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Genetic manipulation of microRNAs: approaches and limitations

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Abstract

MicroRNAs (miRNAs) are endogenous, small regulatory RNAs (20–24 nt) that bind to complementary sites in the target mRNA molecules and lead to their degradation or translational inhibition. miRNAs regulate the spatial–temporal accumulation of target mRNAs, thereby governing several downstream biological processes and pathways. Various studies over the years have revealed that miRNAs play essential roles in controlling key developmental processes such as embryogenesis, development of root and shoot, leaf polarity, and phase transition along with the plant responses toward numerous biotic and/or abiotic stresses. The functional characterization of miRNAs and fine-tuning of the approaches using miRNAs to boost productivity and tolerance towards abiotic or biotic stresses in commercially important crops are very important. Mostly, approaches used for the functional characterization of miRNAs are based on modulating transcription of miRNA genes by employing genetic engineering tools. These approaches include the use of artificial miRNA genes, target mimic, editing of miRNAs using ZNF proteins, meganucleases, TALENs and most newly emerged CRISPR/Cas9. This review offers a brief overview of the biogenesis and functions of miRNAs in governing key biological processes. It also provides an insight into different approaches and bottlenecks to improve biologically and agronomically important traits through the modulation of miRNA function.

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Abbreviations

amiRNA :

Artificial microRNA

ABA :

Abscisic acid

AGO :

ARGONAUTE

ARF :

AUXIN RESPONSE FACTOR

Cas9 :

CRISPR-associated protein 9

CRISPR :

Clustered Regularly Interspaced Short Palindromic Repeats

DCL1 :

DICER-LIKE1

HYL1 :

HYPONASTIC LEAVES1

miPEP :

microRNA encoded peptides

miRNA :

microRNAs

SDN :

SMALL RNA DEGRADING NUCLEASE

siRNA :

small interfering RNA

SPL :

Squamosa Promoter Binding Protein-Like

TALEN :

Transcription activator-like effector-based nuclease

ZFN :

Zinc-finger nucleases

References

  • Agrawal A, Rajamani V, Reddy VS, Mukherjee SK, Bhatnagar RK (2015) Transgenic plants over-expressing insect-specific microRNA acquire insecticidal activity against Helicoverpa armigera: an alternative to Bt-toxin technology. Transgenic Res 24:791–801

    Article  CAS  PubMed  Google Scholar 

  • Ahmad HM, Wang X, Ijaz M, Oranab S, Ali MA, Fiaz S (2022) Molecular aspects of MicroRNAs and phytohormonal signaling in response to drought stress: a review. Curr Issues Mol Biol 44:3695–3710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Bai B, Shi B, Hou N, Cao Y, Meng Y, Bian H, Zhu M, Han N (2017) microRNAs participate in gene expression regulation and phytohormone cross-talk in barley embryo during seed development and germination. BMC Plant Biol 17:150

    Article  PubMed  PubMed Central  Google Scholar 

  • Bajczyk M, Bhat SS, Szewc L, Szweykowska-Kulinska Z, Jarmolowski A, Dolata J (2019) Novel nuclear functions of Arabidopsis ARGONAUTE1: beyond RNA interference. Plant Physiol 179:1030–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrera-Rojas CH, Otoni WC, Nogueira FTS (2021) Shaping the root system: the interplay between miRNA regulatory hubs and phytohormones. J Exp Bot 72:6822–6835

    Article  CAS  PubMed  Google Scholar 

  • Baucher M, Moussawi J, Vandeputte OM, Monteyne D, Mol A, Pérez-Morga D, El Jaziri M (2013) A role for the miR396/GRF network in specification of organ type during flower development, as supported by ectopic expression of Populus trichocarpa miR396c in transgenic tobacco. Plant Biol 15:892–898

    Article  CAS  PubMed  Google Scholar 

  • Begum Y (2022) Regulatory role of microRNAs (miRNAs) in the recent development of abiotic stress tolerance of plants. Gene 821:146283

    Article  CAS  PubMed  Google Scholar 

  • Bhat SS, Bielewicz D, Gulanicz T, Bodi Z, Yu X, Anderson SJ, Szewc L, Bajczyk M, Dolata J, Grzelak N, Smolinski DJ (2020) mRNA adenosine methylase (MTA) deposits m6A on pri-miRNAs to modulate miRNA biogenesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 117:21785–21795

  • Bi H, Fei Q, Li R, Liu B, Xia R, Char SN, Meyers BC, Yang B (2020) Disruption of miRNA sequences by TALENs and CRISPR/Cas9 induces varied lengths of miRNA production. Plant Biotechnol J 18:1526–1536

    Article  CAS  PubMed  Google Scholar 

  • Boke H, Ozhuner E, Turktas M, Parmaksiz I, Ozcan S, Unver T (2015) Regulation of the alkaloid biosynthesis by mi RNA in opium poppy. Plant Biotechnol J 13:409–420

    Article  CAS  PubMed  Google Scholar 

  • Brightbill CM, Sung S (2022) Temperature-mediated regulation of flowering time in Arabidopsis thaliana. aBIOTECH, 1–7

  • Camargo-Ramírez R, Val-Torregrosa B, San Segundo B (2018) MiR858-mediated regulation of flavonoid-specific MYB transcription factor genes controls resistance to pathogen infection in Arabidopsis. Plant Cell Physiol 59:190–204

    Article  PubMed  Google Scholar 

  • Carrera-Castaño G, Calleja-Cabrera J, Pernas M, Gómez L, Oñate-Sánchez L (2020) An updated overview on the regulation of seed germination. Plants 9:703

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaudhary S, Grover A, Sharma PC (2021) MicroRNAs: potential targets for developing stress-tolerant crops. Life 11:289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen QJ, Deng BH, Gao J, Zhao ZY, Chen ZL, Song SR, Wang L, Zhao LP, Xu WP, Zhang CX, Ma C (2020) A miRNA-encoded small peptide, vvi-miPEP171d1, regulates adventitious root formation. Plant Physiol 183:656–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Rechavi O (2022) Plant and animal small RNA communications between cells and organisms. Nat Rev Mol Cell Biol 23:185–203

    Article  CAS  PubMed  Google Scholar 

  • Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549

    Article  CAS  PubMed  Google Scholar 

  • Curaba J, Singh MB, Bhalla PL (2014) miRNAs in the crosstalk between phytohormone signalling pathways. J Exp Bot 65:1425–1438

    Article  CAS  PubMed  Google Scholar 

  • Curaba J, Spriggs A, Taylor J, Li Z, Helliwell C (2012) miRNA regulation in the early development of barley seed. BMC Plant Biol 12:120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng Z, Wu H, Li D, Li L, Wang Z, Yuan W, Xing Y, Li C, Liang D (2021) Root-to-shoot Long-Distance Mobile miRNAs identified from Nicotiana Rootstocks. Int J Mol Sci 22:12821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding SW, Li H, Lu R, Li F, Li WX (2004) RNA silencing: a conserved antiviral immunity of plants and animals. Virus Res 102:109–115

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Tao Y, Zhu C (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot 64:3077–3086

    Article  CAS  PubMed  Google Scholar 

  • Dong Q, Hu B, Zhang C (2022) microRNAs and their roles in Plant Development. Front Plant Sci 13

  • Eamens AL, Agius C, Smith NA, Waterhouse PM, Wang MB (2011) Efficient silencing of endogenous microRNAs using artificial microRNAs in Arabidopsis thaliana. Mol Plant 4:157–170

    Article  CAS  PubMed  Google Scholar 

  • Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944

    Article  CAS  PubMed  Google Scholar 

  • Ferdous J, Whitford R, Nguyen M, Brien C, Langridge P, Tricker PJ (2017) Drought-inducible expression of Hv-miR827 enhances drought tolerance in transgenic barley. Funct Integr Genomics 17:279–292

    Article  CAS  PubMed  Google Scholar 

  • Fornara F, de Montaigu A, Coupland G (2010) Snapshot: control of flowering in Arabidopsis. Cell 141:550–550

    Article  PubMed  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    Article  CAS  PubMed  Google Scholar 

  • Freytes SN, Canelo M, Cerdán PD (2021) Regulation of flowering time: when and where? Curr Opin Plant Biol 63:102049

    Article  CAS  PubMed  Google Scholar 

  • Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043

    Article  CAS  PubMed  Google Scholar 

  • Gaddam SR, Bhatia C, Sharma A, Badola PK, Saxena G, Trivedi PK (2021) miR775 integrates light, sucrose and auxin associated pathways to regulate root growth in Arabidopsis thaliana. Plant Sci 313:111073

    Article  CAS  PubMed  Google Scholar 

  • Gao P, Bai X, Yang L, Lv D, Pan X, Li Y, Cai H, Ji W, Chen Q, Zhu Y (2011) osa-MIR393: a salinity-and alkaline stress-related microRNA gene. Mol Biol Rep 38:237–242

    Article  CAS  PubMed  Google Scholar 

  • Gao N, Qiang XM, Zhai BN, Min J, Shi WM (2015) Transgenic tomato overexpressing ath-miR399d improves growth under abiotic stress conditions. Russ J Plant Physiol 62:360–366

    Article  CAS  Google Scholar 

  • Gautam V, Singh A, Yadav S, Singh S, Kumar P, Sarkar Das S, Sarkar AK (2021) Conserved LBL1-ta-siRNA and miR165/166-RLD1/2 modules regulate root development in maize. Development 148:190033

    Google Scholar 

  • Giudicatti AJ, Tomassi AH, Manavella PA, Arce AL (2021) Extensive analysis of miRNA trimming and tailing indicates that AGO1 has a complex role in miRNA turnover. Plants 10:267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong D, He F, Liu J, Zhang C, Wang Y, Tian S, Sun C, Zhang X (2022) Understanding of hormonal regulation in rice seed germination. Life 12:1021

  • Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu Z, Huang C, Li F, Zhou X (2014) A versatile system for functional analysis of genes and micro RNA s in cotton. Plant Biotechnol J 12:638–649

    Article  CAS  PubMed  Google Scholar 

  • Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of mi R 398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74:840–851

    Article  CAS  PubMed  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hackenberg M, Gustafson P, Langridge P, Shi BJ (2015) Differential expression of micro RNA s and other small RNA s in barley between water and drought conditions. Plant Biotechnol J 13:2–13

    Article  CAS  PubMed  Google Scholar 

  • Hong Y, Meng J, He X, Zhang Y, Liu Y, Zhang C, Qi H, Luan Y (2021) Editing miR482b and miR482c simultaneously by CRISPR/Cas9 enhanced tomato resistance to Phytophthora infestans. Phytopathology 111:1008–1016

    Article  CAS  PubMed  Google Scholar 

  • Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:1–10

    Article  CAS  Google Scholar 

  • Jatan R, Lata C (2019) Role of microRNAs in abiotic and biotic stress resistance in plants. Proc Indian Natl Sci Acad 85:553–567

  • Jeyakumar JM, Ali A, Wang WM, Thiruvengadam M (2020) Characterizing the role of the miR156-SPL network in plant development and stress response. Plants 9:1206

    Article  CAS  Google Scholar 

  • Jia X, Ding N, Fan W, Yan J, Gu Y, Tang X, Li R, Tang G (2015b) Functional plasticity of miR165/166 in plant development revealed by small tandem target mimic. Plant Sci 233:11–21

    Article  CAS  PubMed  Google Scholar 

  • Jia X, Shen J, Liu H, Li F, Ding N, Gao C, Pattanaik S, Patra B, Li R, Yuan L (2015a) Small tandem target mimic-mediated blockage of microRNA858 induces anthocyanin accumulation in tomato. Planta 242:283–293

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat genet 42:541

    Article  CAS  PubMed  Google Scholar 

  • Jin D, Wang Y, Zhao Y, Chen M (2013) MicroRNAs and their cross-talks in plant development. J Genet Genomics 40:161–170

    Article  CAS  PubMed  Google Scholar 

  • Jin L, Yarra R, Zhou L, Zhao Z, Cao H (2020) miRNAs as key regulators via targeting the phytohormone signaling pathways during somatic embryogenesis of plants. 3 Biotech 10:1–11

    Article  Google Scholar 

  • Jodder J (2020) miRNA-mediated regulation of auxin signaling pathway during plant development and stress responses. J Biosci 45:1–10

    Article  Google Scholar 

  • Jung JH, Park CM (2007) MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 225:1327–1338

    Article  CAS  PubMed  Google Scholar 

  • Kai H, Yun W, Zhanpin Z, Yu W, Ruibing C, Lei Z (2022) miR160: an Indispensable Regulator in Plant. Front Plant Sci 716

  • Kim W, Ahn HJ, Chiou TJ, Ahn JH (2011) The role of the miR399-PHO2 module in the regulation of flowering time in response to different ambient temperatures in Arabidopsis thaliana. Mol Cells 32:83–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kis A, Tholt G, Ivanics M, Várallyay É, Jenes B, Havelda Z (2016) Polycistronic artificial miRNA-mediated resistance to w heat dwarf virus in barley is highly efficient at low temperature. Mol Plant Pathol 17:427–437

    Article  CAS  PubMed  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2010) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39:152–157

    Article  Google Scholar 

  • Kumar RS, Singh H, Datta T, Asif MH, Trivedi PK (2022) miRNA408 and its encoded peptide regulate sulphur assimilation and arsenic stress response in Arabidopsis. Plant Physiol kiad033. https://doi.org/10.1093/plphys/kiad033

  • Lauressergues D, Couzigou JM, Clemente HS, Martinez Y, Dunand C, Bécard G, Combier JP (2015) Primary transcripts of microRNAs encode regulatory peptides. Nature 520:90–93

    Article  CAS  PubMed  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  CAS  PubMed  Google Scholar 

  • Li X, Bian H, Song D, Ma S, Han N, Wang J, Zhu M (2013) Flowering time control in ornamental gloxinia (Sinningia speciosa) by manipulation of miR159 expression. Ann Bot 111:791–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Cui X, Meng Z, Huang X, Xie Q, Wu H, Jin H, Zhang D, Liang W (2012) Transcriptional regulation of Arabidopsis MIR168a and argonaute1 homeostasis in abscisic acid and abiotic stress responses. Plant Physiol 158:1279–1292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Gonzalez N, Inzé D, Dubois M (2020) Emerging connections between small RNAs and phytohormones. Trends Plant Sci 25:912–929

    Article  CAS  PubMed  Google Scholar 

  • Li L, Li Q, Davis KE, Patterson C, Oo S, Liu W, Liu J, Wang G, Fontana JE, Thornburg TE, Pratt IS (2021) Response of root growth and development to nitrogen and potassium deficiency as well as microRNA-mediated mechanism in peanut (Arachis hypogaea L.). Front Plant Sci 12:1109

    Google Scholar 

  • Li M, Yu B (2021) Recent advances in the regulation of plant miRNA biogenesis. RNA Boil 18:2087–2096

    Article  CAS  Google Scholar 

  • Li M, Yu H, Liu K, Yang W, Zhou B, Gan L, Li S, Zhang C, Yu B (2021b) Serrate-Associated protein 1, a splicing‐related protein, promotes miRNA biogenesis in Arabidopsis. New Phytol 232:1959–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lian H, Wang L, Ma N, Zhou CM, Han L, Zhang TQ, Wang JW (2021) Redundant and specific roles of individual MIR172 genes in plant development. PLoS Boil 19:3001044

    Article  Google Scholar 

  • Lin Y, Lai Z, Tian Q, Lin L, Lai R, Yang M, Zhang D, Chen Y, Zhang Z (2015) Endogenous target mimics down-regulate miR160 mediation of ARF10-16 and 17 cleavage during somatic embryogenesis in Dimocarpus longan lour. Front Plant Sci 6:956

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Huang S, Xie H (2021) Advances in the regulation of plant development and stress response by miR167. Front Biosci 26:655–665

    Article  CAS  Google Scholar 

  • Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146

    Article  CAS  PubMed  Google Scholar 

  • Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loreti E, Perata P (2022) Mobile plant microRNAs allow communication within and between organisms. New Phytol 235:2176–2182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151

    Article  CAS  PubMed  Google Scholar 

  • Luo X, Yin M, He Y (2021) Molecular genetic understanding of photoperiodic regulation of flowering time in Arabidopsis and soybean. Int J Mol Sci 23:466

    Article  PubMed  PubMed Central  Google Scholar 

  • Lv DK, Bai X, Li Y, Ding XD, Ge Y, Cai H, Ji W, Wu N, Zhu YM (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459:39–47

    Article  CAS  PubMed  Google Scholar 

  • Maizel A, Markmann K, Timmermans M, Wachter A (2020) To move or not to move: roles and specificity of plant RNA mobility. Curr Opin Plant Biol 57:52–60

    Article  CAS  PubMed  Google Scholar 

  • Mencia R, Gonzalo L, Tossolini I, Manavella PA (2022) Keeping up with the miRNAs: current paradigms of the biogenesis pathway. J Exp Bot erac322. https://doi.org/10.1093/jxb/erac322

  • Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci USA 106:22534–22539

  • Natarajan B, Kalsi HS, Godbole P, Malankar N, Thiagarayaselvam A, Siddappa S, Thulasiram HV, Chakrabarti SK, Banerjee AK (2018) MiRNA160 is associated with local defense and systemic acquired resistance against Phytophthora infestans infection in potato. J Exp Bot 69:2023–2036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nazarov PV, Reinsbach SE, Muller A, Nicot N, Philippidou D, Vallar L, Kreis S (2013) Interplay of microRNAs, transcription factors and target genes: linking dynamic expression changes to function. Nucleic Acids Res 41:2817–2831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Negi P, Mishra S, Ganapathi TR, Srivastava (AK (2021) Regulatory short RNAs: a decade’s tale for manipulating salt tolerance in plants. Physiol Plant 173:1535–1555

    Article  CAS  PubMed  Google Scholar 

  • Niu J, Wang J, Hu H, Chen Y, An J, Cai J, Sun R, Sheng Z, Liu X, Lin S (2016) Cross-talk between freezing response and signaling for regulatory transcriptions of MIR475b and its targets by miR475b promoter in Populus suaveolens. Sci Rep 6:1–11

    CAS  Google Scholar 

  • Nonogaki H (2019) Seed germination and dormancy: the classic story, new puzzles, and evolution. J Integr Plant Biol 61:541–563

    Article  PubMed  Google Scholar 

  • Nowak K, Morończyk J, Grzyb M, Szczygieł-Sommer A, Gaj MD (2022) miR172 regulates WUS during somatic embryogenesis in Arabidopsis via AP2. Cells 11:718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I, Alvarez JP (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Gen 39:787–791

    Article  CAS  Google Scholar 

  • O’Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT (2005) c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435:839–843

    Article  PubMed  Google Scholar 

  • Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18:2237–2242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peláez P, Trejo MS, Iñiguez LP, Estrada-Navarrete G, Covarrubias AA, Reyes JL, Sanchez F (2012) Identification and characterization of microRNAs in Phaseolus vulgaris by high-throughput sequencing. BMC Genom 13:83

    Article  Google Scholar 

  • Piya S, Kihm C, Rice JH, Baum TJ, Hewezi T (2017) Cooperative regulatory functions of miR858 and MYB83 during cyst nematode parasitism. Plant Physiol 174:1897–1912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prabu GR, Mandal AKA (2010) Computational identification of miRNAs and their target genes from expressed sequence tags of tea (Camellia sinensis). GPB 8:113–121

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rahimi A, Karami O, Balazadeh S, Offringa R (2022) miR156-independent repression of the ageing pathway by longevity‐promoting AHL proteins in Arabidopsis. New Phytol 235:2424–2438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reichel M, Li Y, Li J, Millar AA (2015) Inhibiting plant micro RNA activity: molecular SPONGEs, target MIMICs and STTMs all display variable efficacies against target micro RNA s. Plant Biotechnol J 13:915–926

    Article  CAS  PubMed  Google Scholar 

  • Reichel M, Millar AA (2015) Specificity of plant microRNA target MIMICs: cross-targeting of miR159 and miR319. J Plant Physiol 180:45–48

    Article  CAS  PubMed  Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137:103–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers ED, Benfey PN (2015) Regulation of plant root system architecture: implications for crop advancement. Curr Opin Biotechnol 32:93–98

    Article  CAS  PubMed  Google Scholar 

  • Rubio-Somoza I, Weigel D (2013) Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet 9:1003374

    Article  Google Scholar 

  • Sanz-Carbonell A, Marques MC, Bustamante A, Fares MA, Rodrigo G, Gomez G (2019) Inferring the regulatory network of the miRNA-mediated response to biotic and abiotic stress in melon. BMC Plant Boil 19:1–17

    Google Scholar 

  • Sarkar Das S, Yadav S, Singh A, Gautam V, Sarkar AK, Nandi AK, Karmakar P, Majee M, Sanan-Mishra N (2018) Expression dynamics of miRNAs and their targets in seed germination conditions reveals miRNA-ta-siRNA crosstalk as regulator of seed germination. Sci Rep 8:1–13

    Article  CAS  Google Scholar 

  • Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Šečić E, Kogel KH, Ladera-Carmona MJ (2021) Biotic stress-associated microRNA families in plants. J Plant Physiol 263:153451

    Article  PubMed  Google Scholar 

  • Sharma A, Badola PK, Bhatia C, Sharma D, Trivedi PK (2020) Primary transcript of miR858 encodes regulatory peptide and controls flavonoid biosynthesis and development in Arabidopsis. Nat Plants 6:1262–1274

    Article  CAS  PubMed  Google Scholar 

  • Sharma D, Tiwari M, Pandey A, Bhatia C, Sharma A, Trivedi PK (2016) MicroRNA858 is a potential regulator of phenylpropanoid pathway and plant development. Plant physiol 171:944–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma A, Badola PK, Gautam H, Trivedi PK (2022) Heterologous expression of Arabidopsis miR858 modulates biosynthesis of secondary metabolites and affects drought tolerance in tobacco. Plant Cell Tissue Organ Cult, pp 1–12

  • Singh A, Singh S, Panigrahi K, Reski R, Sarkar AK (2014) Balanced activity of microRNA166/165 and its target transcripts from the class III homeodomain-leucine zipper family regulates root growth in Arabidopsis thaliana. Plant Cell Rep 33:945–953

    Article  CAS  PubMed  Google Scholar 

  • Skopelitis DS, Hill K, Klesen S, Marco CF, von Born P, Chitwood DH, Timmermans MC (2018) Gating of miRNA movement at defined cell-cell interfaces governs their impact as positional signals. Nat Commun 9:1–10

    Article  CAS  Google Scholar 

  • Spanudakis E, Jackson S (2014) The role of microRNAs in the control of flowering time. J Exp Bot 65:365–380

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, de Almeida Engler J, Engler G, Van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci U SA 94:11102–11107

  • Tang M, Bai X, Niu LJ, Chai X, Chen MS, Xu ZF (2018) miR172 regulates both vegetative and reproductive development in the perennial woody plant Jatropha curcas. Plant Cell Physiol 59:2549–2563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang X, Bian S, Tang M, Lu Q, Li S, Liu X, Tian G, Nguyen V, Tsang EW, Wang A, Rothstein SJ (2012b) MicroRNA–mediated repression of the seed maturation program during vegetative development in Arabidopsis. PLoS Genet 8:1003091

    Article  Google Scholar 

  • Tang G, Yan J, Gu Y, Qiao M, Fan R, Mao Y, Tang X (2012a) Construction of short tandem target mimic (STTM) to block the functions of plant and animal microRNAs. Methods 58:118–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D (2010) A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet 6:1001031

    Article  Google Scholar 

  • Tomassi AH, Re DA, Romani F, Cambiagno DA, Gonzalo L, Moreno JE, Arce AL, Manavella PA (2020) The intrinsically disordered protein CARP9 bridges HYL1 to AGO1 in the nucleus to promote microRNA activity. Plant Physiol 184:316–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trumbo JL, Zhang B, Stewart CN Jr (2015) Manipulating micro RNA s for improved biomass and biofuels from plant feedstocks. Plant Biotechnol J 13:337–354

    Article  CAS  PubMed  Google Scholar 

  • Tuan PA, Kumar R, Rehal PK, Toora PK, Ayele BT (2018) Molecular mechanisms underlying abscisic acid/gibberellin balance in the control of seed dormancy and germination in cereals. Front Plant Sci 9:668

    Article  PubMed  PubMed Central  Google Scholar 

  • Vale M, Rodrigues J, Badim H, Gerós H, Conde A (2021) Exogenous application of non-mature miRNA-encoded miPEP164c inhibits proanthocyanidin synthesis and stimulates anthocyanin accumulation in grape berry cells. Front Plant Sci12

  • Vashisht I, Mishra P, Pal T, Chanumolu S, Singh TR, Chauhan RS (2015) Mining NGS transcriptomes for miRNAs and dissecting their role in regulating growth, development, and secondary metabolites production in different organs of a medicinal herb, Picrorhiza kurroa. Planta 241:1255–1268

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H (2008) Plant argonautes. Trends Plant Sci 13:350–358

    Article  CAS  PubMed  Google Scholar 

  • Wagaba H, Patil BL, Mukasa S, Alicai T, Fauquet CM, Taylor NJ (2016) Artificial microRNA-derived resistance to Cassava brown streak disease. J Virol Methods 231:38–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Gu X, Xu D, Wang W, Wang H, Zeng M, Chang Z, Huang H, Cui X (2011) miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Exp Bot 62:761–773

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Liu N, Yang X, Tu L, Zhang X (2016) Small RNA-mediated responses to low-and high-temperature stresses in cotton. Sci Rep 6:35558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Mei J, Ren G (2019a) Plant microRNAs: biogenesis, homeostasis, and degradation. Front Plant Sci 10:360

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang S, Quan L, Li S, You C, Zhang Y, Gao L, Zeng L, Liu L, Qi Y, Mo B, Chen X (2019b) The PROTEIN PHOSPHATASE4 complex promotes transcription and processing of primary microRNAs in Arabidopsis. Plant Cell 31:486–501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Sun S, Jin J, Fu D, Yang X, Weng X, Xu C, Li X, Xiao J, Zhang Q (2015) Coordinated regulation of vegetative and reproductive branching in rice. Proc Natl Acad Sci USA 112:15504–15509

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

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

  • Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J, Wang Y, Zhang M (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS ONE 7:30039

    Article  Google Scholar 

  • Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu C, Fang X, Lu T, Dean C (2021) Antagonistic cotranscriptional regulation through ARGONAUTE1 and the THO/TREX complex orchestrates FLC transcriptional output. Proc Natl Acad Sci USA 118:2113757118

  • Xue X, Jiao F, Xu H, Jiao Q, Zhang X, Zhang Y, Du S, Xi M, Wang A, Chen J, Wang M (2021) The role of RNA-binding protein, microRNA and alternative splicing in seed germination: a field need to be discovered. BMC Plant Biol 21:1–11

    Article  Google Scholar 

  • Yamaguchi A, Abe M (2012) Regulation of reproductive development by non-coding RNA in Arabidopsis: to flower or not to flower. J Plant Res 125:693–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan Z, Hossain MS, Wang J, Valdés-López O, Liang Y, Libault M, Qiu L, Stacey G (2013) miR172 regulates soybean nodulation. Mol Plant Microbe Interact 26:1371–1377

    Article  CAS  PubMed  Google Scholar 

  • Yan XX, Liu XY, Hong CUI, Zhao MQ (2022) The roles of microRNAs in regulating root formation and growth in plants. J Integr Agric 21:901–916

    Article  Google Scholar 

  • Yan Y, Ham BK (2022) The mobile small RNAs: Important messengers for long-distance communication in plants. Front Plant Sci 2031

  • Yang X, Dong W, Ren W, Zhao Q, Wu F, He Y (2021) Cytoplasmic HYL1 modulates miRNA-mediated translational repression. Plant Cell 33:1980–1996

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang T, Wang Y, Teotia S, Wang Z, Shi C, Sun H, Gu Y, Zhang Z, Tang G (2019) The interaction between miR160 and miR165/166 in the control of leaf development and drought tolerance in Arabidopsis. Sci Rep 9:1–13

    Google Scholar 

  • Yu S, Cao L, Zhou CM, Zhang TQ, Lian H, Sun Y, Wu J, Huang J, Wang G, Wang JW (2013) Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. elife 2:00269

    Article  Google Scholar 

  • Yu S, Wang JW (2020) The crosstalk between microRNAs and gibberellin signaling in plants. Plant Cell Physiol 61:1880–1890

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Chen X (2021) Secrets of the MIR172 family in plant development and flowering unveiled. PLoS Boil 19:3001099

    Article  Google Scholar 

  • Zhang W, Gao S, Zhou X, Chellappan P, Chen Z, Zhou X, Zhang X, Fromuth N, Coutino G, Coffey M, Jin H (2011a) Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol Biol 75:93–105

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Li L (2013) SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis. Plant J 74:98–109

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Xiang Y, Chen S, Shi M, Jiang X, He Z, Gao S (2022b) Mechanisms of MicroRNA Biogenesis and Stability Control in plants. Front Plant Sci 13:844149

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Yang J, Zhang N, Wu J, Si H (2022a) Roles of microRNAs in abiotic stress response and characteristics regulation of plant. Front Plant Sci 13:919243

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang B, You C, Zhang Y, Zeng L, Hu J, Zhao M, Chen X (2020) Linking key steps of microRNA biogenesis by TREX-2 and the nuclear pore complex in Arabidopsis. Nat Plants 6:957–969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YC, Yu Y, Wang CY, Li ZY, Liu Q, Xu J, Liao JY, Wang XJ, Qu LH, Chen F, Xin P (2013) Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31:848–852

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zou Z, Zhang J, Zhang Y, Han Q, Hu T, Xu X, Liu H, Li H, Ye Z (2011b) Over-expression of sly‐miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett 585:435–439

    Article  CAS  PubMed  Google Scholar 

  • Zheng C, Ye M, Sang M, Wu R (2019) A regulatory network for miR156-SPL module in Arabidopsis thaliana. Int J Mol Sci 20:6166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Deng K, Cheng Y, Zhong Z, Tian L, Tang X, Tang A, Zheng X, Zhang T, Qi Y, Zhang Y (2017) CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front plant Sci 8:1598

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Khare T, Kumar V (2020) Recent trends and advances in identification and functional characterization of plant miRNAs. Acta Physiol Plant 42:25

    Article  CAS  Google Scholar 

  • Zhou J, Zhong Z, Chen H, Li Q, Zheng X, Qi Y, Zhang Y (2019) Knocking out microRNA genes in rice with CRISPR-Cas9. In Plant Genome Editing with CRISPR Systems109-119 Humana Press, New York, NY

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Acknowledgements

This research was supported by the Council of Scientific and Industrial Research (CSIR), New Delhi, in the form of NCP Project No. MLP06. P.K.T. also acknowledges the Department of Science and Technology, New Delhi, for financial support in the form of JC Bose National Fellowship. A.S. and H.G. acknowledge the Council of Scientific and Industrial Research, New Delhi for a Senior Research Fellowship. CSIR-CIMAP Publication Number: CIMAP/PUB/2023/26.

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Sharma, A., Gautam, H. & Trivedi, P.K. Genetic manipulation of microRNAs: approaches and limitations. J. Plant Biochem. Biotechnol. 32, 705–717 (2023). https://doi.org/10.1007/s13562-023-00833-5

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