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Regulatory crosstalk between microRNAs and hormone signalling cascades controls the variation on seed dormancy phenotype at Arabidopsis thaliana seed set

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We employed an Illumina sequencing approach to identify candidate microRNA cohorts that may greatly contribute to seed dormancy modulation and to construct a microRNA-gene regulatory network in hormone signalling cascades.

Abstract

MicroRNAs (miRNAs) are important signalling molecules and regulate many developmental programs of plants. Some miRNAs have been integrated into gene regulatory networks (GRNs) and coordinate developmental plasticity, but few study systematically investigated how phenotypical variations are regulated through differential expression of miRNA tags in GRNs during seed set. Using ‘top–down’ analyses (i.e., identify miRNAs associated with known phenotypical variations), we chose two Arabidopsis ecotypes (Cvi-0 and Col-0) with contrasting seed dormancy and sequenced miRNA reads in the first ten phases at seed set. We computationally predicted target genes of miRNAs and implemented statistical analyses for normalized relative expression of top abundant miRNA cohorts between the two ecotypes. We especially focused on miRNA cohorts targeting mRNAs encoding transcription factors in hormone signalling cascades. We report, with high confidence hits, that a cohort of 14 miRNAs (miR-156b, -159b, -160, -161*, -319a, -390a, -396, -773a, -779, -842, -852, -859, -1886*, and a novel sequence in miR8172 family) may greatly contribute to seed dormancy modulation, of which seven are involved in hormone signalling cascades. Moreover, their expression patterns indicated that 5 ± 1 days after flowering (at embryogenesis-to-maturation transition) is a critical phase at seed set. This study reinforces the notion that miRNAs that regulate seed dormancy modulation and provides a novel paradigm of studying the correlation between genotypes (miRNAs) and phenotypes.

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References

  • Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in arabidopsis. J Biol Chem 283:15932–15945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali-Rachedi S, Bouinot D, Wagner MH, Bonnet M, Sotta B, Grappin P, Jullien M (2004) Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana. Planta 219:479–488

    Article  CAS  PubMed  Google Scholar 

  • An J, Lai J, Sajjanhar A, Lehman ML, Nelson CC (2014) miRPlant: An integrated tool for identification of plant miRNA from RNA sequencing data. BMC Bioinform 15:275

    Article  Google Scholar 

  • Baskin CC, Baskin MJ (1998) Seeds: Ecology, biogeography and evolution of dormancy and germination. Academic Press, San Diego

    Google Scholar 

  • Baud S, Boutin JP, Miquel M, Lepiniec L, Rochat C (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 40:151–160

    Article  CAS  Google Scholar 

  • Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2012) Seeds: Physiology of development, germination, and dormancy (3rd ed.). Springer, Berlin

    Google Scholar 

  • Chen XM (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Liu J, Cheng Y, Jia D (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129:1085–1094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen D, Meng Y, Ma X, Mao C, Bai Y, Cao J, Gu H, Wu P, Chen M (2010) Small RNAs in angiosperms: sequence characteristics, distribution and generation. Bioinformatics 26:1391–1394

    Article  CAS  PubMed  Google Scholar 

  • Chu A, Robertson G, Brooks D, Mungall AJ, Birol I, Coope R, Ma Y, Jones S, Marra MA (2015) Large-scale profiling of microRNAs for the cancer genome atlas. Nucleic Acids Res 44:e3

    Article  PubMed  PubMed Central  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Q, Zeng J, He XQ (2014a) Deep sequencing on a genome-wide scale reveals diverse stage-specific microRNAs in cambium during dormancy-release induced by chilling in poplar. BMC Plant Biol 14:267

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding ZJ, Yan JY, Li GX, Wu ZC, Zhang SQ, Zheng SJ (2014b) WRKY41 controls Arabidopsis seed dormancy via direct regulation of ABI3 transcript levels not downstream of ABA. Plant J 79:810–823

    Article  CAS  PubMed  Google Scholar 

  • Donohue K, de Casas RR, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319

    Article  Google Scholar 

  • Drost HG, Bellstädt J, Ó’Maoiléidigh DS, Silva AT, Gabel A, Weinholdt C, Ryan PT, Dekkers BJ, Bentsink L, Hilhorst HW, Ligterink W, Wellmer F, Grosse I, Quint M (2016) Post-embryonic hourglass patterns mark ontogenetic transitions in plant development. Mol Biol Evol 33:1158–1163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dugas DV, Bartel B (2004) MicroRNA regulation of gene expression in plants. Curr Opin Plant Biol 7:512–520

    Article  CAS  PubMed  Google Scholar 

  • Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18:1166–1176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415

    Article  CAS  PubMed  Google Scholar 

  • Gocal GF, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish RW, Dennis ES, Weigel D, King RW (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127:1682–1693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  CAS  PubMed  Google Scholar 

  • Harada JJ (1997) Seed maturation and control of germination. In: Larkins B, Vasil I (eds) Celluar and molecular biology of plant seed development. Kluwer Academic Publishers, Dordrecht, pp 545–592

    Chapter  Google Scholar 

  • Huang DQ, Koh C, Feurtado JA, Tsang EWT, Cutler AJ (2013) MicroRNAs and their putative targets in Brassica napus seed maturation. BMC Genom 14:140

    Article  CAS  Google Scholar 

  • Huo H, Wei S, Bradford KJ (2016) DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proc Natl Acad Sci USA 113:E2199–E2206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant MicroRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    Article  CAS  PubMed  Google Scholar 

  • Kawashima T, Berger F (2014) Epigenetic reprogramming in plant sexual reproduction. Nat Rev Genet 15:613–624

    Article  CAS  PubMed  Google Scholar 

  • Kim JY, Lee HJ, Jung HJ, Maruyama K, Suzuki N, Kang H (2010) Overexpression of microRNA395c or 395e affects differently the seed germination of Arabidopsis thaliana under stress conditions. Planta 232:1447–1454

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Bentsink L, Blankestijn-de Vries H, Debeajon I, Hanhart CJ, Léonkloosterziel KM, Peeters T, Raz V (2000) The genetics of seed dormancy in Arabidopsis thaliana. CAB International, Wallingford

    Book  Google Scholar 

  • Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22:3574–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulik A, Wawer I, Krzywińska E, Bucholc M, Dobrowolska G (2011) SnRK2 protein kinases—key regulators of plant response to abiotic stresses. Omics 15:859–872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci USA 107:8063–8070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Zhang Q, Zhang J, Wu L, Qi Y, Zhou JM (2010) Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 152:2222–2231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li DT, Wang LW, Liu X, Cui DZ, Chen TT, Zhang H, Jiang C, Xu CY, Li P, Li S, Zhao L, Chen HB (2013) Deep sequencing of maize small RNAs reveals a diverse set of microRNA in dry and imbibed seeds. PloS One 8:e55107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li SB, Xie ZZ, Hu CG, Zhang JZ (2016) A review of auxin response factors (ARFs) in plants. Front Plant Sci 7:47

    PubMed  PubMed Central  Google Scholar 

  • Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080

    Article  CAS  PubMed  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 XD, Zhang H, Zhao Y, Feng ZY, Li Q, Yang HQ, Luan S, Li JM, He ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci USA 110:15485–15490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Müller K, El-Kassaby YA, Kermode AR (2015) Changes in hormone flux and signaling in white spruce (Picea glauca) seeds during the transition from dormancy to germination in response to temperature cues. BMC Plant Biol 15:292

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu C, Fedoroff N (2000) A mutation in the arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12:2351–2365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14:1035–1046

    Article  CAS  PubMed  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin RC, Asahina M, Liu PP, Kristof JR, Coppersmith JL, Pluskota WE, Bassel GW, Goloviznina NA, Nguyen TT, Martínez-Andújar C, Kumar MBA, Pupel P, Nonogaki H (2010) The microRNA156 and microRNA172 gene regulation cascades at post-germinative stages in Arabidopsis. Seed Sci Res 20:79–87

    Article  CAS  Google Scholar 

  • Martin RC, Martínez-Andújar C, Nonogaki H (2012) Role of miRNAs in seed development. In: Sunkar R (ed) MicroRNAs in plant development and stress responses. Springer, Heidelberg, pp 109–121

    Chapter  Google Scholar 

  • Müller S, Rycak L, Winter P, Kahl G, Koch I, Rotter B (2013) omiRas: A Web server for differential expression analysis of miRNAs derived from small RNA-Seq data. Bioinformatics 29:2651–2652

    Article  PubMed  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    Article  CAS  PubMed  Google Scholar 

  • Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24:2678–2692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Morea FA, Vicentini R, Silva GFF, Silva EM, Carrer H, Rodrigues AP, Nogueira FTS (2013) Global analysis of the sugarcane microtranscriptome reveals a unique composition of small RNAs associated with axillary bud outgrowth. J Exp Bot 64:2307–2320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raz V, Bergervoet JH, Koornneef M (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development 128:243–252

    CAS  PubMed  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu JK, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63:417–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Resentini F, Felipo-Benavent A, Colombo L, Blázquez MA, Alabadí D, Masiero S (2015) TCP14 and TCP15 mediate the promotion of seed germination by gibberellins in Arabidopsis thaliana. Mol Plant 8:482–485

    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 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  CAS  PubMed  Google Scholar 

  • Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16:258–264

    Article  CAS  PubMed  Google Scholar 

  • Rueda A, Barturen G, Lebrón R, Gómez-Martín C, Alganza A, Oliver JL, Hackenberg M (2015) sRNAtoolbox: an integrated collection of small RNA research tools. Nucleic Acids Res 43:W467–W473

    Article  PubMed  PubMed Central  Google Scholar 

  • Rueda-Romero P, Barrero-Sicilia C, Gómez-Cadenas A, Carbonero P, Oñate-Sánchez L (2012) Arabidopsis thaliana DOF6 negatively affects germination in non-after-ripened seeds and interacts with TCP14. J Exp Bot 63:1937–1949

    Article  CAS  PubMed  Google Scholar 

  • Salehin M, Bagchi R, Estelle M (2015) SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell 27:9–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261

    Article  CAS  PubMed  Google Scholar 

  • Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Wu FQ, Wang XF, Du SY, Jiang T, Zhang XF, Zhao R, Sun HL, Liu R, Yu YT, Zhang DP (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sparks E, Wachsman G, Benfey PN (2013) Spatiotemporal signalling in plant development. Nat Rev Genet 14:631–644

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019

    Article  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, Chen X, Cui Y (2012) MicroRNA-mediated repression of the seed maturation program during vegetative development in Arabidopsis. PLoS Genet 8:e1003091

    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:e1001031

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H, Ashikari M, Matsuoka M (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47:427–444

    Article  CAS  PubMed  Google Scholar 

  • Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D, Meinke D (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135:1206–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    Article  CAS  PubMed  Google Scholar 

  • Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102:9703–9708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 155:1871–1884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218

    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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138:2145–2154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng J, Chen F, Wang Z, Cao H, Li X, Deng X, Soppe WJ, Li Y, Liu Y (2012) A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy. New Phytol 193:605–616

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Wang G, Zhang W (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol Syst Biol 3:103

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu QH, Upadhyaya NM, Gubler F, Helliwell CA (2009) Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol 9:149

    Article  PubMed  PubMed Central  Google Scholar 

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Author contribution statement

Y. L. conceived this study, performed data analyses, and wrote the manuscript. Y. A. E. coordinated the project.

Acknowledgements

We would like to extend our sincere gratitude to Dr. D. Miller (Genome Sciences Centre, BC Cancer Agency) for small RNA sequencing and N. Hodges (UBC) for the technical support on Ubuntu. We are equally thankful to Drs. M. Hackenberg (Universidad de Granada) and L. Jost (GenXPro GmbH) for helping set up software packages, sRNAtoolbox and OmiRas, respectively.

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Correspondence to Yang Liu or Yousry A. El-Kassaby.

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We have no competing interests.

Funding

This project was funded by the Johnson’s Family Forest Biotechnology Endowment and the National Science and Engineering Research Council of Canada Discovery and Industrial Research Chair to Y. A. E.

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Communicated by Nese Sreenivasulu.

The sRNA sequencing data have been deposited at Sequence Read Archive (SRA) in National Center for Biotechnology Information (NCBI) under the accession number, SRP072220.

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Liu, Y., El-Kassaby, Y.A. Regulatory crosstalk between microRNAs and hormone signalling cascades controls the variation on seed dormancy phenotype at Arabidopsis thaliana seed set. Plant Cell Rep 36, 705–717 (2017). https://doi.org/10.1007/s00299-017-2111-6

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