Skip to main content
Log in

Overexpression of Arabidopsis miR157b induces bushy architecture and delayed phase transition in Torenia fournieri

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

Abstract

miR156/157 is a small RNA molecule that is highly conserved among various plant species. Overexpression of miR156/157 has been reported to induce bushy architecture and delayed phase transition in several plant species. To investigate the effect of miR157 overexpression in a horticultural plant, and to explore the applicability of miRNA to molecular breeding, we introduced Arabidopsis MIR157b (AtMIR157b) into torenia (Torenia fournieri). The resulting 35S:AtMIR157b plants showed a high degree of branching along with small leaves, which resembled miR156/157-overexpressing plants of other species. We also isolated torenia SBP-box genes with target miR156/157 sequences and confirmed that their expression was selectively downregulated in 35S:AtMIR157b plants. The reduced accumulation of mRNA was probably due to sequence specificity. Moreover, expression of torenia homologs of the SBP-box protein-regulated genes TfLFY and TfMIR172 was also reduced by AtmiR157 overexpression. These findings suggest that the molecular mechanisms of miR156/157 regulation are conserved between Arabidopsis and torenia. The bushy architecture and small leaves of 35S:AtMIR157b torenia plants could be applied in molecular breeding of various horticultural plants as well as for increasing biomass and crop production.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AtMIR157b :

Arabidopsis thaliana MIR157b

miRNA:

microRNA

SBP:

SQUAMOSA-promoter binding protein

SPL:

SQUAMOSA-promoter binding protein-like

UTR:

Untranslated region

References

  • Aida R, Shibata M (1995) Agrobacterium-mediated transformation of torenia (Torenia fournieri). Breed Sci 45:71–74

    Google Scholar 

  • Aida R, Shibata M (2001) Transgenic Torenia fournieri Lind (torenia). In: Bajaj YPS (ed) Biotechnology in agriculture and forestry: transgenic crops III, vol 48. Springer, Berlin, pp 294–305

    Google Scholar 

  • Aida R, Kishimoto S, Tanaka Y, Shibata M (2000) Modification of flower color in torenia (Torenia fournieri Lind.) by genetic transformation. Plant Sci 153:33–42

    Article  CAS  Google Scholar 

  • Breakfield NW, Corcoran DL, Petricka JJ, Shen J, Sae-Seaw J, Rubio-Somoza I, Weigel D, Ohler U, Benfey PN (2012) High-resolution experimental and computational profiling of tissue-specific known and novel miRNAs in Arabidopsis. Genome Res 22:163–176

    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 J, Li WX, Wie D, Peng JR, Ding SW (2004) Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression. Plant Cell 16:1302–1313

    Article  PubMed  CAS  Google Scholar 

  • Chuck G, Bigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549

    Article  PubMed  CAS  Google Scholar 

  • Gion K, Suzuri R, Shikata M, Mitsuda N, Oshima Y, Koyama T, Ohme-Takagi M, Ohtsubo N, Tanaka Y (2011) Morphological changes of Rosa x hybrida by a chimeric repressor of Arabidopsis TCP3. Plant Biotechnol 28:149–152

    Article  CAS  Google Scholar 

  • Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522

    Article  PubMed  CAS  Google Scholar 

  • Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217

    Article  PubMed  CAS  Google Scholar 

  • Katsumoto Y, Fukuchi-Mizutani M, Fukui Y, Brugliera F, Holton TA, Karan M, Nakamura N, Yonekura-Sakakibara K, Togami J, Pigeaire A et al (2007) Engineering of the rose flavonoid biosynthetic pathway successfully generated blue-hued flowers accumulating delphinidin. Plant Cell Physiol 48:1589–1600

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Legrand S, Valot N, Nicole F, Moja S, Baudino S, Jullien F, Magnard JL, Caissard JC, Legendre L (2010) One-step identification of conserved miRNAs, their targets, potential transcription factors and effector genes of complete secondary metabolism pathways after 454 pyrosequencing of calyx cDNAs from the Labiate Salvia sclarea L. Gene 450:55–62

    Article  PubMed  CAS  Google Scholar 

  • Nakatsuka T, Mishiba K, Kubota A, Abe Y, Yamamura S, Nakamura N, Takana Y, Nishihara M (2010) Genetic engineering of novel flower colour by suppression of anthocyanin modification genes in gentian. J Plant Physiol 167:231–237

    Article  PubMed  CAS  Google Scholar 

  • Nakatsuka T, Saito M, Yamada E, Nishihara M (2011) Production of picotee-type flowers in Japanese gentian by CRES-T. Plant Biotechnol 28:173–180

    Article  CAS  Google Scholar 

  • Narumi T, Aida R, Niki T, Nishijima T, Mitsuda N, Hiratsu K, Ohme-Takagi M, Ohtsubo N (2008) Chimeric AGAMOUS repressor induces serrated petal phenotype in Torenia fournieri similar to that induced by cytokinin application. Plant Biotechnol 25:45–53

    Article  CAS  Google Scholar 

  • Narumi T, Aida R, Koyama T, Yamaguchi H, Sasaki K, Shikata M, Nakayama M, Ohme-Takagi M, Ohtsubo N (2011) Arabidopsis chimeric TCP3 repressor produces novel floral traits in Torenia fournieri and Chrysanthemum morifolium. Plant Biotechnol 28:131–140

    Article  CAS  Google Scholar 

  • Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–361

    Article  PubMed  CAS  Google Scholar 

  • Ono E, Fukuchi-Mizutani M, Nakamura N, Fukui Y, Yonekura-Sakakibara K, Yamaguchi M, Nakayama T, Tanaka T, Kusumi T, Tanaka Y (2006) Yellow flowers generated by expression of the aurone biosynthetic pathway. Proc Natl Acad Sci USA 103:11075–11080

    Article  PubMed  CAS  Google Scholar 

  • Riese M, Höhmann S, Saedler H, Münster T, Huijser P (2007) Comparative analysis of the SBP-box gene families in P. patens and seed plants. Gene 401:28–37

    Article  PubMed  CAS  Google Scholar 

  • Röbbelen G (1957) Über heterophyllie bei Arabidopsis thaliana (L.) Heynh. B er Dtsch Bot Ges 70:39–44

    Google Scholar 

  • Sage-Ono K, Ozeki Y, Hiyama S, Higuchi Y, Kamada H, Mitsuda N, Ohme-Takagi M, Ono M (2011) Induction of double flowers in Pharbitis nil using a class-C MADS-box transcription factor with chimeric repressor. Plant Biotechnol 28:153–165

    Article  CAS  Google Scholar 

  • Salinas M, Xing S, Höhmann S, Berndtgen R, Huijser P (2011) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors. Planta. doi:10.1007/s00425-011-1565-y

    PubMed  Google Scholar 

  • Sasaki K, Yamaguchi H, Narumi T, Shikata M, Oshima Y, Nakata M, Mitsuda N, Ohme-Takagi M, Ohtsubo N (2011) Utilization of a floral organ-expressing AP1 promoter for generation of new floral traits in Torenia fournieri Lind. Plant Biotechnol 28:181–188

    Article  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 

  • Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195

    Article  PubMed  CAS  Google Scholar 

  • Shikata M, Koyama T, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in reproductive phase. Plant Cell Physiol 50:2133–2145

    Article  PubMed  CAS  Google Scholar 

  • Shikata M, Narumi T, Yamaguchi H, Sasaki K, Aida R, Oshima Y, Takiguchi Y, Ohme-Takagi M, Mitsuda N, Ohtsubo N (2011) Efficient production of novel floral traits in torenia by collective transformation with chimeric repressors of Arabidopsis transcription factors. Plant Biotechnol 28:189–199

    Article  CAS  Google Scholar 

  • Tanaka Y, Yamamura T, Oshima Y, Mitsuda N, Koyama T, Ohme-Takagi M, Terakawa T (2011) Creating ruffled flower petals in Cyclamen persicum by expression of the chimeric cyclamen TCP repressor. Plant Biotechnol 28:141–147

    Article  Google Scholar 

  • Tsukaya H (2002) The leaf index was calculated by dividing the lamina length by the lamina width. Plant Cell Physiol 43:372–378

    Article  PubMed  CAS  Google Scholar 

  • Unte US, Sorensen AM, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P (2003) SPL8, an SBP-Box gene that affects pollen sac development in Arabidopsis. Plant Cell 15:1009–1019

    Article  PubMed  CAS  Google Scholar 

  • Usami T, Horiguchi G, Yano S, Tsukaya H (2009) The more and smaller cells mutant of Arabidopsis thaliana identify novel roles for squamosa promoter binding protein-like genes in the control of heteroblasty. Development 136:955–964

    Article  PubMed  CAS  Google Scholar 

  • Vazquez F, Gasciolli V, Crete P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14:346–351

    PubMed  CAS  Google Scholar 

  • Willmann MR, Poethig RS (2007) Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol 10:503–511

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    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 

  • Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293

    Article  PubMed  CAS  Google Scholar 

  • Xing S, Salinas M, Höhmanm S, Berndtgen R, Huijser P (2010) miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22:3935–3950

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Zou Z, Zhang J, Zhang Y, Qinqin Han, Tixu Hu, Xu X, Liu H, Li H, Ye Z (2011) Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive traits alterations and partial phenocopy of the sft mutant. FEBS Lett 585:435–439

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Masaru Ohme-Takagi (National Institute of Advanced Industrial Science and Technology) for his support and helpful comments. We also thank Ms. Satoko Ohtawa, Ms. Yoshiko Kashiwagi, and Ms. Yasuko Taniji for their skilled technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Norihiro Ohtsubo.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shikata, M., Yamaguchi, H., Sasaki, K. et al. Overexpression of Arabidopsis miR157b induces bushy architecture and delayed phase transition in Torenia fournieri . Planta 236, 1027–1035 (2012). https://doi.org/10.1007/s00425-012-1649-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1649-3

Keywords

Navigation