Abstract
As in the cases of the embryo and many lateral organs, lateral root (LR) development is triggered by the phytohormone auxin. LR development is also known to be inhibited by abscisic acid (ABA). Here we show that an auxin response factor ARF3, which participates in pattern formation of aerial lateral organs, such as leaf or flower, is up-regulated by auxin during LR development in Arabidopsis. This study demonstrates that ARF3 expression is regulated at the transcriptional level and by posttranscriptional gene silencing (PTGS), which is mediated by a group of transacting small-interfering RNA (tasiRNA-ARF). The tasiRNA-ARF pathway and ARF3 expression are sensitive to auxin and ABA treatment, suggesting that tasiRNA-ARF-dependent PTGS of ARF3 is linked to auxin promotion of LR development and to ABA inhibition.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen E, Xie Z, Gustafson A, Carrington J (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221
Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658–1673
Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44
Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171
Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554
De Smet I, Tetsumura T, De Rybel B, Frey NF, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inzé D, Bennett MJ, Beeckman T (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690
Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153
Garcia D, Collier SA, Byrne ME, Martienssen RA (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16:933–938
Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386
Himanen K, Boucheron E, Vanneste S, de Almeida, Engler J, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351
Hunter C, Willmann MR, Wu G, Yoshikawa M, de la Luz Gutiérrez-Nava M, Poethig SR (2006) Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133:2973–2981
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root meristems is a two-stage process. Development 121:3303–3310
Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141
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
Nemhauser JL, Feldman LJ, Zambryski PC (2000) Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127:3877–3888
Nogueira FT, Madi S, Chitwood DH, Juarez MT, Timmermans MC (2007) Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 21:750–755
Patrick A, Alan H, David CB, Nicholas PH (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365
Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910
Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260
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
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Yang JH, Han SJ, Yoon EK, Lee WS (2006) Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 34:1892–1899
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572
Yoon EK, Yang JH, Lim J, Kim SH, Kim SK, Lee WS (2009) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res. doi:10.1093/nar/gkp1123
Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175
Acknowledgments
We thank Dr. James Carrington and the Arabidopsis Stock Center for providing the Arabidopsis seeds. We thank Dr. Choong-Ill Cheon for assistance with the transient gene expression experiments. This study was supported by Faculty Research Fund, Sungkyunkwan University, 2006.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yoon, E.K., Yang, J.H. & Lee, W.S. Auxin and Abscisic Acid Responses of Auxin Response Factor 3 in Arabidopsis Lateral Root Development. J. Plant Biol. 53, 150–154 (2010). https://doi.org/10.1007/s12374-010-9100-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-010-9100-4