Abstract
Main conclusion
A robust workflow for the identification of miRNAs and their targets in saffron was developed. MicroRNA-mediated gene regulation in saffron is potentially involved in several biological processes, including the biosynthesis of highly valuable apocarotenoids.
Abstract
Saffron (Crocus sativus L.) is the most expensive spice in the world and a major source of apocarotenoids. Even though miRNAs (20–24 nt non-coding small RNAs) are important regulators of gene expression at transcriptional and post-transcriptional levels, their role in saffron has not been thoroughly investigated. As a result, a workflow for computational identification of miRNAs and their targets can be useful to uncover the regulatory networks underlying biological processes in this valuable plant. The efficiency of several assembly tools such as Trans-ABySS, Trinity, Bridger, rnaSPAdes, and EvidentialGene was evaluated based on both reference-based and reference-free metrics using transcriptome data. A reliable workflow for computational identification of miRNAs and their targets in saffron was described. The EvidentialGene was found to be the most efficient de novo transcriptome assembler for saffron as a complex triploid model, followed by the Trinity. In total, 66 miRNAs from 19 different families that target 2880 genes, including several transcription factors involved in the flowering transition, were identified. Three of the identified targets were involved in the terpenoids backbone biosynthesis. CsCCD and CsUGT genes involved in the apocarotenoids biosynthetic pathway were targeted by csa-miR156g and csa-miR156b-3p, revealing a unique post-transcriptional regulation dynamic in saffron. The identified miRNAs and their targets add to our understanding of the many biological roles of miRNAs in saffron and shed new light on the control of the apocarotenoid biosynthetic pathway in this valuable plant.
Similar content being viewed by others
Data availability
The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Agharbaoui Z, Leclercq M, Remita MA et al (2015) An integrative approach to identify hexaploid wheat miRNAome associated with development and tolerance to abiotic stress. BMC Genomics 16:339. https://doi.org/10.1186/s12864-015-1490-8
Ahrazem O, Argandoña J, Fiore A et al (2019) Multi-species transcriptome analyses for the regulation of crocins biosynthesis in Crocus. BMC Genomics 20:320. https://doi.org/10.1186/s12864-019-5666-5
Alptekin B, Akpinar BA, Budak H (2017) A comprehensive prescription for plant miRNA identification. Front Plant Sci 7:1–28. https://doi.org/10.3389/fpls.2016.02058
Ashraf N, Jain D, Vishwakarma RA (2015) Identification, cloning and characterization of an ultrapetala transcription factor CsULT1 from Crocus: a novel regulator of apocarotenoid biosynthesis. BMC Plant Biol 15:25. https://doi.org/10.1186/s12870-015-0423-7
Axtell MJ, Westholm JO, Lai EC (2011) Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12:221. https://doi.org/10.1186/gb-2011-12-4-221
Baba SA, Mohiuddin T, Basu S et al (2015) Comprehensive transcriptome analysis of Crocus sativus for discovery and expression of genes involved in apocarotenoid biosynthesis. BMC Genomics 16:698. https://doi.org/10.1186/s12864-015-1894-5
Barozai MYK, Baloch IA, Din M (2012) Identification of microRNAs and their targets in Helianthus. Mol Biol Rep 39:2523–2532. https://doi.org/10.1007/s11033-011-1004-y
Bartel DP (2018) Metazoan microRNAs. Cell 173:20–51. https://doi.org/10.1016/j.cell.2018.03.006
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Bonnet E, Wuyts J, Rouze P, Van de Peer Y (2004) Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences. Bioinformatics 20:2911–2917. https://doi.org/10.1093/bioinformatics/bth374
Bonnet E, He Y, Billiau K, Van de Peer Y (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26:1566–1568. https://doi.org/10.1093/bioinformatics/btq233
Budak H, Akpinar BA (2015) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics 15:523–531. https://doi.org/10.1007/s10142-015-0451-2
Burko Y, Shleizer-Burko S, Yanai O et al (2013) A role for APETALA1/FRUITFULL transcription factors in tomato leaf development. Plant Cell 25:2070–2083. https://doi.org/10.1105/tpc.113.113035
Bushmanova E, Antipov D, Lapidus A et al (2016) rnaQUAST: a quality assessment tool for de novo transcriptome assemblies. Bioinformatics 32:2210–2212
Bushmanova E, Antipov D, Lapidus A, Prjibelski AD (2019) rnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data. Gigascience. https://doi.org/10.1093/gigascience/giz100
Catalanotto C, Cogoni C, Zardo G (2016) MicroRNA in control of gene expression: an overview of nuclear functions. Int J Mol Sci 17:1712. https://doi.org/10.3390/ijms17101712
Chang Z, Li G, Liu J et al (2015) Bridger: a new framework for de novo transcriptome assembly using RNA-seq data. Genome Biol 16:30. https://doi.org/10.1186/s13059-015-0596-2
Chen C, Zhong Y, Yu F, Xu M (2020) Deep sequencing identifies miRNAs and their target genes involved in the biosynthesis of terpenoids in Cinnamomum camphora. Ind Crops Prod 145:111853. https://doi.org/10.1016/j.indcrop.2019.111853
Chib S, Thangaraj A, Kaul S et al (2020) Development of a system for efficient callus production, somatic embryogenesis and gene editing using CRISPR/Cas9 in saffron (Crocus sativus L.). Plant Methods 16:47. https://doi.org/10.1186/s13007-020-00589-2
Chopra R, Burow G, Farmer A et al (2014) Comparisons of de novo transcriptome assemblers in diploid and polyploid species using peanut (Arachis spp) RNA-seq data. PLoS ONE 9:e115055. https://doi.org/10.1371/journal.pone.0115055
Chow C-N, Zheng H-Q, Wu N-Y et al (2016) PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Res 44:D1154–D1160. https://doi.org/10.1093/nar/gkv1035
Crooks GE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190. https://doi.org/10.1101/gr.849004
Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222. https://doi.org/10.1046/j.1365-313X.1999.00444.x
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
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159. https://doi.org/10.1093/nar/gkr319
Dai X, Zhuang Z, Zhao PX (2019) psRNATarget V2: a high-performance plant small rna target analysis server. In: plant and animal genome XXVII conference (January 12–16, 2019). PAG
Dehury B, Panda D, Sahu J et al (2013) In silico identification and characterization of conserved miRNAs and their target genes in sweet potato (Ipomoea batatas L.) expressed sequence tags (ESTs). Plant Signal Behav 8:e26543. https://doi.org/10.4161/psb.26543
Fahlgren N, Carrington JC (2010) miRNA target prediction in plants. Plant microRNAs. Springer, pp 51–57
Fileccia V, Bertolini E, Ruisi P et al (2017) Identification and characterization of durum wheat microRNAs in leaf and root tissues. Funct Integr Genomics 17:583–598. https://doi.org/10.1007/s10142-017-0551-2
Fileccia V, Ingraffia R, Amato G et al (2019) Identification of microRNAS differentially regulated by water deficit in relation to mycorrhizal treatment in wheat. Mol Biol Rep 46:5163–5174. https://doi.org/10.1007/s11033-019-04974-6
Gandikota M, Birkenbihl RP, Höhmann S et al (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693. https://doi.org/10.1111/j.1365-313X.2006.02983.x
Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Harpke D, Meng S, Rutten T et al (2013) Phylogeny of Crocus (Iridaceae) based on one chloroplast and two nuclear loci: ancient hybridization and chromosome number evolution. Mol Phylogenet Evol 66:617–627. https://doi.org/10.1016/j.ympev.2012.10.007
He B, Zhao S, Chen Y et al (2015) Optimal assembly strategies of transcriptome related to ploidies of eukaryotic organisms. BMC Genomics 16:65. https://doi.org/10.1186/s12864-014-1192-7
Hölzer M, Marz M (2019) De novo transcriptome assembly: a comprehensive cross-species comparison of short-read RNA-Seq assemblers. Gigascience 8:1–16. https://doi.org/10.1093/gigascience/giz039
Hu J, Liu Y, Tang X et al (2020) Transcriptome profiling of the flowering transition in saffron (Crocus sativus L.). Sci Rep 10:9680. https://doi.org/10.1038/s41598-020-66675-6
Jain M, Srivastava PL, Verma M et al (2016) De novo transcriptome assembly and comprehensive expression profiling in Crocus sativus to gain insights into apocarotenoid biosynthesis. Sci Rep 6:22456. https://doi.org/10.1038/srep22456
Jeong D-H, German MA, Rymarquis LA et al (2010) Abiotic stress-associated miRNAs: detection and functional analysis. Plant microRNAs. Springer, pp 203–230
Jike W, Sablok G, Bertorelle G et al (2018) In silico identification and characterization of a diverse subset of conserved microRNAs in bioenergy crop Arundo donax L. Sci Rep 8:1–13. https://doi.org/10.1038/s41598-018-34982-8
Jung J-H, Seo PJ, Kang SK, Park C-M (2011) miR172 signals are incorporated into the miR156 signaling pathway at the SPL3/4/5 genes in Arabidopsis developmental transitions. Plant Mol Biol 76:35–45. https://doi.org/10.1007/s11103-011-9759-z
Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73. https://doi.org/10.1093/nar/gkt1181
Kozomara A, Birgaoanu M, Griffiths-Jones S (2019) miRBase: from microRNA sequences to function. Nucleic Acids Res 47:D155–D162. https://doi.org/10.1093/nar/gky1141
Kubeczka K-H (2020) History and sources of essential oil research. Handbook of essential oils. CRC Press, pp 3–39
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Kurihara Y, Watanabe Y (2010) Processing of miRNA precursors. Plant microRNAs. Springer, pp 231–241
Kurtoglu KY, Kantar M, Budak H (2014) New wheat microRNA using whole-genome sequence. Funct Integr Genomics 14:363–379. https://doi.org/10.1007/s10142-013-0357-9
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Leinonen R, Sugawara H, Shumway M, Collaboration INSD (2010) The sequence read archive. Nucleic Acids Res 39:D19–D21
Li W-X, Oono Y, Zhu J-KJ et al (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251. https://doi.org/10.1105/tpc.108.059444
Li X-Y, Lin E-P, Huang H-H et al (2018) Molecular characterization of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) gene family in Betula luminifera. Front Plant Sci 9:608. https://doi.org/10.3389/fpls.2018.00608
Liu Q, Feng Y, Zhu Z (2009) Dicer-like (DCL) proteins in plants. Funct Integr Genomics 9:277–286. https://doi.org/10.1007/s10142-009-0111-5
Liu H, Searle IR, Watson-Haigh NS et al (2015) Genome-wide identification of microRNAs in leaves and the developing head of four durum genotypes during water deficit stress. PLoS ONE 10:e0142799. https://doi.org/10.1371/journal.pone.0142799
Liu J, Cheng X, Liu P et al (2017) MicroRNA319-regulated TCPs interact with FBHs and PFT1 to activate CO transcription and control flowering time in Arabidopsis. PLoS Genet 13:e1006833. https://doi.org/10.1371/journal.pgen.1006833
Liu T, Yu S, Xu Z et al (2020) Prospects and progress on crocin biosynthetic pathway and metabolic engineering. Comput Struct Biotechnol J 18:3278–3286. https://doi.org/10.1016/j.csbj.2020.10.019
Lucas SJ, Budak H (2012) Sorting the wheat from the chaff: identifying miRNAs in genomic survey sequences of Triticum aestivum chromosome 1AL. PLoS ONE 7:e40859. https://doi.org/10.1371/journal.pone.0040859
Mamrot J, Legaie R, Ellery SJ et al (2017) De novo transcriptome assembly for the spiny mouse (Acomys cahirinus). Sci Rep 7:8996. https://doi.org/10.1038/s41598-017-09334-7
Martinelli F, Cannarozzi G, Balan B et al (2018) Identification of miRNAs linked with the drought response of tef [Eragrostis tef (Zucc.) Trotter]. J Plant Physiol 224–225:163–172. https://doi.org/10.1016/j.jplph.2018.02.011
Moazzzam Jazi M, Seyedi SM, Ebrahimie E et al (2017) A genome-wide transcriptome map of pistachio (Pistacia vera L.) provides novel insights into salinity-related genes and marker discovery. BMC Genomics 18:627. https://doi.org/10.1186/s12864-017-3989-7
Moreton J, Dunham SP, Emes RD (2014) A consensus approach to vertebrate de novo transcriptome assembly from RNA-seq data: assembly of the duck (Anas platyrhynchos) transcriptome. Front Genet 5:190. https://doi.org/10.3389/fgene.2014.00190
Moriya Y, Itoh M, Okuda S et al (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185. https://doi.org/10.1093/nar/gkm321
Mousavi S, Alisoltani A, Shiran B et al (2014) De novo transcriptome assembly and comparative analysis of differentially expressed genes in Prunus dulcis Mill. in response to freezing stress. PLoS ONE 9:e104541. https://doi.org/10.1371/journal.pone.0104541
Nakashima K, Jan A, Todaka D et al (2014) Comparative functional analysis of six drought-responsive promoters in transgenic rice. Planta 239:47–60. https://doi.org/10.1007/s00425-013-1960-7
Nazarov PV, Reinsbach SE, Muller A et al (2013) Interplay of microRNAs, transcription factors and target genes: linking dynamic expression changes to function. Nucleic Acids Res 41:2817–2831. https://doi.org/10.1093/nar/gks1471
Patro R, Duggal G, Love MI et al (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods 14:417–419. https://doi.org/10.1038/nmeth.4197
Petijová L, Jurčacková Z, Čellárová E (2020) Computational screening of miRNAs and their targets in leaves of Hypericum spp. by transcriptome-mining: a pilot study. Planta 251:49. https://doi.org/10.1007/s00425-020-03342-0
Robertson G, Schein J, Chiu R et al (2010) De novo assembly and analysis of RNA-seq data. Nat Methods 7:909–912. https://doi.org/10.1038/nmeth.1517
Roy S, Nath D, Paul P, Chakraborty S (2020) Computational identification of conserved microRNAs and functional annotation of their target genes in Citrus limon. S Afr J Bot 130:109–116. https://doi.org/10.1016/j.sajb.2019.12.009
Sabzehzari M, Naghavi MR (2019) Phyto-miRNAs-based regulation of metabolites biosynthesis in medicinal plants. Gene 682:13–24. https://doi.org/10.1016/j.gene.2018.09.049
Samad AFA, Sajad M, Nazaruddin N et al (2017) MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci 8:565. https://doi.org/10.3389/fpls.2017.00565
Samad AFA, Rahnamaie-Tajadod R, Sajad M et al (2019) Regulation of terpenoid biosynthesis by miRNA in Persicaria minor induced by Fusarium oxysporum. BMC Genomics 20:1–22
Sarvepalli K, Nath U (2011) Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J 67:595–607. https://doi.org/10.1111/j.1365-313X.2011.04616.x
Schwab R, Palatnik JF, Riester M et al (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527. https://doi.org/10.1016/j.devcel.2005.01.018
Seppey M, Manni M, Zdobnov EM (2019) BUSCO: assessing genome assembly and annotation completeness. Gene prediction. Springer, pp 227–245
Shannon P (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Simão FA, Waterhouse RM, Ioannidis P et al (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212. https://doi.org/10.1093/bioinformatics/btv351
Smith-Unna R, Boursnell C, Patro R et al (2016) TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Res 26:1134–1144. https://doi.org/10.1101/gr.196469.115
Srivastava PK, Moturu T, Pandey P et al (2014) A comparison of performance of plant miRNA target prediction tools and the characterization of features for genome-wide target prediction. BMC Genomics 15:348. https://doi.org/10.1186/1471-2164-15-348
Sunkar R, Zhou X, Zheng Y et al (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25. https://doi.org/10.1186/1471-2229-8-25
Taheri-Dehkordi A, Naderi R, Martinelli F, Salami SA (2020) A robust workflow for indirect somatic embryogenesis and cormlet production in saffron (Crocus sativus L.) and its wild allies C. caspius and C. speciosus. Heliyon 6:e05841. https://doi.org/10.1016/j.heliyon.2020.e05841
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Tan H, Chen X, Liang N et al (2019) Transcriptome analysis reveals novel enzymes for apo-carotenoid biosynthesis in saffron and allows construction of a pathway for crocetin synthesis in yeast. J Exp Bot 70:4819–4834. https://doi.org/10.1093/jxb/erz211
Tang R, Li L, Zhu D et al (2012) Mouse miRNA-709 directly regulates miRNA-15a/16-1 biogenesis at the posttranscriptional level in the nucleus: evidence for a microRNA hierarchy system. Cell Res 22:504–515. https://doi.org/10.1038/cr.2011.137
Tarantilis PA, Tsoupras G, Polissiou M (1995) Determination of saffron (Crocus sativus L.) components in crude plant extract using high-performance liquid chromatography-UV-visible photodiode-array detection-mass spectrometry. J Chromatogr A 699:107–118. https://doi.org/10.1016/0021-9673(95)00044-N
Tholl D (2015) Biosynthesis and biological functions of terpenoids in plants. Biotechnology of isoprenoids. Springer, pp 63–106
Vahedi M, Kabiri M, Salami SA et al (2018) Quantitative HPLC-based metabolomics of some Iranian saffron (Crocus sativus L.) accessions. Ind Crops Prod 118:26–29. https://doi.org/10.1016/j.indcrop.2018.03.024
Verma P, Singh N, Khan SA et al (2020) TIAs pathway genes and associated miRNA identification in Vinca minor: supporting aspidosperma and eburnamine alkaloids linkage via transcriptomic analysis. Physiol Mol Biol Plants 26:1695–1711. https://doi.org/10.1007/s12298-020-00842-x
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63. https://doi.org/10.1038/nrg2484
Wang J-W, Park MY, Wang L-J et al (2011) MiRNA control of vegetative phase change in trees. PLoS Genet 7:e1002012. https://doi.org/10.1371/journal.pgen.1002012
Wang L, Liu N, Wang T et al (2018) The GhmiR157a–GhSPL10 regulatory module controls initial cellular dedifferentiation and callus proliferation in cotton by modulating ethylene-mediated flavonoid biosynthesis. J Exp Bot 69:1081–1093. https://doi.org/10.1093/jxb/erx475
Waterhouse RM, Seppey M, Simão FA et al (2018) BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol 35:543–548
Wei R, Qiu D, Wilson IW et al (2015) Identification of novel and conserved microRNAs in Panax notoginseng roots by high-throughput sequencing. BMC Genomics 16:835. https://doi.org/10.1186/s12864-015-2010-6
Wu L, Zhang Q, Zhou H et al (2009) Rice microRNA effector complexes and targets. Plant Cell 21:3421–3435. https://doi.org/10.1105/tpc.109.070938
Wu H-J, Ma Y-K, Chen T et al (2012) PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Res 40:W22–W28. https://doi.org/10.1093/nar/gks554
Xin M, Wang Y, Yao Y et al (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123. https://doi.org/10.1186/1471-2229-10-123
Ye J, Fang L, Zheng H et al (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297. https://doi.org/10.1093/nar/gkl031
Ye J, Zhang X, Tan J et al (2020) Global identification of Ginkgo biloba microRNAs and insight into their role in metabolism regulatory network of terpene trilactones by high-throughput sequencing and degradome analysis. Ind Crops Prod 148:112289. https://doi.org/10.1016/j.indcrop.2020.112289
Yu B (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935. https://doi.org/10.1126/science.1107130
Zakeel MCM, Safeena MIS, Komathy T (2019) In silico identification of microRNAs and their target genes in watermelon (Citrullus lanatus). Sci Hortic (amsterdam) 252:55–60. https://doi.org/10.1016/j.scienta.2019.02.012
Zhang B, Pan X, Cannon CH et al (2006a) Conservation and divergence of plant microRNA genes. Plant J 46:243–259. https://doi.org/10.1111/j.1365-313X.2006.02697.x
Zhang B, Pan X, Cobb GP, Anderson TA (2006b) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16. https://doi.org/10.1016/j.ydbio.2005.10.036
Zhang BH, Pan XP, Cox SB et al (2006c) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci C 63:246–254. https://doi.org/10.1007/s11033-011-1004-y
Zheng Y, Jiao C, Sun H et al (2016) iTAK: a Program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol Plant 9:1667–1670. https://doi.org/10.1016/j.molp.2016.09.014
Funding
The authors received no financial support for the research.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Ethical approval
No animals or harmful substances have been used for this research.
Additional information
Communicated by Anastasios Melis.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Taheri-Dehkordi, A., Naderi, R., Martinelli, F. et al. Computational screening of miRNAs and their targets in saffron (Crocus sativus L.) by transcriptome mining. Planta 254, 117 (2021). https://doi.org/10.1007/s00425-021-03761-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-021-03761-7