and complex interactionsAnnual Review of Entomology 63:169–191.https://doi.org/10.1146/annurev-ento-020117-043119
-
Viral pathogens hitchhike with insect sperm for paternal transmissionNature Communications 10:955.https://doi.org/10.1038/s41467-019-08860-4
-
Better together: association with “Candidatus Liberibacter asiaticus” increases the reproductive fitness of its insect vector, Diaphorina citri (Hemiptera: Liviidae)Annals of the Entomological Society of America 109:371–376.https://doi.org/10.1093/aesa/saw007
-
Effects of Candidatus Liberibacter asiaticus on the fitness of the vector Diaphorina citriJournal of Applied Microbiology 121:1718–1726.https://doi.org/10.1111/jam.13302
-
The candidatus liberibacter-host interface: Insights into pathogenesis mechanisms and disease controlAnnual Review of Phytopathology 55:451–482.https://doi.org/10.1146/annurev-phyto-080516-035513
-
Lipid homeostasis is essential for oogenesis and embryogenesis in the silkworm, Bombyx moriCellular and Molecular Life Sciences 81:127.https://doi.org/10.1007/s00018-024-05173-8
Article and author information
Author details
Publication history
Copyright
© 2024, Zhang and An
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 360
- views
-
- 46
- downloads
-
- 0
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Mutualistic Relationships: Balancing metabolism and reproduction
eLife 13:e97601.
https://doi.org/10.7554/eLife.97601
Further reading
-
- Ecology
Global change is causing unprecedented degradation of the Earth’s biological systems and thus undermining human prosperity. Past practices have focused either on monitoring biodiversity decline or mitigating ecosystem services degradation. Missing, but critically needed, are management approaches that monitor and restore species interaction networks, thus bridging existing practices. Our overall aim here is to lay the foundations of a framework for developing network management, defined here as the study, monitoring, and management of species interaction networks. We review theory and empirical evidence demonstrating the importance of species interaction networks for the provisioning of ecosystem services, how human impacts on those networks lead to network rewiring that underlies ecosystem service degradation, and then turn to case studies showing how network management has effectively mitigated such effects or aided in network restoration. We also examine how emerging technologies for data acquisition and analysis are providing new opportunities for monitoring species interactions and discuss the opportunities and challenges of developing effective network management. In summary, we propose that network management provides key mechanistic knowledge on ecosystem degradation that links species- to ecosystem-level responses to global change, and that emerging technological tools offer the opportunity to accelerate its widespread adoption.
-
- Ecology
- Evolutionary Biology
Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.
