Dopamine and its receptor DcDop2 are involved in the mutualistic interaction between ‘Candidatus Liberibacter asiaticus’ and Diaphorina citri
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eLife Assessment
Insects can act as vectors of plant diseases, hence the study of insect-pathogen interactions is relevant for agriculture. This important study identifies in Diaphorina citri a dopamine receptor responsive to 'Candidatus Liberibacter asiaticus' infection, demonstrate direct regulation of this receptor by a microRNA, and integrate dopamine signaling into an established insect reproductive hormone framework. Multiple complementary experimental approaches convincingly support the findings, but key conclusions rely on correlative data and the mechanistic evidence for the proposed linear signaling cascade is incomplete. This work will be of interest for insect physiology and vector-pathogen biology, and more broadly for citrus agriculture.
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Abstract
‘Candidatus Liberibacter asiaticus’ (CLas), the causal agent of citrus huanglongbing, is transmitted by the Asian citrus psyllid Diaphorina citri. While CLas-positive (CLas+) females exhibit increased fecundity and metabolic demands, their neuroendocrine regulation remains unclear. We propose CLas manipulates dopamine (DA) signaling to enhance psyllid fecundity and CLas proliferation. Metabolomics revealed elevated DA in CLas+ females. Silencing DA synthesis genes and receptor DcDop2 via RNAi reduced lipid reserves, fecundity, and ovarian CLas titers. Through combined in vivo and in vitro experiments, we demonstrated that the microRNA miR-31a suppresses DcDop2 expression by binding to its 3’ untranslated region. Overexpression of miR-31a resulted in decreased DcDop2 expression and CLas titers in the ovaries, eliciting phenotypic defects akin to DcDop2 knockdown. Furthermore, DcDop2 knockdown and miR-31a overexpression reduced juvenile hormone (JH) levels and adipokinetic hormone (AKH) signaling in fat bodies and ovaries. Consequently, CLas hijacks the DA/DcDop2-miR-31a-AKH-JH signaling cascade to improve D. citri lipid metabolism and fecundity, while simultaneously promoting its replication. These findings suggest a mutualistic interaction between CLas proliferation and ovarian development within the insect host that enrich our understanding of the molecular interplay between plant pathogens and vector insects and offer novel targets and strategies for the field management of HLB.
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eLife Assessment
Insects can act as vectors of plant diseases, hence the study of insect-pathogen interactions is relevant for agriculture. This important study identifies in Diaphorina citri a dopamine receptor responsive to 'Candidatus Liberibacter asiaticus' infection, demonstrate direct regulation of this receptor by a microRNA, and integrate dopamine signaling into an established insect reproductive hormone framework. Multiple complementary experimental approaches convincingly support the findings, but key conclusions rely on correlative data and the mechanistic evidence for the proposed linear signaling cascade is incomplete. This work will be of interest for insect physiology and vector-pathogen biology, and more broadly for citrus agriculture.
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Reviewer #1 (Public review):
I read this paper with great interest based on my experience in insect sciences. I have some minor comments (and recommendations) that I believe the authors should address.
(1) The paper has an original biological question that is overly broad and mechanistically ambitious. The central biological question, namely how CLas infection enhances fecundity of Diaphorina citri via dopamine signaling, is clearly stated and well motivated by previous literature. However, my advice to the authors is that, while the general question is clear, the manuscript attempts to answer multiple mechanistic layers simultaneously. As a result, I feel that the biological narrative becomes diffuse, especially in later sections where DA, miRNA regulation, AKH signaling, and JH signaling are all proposed as parts of a single linear …
Reviewer #1 (Public review):
I read this paper with great interest based on my experience in insect sciences. I have some minor comments (and recommendations) that I believe the authors should address.
(1) The paper has an original biological question that is overly broad and mechanistically ambitious. The central biological question, namely how CLas infection enhances fecundity of Diaphorina citri via dopamine signaling, is clearly stated and well motivated by previous literature. However, my advice to the authors is that, while the general question is clear, the manuscript attempts to answer multiple mechanistic layers simultaneously. As a result, I feel that the biological narrative becomes diffuse, especially in later sections where DA, miRNA regulation, AKH signaling, and JH signaling are all proposed as parts of a single linear cascade. In summary, my key concern is that the paper often moves from correlation to causal hierarchy without fully disentangling whether these pathways act sequentially, in parallel, or redundantly. A more explicitly framed primary hypothesis (e.g., "DA-DcDop2 is necessary and sufficient for CLas-induced fecundity") may improve conceptual clarity.
(2) On the novelty of the data, I feel they are moderately novel, with substantial confirmatory components. If I am correct, the novel contributions include the identification of DcDop2 as the DA receptor responsive to CLas infection in D. citri, the discovery that miR-31a directly targets DcDop2, which is supported by luciferase assays and RIP, and thirdly, the integration of dopamine signaling into the already-described CLas-AKH-JH-fecundity framework. My advice to the authors is to focus more on the manuscript's novelty, which lies more in pathway integration than in discovering fundamentally new biological phenomena. This is appropriate for a mechanistic paper, but should be framed as an extension of existing models rather than a paradigm shift.
(3) On the conclusions, I recommend that the authors modify their statements a little. I feel that there are some overstated or insufficiently supported claims. For instance, the assertion that CLas "hijacks" the DA-DcDop2-miR-31a-AKH-JH cascade implies direct pathogen manipulation, but no CLas-derived effector or mechanism is identified. Also that the model suggests a linear signaling hierarchy, but the data largely show correlation and partial dependency rather than strict epistasis. In third, the term "mutualistic interaction" may be too strong, as host fitness costs outside fecundity (e.g., longevity, immunity) are not evaluated. In conclusion, I confirm that the data support a functional association, but mechanistic causality and evolutionary interpretation are somewhat overstated.
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Reviewer #2 (Public review):
Summary:
Nian and colleagues comprehensively apply metabolomics, molecular, and genetic approaches to demonstrate that CLas hijacks the DA/DcDop2-miR-31a-AKH-JH signaling cascade to enhance lipid metabolism and fecundity in D. citri, while concurrently promoting its own replication.
Strengths:
These findings provide solid evidence of a mutualistic interaction between CLas proliferation and ovarian development in the insect host. This insight significantly advances our understanding of the molecular interplay between plant pathogens and vector insects, and offers novel targets and strategies for HLB field management.
Weaknesses:
While the article investigates the involvement of dopamine signaling and specific microRNAs in enhancing fecundity and pathogen proliferation, it still needs to provide a detailed …
Reviewer #2 (Public review):
Summary:
Nian and colleagues comprehensively apply metabolomics, molecular, and genetic approaches to demonstrate that CLas hijacks the DA/DcDop2-miR-31a-AKH-JH signaling cascade to enhance lipid metabolism and fecundity in D. citri, while concurrently promoting its own replication.
Strengths:
These findings provide solid evidence of a mutualistic interaction between CLas proliferation and ovarian development in the insect host. This insight significantly advances our understanding of the molecular interplay between plant pathogens and vector insects, and offers novel targets and strategies for HLB field management.
Weaknesses:
While the article investigates the involvement of dopamine signaling and specific microRNAs in enhancing fecundity and pathogen proliferation, it still needs to provide a detailed mechanistic understanding of these interactions. The precise molecular pathways and feedback mechanisms by which CLas manipulates dopamine signaling in Diaphorina citri remain unclear.
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