Abstract
Chitin synthase and chitinase play crucial roles in chitin biosynthesis and degradation during insect molting. Silencing of Dicer-1 results in reduced levels of mature miRNAs and severely blocks molting in the migratory locust. However, the regulatory mechanism of miRNAs in the molting process of locusts has remained elusive. In this study, we found that in chitin metabolism, two crucial enzymes, chitin synthase (CHS) and chitinase (CHT) were regulated by miR-71 and miR-263 during nymph molting. The coding sequence of CHS1 and the 3’-untranslated region of CHT10 contain functional binding sites for miR-71 and miR-263, respectively. miR-71/miR-263 displayed cellular co-localization with their target genes in epidermal cells and directly interacted with CHS1 and CHT10 in the locust integument, respectively. Injections of miR-71 and miR-263 agomirs suppressed the expression of CHS1 and CHT10, which consequently altered chitin production of new and old cuticles and resulted in a molting-defective phenotype in locusts. Unexpectedly, reduced expression of miR-71 and miR-263 increased CHS1 and CHT10 mRNA expression and led to molting defects similar to those induced by miRNA delivery. This study reveals a novel function and balancing modulation pattern of two miRNAs in chitin biosynthesis and degradation, and it provides insight into the underlying molecular mechanisms of the molting process in locusts.
Highlights
Molting is a crucial process in insect growth and development [1,2]
We found that miR-71 and miR-263 directly repress two genes, chitin synthase1 (CHS1) and chitinase10 (CHT10), which are required for chitin biosynthesis and degradation in chitin metabolism
To identify the miRNAs associated with molting, we sequenced a transcriptome of small RNAs of the locust integument, which is an important tissue during the molting process in insects
Summary
Molting is a crucial process in insect growth and development [1,2]. Chitin, as a vital component of the cuticle of the epidermis, plays key roles in maintaining morphology and the molting process [3]. Chitin synthases are the key regulatory enzymes for chitin synthesis in insects and represent a specific target of insecticides [12]. Knockdown of the LmCHS1 gene increases the number of non-molting and abnormal molting nymphs [6]. Another paralog LmCHS2 contributes to the biosynthesis of chitin associated with the peritrophic matrix [13]. An interesting feature of CHS1 and CHT10 in locusts is that the abrupt increase and decrease in transcript levels at the end of every nymph stage (before molting) suggest that the two key enzymes are likely precisely modulated in the molting process. The underlying regulatory molecular mechanisms of enzyme-dependent chitin metabolism and the molting process have remained elusive
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