Spätzle Homolog-Mediated Toll-Like Pathway Regulates Innate Immune Responses to Maintain the Homeostasis of Gut Microbiota in the Red Palm Weevil, Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae)

Muhammad, Aliyu Idris; Habineza, Prosper; Wang, Xinghong; Xiao, Rong; Ji, Tianliang; Hou, Youming; Shi, Zhanghong

doi:10.3389/fmicb.2020.00846

Cited by 26 publications

(15 citation statements)

References 70 publications

(107 reference statements)

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“…In a non-infection model, AMPs rapidly respond to ecdysone in the tissue [ 30 , 31 ]. Furthermore, the expression of the Spz homolog was upregulated in the gut and fat body of the red palm weevil R. ferrugineus after systemic and oral inoculation of S. aureus , E. coli , and Beauveria bassiana , which suggested the role of the homolog Spz in systemic and gut-specific immune responses against infections [ 8 ]. TmSpz-4 mRNA expression peaked at 9 and 24 h post-injection with E. coli and S. aureus , which confirmed the gut-specific immunity [ 9 ].…”

Section: Discussionmentioning

confidence: 99%

“…In Rhynchophorus ferrugineus (red palm weevil), the Spz homolog-mediated Toll-like pathway activation regulates AMP response and maintains gut homeostasis. AMPs such as R. ferrugineus Coleoptericin ( RfColeoptericin ) and RfCecropin are downregulated in RfSpz knockdown insects, which suggested that their secretion is regulated by Rf Spätzle-mediated activation of the Toll signaling pathway [ 8 ]. The larvae of T. molitor Spätzle-4 ( TmSpz-4 ) knockdown insects are susceptible to E. coli and C. albicans infections due to the downregulation of AMPs and Toll pathway-related NF-κB factors (Dorsal X1 and Dorsal X2) [ 9 , 10 ].…”

Section: Introductionmentioning

confidence: 99%

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TmSpz-like Plays a Fundamental Role in Response to E. coli but Not S. aureus or C. albican Infection in Tenebrio molitor via Regulation of Antimicrobial Peptide Production

Jang

Patnaik

Kojour

et al. 2021

IJMS

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The cystine knot protein Spätzle is a Toll receptor ligand that modulates the intracellular signaling cascade involved in the nuclear factor kappa B (NF-κB)-mediated regulation of antimicrobial peptide (AMP)-encoding genes. Spätzle-mediated activation of the Toll pathway is critical for the innate immune responses of insects against Gram-positive bacteria and fungi. In this study, the open reading frame (ORF) sequence of Spätzle-like from T. molitor (TmSpz-like) identified from the RNA sequencing dataset was cloned and sequenced. The 885-bp TmSpz-like ORF encoded a polypeptide of 294 amino acid residues. TmSpz-like comprised a cystine knot domain with six conserved cysteine residues that formed three disulfide bonds. Additionally, TmSpz-like exhibited the highest amino acid sequence similarity with T. castaneum Spätzle (TcSpz). In the phylogenetic tree, TmSpz-like and TcSpz were located within a single cluster. The expression of TmSpz-like was upregulated in the Malpighian tubules and gut tissues of T. molitor. Additionally, the expression of TmSpz-like in the whole body and gut of the larvae was upregulated at 24 h post-E. coli infection. The results of RNA interference experiments revealed that TmSpz-like is critical for the viability of E. coli-infected T. molitor larvae. Eleven AMP-encoding genes were downregulated in the E. coli-infected TmSpz-like knockdown larvae, which suggested that TmSpz-like positively regulated these genes. Additionally, the NF-κB-encoding genes (TmDorX1, TmDorX2, and TmRelish) were downregulated in the E. coli-infected TmSpz-like knockdown larvae. Thus, TmSpz-like plays a critical role in the regulation of AMP production in T. molitor in response to E. coli infection.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

TmSpz-like Plays a Fundamental Role in Response to E. coli but Not S. aureus or C. albican Infection in Tenebrio molitor via Regulation of Antimicrobial Peptide Production

Jang

Patnaik

Kojour

et al. 2021

IJMS

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“…In addition, two innate immune signaling pathways were also found to perform different roles in the regulation of RPW gut bacteria homeostasis. Although both the Rf Relish-mediated-IMD-like pathway and Rf Spätzle–mediated-Toll-like pathway mediate the production of antimicrobial peptides to confer protection and maintain the homeostasis of gut microbiota, the IMD-like pathway plays the dominant role [ 68 , 69 ]. In sum, these data suggest that RPW has the tune mechanisms to maintain appropriate intestinal immune intensity to maintain the homeostasis of gut microbiota.…”

Section: The Role Of Immune-related Factors In Maintaining the Homeostasis Of Gut Bacteria In Red Palm Weevilmentioning

confidence: 99%

The Effect of Gut Bacteria on the Physiology of Red Palm Weevil, Rhynchophorus ferrugineus Olivier and Their Potential for the Control of This Pest

Liu

et al. 2021

Insects

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Red Palm Weevil (RPW), Rhynchophorus ferrugineus Olivier, is a notorious pest, which infests palm trees and has caused great economic losses worldwide. At present, insecticide applications are still the main way to control this pest. However, pesticide resistance has been detected in the field populations of RPW. Thus, future management strategies based on the novel association biological control need be developed. Recent studies have shown that the intestinal tract of RPW is often colonized by multiple microbial species as mammals and model insects, and gut bacteria have been found to promote the growth, development and immune activity of RPW larvae by modulating nutrient metabolism. Furthermore, two peptidoglycan recognition proteins (PGRPs), PGRP-LB and PGRP-S1, can act as the negative regulators to modulate the intestinal immunity to maintain the homeostasis of gut bacteria in RPW larvae. Here, we summarized the current knowledge on the gut bacterial composition of RPW and their impact on the physiological traits of RPW larvae. In contrast with metazoans, it is much easier to make genetic engineered microbes to produce some active molecules against pests. From this perspective, because of the profound effects of gut bacteria on host phenotypes, it is promising to dissect the molecular mechanisms behind their effect on host physiology and facilitate the development of microbial resource-based management methods for pest control.

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“…TmAtt1a, TmAtt1b, TmColeA, TmColeB, and TmTLP2 AMPs were expressed in the fat bodies of T. molitor larvae after E. coli, but not S. aureus and C. albicans challenges in the survival assay. The downregulation of RfColeoptericin and RfDefensin was also confirmed in Rhynchophorus ferrugineus spätzle silenced larvae indicating that their secretion is under the regulation of the Rf Spätzle-mediated signaling pathway and was related to the compromising of R. ferrugineus innate immunity and maintenance of homeostasis of gut (Muhammad et al, 2020). This is interesting as Defensin secretion in Drosophila and Coleoptericin secretion in the cereal weevil Sitophilus are IMDdependent (Tingvall et al, 2001;Maire et al, 2018).…”

Section: Discussionmentioning

confidence: 93%

Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides

Bae

Patnaik

et al. 2021

Front. Physiol.

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Innate immunity is the ultimate line of defense against invading pathogens in insects. Unlike in the mammalian model, in the insect model, invading pathogens are recognized by extracellular receptors, which activate the Toll signaling pathway through an extracellular serine protease cascade. In the Toll-NF-κB pathway, the extracellular spätzle protein acts as a downstream ligand for Toll receptors in insects. In this study, we identified a novel Spätzle isoform (TmSpz1b) from RNA sequencing database of Tenebrio molitor. TmSpz1b was bioinformatically analyzed, and functionally characterized for the antimicrobial function by RNA interference (RNAi). The 702 bp open reading frame of TmSpz1b encoded a putative protein of 233 amino acid residues. A conserved cystine-knot domain with seven cysteine residues in TmSpz1b was involved in three disulfide bridges and the formation of a spätzle dimer. TmSpz1b was mostly expressed in the hemocytes of T. molitor late instar larvae. The mRNA expression of TmSpz1b was highly induced in the hemocytes after Escherichia coli, Staphylococcus aureus, and Candida albicans stimulation of T. molitor larvae. TmSpz1b silenced larvae were significantly more susceptible to E. coli infection. In addition, RNAi-based functional assay characterized TmSpz1b to be involved in the positive regulation of antimicrobial peptide genes in hemocytes and fat bodies. Further, the TmDorX2 transcripts were downregulated in TmSpz1b silenced individuals upon E. coli challenge suggesting the relationship to Toll signaling pathway. These results indicate that TmSpz1b is involved in the T. molitor innate immunity, causes the sequestration of Gram-negative bacteria by the regulatory action of antimicrobial peptides, and enhances the survival of T. molitor larvae.

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Spätzle Homolog-Mediated Toll-Like Pathway Regulates Innate Immune Responses to Maintain the Homeostasis of Gut Microbiota in the Red Palm Weevil, Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae)

Cited by 26 publications

References 70 publications

TmSpz-like Plays a Fundamental Role in Response to E. coli but Not S. aureus or C. albican Infection in Tenebrio molitor via Regulation of Antimicrobial Peptide Production

TmSpz-like Plays a Fundamental Role in Response to E. coli but Not S. aureus or C. albican Infection in Tenebrio molitor via Regulation of Antimicrobial Peptide Production

The Effect of Gut Bacteria on the Physiology of Red Palm Weevil, Rhynchophorus ferrugineus Olivier and Their Potential for the Control of This Pest

Tenebrio molitor Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides

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