Phenoloxidases are required for the pea aphid's defence against bacterial and fungal infection

Xu, Liting; Ma, Li; Wang, W.; Li, L.; Lu, Zhiqiang

doi:10.1111/imb.12536

Cited by 26 publications

(28 citation statements)

References 24 publications

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“…Little is known about role of microRNAs in the immune system of aphids to date. Previous studies demonstrated the critical roles of phagocytosis, PPO, and ROS in the pea aphid immune system [14][15][16][17][18][19] and suggested the involvement of JNK signaling in the aphid defense against bacteria [20]. However, the precise role of the JNK pathway and interplay between the JNK pathway and other immune responses in pea aphid remain unclear.…”

Section: Plos Pathogensmentioning

confidence: 99%

“…However, pea aphid exerts a hemocyte-mediated response, including phagocytosis and encapsulation, against bacteria and foreign intrusion [14,15]. Recent studies from our and other groups showed that phenoloxidase (PO) is required and/or involved in the immune defense in pea aphid [16,17]. Additionally, ROS play role in the interaction between pea aphid and bacteria [18,19].…”

Section: Introductionmentioning

confidence: 99%

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JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184

Liu

Zhao

et al. 2020

PLoS Pathog

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Different from holometabolous insects, the hemipteran species such as pea aphid Acyrthosiphon pisum exhibit reduced immune responses with the absence of the genes coding for antimicrobial peptide (AMP), immune deficiency (IMD), peptidoglycan recognition proteins (PGRPs), and other immune-related molecules. Prior studies have proved that phenoloxidase (PO)-mediated melanization, hemocyte-mediated phagocytosis, and reactive oxygen species (ROS) participate in pea aphid defense against bacterial infection. Also, the conserved signaling, Jun N-terminal kinase (JNK) pathway, has been suggested to be involved in pea aphid immune defense. However, the precise role of the JNK signaling, its interplay with other immune responses and its regulation in pea aphid are largely unknown. In this study, using in vitro biochemical assays and in vivo bioassays, we demonstrated that the JNK pathway regulated hemolymph PO activity, hydrogen peroxide concentration and hemocyte phagocytosis in bacteria infected pea aphids, suggesting that the JNK pathway plays a central role in regulating immune responses in pea aphid. We further revealed the JNK pathway is regulated by microRNA-184 in response to bacterial infection. It is possible that in common the JNK pathway plays a key role in immune system of hemipteran insects and microRNA-184 regulates the JNK pathway in animals.

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Section: Plos Pathogensmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184

Liu

Zhao

et al. 2020

PLoS Pathog

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“…Focusing just on the highly-resistant lines, we found that several putative insect immunity genes are upregulated by pea aphids in response to wasp parasitism (S1 Table). These include the gene hemocytin (ACYPI003478), which is released by immune cells and plays a role in cell aggregation [39], a clip-domain serine protease (ACYPI008297) thought to activate phenoloxidase [40][41][42], and several other proteases and inhibitors (e.g. ACYPI003807, ACYPI004531).…”

Section: Resultsmentioning

confidence: 99%

Variation in intrinsic resistance of pea aphids to parasitoid wasps: A transcriptomic basis

McLean

Parker

2020

PLoS ONE

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Evolutionary interactions between parasitoid wasps and insect hosts have been well studied at the organismal level, but little is known about the molecular mechanisms that insects use to resist wasp parasitism. Here we study the interaction between a braconid wasp (Aphidius ervi) and its pea aphid host (Acyrthosiphon pisum). We first identify variation in resistance to wasp parasitism that can be attributed to aphid genotype. We then use transcriptome sequencing to identify genes in the aphid genome that are differentially expressed at an early stage of parasitism, and we compare these patterns in highly resistant and susceptible aphid host lines. We find that resistant genotypes are upregulating genes involved in carbohydrate metabolism and several key innate immune system genes in response to parasitism, but that this response seems to be weaker in susceptible aphid genotypes. Together, our results provide a first look into the complex molecular mechanisms that underlie aphid resistance to wasp parasitism and contribute to a broader understanding of how resistance mechanisms evolve in natural populations.

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“…In insects, PO-mediated melanin formation is involved in a variety of biological functions such as innate immunity, hemolymph clotting, and wound sealing (1–3, 15, 17). Fig.…”

Section: Resultsmentioning

confidence: 99%

Exaggeration and cooption of innate immunity for social defense

Kutsukake

Moriyama

Shigenobu

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Social insects often exhibit striking altruistic behaviors, of which the most spectacular ones may be self-destructive defensive behaviors called autothysis, “self-explosion,” or “suicidal bombing.” In the social aphid Nipponaphis monzeni, when enemies damage their plant-made nest called the gall, soldier nymphs erupt to discharge a large amount of body fluid, mix the secretion with their legs, and skillfully plaster it over the plant injury. Dozens of soldiers come out, erupt, mix, and plaster, and the gall breach is promptly sealed with the coagulated body fluid. What molecular and cellular mechanisms underlie the self-sacrificing nest repair with body fluid for the insect society? Here we demonstrate that the body cavity of soldier nymphs is full of highly differentiated large hemocytes that contain huge amounts of lipid droplets and phenoloxidase (PO), whereas their hemolymph accumulates huge amounts of tyrosine and a unique repeat-containing protein (RCP). Upon breakage of the gall, soldiers gather around the breach and massively discharge the body fluid. The large hemocytes rupture and release lipid droplets, which promptly form a lipidic clot, and, concurrently, activated PO converts tyrosine to reactive quinones, which cross-link RCP and other macromolecules to physically reinforce the clot to seal the gall breach. Here, soldiers’ humoral and cellular immune mechanisms for wound sealing are extremely up-regulated and utilized for colony defense, which provides a striking case of direct evolutionary connection between individual immunity and social immunity and highlights the importance of exaggeration and cooption of preexisting traits to create evolutionary novelties.

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Phenoloxidases are required for the pea aphid's defence against bacterial and fungal infection

Cited by 26 publications

References 24 publications

JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184

JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184

Variation in intrinsic resistance of pea aphids to parasitoid wasps: A transcriptomic basis

Exaggeration and cooption of innate immunity for social defense

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