Skip to main content

Advertisement

Log in

Discovery and profiling of novel and conserved microRNAs during flower development in Carya cathayensis via deep sequencing

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Hickory (Carya cathayensis Sarg.) is an economically important woody plant in China, but its long juvenile phase delays yield. MicroRNAs (miRNAs) are critical regulators of genes and important for normal plant development and physiology, including flower development. We used Solexa technology to sequence two small RNA libraries from two floral differentiation stages in hickory to identify miRNAs related to flower development. We identified 39 conserved miRNA sequences from 114 loci belonging to 23 families as well as two novel and ten potential novel miRNAs belonging to nine families. Moreover, 35 conserved miRNA*s and two novel miRNA*s were detected. Twenty miRNA sequences from 49 loci belonging to 11 families were differentially expressed; all were up-regulated at the later stage of flower development in hickory. Quantitative real-time PCR of 12 conserved miRNA sequences, five novel miRNA families, and two novel miRNA*s validated that all were expressed during hickory flower development, and the expression patterns were similar to those detected with Solexa sequencing. Finally, a total of 146 targets of the novel and conserved miRNAs were predicted. This study identified a diverse set of miRNAs that were closely related to hickory flower development and that could help in plant floral induction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ARF:

Auxin response factor

DAFB:

Days after full bloom

miRNA:

MicroRNA

miRNA*:

miRNA star

qRT-PCR:

Quantitative real-time PCR

SPB:

Squamosa promoter-binding

sRNA:

Small RNA

References

  • Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    Article  PubMed  CAS  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769

    Article  PubMed  CAS  Google Scholar 

  • Barakat A, Wall PK, Diloreto S, Depamphilis CW, Carlson JE (2007) Conservation and divergence of microRNAs in Populus. BMC Genomics 8:481

    Article  PubMed  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2011) GenBank. Nucleic Acids Res 39:D32–D37

    Article  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2005) MicroRNA biogenesis and function in plants. FEBS Lett 579:5923–5931

    Article  PubMed  CAS  Google Scholar 

  • Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR, Bateman A (2009) Rfam: updates to the RNA families database. Nucleic Acids Res 37:D136–D140

    Article  PubMed  CAS  Google Scholar 

  • Glazov EA, Cottee PA, Barris WC, Moore RJ, Dalrymple BP, Tizard ML (2008) A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res 18:957–964

    Article  PubMed  CAS  Google Scholar 

  • Grant-Downton R, Le Trionnaire G, Schmid R, Rodriguez-Enriquez J, Hafidh S, Mehdi S, Twell D, Dickinson H (2009) MicroRNA and tasiRNA diversity in mature pollen of Arabidopsis thaliana. BMC Genomics 10:643

    Article  PubMed  Google Scholar 

  • Griffiths-Jones S (2010) miRBase: microRNA sequences and annotation. Curr Protoc Bioinforma Chapter 12: Unit 12.19.11-10

  • Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132

    Article  PubMed  Google Scholar 

  • Jagadeeswaran G, Zheng Y, Li Y-F, Shukla LI, Matts J, Hoyt P, Macmil SL, Wiley GB, Roe BA, Zhang W, Sunkar R (2009) Cloning and characterization of small RNAs from Medicago truncatula reveals four novel legume-specific microRNA families. New Phytol 184:85–98

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  PubMed  CAS  Google Scholar 

  • Jung JH, Park CM (2007) MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 225:1327–1338

    Article  PubMed  CAS  Google Scholar 

  • Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19:2736–2748

    Article  PubMed  CAS  Google Scholar 

  • Klevebring D, Street NR, Fahlgren N, Kasschau KD, Carrington JC, Lundeberg J, Jansson S (2009) Genome-wide profiling of Populus small RNAs. BMC Genomics 10:620

    Article  PubMed  Google Scholar 

  • Kulcheski FR, de Oliveira LF, Molina LG, Almerao MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimaraes FC, Abdelnoor RV, Nascimento LC, Carazzolle MF, Pereira GA, Margis R (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307

    Article  PubMed  CAS  Google Scholar 

  • Kwak P, Wang Q, Chen X, Qiu C, Yang Z (2009) Enrichment of a set of microRNAs during the cotton fiber development. BMC Genomics 10:457

    Article  PubMed  Google Scholar 

  • Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131:4311–4322

    Article  PubMed  CAS  Google Scholar 

  • Levy YY, Dean C (1998) The transition to flowering. Plant Cell 10:1973–1989

    PubMed  CAS  Google Scholar 

  • Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714

    Article  PubMed  CAS  Google Scholar 

  • Li B, Qin Y, Duan H, Yin W, Xia X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Thong Z, Yu H (2009) Coming into bloom: the specification of floral meristems. Development 136:3379–3391

    Article  PubMed  CAS  Google Scholar 

  • Liu S, Li D, Li Q, Zhao P, Xiang Z, Xia Q (2010) MicroRNAs of Bombyx mori identified by Solexa sequencing. BMC Genomics 11:148

    Article  PubMed  Google Scholar 

  • Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203

    Article  PubMed  CAS  Google Scholar 

  • Lu S, Sun Y-H, Amerson H, Chiang VL (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J 51:1077–1098

    Article  PubMed  CAS  Google Scholar 

  • Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151

    Article  PubMed  CAS  Google Scholar 

  • Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38(Suppl):S31–S36

    Article  PubMed  CAS  Google Scholar 

  • Mathews DH, Sabina J, Zuker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK (2008) Criteria for annotation of plant microRNAS. Plant Cell 20:3186–3190

    Article  PubMed  CAS  Google Scholar 

  • Mohorianu I, Schwach F, Jing R, Lopez-Gomollon S, Moxon S, Szittya G, Sorefan K, Moulton V, Dalmay T (2011) Profiling of short RNAs during fleshy fruit development reveals stage-specific sRNAome expression patterns. Plant J 67:232–246

    Article  PubMed  CAS  Google Scholar 

  • Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14:S111–S130

    PubMed  CAS  Google Scholar 

  • Moxon S, Jing R, Szittya G, Schwach F, Rusholme Pilcher RL, Moulton V, Dalmay T (2008) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res 18:1602–1609

    Article  PubMed  CAS  Google Scholar 

  • Pang M, Woodward AW, Agarwal V, Guan X, Ha M, Ramachandran V, Chen X, Triplett BA, Stelly DM, Chen ZJ (2009) Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genome Biol 10:R122

    Article  PubMed  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150:1541–1555

    Article  PubMed  Google Scholar 

  • Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62:960–976

    PubMed  CAS  Google Scholar 

  • Pidkowich MS, Klenz JE, Haughn GW (1999) The making of a flower: control of floral meristem identity in Arabidopsis. Trends Plant Sci 4:64–70

    Article  PubMed  Google Scholar 

  • Rasko DA, Ravel J, Okstad OA, Helgason E, Cer RZ, Jiang L, Shores KA, Fouts DE, Tourasse NJ, Angiuoli SV, Kolonay J, Nelson WC, Kolsto AB, Fraser CM, Read TD (2004) The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. Nucleic Acids Res 32:977–988

    Article  PubMed  CAS  Google Scholar 

  • Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16:457–465

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    Article  PubMed  CAS  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527

    Article  PubMed  CAS  Google Scholar 

  • Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39:519–525

    Article  PubMed  CAS  Google Scholar 

  • Simpson GG, Dean C (2002) Arabidopsis, the rosetta stone of flowering time? Science 296:285–289

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Wang T, Chen L, Zhao M, Tian Q, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367

    Article  PubMed  CAS  Google Scholar 

  • Wang ZJ, Huang JQ, Huang YJ, Chen FF, Zheng BS (2012) Cloning and characterization of a homologue of the FLORICAULA/LEAFY gene in hickory (Carya cathayensis Sarg.). Plant Mol Biol Rep. doi:10.1007/s11105-011-0389-z

  • Wei LQ, Yan LF, Wang T (2011) Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol 12:R53

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46:243–259

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Xu Y, Huan Q, Chong K (2009) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 10:449

    Article  PubMed  Google Scholar 

  • Zhao CZ, Xia H, Frazier T, Yao YY, Bi Y-P, Li AQ, Li M-J, Li CS, Zhang BH, Wang XJ (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10:3

    Article  PubMed  Google Scholar 

  • Zluvova J, Nicolas M, Berger A, Negrutiu I, Moneger F (2006) Premature arrest of the male flower meristem precedes sexual dimorphism in the dioecious plant Silene latifolia. P Natl Acad Sci USA 103:18854–18859

    Article  CAS  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (30872047, 31170637 and 31070604), the initial project of the National Basic Research Program of China (2011CB111510), the Zhejiang Provincial Natural Science Foundation of China (Z307534 and Y305331), the Fruit Innovation Team Project of Zhejiang Province (2009R50033), the Key Project of the Department of Science and Technology of Zhejiang Province (2007C12023) and the Innovation Team Project of Zhejiang A & F University (Class B) (2007).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bing Song Zheng.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Z.J., Huang, J.Q., Huang, Y.J. et al. Discovery and profiling of novel and conserved microRNAs during flower development in Carya cathayensis via deep sequencing. Planta 236, 613–621 (2012). https://doi.org/10.1007/s00425-012-1634-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1634-x

Keywords

Navigation