Insulin‐like peptides of the legume pod borer, <i>Maruca vitrata</i>, and their mediation effects on hemolymph trehalose level, larval development, and adult reproduction

Baki, Abdullah Al; Lee, Dae‐Weon; Jung, Jin Kyo; Kim, Yonggyun

doi:10.1002/arch.21524

Cited by 9 publications

(9 citation statements)

References 51 publications

(59 reference statements)

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“…Trehalose homeostasis is mainly controlled by enzyme activities of TPS for trehalose synthesis and TRE for trehalose degradation (Becker et al, 1996). Silencing TPS can significantly downregulate hemolymph trehalose level, while silencing TRE expression can upregulate its level in M. vitrata (Al Baki et al, 2019a). In our current study, ILP mutants showed upregulated TPS expression but downregulated TRE expression.…”

Section: Discussionsupporting

confidence: 48%

“…They play important roles in mediating immature growth and adult reproduction (Al Baki et al, 2018a, 2020. Furthermore, their expression patterns are similar among different developmental stages and tissues (Al Baki et al, 2019a). Furthermore, IIS components responding to ILPs are well conserved in M. vitrata (Al Baki et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…A disaccharide, trehalose, is the main hemolymph sugar of M. vitrata larvae, in which its titers fluctuate with feeding activity due to diel rhythmicity of feeding behavior (Al Baki et al, 2018a). Especially, feeding, including nutrient uptake, can stimulate Mv-ILP expression and lead to a basal level of trehalose titer, while starvation can suppress Mv-ILP expression and lead to a hypertrehalosemic state (Al Baki et al, 2019a). Trehalose homeostasis is mainly controlled by enzyme activities of TPS for trehalose synthesis and TRE for trehalose degradation (Becker et al, 1996).…”

Section: Discussionmentioning

confidence: 99%

“…Two ILP deletion mutants of M. vitrata showed impaired adult reproduction. The two ILPs of M. vitrata can mediate ovarian development of adult females of M. vitrata (Al Baki et al, 2019a). Oocyte development in the ovariole begins with active mitotic activity in the germarium, followed by vitellogenesis incorporating Vg into growing oocytes and finalized chorion formation outside mature oocytes.…”

Section: Discussionmentioning

confidence: 99%

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Physiological Alterations in Deletion Mutants of Two Insulin-Like Peptides Encoded in Maruca vitrata Using CRISPR/Cas9

2021

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Most insect species encode multiple insulin-like peptides (ILPs) that exhibit functional overlaps in mediating physiological processes such as development and reproduction. Why do they need multiple ILPs? To address this question, we tested a hypothesis of the requirement of multiple ILPs by generating mutants lacking individual ILP genes using the CRISPR/Cas9 technology. Two ILPs (ILP1 and ILP2) in the legume pod borer, Maruca vitrata, mediate similar physiological processes such as hemolymph sugar level, larval development, and adult reproduction. Individual knock-out mutants (ΔILP1 and ΔILP2) were generated. They showed successful development from larvae to adults. However, they suffered from high hemolymph sugar levels by enhancing trehalose titers in the hemolymph. The hyperglycemic effect was more evident in ΔILP2 mutants than in ΔILP1 mutants. Both mutants showed increased expression of trehalose-6-phosphate synthase but suppressed expression of trehalase. These mutants also showed altered expression patterns of insulin signaling components. Expression levels of insulin receptor and Akt genes were upregulated, while those of FOXO and Target of rapamycin genes were downregulated in these mutants. These alterations of signal components resulted in significant retardation of immature development and reduced body sizes. ΔILP1 or ΔILP2 females exhibited poor oocyte development. Bromo-uridine incorporation was much reduced at the germarium of ovarioles of these mutants compared with wild females. Expression of the vitellogenin gene was also reduced in these mutants. Furthermore, males of these deletion mutants showed impaired reproductive activities when they mated with wild-type females. These results suggest that both ILPs are required for mediating larval development and adult reproduction in M. vitrata.

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Section: Discussionsupporting

confidence: 48%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Physiological Alterations in Deletion Mutants of Two Insulin-Like Peptides Encoded in Maruca vitrata Using CRISPR/Cas9

2021

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“…The expression of TPS3 increased 48 h after GSK-3 interference, probably because the structure of TPS3 is different from that of TPS1 and TPS2, so their functions are also different. Al Baki MA et al found that the chyme content of Alpaki was increased after Ilp and InR RNAi (Al Baki et al, 2019), which is consistent with the results of this study (Figures 6A,B), that is, glycogen and glucose are converted into trehalose after dsGSK-3 injection, which leads to an increase in glucose metabolism and maintains the balance of glucose metabolism in insects, which is consistent with previous studies (Mitsumasu et al, 2010;Tang et al, 2012).…”

Section: Discussionsupporting

confidence: 92%

Regulatory Functions of Nilaparvata lugens GSK-3 in Energy and Chitin Metabolism

Ding

et al. 2020

Front. Physiol.

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Glucose metabolism is a biologically important metabolic process. Glycogen synthase kinase (GSK-3) is a key enzyme located in the middle of the sugar metabolism pathway that can regulate the energy metabolism process in the body through insulin signaling. This paper mainly explores the regulatory effect of glycogen synthase kinase on the metabolism of glycogen and trehalose in the brown planthopper (Nilaparvata lugens) by RNA interference. In this paper, microinjection of the target double-stranded GSK-3 (dsGSK-3) effectively inhibited the expression of target genes in N. lugens. GSK-3 gene silencing can effectively inhibit the expression of target genes (glycogen phosphorylase gene, glycogen synthase gene, trehalose-6-phosphate synthase 1 gene, and trehalose-6-phosphate synthase 2 gene) in N. lugens and trehalase activity, thereby reducing glycogen and glucose content, increasing trehalose content, and regulating insect trehalose balance. GSK-3 can regulate the genes chitin synthase gene and glucose-6-phosphate isomerase gene involved in the chitin biosynthetic pathway of N. lugens. GSK-3 gene silencing can inhibit the synthesis of chitin N. lugens, resulting in abnormal phenotypes and increased mortality. These results indicated that a low expression of GSK-3 in N. lugens can regulate the metabolism of glycogen and trehalose through the insulin signal pathway and energy metabolism pathway, and can regulate the biosynthesis of chitin, which affects molting and wing formation. The relevant research results will help us to more comprehensively explore the molecular mechanism of the regulation of energy and chitin metabolism of insect glycogen synthase kinases in species such as N. lugens.

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Sublethal concentration of emamectin benzoate inhibits the growth of gypsy moth by inducing digestive dysfunction and nutrient metabolism disorder

Bai

et al. 2021

Pest Management Science

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BACKGROUND Gypsy moth (Lymantria dispar) is one of the most important pests in the world. Emamectin benzoate (EMB) is widely used in the control of agricultural and forestry pests. Here, we explored the sublethal effects of EMB on gypsy moths in order to better understand the toxicological mechanism of EMB. RESULTS The sublethal concentration of EMB exposure significantly decreased the larvae body weight. To further explore the mechanism, indicators related to digestion and nutrient metabolism were detected. The results showed that EMB exposure caused midgut damage, reduced the activities of digestive enzymes and changed the content of sugar and amino acids. Moreover, the expression of insulin/phosphoinositide‐3‐kinase (PI3K)/forkhead box protein O (FoxO) pathway and sugar metabolism‐related genes was abnormal. The expression of insulin receptor (InR), chico, PI3K, and protein kinase B (Akt) significantly reduced, and that of phosphatase and tensin homologue (PTEN) and FoxO increased. The expression of glycogen phosphorylase (GP) was upregulation and that of glycogen synthase (GS), trehalase (TRE) and trehalose‐phosphate synthase (TPS) were downregulation. All results indicated that EMB inhibits the growth of gypsy moth by inducing midgut injury, digestive dysfunction and nutrient metabolism disorder. In addition, EMB caused midgut injury may be related to apoptosis or a collateral effect of the damage in other tissues, and more extensive and deeper research is still needed to investigate the detailed mechanism. CONCLUSION Our finding strengthens the understanding of the sublethal effect of EMB, and provides a theoretical basis for the application of EMB in the prevention and control of gypsy moth.

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Insulin‐like peptides of the legume pod borer, Maruca vitrata, and their mediation effects on hemolymph trehalose level, larval development, and adult reproduction

Cited by 9 publications

References 51 publications

Physiological Alterations in Deletion Mutants of Two Insulin-Like Peptides Encoded in Maruca vitrata Using CRISPR/Cas9

Physiological Alterations in Deletion Mutants of Two Insulin-Like Peptides Encoded in Maruca vitrata Using CRISPR/Cas9

Regulatory Functions of Nilaparvata lugens GSK-3 in Energy and Chitin Metabolism

Sublethal concentration of emamectin benzoate inhibits the growth of gypsy moth by inducing digestive dysfunction and nutrient metabolism disorder

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