Please wait a minute...
Journal of Integrative Agriculture  2019, Vol. 18 Issue (4): 729-747    DOI: 10.1016/S2095-3119(18)61976-8
Review Advanced Online Publication | Current Issue | Archive | Adv Search |
Progress and prospects of noncoding RNAs in insects
LI Mei-zhen1, XIAO Hua-mei2, HE Kang1, LI Fei1 
1 Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, P.R.China
2 College of Life Sciences and Resource Environment, Yichun University, Yichun 336000, P.R.China
Download:  PDF (622KB) ( )  
Export:  BibTeX | EndNote (RIS)      
Abstract  
With the rapid development of high-throughput sequencing technology and bioinformatics algorithms, great progress has been made in the field of noncoding RNA (ncRNA) in the last decade.  RNA molecules have been regarded only as a messenger between DNA and protein for decades, but now they have new roles in the biological process as ncRNAs.  A growing number of ncRNAs have been identified in insects from the RNA-Seq data of small RNA libraries or transcriptomes.  ncRNAs have varied regulatory functions at the epigenetic, transcriptional, or post-transcriptional levels, and participate in almost all types of biological processes.  Here, we review the research progress of four kinds of ncRNAs, including microRNA (miRNA), Piwi-interacting RNA (piRNA), circular RNA (circRNA), and long noncoding RNA (lncRNA) in insects.  The discovery, biogenesis mechanisms, and regulatory functions of these ncRNAs are presented here to provide a comprehensive understanding of insect ncRNAs and to promote the application of ncRNAs in insect pest control. 
Keywords:  miRNA        piRNA        circRNA        lncRNA        biogenesis        prediction        regulatory functions  
Received: 25 December 2017   Accepted:
Fund: The study was supported by the National Key Research and Development Program (2017YFD0200900, 2017YFD0200904, 2017YFC1200602 and 2016YFC1200600), and the National Natural Science Foundation of China (31772238, 31760514 and 31701785).
Corresponding Authors:  Correspondence XIAO Hua-mei, E-mail: xiaohuamei625@163.com; LI Fei, E-mail: lifei18@zju.edu.cn   
About author:  LI Mei-zhen, E-mail: limeizhen@zju.edu.cn;

Cite this article: 

LI Mei-zhen, XIAO Hua-mei, HE Kang, LI Fei. 2019. Progress and prospects of noncoding RNAs in insects. Journal of Integrative Agriculture, 18(4): 729-747.

Aravin A A, Hannon G J, Brennecke J. 2007. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science, 318, 761–764.
Aravin A A, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, Gaasterland T, Meyer J, Tuschl T. 2003. The small RNA profile during Drosophila melanogaster development. Developmental Cell, 5, 337–350.
Aravin A A, Naumova N M, Tulin A V, Vagin V V, Rozovsky Y M, Gvozdev V A. 2001. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Current Biology, 11, 1017–1027.
Asgari S. 2013. MicroRNA functions in insects. Insect Biochemistry and Molecular Biology, 43, 388–397.
Ashby R, Foret S, Searle I, Maleszka R. 2016. MicroRNAs in honey bee caste determination. Scientific Reports, 6, 18794.
Ashwal-Fluss R, Meyer M, Pamudurti N R, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S. 2014. circRNA biogenesis competes with pre-mRNA splicing. Molecular Cell, 56, 55–66.
Bartel D P. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.
Bartel D P. 2009. MicroRNAs: Target recognition and regulatory functions. Cell, 136, 215–233.
Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E. 2006. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes & Development, 20, 1885–1898.
Behura S K,Whitfield C W. 2010. Correlated expression patterns of microRNA genes with age-dependent behavioural changes in honeybee. Insect Molecular Biology, 19, 431–439.
Bejarano F, Smibert P, Lai E C. 2010. miR-9a prevents apoptosis during wing development by repressing Drosophila LIM-only. Developmental Biology, 338, 63–73.
Belles X. 2017. MicroRNAs and the evolution of insect metamorphosis. Annual Review of Entomology, 62, 111–125.
Bertone P, Stolc V, Royce T E, Rozowsky J S, Urban A E, Zhu X, Rinn J L, Tongprasit W, Samanta M, Weissman S, Gerstein M, Snyder M. 2004. Global identification of human transcribed sequences with genome tiling arrays. Science, 306, 2242–2246.
Borchert G M, Lanier W, Davidson B L. 2006. RNA polymerase III transcribes human microRNAs. Nature Structural & Molecular Biology, 13, 1097–1101.
Brennecke J, Aravin A A, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon G J. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell, 128, 1089–1103.
Brennecke J, Malone C D, Aravin A A, Sachidanandam R, Stark A, Hannon G J. 2008. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science, 322, 1387–1392.
Brockdorff N, Ashworth A, Kay G F, McCabe V M, Norris D P, Cooper P J, Swift S, Rastan S. 1992. The product of the mouse XIST gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell, 71, 515–526.
Brown C J, Hendrich B D, Rupert J L, Lafreniere R G, Xing Y, Lawrence J, Willard H F. 1992. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell, 71, 527–542.
Carninci P, Kasukawa T, Katayama S, Gough J, Frith M C, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic V B, Brenner S E, Batalov S, Forrest A R, Zavolan M, Davis M J, Wilming L G, Aidinis V, et al. 2005. The transcriptional landscape of the mammalian genome. Science, 309, 1559–1563.
Caygill E E, Johnston L A. 2008. Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Current Biology, 18, 943–950.
Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I. 2011. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell, 147, 358–369.
Chambeyron S, Popkova A, Payen-Groschene G, Brun C, Laouini D, Pelisson A, Bucheton A. 2008. piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proceedings of the National Academy of Sciences of the United States of America, 105, 14964–14969.
Cheloufi S, Dos Santos C O, Chong M M, Hannon G J. 2010. A Dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature, 465, 584–589.
Chen B, Zhang Y, Zhang X, Jia S, Chen S, Kang L. 2016. Genome-wide identification and developmental expression profiling of long noncoding RNAs during Drosophila metamorphosis. Scientific Reports, 6, 23330.
Chen J, Liang Z, Liang Y, Pang R, Zhang W. 2013. Conserved microRNAs miR-8-5p and miR-2a-3p modulate chitin biosynthesis in response to 20-hydroxyecdysone signaling in the brown planthopper, Nilaparvata lugens. Insect Biochemistry and Molecular Biology, 43, 839–848.
Chen L L. 2016. The biogenesis and emerging roles of circular RNAs. Nature Reviews: Molecular Cell Biology, 17, 205–211.
Chen M J, Chen L K, Lai Y S, Lin Y Y, Wu D C, Tung Y A, Liu K Y, Shih H T, Chen Y J, Lin Y L, Ma L T, Huang J L, Wu P C, Hong M Y, Chu F H, Wu J T, Li W H, Chen C Y. 2016. Integrating RNA-seq and ChIP-seq data to characterize long non-coding RNAs in Drosophila melanogaster. BMC Genomics, 17, 220.
Chen Y, Dai H, Chen S, Zhang L, Long M. 2011. Highly tissue specific expression of Sphinx supports its male courtship related role in Drosophila melanogaster. PLoS ONE, 6, e18853.
Conn S J, Pillman K A, Toubia J, Conn V M, Salmanidis M, Phillips C A, Roslan S, Schreiber A W, Gregory P A, Goodall G J. 2015. The RNA binding protein quaking regulates formation of circRNAs. Cell, 160, 1125–1134.
Conrad T, Akhtar A. 2012. Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nature Reviews Genetics, 13, 123–134.
Cox D N, Chao A, Baker J, Chang L, Qiao D, Lin H. 1998. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes & Development, 12, 3715–3727.
Cristino A S, Tanaka E D, Rubio M, Piulachs M D, Belles X. 2011. Deep sequencing of organ- and stage-specific microRNAs in the evolutionarily basal insect Blattella germanica (L.) (Dictyoptera, Blattellidae). PLoS ONE, 6, e19350.
Deng W, Lin H. 2002. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Developmental Cell, 2, 819–830.
Denli A M, Tops B B, Plasterk R H, Ketting R F, Hannon G J. 2004. Processing of primary microRNAs by the microprocessor complex. Nature, 432, 231–235.
Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles D G, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown J B, Lipovich L, Gonzalez J M, Thomas M, Davis C A, et al. 2012. The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Research, 22, 1775–1789.
Ebert M S, Neilson J R, Sharp P A. 2007. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nature Methods, 4, 721–726.
Epstein Y, Perry N, Volin M, Zohar-Fux M, Braun R, Porat-Kuperstein L, Toledano H. 2017. miR-9a modulates maintenance and ageing of Drosophila germline stem cells by limiting N-cadherin expression. Nature Communications, 8, 600.
Etebari K, Asad S, Zhang G, Asgari S. 2016. Identification of Aedes aegypti long intergenic non-coding RNAs and their association with wolbachia and dengue virus infection. PLoS Neglected Tropical Diseases, 10, e0005069.
Etebari K, Furlong M J, Asgari S. 2015. Genome wide discovery of long intergenic non-coding RNAs in diamondback moth (Plutella xylostella) and their expression in insecticide resistant strains. Scientific Reports, 5, 14642.
Fatica A, Bozzoni I. 2014. Long non-coding RNAs: new players in cell differentiation and development. Nature Reviews Genetics, 15, 7–21.
Forman J J, Legesse-Miller A, Coller H A. 2008. A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proceedings of the National Academy of Sciences of the United States of America, 105, 14879–14884.
Freitas F C P, Pires C V, Claudianos C, Cristino A S, Simoes Z L P. 2017. MicroRNA-34 directly targets pair-rule genes and cytoskeleton component in the honey bee. Scientific Reports, 7, 40884.
Gomez-Orte E, Belles X. 2009. MicroRNA-dependent metamorphosis in hemimetabolan insects. Proceedings of the National Academy of Sciences of the United States of America, 106, 21678–21682.
Griffiths-Jones S, Grocock R J, van Dongen S, Bateman A, Enright A J. 2006. miRBase: MicroRNA sequences, targets and gene nomenclature. Nucleic Acids Research, 34, D140–D144.
Grimaud C, Becker P B. 2009. The dosage compensation complex shapes the conformation of the X chromosome in Drosophila. Genes & Development, 23, 2490–2495.
Gunawardane L S, Saito K, Nishida K M, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi M C. 2007. A slicer-mediated mechanism for repeat-associated siRNA 5´ end formation in Drosophila. Science, 315, 1587–1590.
Ha M, Kim V N. 2014. Regulation of microRNA biogenesis. Nature Reviews: Molecular Cell Biology, 15, 509–524.
Hammond S M, Boettcher S, Caudy A A, Kobayashi R, Hannon G J. 2001. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science, 293, 1146–1150.
Han B W, Wang W, Li C, Weng Z, Zamore P D. 2015. Noncoding RNA. piRNA-guided transposon cleavage initiates Zucchini-dependent, phased piRNA production. Science, 348, 817–821.
Han J, Lee Y, Yeom K H, Kim Y K, Jin H, Kim V N. 2004. The Drosha-DGCR8 complex in primary microRNA processing. Genes & Development, 18, 3016–3027.
Han J, Lee Y, Yeom K H, Nam J W, Heo I, Rhee J K, Sohn S Y, Cho Y, Zhang B T, Kim V N. 2006. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell, 125, 887–901.
Harries L W. 2014. MicroRNAs as mediators of the ageing process. Genes, 5, 656–670.
Hayashi R, Schnabl J, Handler D, Mohn F, Ameres S L, Brennecke J. 2016. Genetic and mechanistic diversity of piRNA 3´-end formation. Nature, 539, 588–592.
He K, Sun Y, Xiao H, Ge C, Li F, Han Z. 2017. Multiple miRNAs jointly regulate the biosynthesis of ecdysteroid in the holometabolous insects, Chilo suppressalis. RNA, 23, 1817–1833.
Herzog V A, Lempradl A, Trupke J, Okulski H, Altmutter C, Ruge F, Boidol B, Kubicek S, Schmauss G, Aumayr K, Ruf M, Pospisilik A, Dimond A, Senergin H B, Vargas M L, Simon J A, Ringrose L. 2014. A strand-specific switch in noncoding transcription switches the function of a Polycomb/Trithorax response element. Nature Genetics, 46, 973–981.
Huang S, Yang B, Chen B J, Bliim N, Ueberham U, Arendt T, Janitz M. 2017. The emerging role of circular RNAs in transcriptome regulation. Genomics, 109, 401–407.
Humann F C, Tiberio G J, Hartfelder K. 2013. Sequence and expression characteristics of long noncoding RNAs in honey bee caste development - Potential novel regulators for transgressive ovary size. PLoS ONE, 8, e78915.
Huntzinger E, Izaurralde E. 2011. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nature Reviews: Genetics, 12, 99–110.
Hussain M, Asgari S. 2010. Functional analysis of a cellular microRNA in insect host-ascovirus interaction. Journal of Virology, 84, 612–620.
Hussain M, Asgari S. 2014. MicroRNAs as mediators of insect host-pathogen interactions and immunity. Journal of Insect Physiology, 70, 151–158.
Huttenhofer A, Schattner P, Polacek N. 2005. Non-coding RNAs: hope or hype? Trends in Genetics, 21, 289–297.
Ipsaro J J, Haase A D, Knott S R, Joshua-Tor L, Hannon G J. 2012. The structural biochemistry of zucchini implicates it as a nuclease in piRNA biogenesis. Nature, 491, 279–283.
Iwasaki Y W, Siomi M C, Siomi H. 2015. PIWI-Interacting RNA: Its biogenesis and functions. Annual Review of Biochemistry, 84, 405–433.
Izumi N, Shoji K, Sakaguchi Y, Honda S, Kirino Y, Suzuki T, Katsuma S,Tomari Y. 2016. Identification and functional analysis of the Pre-piRNA 3´ Trimmer in silkworms. Cell, 164, 962–973.
Jeck W R, Sharpless N E. 2014. Detecting and characterizing circular RNAs. Nature Biotechnology, 32, 453–461.
Jeck W R, Sorrentino J A, Wang K, Slevin M K, Burd C E, Liu J, Marzluff W F, Sharpless N E. 2013. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA, 19, 141–157.
Jiang J, Ge X, Li Z, Wang Y, Song Q, Stanley D W, Tan A, Huang Y. 2013. MicroRNA-281 regulates the expression of ecdysone receptor (EcR) isoform B in the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology, 43, 692–700.
Jonas S, Izaurralde E. 2015. Towards a molecular understanding of microRNA-mediated gene silencing. Nature Reviews Genetics, 16, 421–433.
Kamminga L M, Luteijn M J, den Broeder M J, Redl S, Kaaij L J, Roovers E F, Ladurner P, Berezikov E, Ketting R F. 2010. Hen1 is required for oocyte development and piRNA stability in zebrafish. EMBO Journal, 29, 3688–3700.
Kapranov P, Cawley S E, Drenkow J, Bekiranov S, Strausberg R L, Fodor S P, Gingeras T R. 2002. Large-scale transcriptional activity in chromosomes 21 and 22. Science, 296, 916–919.
Karres J S, Hilgers V, Carrera I, Treisman J, Cohen S M. 2007. The conserved microRNA MiR-8 tunes atrophin levels to prevent neurodegeneration in drosophila. Cell, 131, 136–145.
Kawaoka S, Hayashi N, Katsuma S, Kishino H, Kohara Y, Mita K,Shimada T. 2008. Bombyx small RNAs: Genomic defense system against transposons in the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology, 38, 1058–1065.
Kawaoka S, Izumi N, Katsuma S, Tomari Y. 2011. 3´ end formation of PIWI-interacting RNAs in vitro. Molecular Cell, 43, 1015–1022.
Khalil A M, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein B E, van Oudenaarden A, Regev A, Lander E S, Rinn J L. 2009. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proceedings of the National Academy of Sciences of the United States of America, 106, 11667–11672.
Khurana J S, Wang J, Xu J, Koppetsch B S, Thomson T C, Nowosielska A, Li C, Zamore P D, Weng Z, Theurkauf W E. 2011. Adaptation to P element transposon invasion in Drosophila melanogaster. Cell, 147, 1551–1563.
Khurana J S, Xu J, Weng Z, Theurkauf W E. 2010. Distinct functions for the Drosophila piRNA pathway in genome maintenance and telomere protection. PLoS Genetics, 6, e1001246.
Khvorova A, Reynolds A, Jayasena S D. 2003. Functional siRNAs and miRNAs exhibit strand bias. Cell, 115, 209–216.
Kidwell M G, Kidwell J F, Sved J A. 1977. Hybrid dysgenesis in DROSOPHILA MELANOGASTER: A syndrome of aberrant traits including mutation, sterility and male recombination. Genetics, 86, 813–833.
Kim T K, Hemberg M, Gray J M, Costa A M, Bear D M, Wu J, Harmin D A, Laptewicz M, Barbara-Haley K, Kuersten S, Markenscoff-Papadimitriou E, Kuhl D, Bito H, Worley P F, Kreiman G, Greenberg M E. 2010. Widespread transcription at neuronal activity-regulated enhancers. Nature, 465, 182–187.
Kim V N, Han J, Siomi M C. 2009. Biogenesis of small RNAs in animals. Nature Reviews: Molecular Cell Biology, 10, 126–139.
Kiuchi T, Koga H, Kawamoto M, Shoji K, Sakai H, Arai Y, Ishihara G, Kawaoka S, Sugano S, Shimada T, Suzuki Y, Suzuki M G, Katsuma S. 2014. A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature, 509, 633–636.
Kiya T, Kunieda T, Kubo T. 2008. Inducible- and constitutive-type transcript variants of kakusei, a novel non-coding immediate early gene, in the honeybee brain. Insect Molecular Biology, 17, 531–536.
Knight S W, Bass B L. 2001. A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science, 293, 2269–2271.
Kozomara A, Griffiths-Jones S. 2014. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Research, 42, D68–D73.
Kramer M C, Liang D, Tatomer D C, Gold B, March Z M, Cherry S, Wilusz J E. 2015. Combinatorial control of Drosophila circular RNA expression by intronic repeats, hnRNPs, and SR proteins. Genes & Development, 29, 2168–2182.
Krol J, Loedige I, Filipowicz W. 2010. The widespread regulation of microRNA biogenesis, function and decay. Nature Reviews: Genetics, 11, 597–610.
Lagarde J, Uszczynska-Ratajczak B, Carbonell S, Perez-Lluch S, Abad A, Davis C, Gingeras T R, Frankish A, Harrow J, Guigo R, Johnson R. 2017. High-throughput annotation of full-length long noncoding RNAs with capture long-read sequencing. Nature Genetics, 49, 1731–1740.
Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. 2001. Identification of novel genes coding for small expressed RNAs. Science, 294, 853–858.
Lakhotia S C, Mallik M, Singh A K, Ray M. 2012. The large noncoding hsrω-n transcripts are essential for thermotolerance and remobilization of hnRNPs, HP1 and RNA polymerase II during recovery from heat shock in Drosophila. Chromosoma, 121, 49–70.
Lasda E, Parker R. 2014. Circular RNAs: Diversity of form and function. RNA, 20, 1829–1842.
Lau N C, Seto A G, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel D P, Kingston R E. 2006. Characterization of the piRNA complex from rat testes. Science, 313, 363–367.
Lauressergues D, Couzigou J M, Clemente H S, Martinez Y, Dunand C, Becard G, Combier J P. 2015. Primary transcripts of microRNAs encode regulatory peptides. Nature, 520, 90–93.
Lee J T. 2009. Lessons from X-chromosome inactivation: long ncRNA as guides and tethers to the epigenome. Genes & Development, 23, 1831–1842.
Lee J T. 2012. Epigenetic regulation by long noncoding RNAs. Science, 338, 1435–1439.
Lee J T, Bartolomei M S. 2013. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell, 152, 1308–1323.
Lee R C, Ambros V. 2001. An extensive class of small RNAs in Caenorhabditis elegans. Science, 294, 862–864.
Lee R C, Feinbaum R L, Ambros V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843–854.
Lee Y, Kim M, Han J, Yeom K H, Lee S, Baek S H, Kim V N. 2004. MicroRNA genes are transcribed by RNA polymerase II.
EMBO Journal, 23, 4051–4060.
Lewis B P, Shih I H, Jones-Rhoades M W, Bartel D P, Burge C B. 2003. Prediction of mammalian microRNA targets. Cell, 115, 787–798.
Li F, Ma F, Ji X L, Wang S P, Sun Y, Yu L, Li G Q, Han Z J. 2012. Methods for identifying small RNA genes. Small Rnas: Their Diversity, Roles and Practical Uses, 42, 155–194.
Li F, Schiemann A H, Scott M J. 2008. Incorporation of the noncoding roX RNAs alters the chromatin-binding specificity of the Drosophila MSL1/MSL2 complex. Molecular and Cellular Biology, 28, 1252–1264.
Li J, Cai Y, Ye L, Wang S, Che J, You Z, Yu J, Zhong B. 2014. MicroRNA expression profiling of the fifth-instar posterior silk gland of Bombyx mori. BMC Genomics, 15, 410.
Li M, Wen S, Guo X, Bai B, Gong Z, Liu X, Wang Y, Zhou Y, Chen X, Liu L, Chen R. 2012. The novel long non-coding RNA CRG regulates Drosophila locomotor behavior. Nucleic Acids Research, 40, 11714–11727.
Li W, Notani D, Rosenfeld M G. 2016. Enhancers as non-coding RNA transcription units: Recent insights and future perspectives. Nature Reviews: Genetics, 17, 207–223.
Li X, Carthew R W. 2005. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell, 123, 1267–1277.
Li X, Guo L, Zhou X, Gao X, Liang P. 2015. miRNAs regulated overexpression of ryanodine receptor is involved in chlorantraniliprole resistance in Plutella xylostella (L.). Scientific Reports, 5, 14095.
Li Y, Wang F, Lee J A, Gao F B. 2006. MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes & Development, 20, 2793–2805.
Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, Zhong G, Yu B, Hu W, Dai L, Zhu P, Chang Z, Wu Q, Zhao Y, Jia Y, Xu P, Liu H, Shan G. 2015. Exon-intron circular RNAs regulate transcription in the nucleus. Nature Structural & Molecular Biology, 22, 256–264.
Ling L, Ge X, Li Z, Zeng B, Xu J, Aslam A F, Song Q, Shang P, Huang Y, Tan A. 2014. MicroRNA Let-7 regulates molting and metamorphosis in the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology, 53, 13–21.
Ling L, Kokoza V A, Zhang C Y, Aksoy E, Raikhel A S. 2017. MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes. Proceedings of the National Academy of Sciences of the United States of America, 114, E8017–E8024.
Liu F, Guo D, Yuan Z, Chen C,Xiao H. 2017. Genome-wide identification of long non-coding RNA genes and their association with insecticide resistance and metamorphosis in diamondback moth, Plutella xylostella. Scientific Reports, 7, 15870.
Liu S J, Nowakowski T J, Pollen A A, Lui J H, Horlbeck M A, Attenello F J, He D, Weissman J S, Kriegstein A R, Diaz A A, Lim D A. 2016. Single-cell analysis of long non-coding RNAs in the developing human neocortex. Genome Biology, 17, 67.
Lozano J, Montanez R, Belles X. 2015. MiR-2 family regulates insect metamorphosis by controlling the juvenile hormone signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 112, 3740–3745.
Lucas K J, Roy S, Ha J, Gervaise A L, Kokoza V A, Raikhel A S. 2015. MicroRNA-8 targets the Wingless signaling pathway in the female mosquito fat body to regulate reproductive processes. Proceedings of the National Academy of Sciences of the United States of America, 112, 1440–1445.
Lund E, Guttinger S, Calado A, Dahlberg J E, Kutay U. 2004. Nuclear export of microRNA precursors. Science, 303, 95–98.
Luteijn M J, Ketting R F. 2013. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nature Reviews: Genetics, 14, 523–534.
Malone C D, Brennecke J, Dus M, Stark A, McCombie W R, Sachidanandam R, Hannon G J. 2009. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell, 137, 522–535.
Mattick J S, Rinn J L. 2015. Discovery and annotation of long noncoding RNAs. Nature Structural & Molecular Biology, 22, 5–7.
Meller V H, Rattner B P. 2002. The roX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex. EMBO Journal, 21, 1084–1091.
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak S D, Gregersen L H, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N. 2013. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 495, 333–338.
Mercer T R, Dinger M E, Sunkin S M, Mehler M F, Mattick J S. 2008. Specific expression of long noncoding RNAs in the mouse brain. Proceedings of the National Academy of Sciences of the United States of America, 105, 716–721.
Mohn F, Handler D, Brennecke J. 2015. Noncoding RNA. piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science, 348, 812–817.
Morazzani E M, Wiley M R, Murreddu M G, Adelman Z N, Myles K M. 2012. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathogens, 8, e1002470.
Mortazavi A, Williams B A, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods, 5, 621–628.
Murota Y, Ishizu H, Nakagawa S, Iwasaki Y W, Shibata S, Kamatani M K, Saito K, Okano H, Siomi H, Siomi M C. 2014. Yb integrates piRNA intermediates and processing factors into perinuclear bodies to enhance piRISC assembly. Cell Reports, 8, 103–113.
Natoli G, Andrau J C. 2012. Noncoding transcription at enhancers: general principles and functional models. Annual Review of Genetics, 46, 1–19.
Nigro J M, Cho K R, Fearon E R, Kern S E, Ruppert J M, Oliner J D, Kinzler K W, Vogelstein B. 1991. Scrambled exons. Cell, 64, 607–613.
Ninova M, Ronshaugen M, Griffiths-Jones S. 2016. MicroRNA evolution, expression, and function during short germband development in Tribolium castaneum. Genome Research, 26, 85–96.
Nishida K M, Sakakibara K, Iwasaki Y W, Yamada H, Murakami R, Murota Y, Kawamura T, Kodama T, Siomi H, Siomi M C. 2018. Hierarchical roles of mitochondrial Papi and zucchini in Bombyx germline piRNA biogenesis. Nature, 555, 260–264.
Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H, Yamanaka I, Kiyosawa H, Yagi K, Tomaru Y, Hasegawa Y, Nogami A, Schonbach C, Gojobori T, Baldarelli R, Hill D P, Bult C, et al. 2002. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature, 420, 563–573.
Olivieri D, Sykora M M, Sachidanandam R, Mechtler K, Brennecke J. 2010. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO Journal, 29, 3301–3317.
Orom U A, Nielsen F C, Lund A H. 2008. MicroRNA-10a binds the 5´UTR of ribosomal protein mRNAs and enhances their translation. Molecular Cell, 30, 460–471.
Pane A, Wehr K, Schupbach T. 2007. zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Developmental Cell, 12, 851–862.
Park J E, Heo I, Tian Y, Simanshu D K, Chang H, Jee D, Patel D J, Kim V N. 2011. Dicer recognizes the 5´ end of RNA for efficient and accurate processing. Nature, 475, 201–205.
Pek J W, Lim A K, Kai T. 2009. Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Developmental Cell, 17, 417–424.
Puthiyakunnon S, Yao Y, Li Y, Gu J, Peng H, Chen X. 2013. Functional characterization of three MicroRNAs of the Asian tiger mosquito, Aedes albopictus. Parasit Vectors, 6, 230.
Quinn J J, Chang H Y. 2016. Unique features of long non-coding RNA biogenesis and function. Nature Reviews: Genetics, 17, 47–62.
Rehwinkel J, Behm-Ansmant I, Gatfield D, Izaurralde E. 2005. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA, 11, 1640–1647.
Reinhart B J, Slack F J, Basson M, Pasquinelli A E, Bettinger J C, Rougvie A E, Horvitz H R, Ruvkun G. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403, 901–906.
Reynolds J A, Peyton J T, Denlinger D L. 2017. Changes in microRNA abundance may regulate diapause in the flesh fly, Sarcophaga bullata. Insect Biochemistry and Molecular Biology, 84, 1–14.
Rinn J L, Chang H Y. 2012. Genome regulation by long noncoding RNAs. Annual Review of Biochemistry, 81, 145–166.
Rinn J L, Euskirchen G, Bertone P, Martone R, Luscombe N M, Hartman S, Harrison P M, Nelson F K, Miller P, Gerstein M, Weissman S, Snyder M. 2003. The transcriptional activity of human chromosome 22. Genes & Development, 17, 529–540.
Rios-Barrera L D, Gutierrez-Perez I, Dominguez M, Riesgo-Escovar J R. 2015. Acal is a long non-coding RNA in JNK signaling in epithelial shape changes during Drosophila dorsal closure. PLoS Genetics, 11, e1004927.
Robine N, Lau N C, Balla S, Jin Z, Okamura K, Kuramochi-Miyagawa S, Blower M D, Lai E C. 2009. A broadly conserved pathway generates 3´UTR-directed primary piRNAs. Current Biology, 19, 2066–2076.
Rouget C, Papin C, Boureux A, Meunier A C, Franco B, Robine N, Lai E C, Pelisson A, Simonelig M. 2010. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature, 467, U1128-U1144.
Ruby J G, Jan C H, Bartel D P. 2007. Intronic microRNA precursors that bypass Drosha processing. Nature, 448, 83–86.
De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi B K, Muller H, Ragoussis J, Wei C L, Natoli G. 2010. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biology, 8, e1000384.
Saito K, Inagaki S, Mituyama T, Kawamura Y, Ono Y, Sakota E, Kotani H, Asai K, Siomi H, Siomi M C. 2009. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature, 461, 1296–1299.
Saito K, Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida K M, Siomi H, Siomi M C. 2010. Roles for the Yb body components armitage and Yb in primary piRNA biogenesis in Drosophila. Genes & Development, 24, 2493–2498.
Saito K, Nishida K M, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi M C. 2006. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes & Development, 20, 2214–2222.
Saito K, Sakaguchi Y, Suzuki T, Suzuki T, Siomi H, Siomi M C. 2007. Pimet, the Drosophila homolog of HEN1, mediates 2’-O-methylation of Piwi- interacting RNAs at their 3’ ends. Genes & Development, 21, 1603–1608.
Salzman J. 2016. Circular RNA expression: Its potential regulation and function. Trends in Genetics, 32, 309–316.
Salzman J, Gawad C, Wang P L, Lacayo N, Brown P O. 2012. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS ONE, 7, e30733.
Sawata M, Takeuchi H, Kubo T. 2004. Identification and analysis of the minimal promoter activity of a novel noncoding nuclear RNA gene, AncR-1, from the honeybee (Apis mellifera L.). RNA, 10, 1047–1058.
Sawata M, Yoshino D, Takeuchi H, Kamikouchi A, Ohashi K, Kubo T. 2002. Identification and punctate nuclear localization of a novel noncoding RNA, Ks-1, from the honeybee brain. RNA, 8, 772–785.
Schwarz D S, Hutvagner G, Du T, Xu Z, Aronin N, Zamore P D. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell, 115, 199–208.
Senti K A, Brennecke J. 2010. The piRNA pathway: A fly’s perspective on the guardian of the genome. Trends in Genetics, 26, 499–509.
Sleutels F, Zwart R, Barlow D P. 2002. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature, 415, 810–813.
Sokol N S, Ambros V. 2005. Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes & Development, 19, 2343–2354.
Sokol N S, Xu P, Jan Y N, Ambros V. 2008. Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes & Development, 22, 1591–1596.
Soshnev A A, Ishimoto H, McAllister B F, Li X, Wehling M D, Kitamoto T, Geyer P K. 2011. A conserved long noncoding RNA affects sleep behavior in Drosophila. Genetics, 189, 455–468.
Tadano H, Yamazaki Y, Takeuchi H, Kubo T. 2009. Age- and division-of-labour-dependent differential expression of a novel non-coding RNA, Nb-1, in the brain of worker honeybees, Apis mellifera L. Insect Molecular Biology, 18, 715–726.
Tay Y, Zhang J, Thomson A M, Lim B, Rigoutsos I. 2008. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature, 455, 1124–1128.
Tennessen J M, Thummel C S. 2008. Developmental timing: let-7 function conserved through evolution. Current Biology, 18, R707–R708.
Le Thomas A, Rogers A K, Webster A, Marinov G K, Liao S E, Perkins E M, Hur J K, Aravin A A, Toth K F. 2013. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes & Development, 27, 390–399.
Ulitsky I. 2016. Evolution to the rescue: using comparative genomics to understand long non-coding RNAs. Nature Reviews: Genetics, 17, 601–614.
Vagin V V, Sigova A, Li C, Seitz H, Gvozdev V, Zamore P D. 2006. A distinct small RNA pathway silences selfish genetic elements in the germline. Science, 313, 320–324.
Varghese J, Cohen S M. 2007. microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Development, 21, 2277–2282.
Vucicevic D, Corradin O, Ntini E, Scacheri P C, Orom U A. 2015. Long ncRNA expression associates with tissue-specific enhancers. Cell Cycle, 14, 253–260.
Wang K, Liang C, Liu J D, Xiao H M, Huang S Q, Xu J H, Li F. 2014. Prediction of piRNAs using transposon interaction and a support vector machine. BMC Bioinformatics, 15, 419.
Wang S H, Elgin S C. 2011. Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proceedings of the National Academy of Sciences of the United States of America, 108, 21164–21169.
Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld M G, Glass C K, Kurokawa R. 2008. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature, 454, 126–130.
Wang Y, Xu T, He W, Shen X, Zhao Q, Bai J, You M. 2017. Genome-wide identification and characterization of putative lncRNAs in the diamondback moth, Plutella xylostella (L.). Genomics, 110, 35–42.
Wang Y L, Yang M L, Jiang F, Zhang J Z, Kang L. 2013. MicroRNA-dependent development revealed by RNA interference-mediated gene silencing of LmDicer1 in the migratory locust. Insect Science, 20, 53–60.
Weick E M, Miska E A. 2014. piRNAs: from biogenesis to function. Development, 141, 3458–3471.
Westholm J O, Miura P, Olson S, Shenker S, Joseph B, Sanfilippo P, Celniker S E, Graveley B R, Lai E C. 2014. Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Reports, 9, 1966–1980.
Williams J, Smith F, Kumar S, Vijayan M, Reddy P H. 2017. Are microRNAs true sensors of ageing and cellular senescence? Ageing Research Reviews, 35, 350–363.
Wu H M, Huang C P, Taki F A, Zhang Y Q, Dobbins D L, Li L, Yan H T, Pan X P. 2015. Benzo-alpha-pyrene induced oxidative stress in Caenorhabditis elegans and the potential involvements of microRNA. Chemosphere, 139, 496–503.
Wu P, Jiang X, Guo X, Li L, Chen T. 2016. Genome-wide analysis of differentially expressed microrna in Bombyx mori infected with nucleopolyhedrosis virus. PLoS ONE, 11, e0165865.
Wu W, Xiong W, Li C, Zhai M, Li Y, Ma F, Li B. 2017. MicroRNA-dependent regulation of metamorphosis and identification of microRNAs in the red flour beetle, Tribolium castaneum. Genomics, 109, 362–373.
Xiao H, Yuan Z, Guo D, Hou B, Yin C, Zhang W, Li F. 2015. Genome-wide identification of long noncoding RNA genes and their potential association with fecundity and virulence in rice brown planthopper, Nilaparvata lugens. BMC Genomics, 16, 749.
Yamakuchi M, Ferlito M, Lowenstein C J. 2008. miR-34a repression of SIRT1 regulates apoptosis. Proceedings of the National Academy of Sciences of the United States of America, 105, 13421–13426.
Yang J R, Chen D P, He Y N, Melendez A, Feng Z, Hong Q, Bai X Y, Li Q G, Cai G Y, Wang J Z, Chen X M. 2013. MiR-34 modulates Caenorhabditis elegans lifespan via repressing the autophagy gene atg9. Age, 35, 11–22.
Yang M, Wei Y, Jiang F, Wang Y, Guo X, He J, Kang L. 2014. MicroRNA-133 inhibits behavioral aggregation by controlling dopamine synthesis in locusts. PLoS Genetics, 10, e1004206.
Yekta S, Shih I H, Bartel D P. 2004. MicroRNA-directed cleavage of HOXB8 mRNA. Science, 304, 594–596.
Yi R, Qin Y, Macara I G, Cullen B R. 2003. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes & Development, 17, 3011–3016.
Young R S, Marques A C, Tibbit C, Haerty W, Bassett A R, Liu J L, Ponting C P. 2012. Identification and properties of 1,119 candidate lincRNA loci in the Drosophila melanogaster genome. Genome Biology and Evolution, 4, 427–442.
Yu X M, Zhou Q, Li S C, Luo Q B, Cai Y M, Lin W C, Chen H, Yang Y, Hu S N, Yu J. 2008. The silkworm (Bombyx mori) microRNAs and their expressions in multiple developmental sages. PLoS ONE, 3, e2997.
Zekri L, Huntzinger E, Heimstadt S, Izaurralde E. 2009. The silencing domain of GW182 interacts with PABPC1 to promote translational repression and degradation of microRNA targets and is required for target release. Molecular Cell Biology, 29, 6220–6231.
Zhang Y, Wang X H, Kang L. 2011. A k-mer scheme to predict piRNAs and characterize locust piRNAs. Bioinformatics, 27, 771–776.
Zhang Y, Zhao B, Roy S, Saha T T, Kokoza V A, Li M, Raikhel A S. 2016. microRNA-309 targets the homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America, 113, E4828–E4836.
Zhang Y, Zhou X, Ge X, Jiang J, Li M, Jia S, Yang X, Kan Y, Miao X, Zhao G, Li F, Huang Y. 2009. Insect-specific microRNA involved in the development of the silkworm Bombyx mori. PLoS ONE, 4, e4677.
Zhang Y L, Huang Q X, Yin G H, Lee S, Jia R Z, Liu Z X, Yu N T, Pennerman K K, Chen X, Guo A P. 2015. Identification of microRNAs by small RNA deep sequencing for synthetic microRNA mimics to control Spodoptera exigua. Gene, 557, 215–221.
Zhao B, Lucas K J, Saha T T, Ha J S, Ling L, Kokoza V A, Roy S, Raikhel A S. 2017. MicroRNA-275 targets sarco/endoplasmic reticulum Ca2+ adenosine triphosphatase (SERCA) to control key functions in the mosquito gut. PLoS Genetics, 13, e1006943.
Zheng G X, Do B T, Webster D E, Khavari P A, Chang H Y. 2014. Dicer-microRNA-Myc circuit promotes transcription of hundreds of long noncoding RNAs. Nature Structural & Molecular Biology, 21, 585–590.
Zhou H, Rigoutsos I. 2014. MiR-103a-3p targets the 5´ UTR of GPRC5A in pancreatic cells. RNA, 20, 1431–1439.
Zhu B, Liang P, Gao X W. 2016. Long noncoding RNAs (lncRNAs) and their research advances in entomology. Acta Entomologica Sinica, 59, 1272–1281. (in Chinese)
Zhu K A, Liu M H, Fu Z, Zhou Z, Kong Y, Liang H W, Lin Z G, Luo J, Zheng H Q, Wan P, Zhang J F, Zen K, Chen J, Hu F L, Zhang C Y, Ren J, Chen X. 2017. Plant microRNAs in larval food regulate honeybee caste development. PLoS Genetics, 13, e1006946.
[1] ZHANG Jiao-jiao, LI Ya-qi, SHI Mei, WANG Yu-sha, TANG Yao, WANG Xian-zhong. Cold plasma promotes Sertoli cell proliferation via AMPK-mTOR signaling pathway[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2700-2719.
[2] SONG Xiao-fei, GE Dan-feng, XIE Yang, LI Xiao-li, SUN Cheng-zhen, CUI Hao-nan, ZHU Xue-yun, LIU Ren-yi, YAN Li-ying. Genome-scale mRNA and miRNA transcriptomic insights into the regulatory mechanism of cucumber corolla opening[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2603-2614.
[3] XIAO Shan, FANG Qi, LIU Ming-ming, ZHANG Jiao, WANG Bei-bei, YAN Zhi-chao, WANG Fang, David W. STANLEY, YE Gong-yin. Genome-wide characterization of miRNA and siRNA pathways in the parasitoid wasp Pteromalus puparum[J]. >Journal of Integrative Agriculture, 2022, 21(4): 1106-1115.
[4] ZHU Lu, JING Jing, QIN Shuai-qi, LU Jia-ni, ZHU Cui-yun, ZHENG Qi, LIU Ya, FANG Fu-gui, LI Yun-sheng, ZHANG Yun-hai, LING Ying-hui. miR-99a-5p inhibits target gene FZD5 expression and steroid hormone secretion from goat ovarian granulosa cells[J]. >Journal of Integrative Agriculture, 2022, 21(4): 1137-1145.
[5] CHEN Bing-yu, LI Qi-zhai, HU Hui, MENG Shi, Faisal SHAH, WANG Qiang, LIU Hong-zhi . An optimized industry processing technology of peanut tofu and the novel prediction model for suitable peanut varieties[J]. >Journal of Integrative Agriculture, 2020, 19(9): 2340-2351.
[6] Dong Yun, Wang Yi, Jin Feng-wei, Xing Li-juan, Fang Yan, Zhang Zheng-ying, ZOU Jun-jie, Wang Lei, Xu Miao-yun. Differentially expressed miRNAs in anthers may contribute to the fertility of a novel Brassica napus genic male sterile line CN12A[J]. >Journal of Integrative Agriculture, 2020, 19(7): 1731- 1742.
[7] Gniewko Niedbała. Simple model based on artificial neural network for early prediction and simulation winter rapeseed yield[J]. >Journal of Integrative Agriculture, 2019, 18(1): 54-61.
[8] SHI Gui-qing, FU Jing-ying, RONG Ling-jie, ZHANG Pei-yue, GUO Cheng-jin, XIAO Kai. TaMIR1119, a miRNA family member of wheat (Triticum aestivum), is essential in the regulation of plant drought tolerance[J]. >Journal of Integrative Agriculture, 2018, 17(11): 2369-2378.
[9] SUN Ping, ZHANG Zhen-lu, ZHU Qiu-fang, ZHANG Guo-ying, XIANG Ping, LIN Yu-ling, LAI Zhongxiong, LIN Jin-ke. Identification of miRNAs and target genes regulating catechin biosynthesis in tea (Camellia sinensis)[J]. >Journal of Integrative Agriculture, 2018, 17(05): 1154-1164.
[10] MIAO Xiang-yang. Recent advances in understanding the role of miRNAs in exosomes and their therapeutic potential[J]. >Journal of Integrative Agriculture, 2017, 16(04): 753-761.
[11] M Gagaoua, E M C Terlouw, D Micol, J-F Hocquette, A P Moloney, K Nuernberg, D Bauchart, A Boudjellal, N D Scollan, R I Richardson, B Picard. Sensory quality of meat from eight different types of cattle in relation with their biochemical characteristics[J]. >Journal of Integrative Agriculture, 2016, 15(7): 1550-1565.
[12] ZHAO Xu, SHAN Ya-nan, ZHAO Yan, WANG Ai-rong, WANG Zong-hua. A novel Arabidopsis miRNA, ath-miR38-3P, is involved in response to Sclerotinia sclerotiorum infection[J]. >Journal of Integrative Agriculture, 2016, 15(11): 2556-2562.
[13] HU Hai-yan, LI Zhao-jun, FENG Yao, LIU Yuan-wang, XUE Jian-ming, Murray Davis, LIANG Yong-chao. Prediction model for mercury transfer from soil to corn grain and its cross-species extrapolation[J]. >Journal of Integrative Agriculture, 2016, 15(10): 2393-2402.
[14] MA Yan-jiao, YANG Ya-lan, SUN Wei, ZHOU Rong, LI Kui, TANG Zhong-lin. SFRP2 affects prenatal muscle development and is regulated by microRNA-1/206 in pigs[J]. >Journal of Integrative Agriculture, 2016, 15(1): 153-161.
[15] LI Jing, LIU Yong-xin, HAN Ying-peng, LI Yong-guang, GUO Mao-zu , LI Wen-bin. MicroRNA Primary Transcripts and Promoter Elements Analysis in Soybean (Glycine max L. Merril.)[J]. >Journal of Integrative Agriculture, 2013, 12(9): 1522-1529.
No Suggested Reading articles found!