Genome-wide analysis of Panonychus citri microRNAs with a focus on potential insecticidal activity of 4 microRNAs to eggs and nymphs.

Panonychus citri McGregor (Acari: Tetranychidae), a destructive citrus pest, causes considerable annual economic losses due to its short lifespan and rapid resistance development. MicroRNA (miRNA)-induced RNA interference is a promising approach for pest control because of endogenous regulation of pest growth and development. To search for miRNAs with potential insecticidal activity in P. citri, genome-wide analysis of miRNAs at different developmental stages was conducted, resulting in the identification of 136 miRNAs, including 73 known and 63 novel miRNAs. A total of 17 isomiRNAs and 12 duplicated miRNAs were characterized. MiR-1 and miR-252-5p were identified as reference miRNAs for P. citri and Tetranychus urticae. Based on differential expression analysis, treatments with miR-let-7a and miR-315 mimics and the miR-let-7a antagomir significantly reduced the egg hatch rate and resulted in abnormal egg development. Overexpression or downregulation of miR-34-5p and miR-305-5p through feeding significantly decreased the adult eclosion rate and caused molting defects. The 4 miRNAs, miR-let-7a, miR-315, miR-34-5p, and miR-305-5p, had important regulatory functions and insecticidal properties in egg hatching and adult eclosion. In general, these data advance our understanding of miRNAs in mite biology, which can assist future studies on insect-specific miRNA-based green pest control technology.

[1]  Zongnan Li,et al.  The Key Role of Fatty Acid Synthase in Lipid Metabolism and Metamorphic Development in a Destructive Insect Pest, Spodoptera litura (Lepidoptera: Noctuidae) , 2022, International journal of molecular sciences.

[2]  Xiwu Gao,et al.  MicroRNA-263b confers imidacloprid resistance in Sitobion miscanthi (Takahashi) by regulating the expression of the nAChRβ1 subunit. , 2022, Pesticide biochemistry and physiology.

[3]  M. Gong,et al.  Identification and profiling of Sogatella furcifera microRNAs and their potential roles in regulating the developmental transitions of nymph–adult , 2022, Insect molecular biology.

[4]  B. Pang,et al.  MicroRNA miR‐2765‐3p regulates reproductive diapause by targeting FoxO in Galeruca daurica , 2022, Insect science.

[5]  Zhen Li,et al.  MicroRNAs miR-14 and miR-2766 regulate tyrosine hydroxylase to control larval-pupal metamorphosis in Helicoverpa armigera. , 2022, Pest management science.

[6]  Qinghe Zhang,et al.  Selection and Evaluation of Reference Genes for miRNA Expression Analysis in Bemisia tabaci Under Insecticide Tolerance , 2022, Frontiers in Genetics.

[7]  A. Christoffels,et al.  microRNA profile of Hermetia illucens (black soldier fly) and its implications on mass rearing , 2022, PloS one.

[8]  Linhong Li,et al.  miR-34-5p, a novel molecular target against lepidopteran pests , 2022, Journal of Pest Science.

[9]  F. Feng,et al.  MiR‐3017b contributes to metamorphosis by targeting sarco/endoplasmic reticulum Ca2+ ATPase in Tribolium castaneum , 2022, Insect molecular biology.

[10]  Yongjun Lin,et al.  Trans-kingdom expression of an insect endogenous microRNA in rice enhances resistance to striped stem borer Chilo suppressalis. , 2021, Pest management science.

[11]  A. Raikhel,et al.  Juvenile hormone regulation of microRNAs is mediated by E75 in the Dengue vector mosquito Aedes aegypti , 2021, Proceedings of the National Academy of Sciences.

[12]  C. Pirovani,et al.  Genome-wide identification of miRNAs and target regulatory network in the invasive ectoparasitic mite Varroa destructor. , 2021, Genomics.

[13]  Yi-jun Zhou,et al.  MicroRNA-315-5p promotes rice black-streaked dwarf virus infection by targeting a melatonin receptor in the small brown planthopper. , 2021, Pest management science.

[14]  B. Alto,et al.  Mosquito responses to lethal and nonlethal effects of predation and an insect growth regulator , 2021, Ecosphere.

[15]  Sheng Li,et al.  The steroid‐induced microRNA let‐7 regulates developmental growth by targeting cdc7 in the Drosophila fat body , 2020, Insect science.

[16]  V. Grbić,et al.  A Leaf-Mimicking Method for Oral Delivery of Bioactive Substances Into Sucking Arthropod Herbivores , 2020, Frontiers in Plant Science.

[17]  P. Jin,et al.  Drosophila Myc restores immune homeostasis of Imd pathway via activating miR-277 to inhibit imd/Tab2 , 2020, PLoS genetics.

[18]  Zhaofei Li,et al.  JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184 , 2020, PLoS pathogens.

[19]  Xu Yang,et al.  miR-34 regulates larval growth and wing morphogenesis by directly modulating ecdysone signalling and cuticle protein in Bombyx mori , 2020, RNA biology.

[20]  Zhi-qiang Tian,et al.  MicroRNA-277 regulates dopa decarboxylase to control larval-pupal and pupal-adult metamorphosis of Helicoverpa armigera. , 2020, Insect biochemistry and molecular biology.

[21]  J. Niu,et al.  RNAi of the nuclear receptor HR3 suggests a role in the molting process of the spider mite Panonychus citri , 2020, Experimental and Applied Acarology.

[22]  Jinsong Zhu,et al.  Broad spectrum immunomodulatory effects of Anopheles gambiae microRNAs and their use for transgenic suppression of Plasmodium , 2020, PLoS pathogens.

[23]  Ying Lin,et al.  bmo-miR-2739 and the novel microRNA miR-167 coordinately regulate the expression of the vitellogenin receptor in Bombyx mori oogenesis , 2020, Development.

[24]  J. Qian,et al.  MiR-315 is required for neural development and represses the expression of dFMR1 in Drosophila melanogaster. , 2020, Biochemical and biophysical research communications.

[25]  A. Handler,et al.  miRNA-1-3p is an early embryonic male sex-determining factor in the Oriental fruit fly Bactrocera dorsalis , 2020, Nature Communications.

[26]  ChuanShan Zou,et al.  Fenoxycarb and methoxyfenozide (RH-2485) affected development and chitin synthesis through disturbing glycometabolism in Lymantria dispar larvae. , 2020, Pesticide biochemistry and physiology.

[27]  Q. Song,et al.  Jinggangmycin-Induced UDP-Glycosyltransferase 1-2-Like Is a Positive Modulator of Fecundity and Population Growth in Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) , 2019, Front. Physiol..

[28]  Hong-yu Zhang,et al.  MicroRNA Let‐7 targets the ecdysone signaling pathway E75 gene to control larval–pupal development in Bactrocera dorsalis , 2019, Insect science.

[29]  G. Smagghe,et al.  Genome-Wide Analysis of MicroRNAs in Relation to Pupariation in Oriental Fruit Fly , 2019, Front. Physiol..

[30]  Jiasheng Song,et al.  The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Krüppel-homolog 1 , 2018, Development.

[31]  J. Jen,et al.  A Comprehensive Approach to Sequence-oriented IsomiR annotation (CASMIR): demonstration with IsomiR profiling in colorectal neoplasia , 2018, BMC Genomics.

[32]  A. Raikhel,et al.  HR38, an ortholog of NR4A family nuclear receptors, mediates 20-hydroxyecdysone regulation of carbohydrate metabolism during mosquito reproduction. , 2018, Insect biochemistry and molecular biology.

[33]  K. Etebari,et al.  A comparative analysis of corpora allata-corpora cardiaca microRNA repertoires revealed significant changes during mosquito metamorphosis. , 2018, Insect biochemistry and molecular biology.

[34]  Junjie Luo,et al.  MicroRNA duplication accelerates the recruitment of new targets during vertebrate evolution , 2018, RNA.

[35]  G. Smagghe,et al.  Characterization and expression patterns of key ecdysteroid biosynthesis and signaling genes in a spider mite (Panonychus citri). , 2017, Insect biochemistry and molecular biology.

[36]  Yuhui Yang,et al.  Identification and Evaluation of Suitable Reference Genes for Normalization of MicroRNA Expression in Helicoverpa armigera (Lepidoptera: Noctuidae) Using Quantitative Real-Time PCR , 2017, Journal of insect science.

[37]  Yanchao Liu,et al.  Identification of Differentially Expressed microRNAs between the Fenpropathrin Resistant and Susceptible Strains in Tetranychus cinnabarinus , 2016, PloS one.

[38]  Dahua Chen,et al.  MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts , 2016, Proceedings of the National Academy of Sciences.

[39]  X. Hong,et al.  Identification of Wolbachia-responsive microRNAs in the two-spotted spider mite, Tetranychus urticae , 2014, BMC Genomics.

[40]  W. Dou,et al.  An analysis of the small RNA transcriptome of four developmental stages of the citrus red mite (Panonychus citri) , 2014, Insect molecular biology.

[41]  Xuguo Zhou,et al.  Identification and Developmental Profiling of microRNAs in Diamondback Moth, Plutellaxylostella (L.) , 2013, PloS one.

[42]  Jing Xia,et al.  A meta-analysis revealed insights into the sources, conservation and impact of microRNA 5′-isoforms in four model species , 2013, Nucleic acids research.

[43]  M. Lorenzen,et al.  Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum , 2013, BMC Genomics.

[44]  Eugene Berezikov,et al.  Evolution of microRNA diversity and regulation in animals , 2011, Nature Reviews Genetics.

[45]  Sebastian D. Mackowiak,et al.  miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades , 2011, Nucleic acids research.

[46]  Jun Wang,et al.  Monitoring of resistance to spirodiclofen and five other acaricides in Panonychus citri collected from Chinese citrus orchards. , 2010, Pest management science.

[47]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[48]  Norbert Perrimon,et al.  Functional screening identifies miR-315 as a potent activator of Wingless signaling , 2007, Proceedings of the National Academy of Sciences.

[49]  Jason S. Cumbie,et al.  High-Throughput Sequencing of Arabidopsis microRNAs: Evidence for Frequent Birth and Death of MIRNA Genes , 2007, PloS one.

[50]  T. Gotoh,et al.  Geographic variation of susceptibility to acaricides in two spider mite species, Panonychus osmanthi and P. citri (Acari: Tetranychidae) in Japan , 2004 .

[51]  Ivo L. Hofacker,et al.  Vienna RNA secondary structure server , 2003, Nucleic Acids Res..

[52]  Q. Wang,et al.  Effects of Three Insect Growth Regulators on Encarsia formosa (Hymenoptera: Aphelinidae), an Endoparasitoid of Bemisia tabaci (Hemiptera: Aleyrodidae) , 2016, Journal of Economic Entomology.