Skip to main content
SpringerLink
Log in

Genome-Wide Analysis of MicroRNAs in Sacred Lotus, Nelumbo nucifera (Gaertn)

  • Published:
Tropical Plant Biology Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are small non-coding regulatory RNAs that degrade or repress protein synthesis of their messenger RNA targets. This mode of posttranscriptional gene regulation is critical for plant growth and development as well as adaptation to stress conditions. Sacred lotus (Nelumbo nucifera) is a land plant but adapted to the aquatic environment. It is a basal eudicot in the order Proteales, with significant taxonomic importance. Thus identification of miRNAs in sacred lotus could provide information about miRNA evolution, particularly the conservation as well as divergence of miRNAs in dicots. To identify conserved and novel miRNAs in sacred lotus, small RNA libraries from leaves and flowers were sequenced as well as computational strategy was employed. These approaches resulted in identification of 81 miRNAs that can be grouped into 41 conserved/known miRNA families and 52 novel miRNAs forming 49 novel miRNA families. Using 3 mismatches between miRNAs and their mRNA targets as cutoff, we have predicted 137 genes as targets for the conserved and known miRNAs. Overall, this analysis provided a glimpse of miRNA-dependent posttranscriptional gene regulations in sacred lotus.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AGO:

Argonaute

ARF:

Auxin response factor

AP2-like:

Apetala 2-like transcription factor

CSD:

Cu/Zn superoxide dismutase

DCL1:

Dicer like-1

GRFs:

Growth regulating factors

HD-Zip factors:

Homeodomain leucine zipper family of transcription factors

HEN1:

Hua Enhancer 1

HYL1:

Hyponastic leaves 1

miRNAs:

MicroRNAs

NAC factors:

NAM, ATAF1/2 and CUC2 domain containing transcription factors

NBS-LRR genes:

Nucleoside-binding site leucine rich repeat genes

RISC:

RNA-induced silencing complex

RPTM:

Reads per ten million

SE:

Serrate 1

SPL:

Squamosa promoter binding protein-like

tasiRNAs:

Trans-acting small interfering RNAs

TCP factors:

Teosinte branched 1, Cycloidea, PCF (TCP)-domain protein family

TIR1:

Transport inhibitor response 1

References

  • Allen E, Howell MD (2010) miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Semin Cell Dev Biol 21:798–804

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Mol Biol 215:403–410

    CAS  Google Scholar 

  • Arenas-Huertero C, Perez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G et al (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44

    Article  PubMed  Google Scholar 

  • Chen H-M, Chen L-T, Patel K, Li Y-H, Baulcombe DC, Wu S-H (2010) 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc Natl Acad Sci U S A 107:15269–15274

    Article  PubMed  CAS  Google Scholar 

  • Cuperus JT, Carbonell A, Fahlgren N, Garcia-Ruiz H, Burke RT, Takeda A, Sullivan CM, Gilbert SD, Montgomery TA, Carrington JC (2010) Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat Struct Mol Biol 17:997–1003

    Article  PubMed  CAS  Google Scholar 

  • Hayden KE, Willard HF (2012) Composition and organization of active centromere sequences in complex genomes. BMC Genomics 13:324

    Article  PubMed  CAS  Google Scholar 

  • Jagadeeswaran G, Zheng Y, Li Y, Shukla L, Matts J, Hoyt P, Graham MS, Roe BA, Zhang W, Sunkar R (2009) Sequencing of a small RNA library from Medicago truncatula revealed four families of novel legume-specific and candidate microRNAs. New Phytol 184:85–98

    Article  PubMed  CAS  Google Scholar 

  • Jagadeeswaran G, Nimmakayala P, Zheng Y, Gowdu K, Reddy UK, Sunkar R (2012) Characterization of small RNA component of the leaves and fruits from four cucurbit species. BMC Genomics 13(1):329

    Article  PubMed  CAS  Google Scholar 

  • Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207

    Article  PubMed  CAS  Google Scholar 

  • Johnson C, Kasprzewska A, Tennessen K, Fernandes J, Nan GL, Walbot V, Sundaresan V, Vance V, Bowman LH (2009) Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res 19:1429–1440

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R, Frank W (2010) Transcriptional control of gene expression by microRNAs. Cell 140:111–122

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Zheng Y, Jagadeeswaran G, Li Y, Gowdu K, Sunkar R (2011) Identification and temporal expression analysis of conserved and novel miRNAs in Sorghum. Genomics 98:460–468

    Article  PubMed  Google Scholar 

  • Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B (2012) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci U S A 109:1790–1795

    Article  PubMed  CAS  Google Scholar 

  • Lu C et al (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci U S A 105:4951–4956

    Article  PubMed  CAS  Google Scholar 

  • Manavella PA, Koenig D, Rubio-Somoza I, Burbano HA, Becker C, Weigel D (2013) Tissue-specific silencing of Arabidopsis SU(VAR)3-9 HOMOLOG8 by miR171a. Plant Physiol 161:805–812

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Axtell MJ, Bartel B et al (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190

    Article  PubMed  CAS  Google Scholar 

  • Ming R, VanBuren R, Liu Y et al. (2013) The genome of the long-living sacred lotus (Nelumbo nucifera, Gaertn.). Genome Biol 14:R41

  • Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  PubMed  CAS  Google Scholar 

  • Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genet Dev 19:374–378

    Article  PubMed  CAS  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    Article  PubMed  CAS  Google Scholar 

  • Song X et al (2012) Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 69:462–474

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Jagadeeswaran G (2008) In silico identification of conserved miRNAs in large number of diverse plant species. BMC Plant Biol 8:37

    Article  PubMed  Google Scholar 

  • Sunkar R, Zhu JK (2007) Micro RNAs and short-interfering RNAs in plants. J Integr Plant Biol 49:817–826

    Article  CAS  Google Scholar 

  • Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu J-K (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25

    Article  PubMed  Google Scholar 

  • Sunkar R, Li Y, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H (2009) AGO1 Homeostasis involves differential production of 21-nt and 22-nt miR168 Species by MIR168a and MIR168b. PLoS One 4:e6442

    Article  PubMed  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    Article  PubMed  CAS  Google Scholar 

  • Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475

    Article  PubMed  CAS  Google Scholar 

  • Zanca AS, Vicentini R, Ortiz-Morea FA, Del Bem LE, da Silva MJ, Vincentz M, Nogueira FT (2010) Identification and expression analysis of microRNAs and targets in the biofuel crop sugarcane. BMC Plant Biol 10:260

    Article  PubMed  Google Scholar 

  • Zhai J et al (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Chia JM, Kumari S, Stein JC, Liu Z, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5:e1000716

    Article  PubMed  Google Scholar 

  • Zhang X, Zhao H, Gao S, Wang WC, Katiyar-Agarwal S, Huang HD, Raikhel N, Jin H (2011) Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(*)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 42:356–366

    Article  PubMed  CAS  Google Scholar 

  • Zheng Y, Zhang W (2010) Animal microRNA target prediction using diverse sequence-specific determinants. J Bioinform Comput Biol 8: 763–788

    Google Scholar 

  • Zheng Y, Li Y-F, Sunkar R, Zhang W (2012) SeqTar: An effective method for identifying microRNA guided cleavage sites from degradome of polyadenylated transcripts in plants. Nucleic Acids Res 40:e28

    Article  PubMed  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 research was supported by the Oklahoma Agricultural Experiment Station to RS and by a start-up grant of Fudan University to YZ.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, OK, 74074, USA

    Yun Zheng, Guru Jagadeeswaran, Kanchana Gowdu & Ramanjulu Sunkar

  2. Institute of Developmental Biology and Molecular Medicine, School of Life Sciences, Fudan University, Shanghai, 200433, China

    Yun Zheng

  3. Key Laboratory of Plant Germplasm Enhancement and Speciality Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, China

    Nian Wang & Shaohua Li

  4. Department of Plant Biology, University of Illinois, UIUC, Urbana Champaign, IL, USA

    Ray Ming

  5. Department of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, OK, 74078, USA

    Ramanjulu Sunkar

Authors
  1. Yun Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guru Jagadeeswaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kanchana Gowdu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shaohua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ray Ming
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ramanjulu Sunkar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ramanjulu Sunkar.

Additional information

Communicated by: Luiz Vieira

Electronic Supplementary Materials

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 30 kb)

ESM 2

(XLSX 43 kb)

ESM 3

(PDF 61 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zheng, Y., Jagadeeswaran, G., Gowdu, K. et al. Genome-Wide Analysis of MicroRNAs in Sacred Lotus, Nelumbo nucifera (Gaertn). Tropical Plant Biol. 6, 117–130 (2013). https://doi.org/10.1007/s12042-013-9127-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12042-013-9127-z

Keywords

Search

Navigation