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      Dichotomous sperm in Lepidopteran insects: a biorational target for pest management

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          Abstract

          Lepidoptera are unusual in possessing two distinct kinds of sperm, regular nucleated (eupyrene) sperm and anucleate (apyrene) sperm (‘parasperm’). Sperm of both types are transferred to the female and are required for male fertility. Apyrene sperm play ‘helper’ roles, assisting eupyrene sperm to gain access to unfertilized eggs and influencing the reproductive behavior of mated female moths. Sperm development and behavior are promising targets for environmentally safer, target-specific biorational control strategies in lepidopteran pest insects. Sperm dimorphism provides a wide window in which to manipulate sperm functionality and dynamics, thereby impairing the reproductive fitness of pest species. Opportunities to interfere with spermatozoa are available not only while sperm are still in the male (before copulation), but also in the female (after copulation, when sperm are still in the male-provided spermatophore, or during storage in the female’s spermatheca). Biomolecular technologies like RNAi, miRNAs and CRISPR-Cas9 are promising strategies to achieve lepidopteran pest control by targeting genes directly or indirectly involved in dichotomous sperm production, function, or persistence.

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          Most cited references236

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          A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity.

          Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated (Cas) systems provide bacteria and archaea with adaptive immunity against viruses and plasmids by using CRISPR RNAs (crRNAs) to guide the silencing of invading nucleic acids. We show here that in a subset of these systems, the mature crRNA that is base-paired to trans-activating crRNA (tracrRNA) forms a two-RNA structure that directs the CRISPR-associated protein Cas9 to introduce double-stranded (ds) breaks in target DNA. At sites complementary to the crRNA-guide sequence, the Cas9 HNH nuclease domain cleaves the complementary strand, whereas the Cas9 RuvC-like domain cleaves the noncomplementary strand. The dual-tracrRNA:crRNA, when engineered as a single RNA chimera, also directs sequence-specific Cas9 dsDNA cleavage. Our study reveals a family of endonucleases that use dual-RNAs for site-specific DNA cleavage and highlights the potential to exploit the system for RNA-programmable genome editing.
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            Identification of novel genes coding for small expressed RNAs.

            In Caenorhabditis elegans, lin-4 and let-7 encode 22- and 21-nucleotide (nt) RNAs, respectively, which function as key regulators of developmental timing. Because the appearance of these short RNAs is regulated during development, they are also referred to as small temporal RNAs (stRNAs). We show that many 21- and 22-nt expressed RNAs, termed microRNAs, exist in invertebrates and vertebrates and that some of these novel RNAs, similar to let-7 stRNA, are highly conserved. This suggests that sequence-specific, posttranscriptional regulatory mechanisms mediated by small RNAs are more general than previously appreciated.
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              TAL effectors: customizable proteins for DNA targeting.

              Generating and applying new knowledge from the wealth of available genomic information is hindered, in part, by the difficulty of altering nucleotide sequences and expression of genes in living cells in a targeted fashion. Progress has been made in engineering DNA binding domains to direct proteins to particular sequences for mutagenesis or manipulation of transcription; however, achieving the requisite specificities has been challenging. Transcription activator-like (TAL) effectors of plant pathogenic bacteria contain a modular DNA binding domain that appears to overcome this challenge. Comprising tandem, polymorphic amino acid repeats that individually specify contiguous nucleotides in DNA, this domain is being deployed in DNA targeting for applications ranging from understanding gene function in model organisms to improving traits in crop plants to treating genetic disorders in people.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/189602
                Journal
                Front Insect Sci
                Front Insect Sci
                Front. Insect Sci.
                Frontiers in Insect Science
                Frontiers Media S.A.
                2673-8600
                2673-8600
                23 August 2023
                2023
                : 3
                : 1198252
                Affiliations
                [1] 1 Department of Zoology, University of Delhi , Delhi, India
                [2] 2 Department of Life Sciences, University of Bath , Bath, United Kingdom
                [3] 3 Milner Centre for Evolution, University of Bath , Bath, United Kingdom
                Author notes

                Edited by: Bernard Moussian, Université Côte d’Azur, France

                Reviewed by: Romano Dallai, University of Siena, Italy; Bruce Hay, California Institute of Technology, United States

                *Correspondence: Stuart E. Reynolds, s.e.reynolds@ 123456bath.ac.uk
                Article
                10.3389/finsc.2023.1198252
                10926456
                38469506
                65d6ea60-beec-4aa1-94e5-17932c637f66
                Copyright © 2023 Seth, Yadav and Reynolds

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 31 March 2023
                : 31 July 2023
                Page count
                Figures: 4, Tables: 3, Equations: 0, References: 236, Pages: 26, Words: 15892
                Funding
                RS sincerely acknowledges the financial support from International Atomic Energy Agency(IAEA), Vienna funded under FAO/IAEA Coordinated Research Projects.
                Categories
                Insect Science
                Review
                Custom metadata
                Insect Physiology

                spermatozoa,sperm activation,sperm motility,initiatorin,serine endopeptidase,lepidoptera,pest management,rnai

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