Skip to main content
SpringerLink
Log in

MicroRNAs expression patterns in the response of poplar woody root to bending stress

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

Abstract

Main conclusion

The paper reports for the first time, in poplar woody root, the expression of five mechanically-responsive miRNAs. The observed highly complex expression pattern of these miRNAs in the bent root suggest that their expression is not only regulated by tension and compression forces highlighting their role in several important processes, i.e., lateral root formation, lignin deposition, and response to bending stress.

Mechanical stress is one of the major abiotic stresses significantly affecting plant stability, growth, survival, and reproduction. Plants have developed complex machineries to detect mechanical perturbations and to improve their anchorage. MicroRNAs (miRNAs), small non-coding RNAs (18–24 nucleotides long), have been shown to regulate various stress-responsive genes, proteins and transcription factors, and play a crucial role in counteracting adverse conditions. Several mechanical stress-responsive miRNAs have been identified in the stem of Populus trichocarpa plants subjected to bending stress. However, despite the pivotal role of woody roots in plant anchorage, molecular mechanisms regulating poplar woody root responses to mechanical stress have still been little investigated. In the present paper, we investigate the spatial and temporal expression pattern of five mechanically-responsive miRNAs in three regions of bent poplar woody taproot and unstressed controls by quantitative RT-PCR analysis. Alignment of the cloned and sequenced amplified fragments confirmed that their nucleotide sequences are homologous to the mechanically-responsive miRNAs identified in bent poplar stem. Computational analysis identified putative target genes for each miRNA in the poplar genome. Additional miRNA target sites were found in several mechanical stress-related factors previously identified in poplar root and a subset of these was further analyzed for expression at the mRNA or protein level. Integrating the results of miRNAs expression patterns and target gene functions with our previous morphological and proteomic data, we concluded that the five miRNAs play crucial regulatory roles in reaction woody formation and lateral root development in mechanically-stressed poplar taproot.

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
Fig. 4

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ABS:

Above-bending sector

AP2:

APETALA 2

BBP:

Blue basic copper protein

BBS:

Below-bending sector

BS:

Bending sector

BTF3:

Basic transcription factor 3

ERF:

Ethylene responsive factor

GA:

Gibberellic acid

GAI:

Gibberellins insensitive

IAA:

Indole-3-acetic acid

NAC:

Nascent polypeptide associated complex

RGL1:

Repressor of ga1-3(RGA)-like 1

SCR:

Scarecrow

STK:

Serine/threonine protein kinase

References

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

    Article  CAS  PubMed  Google Scholar 

  • Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165

    Article  PubMed  Google Scholar 

  • Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP (2008) The impact of microRNAs on protein output. Nature 455:64–71

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barrera-Figueroa BE, Gao L, Wu Z, Zhou X, Zhu J, Jin H, Liu R, Zhu JK (2012) High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol 12:132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brennecke J, Stark A, Russell RB, Cohen SM (2005) Principles of microRNA target recognition. PLoS Biol 3:e85

    Article  PubMed Central  PubMed  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    Article  PubMed  Google Scholar 

  • Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ding Q, Zeng J, He XQ (2014) 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 Central  PubMed  Google Scholar 

  • Ditengout FA, Teale WD, Kochersperger P, Flittner KA, Kneuper I, van der Graaff E, Nziengui H, Pinosa F, Li X, Nitschke R (2008) Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:18818–18823

    Article  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    Article  CAS  PubMed  Google Scholar 

  • Funada R, Miura T, Shimizu Y, Kinase T, Nakaba S, Kubo T, Sano Y (2008) Gibberellin induced formation of tension wood in angiosperm trees. Planta 227:1409–1414

    Article  CAS  PubMed  Google Scholar 

  • Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:D154–D158

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to down-regulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    Article  CAS  PubMed  Google Scholar 

  • Heidstra R, Welch D, Scheres B (2004) Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev 18:1964–1969

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORTROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    Article  CAS  PubMed  Google Scholar 

  • Himanem K, Boucheron E, Vanneste S, de Almeida-Engler J, Inze D, Beeckman T (2002) Auxin mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351

    Article  Google Scholar 

  • Jensen MK, Hagedorn PH, de Torres-Zabala M, Grant MR, Rung JH, Collinge DB, Lyngkjaer MF (2008) Transcriptional regulation by an NAC (NAMATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J 56:867–880

    Article  CAS  PubMed  Google Scholar 

  • Jia X, Ren L, Chen Q, Li R, Tang G (2009) UV-B-responsive microRNAs in Populus tremula. J Plant Physiol 166:2046–2057

    Article  CAS  PubMed  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 

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

    Article  CAS  PubMed  Google Scholar 

  • Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genomic 10:493–507

    Article  CAS  Google Scholar 

  • Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39:D152–D157

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee Y, Jeon K, Lee JT, Kim S, Kim VN (2002) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 21:4663–4670

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Love J, Björklund S, Vahala J, Hertzberg M, Kangasjärvi J, Sundberg B (2009) Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. Proc Natl Acad Sci USA 106:5984–5989

    Article  CAS  PubMed Central  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu S, Li L, Yi X, Joshi CP, Chiang VL (2008a) Differential expression of three eucalyptus secondary cell wall-related cellulose synthase genes in response to tension stress. J Exp Bot 59:681–695

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mayrose M, Ekengren SK, Melech-Bonfil S, Martin GB, Sessa G (2006) A novel link between tomato GRAS genes, plant disease resistance and mechanical stress response. Mol Plant Phathol 7:593–604

    Article  CAS  Google Scholar 

  • Mihr C, Braun HP (2003) Proteomics in plant biology. In: Conn PM (ed) Handbook of proteomic methods. Humana Press, Totowa, pp 409–416

    Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K (2008) Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55:65–76

    Article  CAS  PubMed  Google Scholar 

  • Richter GL, Monshausen GB, Krol A, Gilroy S (2009) Mechanical stimuli modulate lateral root organogenesis. Plant Physiol 151:1855–1866

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rigal A, Yordanov YS, Perrone I, Karlberg A, Tisserant E, Bellini C et al (2012) The AINTEGUMENTA LIKE1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol 160:1996–2006

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100:10096–10101

    Article  CAS  PubMed Central  PubMed  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  CAS  PubMed  Google Scholar 

  • Scippa GS, Trupiano D, Rocco M, Di Iorio A, Chiatante D (2008) Unravelling the response of poplar (Populus nigra) roots to mechanical stress imposed by bending. Plant Biosyst 142(2):401–413

    Article  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tiimonen H, Häggman H, Tsai CJ, Chiang V, Aronen T (2007) The seasonal activity and the effect of mechanical bending and wounding on the PtCOMT promoter in Betula pendula roth. Plant Cell Rep 26:1205–1214

    Article  CAS  PubMed  Google Scholar 

  • Trindade I, Capitão C, Dalmay T, Fevereiro MP, Santos DM (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231:705–716

    Article  CAS  PubMed  Google Scholar 

  • Trupiano D, Renzoni G, Rocco M, Scaloni A, Viscosi V, Chiatante D, Scippa GS (2012a) The proteome of Populus nigra woody root: response to bending. Ann Bot 110:415–432

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trupiano D, Di Iorio A, Montagnoli A, Lasserre B, Rocco M, Grosso A, Scaloni A, Marra M, Chiatante D, Scippa GS (2012b) Involvement of lignin and hormones in the response of woody poplar taproots to mechanical stress. Physiol Plant 146:39–52

    Article  CAS  PubMed  Google Scholar 

  • Trupiano D, Yordanov Y, Regan S, Meilan R, Tschaplinski T, Scippa GS, Busov V (2013a) Identification, characterization of genes affecting adventitious root formation in Populus via activation tagging. Planta 238:271–282

    Article  CAS  PubMed  Google Scholar 

  • Trupiano D, Rocco M, Renzone G, Scaloni A, Montagnoli A, Terzaghi M, Di Iorio A, Chiatante D, Scippa GS (2013b) Poplar woody root proteome during the transition dormancy-active growth. Plant Biosyst 147:1–6

    Article  Google Scholar 

  • Trupiano D, Rocco M, Scaloni A, Renzoni G, Rossi M, Viscosi V, Chiatante D, Scippa GS (2014) Temporal analysis of poplar woody root response to bending stress. Physiol Plant 150:174–193

    Article  CAS  PubMed  Google Scholar 

  • Xie Z, Kasschau KD, Carrington JC (2003) Negative feedback regulation of Dicer-like1(DCL1) in Arabidopsis by microRNA-guided mRNA degradation. Curr Biol 13:784–789

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) Vascular-related NACDOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55:652–664

    Article  CAS  PubMed  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 Genom 10:449

    Article  Google Scholar 

  • Zhang W, Gao S, Zhou X, Xia J, Chellappan P, Zhang X, Jin H (2010) Multiple distinct small RNAs originate from the same microRNA precursors. Genome Biol 11:R81

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhao C, Avci U, Grant EH, Haigler CH, Beers EP (2008) XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J 53:425–436

    Article  CAS  PubMed  Google Scholar 

  • Zhao JP, Jiang XL, Zhang BY, Su XH (2012) Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS ONE 7:e44968

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, Lee C, Ye ZH (2009) Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiol 152:1044–1055

    Article  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 Central  PubMed  Google Scholar 

  • Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168

    Article  CAS  PubMed  Google Scholar 

  • Zhou M, Gu LF, Li PC, Song XW, Wei LY, Chen ZY, Cao XF (2010) Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp. indica). Front Biol 5:67–90

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dipartimento di Bioscienze e Territorio, University of Molise, C.da Fonte Lappone, 86090, Pesche (IS), Italy

    Miriam Rossi, Dalila Trupiano & Gabriella S. Scippa

  2. Dipartimento di Medicina e Scienze della Salute, University of Molise, 86100, Campobasso, Italy

    Manuela Tamburro & Giancarlo Ripabelli

  3. Dipartimento di Biotecnologie e Scienze della Vita, University of Insubria, 21100, Varese, Italy

    Antonio Montagnoli & Donato Chiatante

Authors
  1. Miriam Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dalila Trupiano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manuela Tamburro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Giancarlo Ripabelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Antonio Montagnoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Donato Chiatante
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gabriella S. Scippa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriella S. Scippa.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 322 kb)

Supplementary material 2 (XLS 45 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rossi, M., Trupiano, D., Tamburro, M. et al. MicroRNAs expression patterns in the response of poplar woody root to bending stress. Planta 242, 339–351 (2015). https://doi.org/10.1007/s00425-015-2311-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2311-7

Keywords

Search

Navigation