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PLOS ONE  2014 

Analysis of miRNAs and Their Targets during Adventitious Shoot Organogenesis of Acacia crassicarpa

DOI: 10.1371/journal.pone.0093438

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Organogenesis is an important process for plant regeneration by tissue or cell mass differentiation to regenerate a complete plant. MicroRNAs (miRNAs) play an essential role in regulating plant development by mediating target genes at transcriptional and post-transcriptional levels, but the diversity of miRNAs and their potential roles in organogenesis of Acacia crassicarpa have rarely been investigated. In this study, approximately 10 million sequence reads were obtained from a small RNA library, from which 189 conserved miRNAs from 57 miRNA families, and 7 novel miRNAs from 5 families, were identified from A. crassicarpa organogenetic tissues. Target prediction for these miRNAs yielded 237 potentially unique genes, of which 207 received target Gene Ontology annotations. On the basis of a bioinformatic analysis, one novel and 13 conserved miRNAs were selected to investigate their possible roles in A. crassicarpa organogenesis by qRT-PCR. The stage-specific expression patterns of the miRNAs provided information on their possible regulatory functions, including shoot bud formation, modulated function after transfer of the culture to light, and regulatory roles during induction of organogenesis. This study is the first to investigate miRNAs associated with A. crassicarpa organogenesis. The results provide a foundation for further characterization of miRNA expression profiles and roles in the regulation of diverse physiological pathways during adventitious shoot organogenesis of A. crassicarpa.


[1]  Pan ZG, You Y (1994) Introduction and provenance test of Acacia crassicarpa. Forest Research (China) 7: 498–505.
[2]  Beilharz VC, Pascoe IG, Wingfield MJ, Tjahjono B, Crous PW (2004) Passalora perplexa, an important pleoanamorphic leaf blight pathogen of Acacia crassicarpa in Australia and Indonesia. Stud Mycol 50: 471–479.
[3]  Midgley S (2000) Acacia crassicarpa: a tree in the domestication fast lane. Australian Tree Resources News 6: 1–2.
[4]  Engelmann F (1991) In vitro conservation of tropical plant germplasm-a review. Euphytica 57: 227–243. doi: 10.1007/bf00039669
[5]  Benson EE (2000) Sepecial symposium: In vitro plant recalcitrance in vitro plant recalcitrance: An introduction. In Vitro Cell Dev-Pl 36: 141–148. doi: 10.1007/s11627-000-0029-z
[6]  Che P, Gingerich DJ, Lall S, Howell SH (2002) Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell 14: 2771–2785. doi: 10.1105/tpc.006668
[7]  Van MTT (1973) Direct flower neoformation from superficial tissue of small explants of Nicotiana tabacum L. Planta. 115: 87–92. doi: 10.1007/bf00388609
[8]  Carraro N, Peaucelle A, Laufs P, Traas J (2006) Cell differentiation and organ initiation at the shoot apical meristem. Plant Mol Biol 60: 811–826. doi: 10.1007/s11103-005-2761-6
[9]  Dewan A, Nanda K, Gupta SC (1992) In vitro micropropagation of Acacia nilotica subsp. indica 10.Brenan via cotyledonary nodes. Plant Cell Rep 12: 18–21. doi: 10.1007/bf00232415
[10]  He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522–531. doi: 10.1038/nrg1379
[11]  Worm J, Stenvang J, Petri A, Frederiksen KS, Obad S, et al. (2009) Silencing of microRNA-155 in mice during acute inflammatory response leads to derepression of c/ebp Beta and down-regulation of G-CSF. Nucleic Acids Res 37: 5784–5792. doi: 10.1093/nar/gkp577
[12]  Yang M, Li Y, Padgett RW (2005) MicroRNAs: Small regulators with a big impact. Cytokine Growth F R 16: 387–393. doi: 10.1016/j.cytogfr.2005.02.008
[13]  Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669–687. doi: 10.1016/j.cell.2009.01.046
[14]  Ehrenreich LM, Purugganan M (2008) MicroRNAs in plants. Plant Signaling & Behavior 3: 829–830. doi: 10.4161/psb.3.10.5914
[15]  Martin K (2003) Plant regeneration through somatic embryogenesis on Holostemma ada-kodien, a rare medicinal plant. Plant Cell Tiss Org 72: 79–82. doi: 10.1007/s00299-002-0483-7
[16]  Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132: 3657–3668. doi: 10.1242/dev.01942
[17]  Vernoux T, Benfey PN (2005) Signals that regulate stem cell activity during plant development. Curr Opin Genet Dev 15: 388–394. doi: 10.1016/j.gde.2005.06.008
[18]  Yao D, Jin Y, Liu W, Wang X, Guo H, et al. (2013) Plant regeneration from mature zygotic embryo explants of Acacia crassicapa A. Cunn. ex Benth. via adventitous shoots organogenesis. Propag Ornam Plants 13: 86–92.
[19]  Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, et al. (2002) Prediction of plant microRNA targets. Cell 110: 513–520. doi: 10.1016/s0092-8674(02)00863-2
[20]  Quandt K, Frech K, Karas H, Wingender E, Werner T (1995) Matlnd and Matlnspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23: 4878–4884. doi: 10.1093/nar/23.23.4878
[21]  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2?ΔΔCT method. Methods 25: 402–408. doi: 10.1006/meth.2001.1262
[22]  Ong SS, Wickneswari R (2011) Expression profile of small RNAs in Acacia mangium secondary xylem tissue with contrasting lignin content-potential regulatory sequences in monolignol biosynthetic pathway. BMC genomics 12: S13. doi: 10.1186/1471-2164-12-s3-s13
[23]  Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, et al. (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20: 3186–3190. doi: 10.1105/tpc.108.064311
[24]  Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, et al. (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408: 86–89.
[25]  Zhang X, Zhao H, Gao S, Wang W-C, Katiyar-Agarwal S, et al. (2011) Arabidopsis argonaute 2 regulatesinnate immunity via miRNA393-mediated silencing of a golgi-localized SNARE gene, MEMB12. Mol Cell 42: 356–366. doi: 10.1016/j.molcel.2011.04.010
[26]  Kidner CA, Martienssen RA (2005) The developmental role of microRNA in plants. Curr Opin Plant Biol 8: 38–44. doi: 10.1016/j.pbi.2004.11.008
[27]  Yin Z, Li C, Han X, Shen F (2008) Identification of conserved microRNAs and their target genes in tomato (Lycopersicon esculentum). Gene 414: 60–66. doi: 10.1016/j.gene.2008.02.007
[28]  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. doi: 10.1105/tpc.105.031716
[29]  Ohler U, Yekta S, Lim LP, Bartel DP, Burge CB (2004) Patterns of flanking sequence conservation and a characteristic upstream motif for microRNA gene identification. Rna 10: 1309–1322. doi: 10.1261/rna.5206304
[30]  Wang JW, Czech B, Weigel D (2009) miR156-Regulated SPL Transcription Factors Define an Endogenous Flowering Pathway in Arabidopsis thaliana. Cell 138: 738–749. doi: 10.1016/j.cell.2009.06.014
[31]  Allen RS, Li J, Stahle MI, Dubroue’ A, Gubler F, et al. (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. P Natl Acad Sci USA 104: 16371–16376. doi: 10.1073/pnas.0707653104
[32]  Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, et al. (2007) Sequence and Expression Differences Underlie Functional Specialization of Arabidopsis MicroRNAs miR159 and miR319. Dev Cell 13: 115–125. doi: 10.1016/j.devcel.2007.04.012
[33]  Xie Z, Kasschau KD, Carrington JC (2003) Negative Feedback Regulation of Dicer-Like1 in Arabidopsis by microRNA-Guided mRNA Degradation. Curr Biol 13: 784–789. doi: 10.1016/s0960-9822(03)00281-1
[34]  Hasson A, Plessis A, Blein T, Adroher B, Grigg S, et al. (2011) Evolution and diverse roles of the CUP-SHAPED COTYLEDON genes in Arabidopsis leaf development. Plant Cell 23: 54–68. doi: 10.1105/tpc.110.081448
[35]  Zhu H, Hu F, Wang R, Zhou R, Sze S, et al. (2011) Arabidopsis Argonaute10 Specifically Sequesters miR166/165 to Regulate Shoot Apical Meristem Development. Cell 145: 242–256. doi: 10.1016/j.cell.2011.03.024
[36]  Kinoshita N, Wang H, Kasahara H, Liu J, MacPherson C, et al. (2012) IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress. Plant Cell 24: 3590–3602. doi: 10.1105/tpc.112.097006
[37]  Vaucheret H, Vazquez F, Crété P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Gene Dev 18: 1187–1197. doi: 10.1101/gad.1201404
[38]  Siré C, Moreno AB, Garcia-Chapa M, López-Moya JJ, Segundo BS (2009) Diurnal oscillation in the accumulation of Arabidopsis microRNAs, miR167, miR168, miR171 and miR398. FEBS lett 58: 1039–1044. doi: 10.1016/j.febslet.2009.02.024
[39]  Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, et al. (2003) Control of leaf morphogenesis by microRNAs. Nature 425: 257–263. doi: 10.1038/nature01958
[40]  Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, et al. (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA Affects Developmental Timing and Patterning in Arabidopsis. Curr Biol 16: 939–944. doi: 10.1016/j.cub.2006.03.065
[41]  Wang L, Gu X, Xu D, Wang W, Wang H, et al. (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. doi: 10.1093/jxb/erq307
[42]  Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57: 19–53. doi: 10.1146/annurev.arplant.57.032905.105218
[43]  Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18(8): 2051–2065. doi: 10.1105/tpc.106.041673
[44]  Design R-TPP (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39: 519–525. doi: 10.2144/000112010
[45]  Sugiyama M (1999) Organogenesis in vitro. Current opinion in plant biology 2: 61–64. doi: 10.1016/s1369-5266(99)80012-0
[46]  Che P, Lall S, Howell SH (2007) Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture. Planta 226: 1183–1194. doi: 10.1007/s00425-007-0565-4
[47]  Irish VF (2008) The Arabidopsis petal: a model for plant organogenesis. Trends Plant Sci 13: 430–436. doi: 10.1016/j.tplants.2008.05.006
[48]  Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant physiol 155: 1871–1884. doi: 10.1104/pp.110.171355
[49]  Luo Y-C, Zhou H, Li Y, Chen J-Y, Yang J-H, et al. (2006) Rice embryogenic calli express a unique set of microRNAs, suggesting regulatory roles of microRNAs in plant post-embryogenic development. FEBS lett 580: 5111–5116. doi: 10.1016/j.febslet.2006.08.046
[50]  Zhang J, Zhang S, Han S, Wu T, Li X, et al. (2012) Genome-wide identification of microRNAs in larch and stage-specific modulation of 11 conserved microRNAs and their targets during somatic embryogenesis. Planta 236: 647–657. doi: 10.1007/s00425-012-1643-9
[51]  Wu X-M, Liu M-Y, Ge X-X, Xu Q, Guo W-W (2011) Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of Valencia sweet orange. Planta 233: 495–505. doi: 10.1007/s00425-010-1312-9
[52]  Li T, Chen J, Qiu S, Zhang Y, Wang P, et al. (2012) Deep sequencing and microarray hybridization identify conserved and species-specific microRNAs during somatic embryogenesis in hybrid Yellow Poplar. PloS One 7: e43451. doi: 10.1371/journal.pone.0043451
[53]  Oh TJ, Wartell RM, Cairney J, Pullman GS (2008) Evidence for stage-specific modulation of specific microRNAs (miRNAs) and miRNA processing components in zygotic embryo and female gametophyte of loblolly pine (Pinus taeda). New Phytol 179: 67–80. doi: 10.1111/j.1469-8137.2008.02448.x
[54]  Lin Y, Lai Z (2013) Comparative Analysis Reveals Dynamic Changes in miRNAs and Their Targets and Expression during Somatic Embryogenesis in Longan (Dimocarpus longan Lour.). PloS One 8: e60337. doi: 10.1371/journal.pone.0060337
[55]  Axtell MJ (2008) Evolution of microRNAs and their targets: are all microRNAs biologically relevant? BBA-Gene Regul Mech 1779: 725–734. doi: 10.1016/j.bbagrm.2008.02.007
[56]  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. doi: 10.1111/j.1365-313x.2006.02980.x
[57]  Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17: 705–721. doi: 10.1105/tpc.104.027920
[58]  Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. P Natl Acad Sci USA 106: 22534–22539. doi: 10.1073/pnas.0908718106
[59]  Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297: 2053–2056. doi: 10.1126/science.1076311
[60]  Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, et al. (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137: 103–112. doi: 10.1242/dev.043067
[61]  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. doi: 10.1016/j.cub.2004.06.022
[62]  Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16: 457–465. doi: 10.1038/
[63]  Wang Y, Hu Z, Yang Y, Chen X, Chen G (2009) Function annotation of an SBP-box gene in Arabidopsis based on analysis of co-expression networks and promoters. Int J Mol Sci 10: 116–132. doi: 10.3390/ijms10010116
[64]  Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133: 3539–3547. doi: 10.1242/dev.02521
[65]  Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001–2019. doi: 10.1105/tpc.104.022830
[66]  Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol cell 14: 787–799. doi: 10.1016/j.molcel.2004.05.027


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