Abstract
MiRNAs modulate target genes expression at post-transcriptional levels, by reducing spatial abundance of mRNAs. MiRNAs regulats plant metabolism, and emerged as regulators of plant stress responses. Which make miRNAs promising candidates for fine tuning to affectively alter crop stress tolerance and other important traits. With recent advancements in the computational biology and biotechnology miRNAs structure and target prediction is possible resulting in pin point editing; miRNA modulation can be done by up or down regulating miRNAs using recently available biotechnological tools (CRISPR Cas9, TALENS and RNAi). In this review we have focused on miRNA biogenesis, miRNA roles in plant development, plant stress responses and roles in signaling pathways. Additionally we have discussed latest computational prediction models for miRNA to target gene interaction and biotechnological systems used recently for miRNA modulation. We have also highlighted setbacks and limitations in the way of miRNA modulation; providing entirely a new direction for improvement in plant genomics primarily focusing miRNAs.
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References
Ahmed W, Azmat R, Khojah E, Ahmed R, Qayyum A, Shah AN, Abbas A, Moin S, Samra BN (2022) The development of a green innovative bioactive film for industrial application as a new emerging technology to protect the quality of fruits. Molecules 27:486
Shabala S, Chen G, Chen Z-H, Pottosin I (2020) The energy cost of the tonoplast futile sodium leak. New Phytol 225:1105–1110. https://doi.org/10.1111/nph.15758
Tanveer M, Yousaf U (2020) Plant single-cell biology and abiotic stress tolerance. In: Tripathi DK, Pratap Singh V, Chauhan DK, Sharma S, Prasad SM, Dubey NK, Ramawat N (eds) Plant life under changing environment. Academic Press, Cambridge, pp 611–626. https://doi.org/10.1016/B978-0-12-818204-8.00026-6
Tanveer M (2019) Role of 24-epibrassinolide in inducing thermo-tolerance in plants. J Plant Growth Regul 38:945–955. https://doi.org/10.1007/s00344-018-9904-x
Djami-Tchatchou AT, Sanan-Mishra N, Ntushelo K, Dubery IA (2017) Functional roles of microRNAs in agronomically important plants—potential as targets for crop improvement and protection. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00378
Morf J, Wingett SW, Farabella I, Cairns J, Furlan-Magaril M, Jiménez-García LF, Liu X, Craig FF, Walker S, Segonds-Pichon A et al (2019) RNA proximity sequencing reveals the spatial organization of the transcriptome in the nucleus. Nat Biotechnol 37:793–802. https://doi.org/10.1038/s41587-019-0166-3
Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338. https://doi.org/10.1126/science.1085242
Djuranovic S, Nahvi A, Green R (2011) A parsimonious model for gene regulation by miRNAs. Science 331:550–553. https://doi.org/10.1126/science.1191138
Nithin C, Patwa N, Thomas A, Bahadur RP, Basak J (2015) Computational prediction of miRNAs and their targets in Phaseolus vulgaris using simple sequence repeat signatures. BMC Plant Biol 15:140. https://doi.org/10.1186/s12870-015-0516-3
Hõrak H (2020) Telling footprints: exon junction complexes mark targets of nonsense- and miRNA-mediated mRNA decay. Plant Cell 32:787–788. https://doi.org/10.1105/tpc.20.00090
Lau NC, Lim LP, Weinstein EG, Bartel DP (2001) An abundant class of tiny RNAs with probable regulatory roles in C. elegans. Science 294:858–862
Lee RC, Ambros V (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862–864. https://doi.org/10.1126/science.1065329
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
Wightman B, Ha I, Ruvkun G (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75:855–862
Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–442. https://doi.org/10.1105/tpc.110.082784
Nozawa M, Miura S, Nei M (2012) Origins and evolution of microRNA genes in plant species. Genome Biol Evol 4:230–239. https://doi.org/10.1093/gbe/evs002
Zhang S, Liu Y, Yu B (2015) New insights into pri-miRNA processing and accumulation in plants. Wiley Interdiscip Rev: RNA 6:533–545. https://doi.org/10.1002/wrna.1292
Kozomara A, Birgaoanu M, Griffiths-Jones S (2018) miRBase: from microRNA sequences to function. Nucleic Acids Res 47:D155–D162. https://doi.org/10.1093/nar/gky1141
Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658–1673. https://doi.org/10.1105/tpc.105.032185
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. https://doi.org/10.1016/j.molcel.2004.05.027
Chang H, Yi B, Ma R, Zhang X, Zhao H, Xi Y (2016) CRISPR/cas9, a novel genomic tool to knock down microRNA in vitro and in vivo. Sci Rep 6:22312. https://doi.org/10.1038/srep22312
Liu S-R, Zhou J-J, Hu C-G, Wei C-L, Zhang J-Z (2017) MicroRNA-mediated gene silencing in plant defense and viral counter-defense. Front Microbiol 8:1801–1801. https://doi.org/10.3389/fmicb.2017.01801
Eckardt NA (2012) A microRNA cascade in plant defense. Plant Cell 24:840–840. https://doi.org/10.1105/tpc.112.240311
Song X, Li Y, Cao X, Qi Y (2019) MicroRNAs and their regulatory roles in plant-environment interactions. Annu Rev Plant Biol 70:489–525. https://doi.org/10.1146/annurev-arplant-050718-100334
Basso MF, Ferreira PCG, Kobayashi AK, Harmon FG, Nepomuceno AL, Molinari HBC, Grossi-de-Sa MF (2019) MicroRNAs and new biotechnological tools for its modulation and improving stress tolerance in plants. Plant Biotechnol J 17:1482–1500. https://doi.org/10.1111/pbi.13116
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. https://doi.org/10.1111/pbi.13315
Zhou J, Zhong Z, Chen H, Li Q, Zheng X, Qi Y, Zhang Y (2019) Knocking out microRNA genes in rice with CRISPR-Cas9. Methods Mol Boil (Clifton, N.J.) 1917:109–119. https://doi.org/10.1007/978-1-4939-8991-1_9
Damodharan S, Corem S, Gupta SK, Arazi T (2018) Tuning of SlARF10A dosage by sly-miR160a is critical for auxin-mediated compound leaf and flower development. Plant J 96:855–868. https://doi.org/10.1111/tpj.14073
Manghwar H, Li B, Ding X, Hussain A, Lindsey K, Zhang X, Jin S (2020) CRISPR/Cas systems in genome editing: methodologies and tools for sgRNA design, off-target evaluation, and strategies to mitigate off-target effects. Adv Sci 7:1902312. https://doi.org/10.1002/advs.201902312
Gualtieri C, Leonetti P, Macovei A (2020) Plant miRNA cross-kingdom transfer targeting parasitic and mutualistic organisms as a tool to advance modern agriculture. Front Plant Sci 11:930–930. https://doi.org/10.3389/fpls.2020.00930
Mattioli C, Pianigiani G, Pagani F (2014) Cross talk between spliceosome and microprocessor defines the fate of pre-mRNA. Wiley Interdiscip Rev: RNA 5:647–658. https://doi.org/10.1002/wrna.1236
Schier AC, Taatjes DJ (2020) Structure and mechanism of the RNA polymerase II transcription machinery. Genes Dev 34:465–488. https://doi.org/10.1101/gad.335679.119
Stepien A, Knop K, Dolata J, Taube M, Bajczyk M, Barciszewska-Pacak M, Pacak A, Jarmolowski A, Szweykowska-Kulinska Z (2017) Posttranscriptional coordination of splicing and miRNA biogenesis in plants. Wiley Interdiscip Rev: RNA 8:e1403. https://doi.org/10.1002/wrna.1403
Treiber T, Treiber N, Meister G (2019) Regulation of microRNA biogenesis and its crosstalk with other cellular pathways. Nat Rev Mol Cell Biol 20:5–20. https://doi.org/10.1038/s41580-018-0059-1
O’Brien J, Hayder H, Zayed Y, Peng C (2018) Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol. https://doi.org/10.3389/fendo.2018.00402
Wu Q, Song R, Ortogero N, Zheng H, Evanoff R, Small CL, Griswold MD, Namekawa SH, Royo H, Turner JM et al (2012) The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. J Biol Chem 287:25173–25190. https://doi.org/10.1074/jbc.M112.362053
Sheng P, Fields C, Aadland K, Wei T, Kolaczkowski O, Gu T, Kolaczkowski B, Xie M (2018) Dicer cleaves 5′-extended microRNA precursors originating from RNA polymerase II transcription start sites. Nucleic Acids Res 46:5737–5752. https://doi.org/10.1093/nar/gky306
Kurzynska-Kokorniak A, Koralewska N, Pokornowska M, Urbanowicz A, Tworak A, Mickiewicz A, Figlerowicz M (2015) The many faces of Dicer: the complexity of the mechanisms regulating Dicer gene expression and enzyme activities. Nucleic Acids Res 43:4365–4380. https://doi.org/10.1093/nar/gkv328
Sun Q, Liu X, Yang J, Liu W, Du Q, Wang H, Fu C, Li W-X (2018) MicroRNA528 affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Mol Plant 11:806–814. https://doi.org/10.1016/j.molp.2018.03.013
Dolata J, Taube M, Bajczyk M, Jarmolowski A, Szweykowska-Kulinska Z, Bielewicz D (2018) Regulation of plant microprocessor function in shaping microRNA landscape. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00753
Wang J, Mei J, Ren G (2019) Plant microRNAs: biogenesis, homeostasis, and degradation. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00360
Schauer SE, Golden TA, Merchant DS, Patra BN, Lang JD, Ray S, Chakravarti B, Chakravarti D, Ray A (2013) DCL1, a protein that produces plant microRNA, coordinates meristem activity. bioRxiv. https://doi.org/10.1101/001438
Song J, Wang X, Song B, Gao L, Mo X, Yue L, Yang H, Lu J, Ren G, Mo B et al (2019) Prevalent cytidylation and uridylation of precursor miRNAs in Arabidopsis. Nature Plants 5:1260–1272. https://doi.org/10.1038/s41477-019-0562-1
Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495
Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci 102:3691–3696
Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102:11928–11933. https://doi.org/10.1073/pnas.0505461102
Iki T, Yoshikawa M, Meshi T, Ishikawa M (2012) Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J 31:267–278. https://doi.org/10.1038/emboj.2011.395
Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, Mitsuhara I, Meshi T, Ishikawa M (2010) In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol Cell 39:282–291. https://doi.org/10.1016/j.molcel.2010.05.014
Chung BYW, Valli A, Deery MJ, Navarro FJ, Brown K, Hnatova S, Howard J, Molnar A, Baulcombe DC (2019) Distinct roles of Argonaute in the green alga Chlamydomonas reveal evolutionary conserved mode of miRNA-mediated gene expression. Sci Rep 9:11091. https://doi.org/10.1038/s41598-019-47415-x
Sun G (2012) MicroRNAs and their diverse functions in plants. Plant Mol Biol 80:17–36. https://doi.org/10.1007/s11103-011-9817-6
Okamura K, Phillips MD, Tyler DM, Duan H, Chou YT, Lai EC (2008) The regulatory activity of microRNA* species has substantial influence on microRNA and 3’ UTR evolution. Nat Struct Mol Biol 15:354–363. https://doi.org/10.1038/nsmb.1409
Jung JH, Seo PJ, Park CM (2009) MicroRNA biogenesis and function in higher plants. Plant Biotechnol Rep 3:111–126
Floyd SK, Bowman JL (2004) Ancient microRNA target sequences in plants. Nature 428:485–486. https://doi.org/10.1038/428485a
Zhang B, Wang Q, Wang K, Pan X, Liu F, Guo T, Cobb GP, Anderson TA (2007) Identification of cotton microRNAs and their targets. Gene 397:26–37. https://doi.org/10.1016/j.gene.2007.03.020
Zhao Y, Mo B, Chen X (2012) Mechanisms that impact microRNA stability in plants. RNA Biol 9:1218–1223. https://doi.org/10.4161/rna.22034
Hajheidari M, Farrona S, Huettel B, Koncz Z, Koncz C (2012) CDKF;1 and CDKD protein kinases regulate phosphorylation of serine residues in the C-terminal domain of Arabidopsis RNA polymerase II. Plant Cell 24:1626–1642. https://doi.org/10.1105/tpc.112.096834
Zhang S, Liu Y, Yu B (2014) PRL1, an RNA-binding protein, positively regulates the accumulation of miRNAs and siRNAs in Arabidopsis. PLoS Genet 10:e1004841–e1004841. https://doi.org/10.1371/journal.pgen.1004841
Zhang S, Dou Y, Li S, Ren G, Chevalier D, Zhang C, Yu B (2018) DAWDLE interacts with DICER-LIKE proteins to mediate small RNA biogenesis. Plant Physiol 177:1142–1151. https://doi.org/10.1104/pp.18.00354
Zhang X, Niu D, Carbonell A, Wang A, Lee A, Tun V, Wang Z, Carrington JC, Chang CE, Jin H (2014) ARGONAUTE PIWI domain and microRNA duplex structure regulate small RNA sorting in Arabidopsis. Nat Commun 5:5468. https://doi.org/10.1038/ncomms6468
Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12:99–110. https://doi.org/10.1038/nrg2936
Hausser J, Zavolan M (2014) Identification and consequences of miRNA–target interactions—beyond repression of gene expression. Nat Rev Genet 15:599. https://doi.org/10.1038/nrg3765
Helwak A, Kudla G, Dudnakova T, Tollervey D (2013) Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153:654–665. https://doi.org/10.1016/j.cell.2013.03.043
Seok H, Ham J, Jang ES, Chi SW (2016) MicroRNA target recognition: insights from transcriptome-wide non-canonical interactions. Mol Cells 39:375–381. https://doi.org/10.14348/molcells.2016.0013
Brennecke J, Stark A, Russell RB, Cohen SM (2005) Principles of microRNA–target recognition. PLoS Biol 3:e85. https://doi.org/10.1371/journal.pbio.0030085
Khorshid M, Hausser J, Zavolan M, van Nimwegen E (2013) A biophysical miRNA-mRNA interaction model infers canonical and noncanonical targets. Nat Methods 10:253. https://doi.org/10.1038/nmeth.2341
Lee D, Shin C (2012) MicroRNA-target interactions: new insights from genome-wide approaches. Ann N Y Acad Sci 1271:118–128. https://doi.org/10.1111/j.1749-6632.2012.06745.x
Pasquinelli AE (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13:271–282. https://doi.org/10.1038/nrg3162
Garcia DM, Baek D, Shin C, Bell GW, Grimson A, Bartel DP (2011) Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat Struct Mol Biol 18:1139. https://doi.org/10.1038/nsmb.2115
Ren W, Wu F, Bai J, Li X, Yang X, Xue W, Liu H, He Y (2020) BcpLH organizes a specific subset of microRNAs to form a leafy head in Chinese cabbage (Brassica rapa ssp. pekinensis). Hortic Res 7:1. https://doi.org/10.1038/s41438-019-0222-7
Juárez-González VT, López-Ruiz BA, Baldrich P, Luján-Soto E, Meyers BC, Dinkova TD (2019) The explant developmental stage profoundly impacts small RNA-mediated regulation at the dedifferentiation step of maize somatic embryogenesis. Sci Rep 9:14511. https://doi.org/10.1038/s41598-019-50962-y
Mutum RD, Kumar S, Balyan S, Kansal S, Mathur S, Raghuvanshi S (2016) Identification of novel miRNAs from drought tolerant rice variety Nagina 22. Sci Rep 6:30786. https://doi.org/10.1038/srep30786
Yang M, Lu H, Xue F, Ma L (2019) Identifying high confidence microRNAs in the developing seeds of Jatropha curcas. Sci Rep 9:4510. https://doi.org/10.1038/s41598-019-41189-y
Gao Y, Li D, Zhang L-L, Borthakur D, Li Q-S, Ye J-H, Zheng X-Q, Lu J-L (2019) MicroRNAs and their targeted genes associated with phase changes of stem explants during tissue culture of tea plant. Sci Rep 9:20239. https://doi.org/10.1038/s41598-019-56686-3
Chen H, Zhang J, Neff MM, Hong S-W, Zhang H, Deng X-W, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105:4495–4500. https://doi.org/10.1073/pnas.0710778105
Jin X, Fu Z, Lv P, Peng Q, Ding D, Li W, Tang J (2015) Identification and characterization of microRNAs during maize grain filling. PLoS ONE 10:e0125800–e0125800. https://doi.org/10.1371/journal.pone.0125800
Pirrò S, Matic I, Guidi A, Zanella L, Gismondi A, Cicconi R, Bernardini R, Colizzi V, Canini A, Mattei M et al (2019) Identification of microRNAs and relative target genes in Moringa oleifera leaf and callus. Sci Rep 9:15145. https://doi.org/10.1038/s41598-019-51100-4
Merelo P, Ram H, Pia Caggiano M, Ohno C, Ott F, Straub D, Graeff M, Cho SK, Yang SW, Wenkel S et al (2016) Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity. Proc Natl Acad Sci USA 113:11973–11978. https://doi.org/10.1073/pnas.1516110113
Shah AN, Tanveer M, Abbas A, Fahad S, Baloch MS, Ahmad MI, Saud S, Song Y (2021) Targeting salt stress coping mechanisms for stress tolerance in Brassica: a research perspective. Plant Physiol Biochem 158:53–64. https://doi.org/10.1016/j.plaphy.2020.11.044
Luo M, Tai R, Yu C-W, Yang S, Chen C-Y, Lin W-D, Schmidt W, Wu K (2015) Regulation of flowering time by the histone deacetylase HDA5 in Arabidopsis. Plant J 82:925–936. https://doi.org/10.1111/tpj.12868
Prakash P, Rajakani R, Gupta V (2016) Transcriptome-wide identification of Rauvolfia serpentina microRNAs and prediction of their potential targets. Comput Biol Chem 61:62–74. https://doi.org/10.1016/j.compbiolchem.2015.12.002
Yang C, Li D, Liu X, Ji C, Hao L, Zhao X, Li X, Chen C, Cheng Z, Zhu L (2014) OsMYB103L, an R2R3-MYB transcription factor, influences leaf rolling and mechanical strength in rice (Oryza sativa L.). BMC Plant Biol 14:158–158. https://doi.org/10.1186/1471-2229-14-158
Gao F, Wang N, Li H, Liu J, Fu C, Xiao Z, Wei C, Lu X, Feng J, Zhou Y (2016) Identification of drought-responsive microRNAs and their targets in Ammopiptanthus mongolicus by using high-throughput sequencing. Sci Rep 6:34601. https://doi.org/10.1038/srep34601
Guo Y, Zhao S, Zhu C, Chang X, Yue C, Wang Z, Lin Y, Lai Z (2017) Identification of drought-responsive miRNAs and physiological characterization of tea plant (Camellia sinensis L.) under drought stress. BMC Plant Biol 17:211. https://doi.org/10.1186/s12870-017-1172-6
Niu C, Li H, Jiang L, Yan M, Li C, Geng D, Xie Y, Yan Y, Shen X, Chen P et al (2019) Genome-wide identification of drought-responsive microRNAs in two sets of Malus from interspecific hybrid progenies. Hortic Res 6:75. https://doi.org/10.1038/s41438-019-0157-z
Riaz M, Arif MS, Ashraf MA, Mahmood R, Yasmeen T, Shakoor MB, Shahzad SM, Ali M, Saleem I, Arif M et al (2019) A comprehensive review on rice responses and tolerance to salt stress. In: Hasanuzzaman M, Fujita M, Nahar K, Biswas JK (eds) Advances in rice research for abiotic stress tolerance. Woodhead Publishing, Sawston, pp 133–158. https://doi.org/10.1016/B978-0-12-814332-2.00007-1
Mondal TK, Panda AK, Rawal HC, Sharma TR (2018) Discovery of microRNA-target modules of African rice (Oryza glaberrima) under salinity stress. Sci Rep 8:570. https://doi.org/10.1038/s41598-017-18206-z
Parmar S, Gharat SA, Tagirasa R, Chandra T, Behera L, Dash SK, Shaw BP (2020) Identification and expression analysis of miRNAs and elucidation of their role in salt tolerance in rice varieties susceptible and tolerant to salinity. PLoS ONE 15:e0230958. https://doi.org/10.1371/journal.pone.0230958
Alzahrani SM, Alaraidh IA, Khan MA, Migdadi HM, Alghamdi SS, Alsahli AA (2019) Identification and characterization of salt-responsive microRNAs in Vicia faba by high-throughput sequencing. Genes 10:303. https://doi.org/10.3390/genes10040303
Noman A, Aqeel M (2017) miRNA-based heavy metal homeostasis and plant growth. Environ Sci Pollut Res 24:10068–10082. https://doi.org/10.1007/s11356-017-8593-5
Li C, Zhang B (2016) MicroRNAs in control of plant development. J Cell Physiol 231:303–313. https://doi.org/10.1002/jcp.25125
Tang Y, Liu H, Guo S, Wang B, Li Z, Chong K, Xu Y (2018) OsmiR396d affects gibberellin and brassinosteroid signaling to regulate plant architecture in rice. Plant Physiol 176:946–959. https://doi.org/10.1104/pp.17.00964
de Felippes FF (2019) Gene regulation mediated by microRNA-triggered secondary small RNAs in plants. Plants 8:112
Zheng X, Yang L, Li Q, Ji L, Tang A, Zang L, Deng K, Zhou J, Zhang Y (2018) MIGS as a simple and efficient method for gene silencing in rice. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00662
Cheng C, Liu F, Sun X, Tian N, Mensah RA, Li D, Lai Z (2019) Identification of Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4) responsive miRNAs in banana root. Sci Rep 9:13682. https://doi.org/10.1038/s41598-019-50130-2
Zhu H, Zhang Y, Tang R, Qu H, Duan X, Jiang Y (2019) Banana sRNAome and degradome identify microRNAs functioning in differential responses to temperature stress. BMC Genom 20:33–33. https://doi.org/10.1186/s12864-018-5395-1
Das A, Nigam D, Junaid A, Tribhuvan KU, Kumar K, Durgesh K, Singh NK, Gaikwad K (2019) Expressivity of the key genes associated with seed and pod development is highly regulated via lncRNAs and miRNAs in Pigeonpea. Sci Rep 9:18191. https://doi.org/10.1038/s41598-019-54340-6
Liang G, Ai Q, Yu D (2015) Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis. Sci Rep 5:11813. https://doi.org/10.1038/srep11813
Choi C, Han J, Thao Tran NT, Yoon S, Kim G, Song S, Kim Y, Ryu S (2017) Effective experimental validation of miRNA targets using an improved linker reporter assay. Genet Res 99:e2. https://doi.org/10.1017/s001667231600015x
Mittal N, Zavolan M (2014) Seq and CLIP through the miRNA world. Genome Biol 15:202. https://doi.org/10.1186/gb4151
Lu Y, Leslie CS (2016) Learning to predict miRNA-mRNA interactions from AGO CLIP sequencing and CLASH data. PLoS Comput Biol 12:e1005026–e1005026. https://doi.org/10.1371/journal.pcbi.1005026
Zisoulis DG, Lovci MT, Wilbert ML, Hutt KR, Liang TY, Pasquinelli AE, Yeo GW (2010) Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat Struct Mol Biol 17:173. https://doi.org/10.1038/nsmb.1745
Majoros WH, Lekprasert P, Mukherjee N, Skalsky RL, Corcoran DL, Cullen BR, Ohler U (2013) MicroRNA target site identification by integrating sequence and binding information. Nat Methods 10:630. https://doi.org/10.1038/nmeth.2489
Erhard F, Dölken L, Jaskiewicz L, Zimmer R (2013) PARma: identification of microRNA target sites in AGO-PAR-CLIP data. Genome Biol 14:R79. https://doi.org/10.1186/gb-2013-14-7-r79
Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55. https://doi.org/10.1038/nrm3486
Petolino JF (2015) Genome editing in plants via designed zinc finger nucleases. In Vitro Cell Dev Biol Plant 51:1–8. https://doi.org/10.1007/s11627-015-9663-3
Porteus MH, Carroll D (2005) Gene targeting using zinc finger nucleases. Nat Biotechnol 23:967–973. https://doi.org/10.1038/nbt1125
Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, Joung JK (2012) FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 30:460–465. https://doi.org/10.1038/nbt.2170
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821. https://doi.org/10.1126/science.1225829
Zhou J, Deng K, Cheng Y, Zhong Z, Tian L, Tang X, Tang A, Zheng X, Zhang T, Qi Y et al (2017) CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01598
Tang X, Zheng X, Qi Y, Zhang D, Cheng Y, Tang A, Voytas Daniel F, Zhang Y (2016) A single transcript CRISPR-Cas9 system for efficient genome editing in plants. Mol Plant 9:1088–1091. https://doi.org/10.1016/j.molp.2016.05.001
Zhao Y, Zhang C, Liu W, Gao W, Liu C, Song G, Li W-X, Mao L, Chen B, Xu Y et al (2016) An alternative strategy for targeted gene replacement in plants using a dual-sgRNA/Cas9 design. Sci Rep 6:23890–23890. https://doi.org/10.1038/srep23890
Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:16. https://doi.org/10.1186/s12896-015-0131-2
Uhde-Stone C, Sarkar N, Antes T, Otoc N, Kim Y, Jiang YJ, Lu B (2014) A TALEN-based strategy for efficient bi-allelic miRNA ablation in human cells. RNA 20:948–955. https://doi.org/10.1261/rna.042010.113
Hu R, Wallace J, Dahlem TJ, Grunwald DJ, O’Connell RM (2013) Targeting human microRNA genes using engineered tal-effector nucleases (TALENs). PLoS ONE 8:e63074. https://doi.org/10.1371/journal.pone.0063074
Aman R, Ali Z, Butt H, Mahas A, Aljedaani F, Khan MZ, Ding S, Mahfouz M (2018) RNA virus interference via CRISPR/Cas13a system in plants. Genome Biol 19:1. https://doi.org/10.1186/s13059-017-1381-1
Ming M, Ren Q, Pan C, He Y, Zhang Y, Liu S, Zhong Z, Wang J, Malzahn AA, Wu J et al (2020) CRISPR-Cas12b enables efficient plant genome engineering. Nat Plants 6:202–208. https://doi.org/10.1038/s41477-020-0614-6
Qin R, Li J, Liu X, Xu R, Yang J, Wei P (2020) SpCas9-NG self-targets the sgRNA sequence in plant genome editing. Nature Plants 6:197–201. https://doi.org/10.1038/s41477-020-0603-9
Maher MF, Nasti RA, Vollbrecht M, Starker CG, Clark MD, Voytas DF (2020) Plant gene editing through de novo induction of meristems. Nat Biotechnol 38:84–89. https://doi.org/10.1038/s41587-019-0337-2
Bortesi L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52. https://doi.org/10.1016/j.biotechadv.2014.12.006
Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S, Kim J-S (2014) Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24:132–141. https://doi.org/10.1101/gr.162339.113
Doman JL, Raguram A, Newby GA, Liu DR (2020) Evaluation and minimization of Cas9-independent off-target DNA editing by cytosine base editors. Nat Biotechnol. https://doi.org/10.1038/s41587-020-0414-6,10.1038/s41587-020-0414-6
D’Ario M, Griffiths-Jones S, Kim M (2017) Small RNAs: big impact on plant development. Trends Plant Sci 22:1056–1068. https://doi.org/10.1016/j.tplants.2017.09.009
Baldrich P, Kakar K, Siré C, Moreno AB, Berger A, García-Chapa M, López-Moya JJ, Riechmann JL, San Segundo B (2014) Small RNA profiling reveals regulation of Arabidopsis miR168 and heterochromatic siRNA415 in response to fungal elicitors. BMC Genom 15:1083. https://doi.org/10.1186/1471-2164-15-1083
Šečić E, Kogel K-H, Ladera-Carmona MJ (2021) Biotic stress-associated microRNA families in plants. J Plant Physiol 263:153451. https://doi.org/10.1016/j.jplph.2021.153451
Barciszewska-Pacak M, Milanowska K, Knop K, Bielewicz D, Nuc P, Plewka P, Pacak A, Vazquez F, Karlowski W, Jarmolowski A et al (2015) Arabidopsis microRNA expression regulation in a wide range of abiotic stress responses. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00410
Patel P, Yadav K, Srivastava AK, Suprasanna P, Ganapathi TR (2019) Overexpression of native Musa-miR397 enhances plant biomass without compromising abiotic stress tolerance in banana. Sci Rep 9:16434. https://doi.org/10.1038/s41598-019-52858-3
Tripathi AM, Singh A, Singh R, Verma AK, Roy S (2019) Modulation of miRNA expression in natural populations of A. thaliana along a wide altitudinal gradient of Indian Himalayas. Sci Rep 9:441. https://doi.org/10.1038/s41598-018-37465-y
Bustamante A, Marques MC, Sanz-Carbonell A, Mulet JM, Gomez G (2018) Alternative processing of its precursor is related to miR319 decreasing in melon plants exposed to cold. Sci Rep 8:15538. https://doi.org/10.1038/s41598-018-34012-7
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The authors would like to acknowledge the Deanship of Scientific Research at King Khalid University, Saudi Arabia, for their technical support RGP.2/169/42
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Abbas, A., Shah, A.N., Tanveer, M. et al. MiRNA fine tuning for crop improvement: using advance computational models and biotechnological tools. Mol Biol Rep 49, 5437–5450 (2022). https://doi.org/10.1007/s11033-022-07231-5
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DOI: https://doi.org/10.1007/s11033-022-07231-5