Abstract
Key message
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.
Similar content being viewed by others
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
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
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
Baskin CC, Baskin MJ (1998) Seeds: Ecology, biogeography and evolution of dormancy and germination. Academic Press, San Diego
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
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2012) Seeds: Physiology of development, germination, and dormancy (3rd ed.). Springer, Berlin
Chen XM (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025
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
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
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
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159
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
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
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
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
Dugas DV, Bartel B (2004) MicroRNA regulation of gene expression in plants. Curr Opin Plant Biol 7:512–520
Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18:1166–1176
Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627
Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415
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
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460
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
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
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
Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560
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
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant MicroRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Kawashima T, Berger F (2014) Epigenetic reprogramming in plant sexual reproduction. Nat Rev Genet 15:613–624
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
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
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
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
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220
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
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
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
Li SB, Xie ZZ, Hu CG, Zhang JZ (2016) A review of auxin response factors (ARFs) in plants. Front Plant Sci 7:47
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
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
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
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
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
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
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
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
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
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
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
Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24:2678–2692
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
Raz V, Bergervoet JH, Koornneef M (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development 128:243–252
Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626
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
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
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
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520
Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16:258–264
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
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
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
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
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
Sparks E, Wachsman G, Benfey PN (2013) Spatiotemporal signalling in plant development. Nat Rev Genet 14:631–644
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
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
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
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
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
Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749
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
Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 155:1871–1884
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
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
Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138:2145–2154
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
Zhou X, Wang G, Zhang W (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol Syst Biol 3:103
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
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.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
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.
Additional information
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.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-017-2111-6