Salient Genetic Notes on Small-RNAs and their Applications in Agricultural Biotechnology

Main Article Content

Samuel Amiteye

Abstract

Small-RNAs are 20 to 27 nucleotides long non-protein-coding RNAs that act on either DNA or RNA to effect the regulation of gene expression. Small-RNAs are key in genetic and epigenetic regulation of diverse biological processes and pathways in response to biotic and abiotic environmental stresses. The gene regulatory functions of small-RNA molecules enhance healthy plant growth and normal development by controlling biological processes such as flowering programming, fruit development, disease and pests resistance. Small-RNAs comprise mainly microRNA and small interfering RNA species. MicroRNAs have been proven to primarily engage in posttranscriptional gene regulation while small interfering RNA have been implicated mainly in transcriptional gene regulation. This review covers the recent advancements in small-RNA research in plants, with emphasis on particularly microRNAs and small interfering RNA biogenesis, biological functions and their relevance in the regulation of traits of agronomic importance in plants. Also discussed extensively is the potential biotechnological applications of these small-RNAs for crop improvement.

Keywords:
Genetics, small RNAs, microRNAs, agriculture, biotechnology, gene silencing.

Article Details

How to Cite
Amiteye, S. (2020). Salient Genetic Notes on Small-RNAs and their Applications in Agricultural Biotechnology. Journal of Advances in Biology & Biotechnology, 22(4), 1-17. https://doi.org/10.9734/jabb/2019/v22i430131
Section
Review Article

References

Borges F, Martienssen RA. The expanding world of small-RNAs in plants. Nat. Rev. Mol. Cell Biol. 2015;16:727–741.

Chen C, Zeng Z, Liu Z, Xia R. Small-RNAs, emerging regulators critical for the development of horticultural traits. Horti-culture Research. 2018;5:63.

Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP. Micro-RNAs in plants. Genes and Dev. 2002;16:1616-1626.

D’Ario M, Griffiths-Jones S, Kim M. Small-RNAs: Big impact on plant development. Trends Plant Sci. 2017;22:1056–1068.

Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, et al. High-throughput sequencing of Arabidopsis microRNAs: Evidence for frequent birth and death of MIRNA genes. PLoS ONE. 2007;2:e219.

Sunkar R, Girke T, Jain PK, Zhu JK. Cloning and characterization of microRNAs from rice. The Plant Cell. 2005;17:1397-1411.

Moxon S, Jing R, Szittya G, Schwach F, Rusholme Pilcher RL, et al. Deep sequencing of tomato short RNAs identifies microRNAs targeting genes in-volved in fruit ripening. Genome Research. 2008;18:1602–1609.

Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q. Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biology. 2007;8:R96.

Amiteye S, Corral JM, Sharbel TF. Overview of the potential of microRNAs and their target gene detection for cassava (Manihot esculenta) improvement. African Journal of Biotechnology. 2011a;10(14): 2562-2573.

Amiteye S, Corral JM, Vogel H, Sharbel TF. Analysis of conserved microRNAs in floral tissues of sexual and apomictic Boechera species. BMC Genomics. 2011b; 12: 500.

Achkar NP, Cambiagno DA, Manavella PA. MiRNA biogenesis: A dynamic pathway. Trends Plant Sci. 2016;21:1034–1044.

Axtell MJ. Classification and comparison of small-RNAs from plants. Annu. Rev. Plant Biol. 2013;64:137–159.

Meng Y, Shao C, Wang H, Chen M. The regulatory activities of plant MicroRNAs: A more dynamic perspective. Plant Physiology. 2011;157:1583–1595.

Cuperus JT, Fahlgren N, Carrington JC. Evolution and functional diversification of MIRNA genes. The Plant Cell. 2011;23: 431–442.

Yang L, Liu Z, Lu F, Dong A, Huang H. SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. The Plant Journal. 2006;47: 841-850.

Ma W, et al. Coupling of microRNA-directed phased small interfering RNA generation from long noncoding genes with alternative splicing and alternative polyadenylation in small RNA-mediated gene silencing. New Phytol. 2018;217: 1535–1550.

Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 2006;57:19–53.

Kim VN. MicroRNA biogenesis: Coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 2005;6:376–385.

Mallory AC, Vaucheret H. Functions of microRNAs and related small-RNAs in plants. Nat. Genet. 2006;38:31-36.

Fujioka Y, Utsumi M, Ohba Y, Watanabe Y. Location of a possible miRNA processing site in SmD3/SmB nuclear bodies in Arabidopsis. Plant Cell Physiology. 2007;48:1243–1253.

Tamiru M, Hardcastle TJ, Lewsey MG. Regulation of genome-wide DNA methyl-tion by mobile small RNAs. New Phytol. 2018;217(2):540-546.

Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003;17:3011–3016.

Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell. 2003;115:209–216.

Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O. Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. The Plant Cell. 2004;16: 1235–1250.

Schwab R, Palatnik JF, Riester M, et al. Specific effects of microRNAs on the plant transcriptome. Dev. Cell. 2005;8:517–27.

Vazquez F, Gasciolli V, Crete P, Vaucheret H. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Current Biology. 2004a;14:346–351.

Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, et al. Endogenous trans-acting siRNAs Regulate the Accumulation of Arabidopsis mRNAs. Molecular Cell. 2004b;16:69-79.

Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, et al. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Current Biology. 2006;16:939–944.

Garcia D, Collier SA, Byrne ME, Martienssen RA. Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Current Biology. 2006;16: 933–938.

Eamens A, Wang MB, Smith NA, Waterhouse PM. RNA silencing in Plants: Yesterday, today and tomorrow. Plant Physiology. 2008;147:456-468.

Nakazawa Y, Hiraguri A, Moriyama H, Fukuhara T. The dsRNA-binding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway. Plant Molecular Biology. 2007;63:777-785.

Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, et al. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell. 2008;133:128- 141.

Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell. 2005;123:1279–1291.

Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A, et al. A pathogen-inducible endogenous siRNA in plant immunity. Proc. Natl. Acad. Sci. USA. 2006;103(47):18002–18007.

Schröder JA, Jullien PE. The diversity of plant small RNAs silencing mechanisms. Chimia. 2019;73(6):362-367.

Wassenegger M. The role of the RNAi machinery in heterochromatin formation. Cell. 2005;122:13-16.

Wassenegger M, Heimes S, Riedel L, Sänger HL. RNA-directed de novo methylation of genomic sequences in plants. Cell. 1994;76:567-576.

Jones AL, Thomas CL, Maule AJ. De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. The EMBO Journal. 1998;17:6385-6393.

Farazi TA, Juranek SA, Tuschl T. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development. 2008;135: 1201–1214.

Kurihara Y, Takashi Y, Watanabe Y. The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA. 2006;12: 206–212.

Vazquez F, Blevins T, Ailhas J, Boller T, Meins F. Jr. Evolution of arabidopsis MIR genes generates novel microRNA classes. Nucleic Acids Research. 2008;36:6429–6438.

Hiraguri A, Itoh R, Kondo N, Nomura Y, Aizawa D, et al. Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 2005;57:173-188.

Dong Z, Han MH, Fedoroff N. The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc. Natl. Acad. Sci. USA. 2008;105:9970-9975.

Yu B, Bi L, Zheng B, Ji L, Chevalier D, et al. The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc. Natl. Acad. Sci. USA. 2008;105:10073-10078.

Pouch-Pelissier MN, Pelissier T, Elmayan T, Vaucheret H, Boko D, et al. SINE RNA induces severe developmental defects in Arabidopsis thaliana and interacts with HYL1 (DRB1), a key member of the DCL1 complex. PLoS Genetics. 2008;4: e1000096.

Voinnet O. Origin, biogenesis and activity of plant MicroRNAs. Cell. 2009;136:669–687.

Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y. DNA methylation mediated by a microRNA pathway. Molecular Cell. 2010; 38:465-475.

Chellappan P, Xia J, Zhou X, Gao S, Zhang X, et al. SiRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic Acids Research. 2010;38:6883-6894.

Kufel J, Grzechnik P. Small nucleolar RNAs tell a different tale. Trends in Genetics. 2019;35(2):104-117,

Song L, Axtell MJ, Fedoroff NV. RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Current Biology. 2010;20 (1): 37-41.

Liang L, Wong CM, Ying Q, Fan DN, Huang S, et al. MicroRNA-125b suppressed human liver cancer cell proliferation and metastasis by directly targeting oncogene LIN28B2. Hepatology. 2010;52:1731–1740.

Fei Q, Xia R, Meyers BC. Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell. 2013;25:2400–2415.

Ramachandran V, Chen X. Degradation of microRNAs by a family of exo-ribonucleases in Arabidopsis. Science. 2008;321:1490–1492.

Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature. 2006; 443:1008-1012.

Vaucheret H. Plant ARGONAUTES. Trends Plant Science. 2008;13:350-358.

Mi S, Cai T, Hu Y, Chen Y, Hodges E, et al. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5' terminal nucleotide. Cell. 2008;133:116-127.

Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, et al. Widespread translational inhibition by plant miRNAs and siRNAs. Science. 2008;320:1185-1190.

Morel J-B, Gordon C, Mourrain P, Beclin C, Boutet S, et al. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. The Plant Cell. 2002;14: 629–639.

Mattick JS. The functional genomics of noncoding RNA. Science. 2005;309:1527-1528.

Chapman EJ, Carrington JC. Specializa-tion and evolution of endogenous small RNA pathways. Nature Reviews Genetics. 2007;8:884–896.

Willmann MR, Endres MW, Cook RT, Gregory BD. The Functions of RNA-Dependent RNA Polymerases in Arabidopsis. The Arabidopsis Book. 2011; e0146.

Huang CY, Wang H, Hu P, Hamby R, Jin H. Small RNAs - Big Players in Plant-Microbe Interactions. Cell Host Microbe. 2019;26(2):173-182.

Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D. Control of leaf morphogenesis by microRNAs. Nature. 2003;425:257-263.

Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, et al. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nature Genetics. 2007;39:787–791.

Xia R, Xu J, Arikit S, Meyers BC. Extensive families of miRNAs and PHAS loci in norway spruce demonstrate the origins of complex phasiRNA networks in seed plants. Mol. Biol. Evol. 2015;32:2905–2918.

Adai CJ, Mlotshwa S, Archer-Evans S, Manocha V, Vance V, Sundaresan V. Computational prediction of miRNAs in Arabidopsis thaliana. Genome Research. 2005;15:78–91.

Xu M, et al. Developmental functions of miR156-regulated Squamosa promoter binding Protein-Like (SPL) genes in Arabidopsis thaliana. PLoS Genet. 2016; 12:e1006263.

Wu G, Poethig RS. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development. 2006;133:3539-3547.

Manning K, Tör M, Poole M, Hong Y, Thompson AJ, et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature Genetics. 2006;38:948–952.

Xie Z, Allen E, Wilken A, Carrington JC. DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 2005; 102:12984–12989.

Achard P, Herr A, Baulcombe DC, Harberd NP. Modulation of floral development by a gibberellin-regulated microRNA. Develop-ment. 2004;131:3357-3365.

Millar AA, Gubler F. The Arabidopsis GAMYB-like Genes, MYB33 and MYB65. Are microRNA-regulated genes that redundantly facilitate anther development? The Plant Cell. 2005;17:705–721.

Allen RS, Li J, Stahle MI, Dubroue A, Gubler F, Millar AA. Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc. Natl. Acad. Sci. USA. 2007;104:16371-16376.

Reyes JL, Chua N-H. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. The Plant Journal. 2007;49: 592-606.

Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC. Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development. 2005;132:3657–3668.

Bradley D, et al. Evolution of flower color pattern through selection on regulatory small RNAs. Science. 2017;358:925–928.

Bao N, Lye KW, Barton MK. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNA are required for methylation of the template chromosome. Dev. Cell. 2004;7:653-662.

Aukerman MJ, Sakai H. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. The Plant Cell. 2003;15:2730–2741.

Yao JL, Tomes S, Xu J, Gleave AP. How microRNA172 affects fruit growth in different species is dependent on fruit type. Plant Signal. Behav. 2016;11:e1156833.

Chuck G, Cigan AM, Saeteurn K, Hake S. The heterochronic maize mutant corngrass1 results from over expression of a tandem microRNA. Nature Genetics. 2007;39:544-549.

José RJ, et al. MicroRNA regulation of fruit growth. Nat. Plants. 2015;1:15036.

Hardtke CS. Root development branching into novel spheres. Current Opinion in Plant Biology. 2006;9:66-71.

Mallory AC, Bartel DP, Bartel B. MicroRNA directed regulation of Arabidopsis auxin response factor17 is essential for proper development and modulates expression of early auxin response genes. The Plant Cell. 2005;17:1360–1375.

Wang XJ, Gaasterland T, Chua NH. Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biology. 2005;6(4):R30.

Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM. Redundancy and specialization among plant microRNAs: Role of the MIR164 family in developmental robustness. Development. 2007;134:1051-1060.

Mallory AC, Dugas DV, Bartel DP, Bartel B. MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegeta-tive, and floral organs. Current Biology. 2004a;14:1035–1046.

Mallory AC, Reinhart BJ, Jones-Rhoades MW. MicroRNA control of Phabulosa in leaf development: Importance of pairing to the microRNA 5’ region. The EMBO Journal. 2004b;23(16):3356-3364.

Laufs P, Peaucelle A, Morin H, Traas J. MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development. 2004;131:4311–4322.

Aida M, Ishida T, Tasaka M. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: Interaction among the cup-shaped cotyledon and shoot meristemless genes. Development. 1999;126:1563-1570.

Baker CC, Sieber P, Wellmer F, Meyerowitz EM. The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Current Biology. 2005;15: 303-315.

Liu N, et al. Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J. Exp. Bot. 2014;65:2507–2520.

Wu MF, Tian Q, Reed JW. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Develop-ment 2006;133:4211-4218.

Vaucheret H, Mallory AC, Bartel DP. AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Molecular Cell. 2006;22:129-136.

Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, et al. The short-root gene controls radial patterning of the Arabidopsis root through radial signaling. Cell. 2000;101:555-567.

Llave C, Xie Z, Kasschau KD, Carrington JC. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science. 2002;297:2053–2056.

Guan X, et al. MiR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat. Commun. 2014;5:3050.

Wu XM, et al. Genomewide analysis of small-RNAs in nonembryogenic and embryogenic tissues of citrus: microRNA- and siRNA-mediated transcript cleavage involved in somatic embryogenesis. Plant Biotechnol. J 2015;13:383–394.

Yang F, Cai J, Yang Y, Liu Z. Over expression of microRNA828 reduces anthocyanin accumulation in Arabidopsis. Plant Cell Tissue Organ Cult. 2013;115: 159–167.

Jia X et al. Small tandem target mimic-mediated blockage of microRNA858 induces anthocyanin accumulation in tomato. Planta. 2015;242:283–293.

Xue C, et al. PbrmiR397a regulates lignification during stone cell development in pear fruit. Plant Biotechnol J. 2018; 1467–7644.

Sagar M, et al. SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit develop-ment. Plant Physiol. 2013;161:1362– 1374.

Bari R, Pant BD, Stitt M, Golm SP. PHO2, microRNA399 and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 2006;141:988–999.

Shivaprasad PV, et al. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell. 2012;24:859–874.

Zhu QH, et al. MiR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLoS ONE. 2013;8:e84390.

Wu J et al. ROS accumulation and antiviral defense control by microRNA528 in rice. Nat. Plants. 2017;3:16203.

Lilley CJ, Bakhetia M, Charlton WL, Urwin PE. Recent progress in the development of RNA interference for plant parasitic nematodes. Molecular Plant Pathology. 2007;8(5):701-711.

Fritz J, Girardin S, Philpott D. Innate immune defense through RNA inter-ference. Sci. STKE. 2006;(339):pe27.

Melnyk CW, Molnar A, Baulcombe DC. Intercellular and systemic movement of RNA silencing signals. The EMBO Journal. 2011;30:3553–3563.

Kidner CA, Martienssen RA. Spatially restricted microRNA directs leaf polarity via Argonaute1. Nature. 2004;428:81-84.

Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391:806–811.

Mérai Z, Kerényi Z, Kertész S, Magna M, Lakatos L, Silhavy D. Double-stranded RNA binding may be a general plant RNA viral strategy to suppress RNA silencing. J. Virol. 2006;80(12):5747–5756.

Sunilkumar G, Campbell L, Puckhaber L, Stipanovic R, Rathore K. Engineering cottonseed for use in human nutrition by tissue-specific reduction of toxic gossypol. Proc. Natl. Acad. Sci. USA. 2006;103(48): 18054–18059.

Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nature Genetics. 2004;36:1282–1290.

Sanders RA, Hiatt W. Tomato transgene structure and silencing. Nature Bio-technology. 2005;23:287–9.