Skip to main content

Advertisement

Log in

Alteration of osa-miR156e expression affects rice plant architecture and strigolactones (SLs) pathway

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Overexpressing osa - miR156e in rice produced a bushy mutant and osa - miR156e regulation of tillering may do this through the strigolactones (SLs) pathway. Appropriate downregulation of osa - miR156 expression contributed to the improvement of plant architecture.

Abstract

Tillering is one of the main determinants for rice architecture and yield. In this study, a bushy mutant of rice was identified with increased tiller number, reduced plant height, prolonged heading date, low seed setting, and small panicle size due to a T-DNA insertion which essentially elevated the expression of osa-miR156e. Transgenic plants with constitutive expression of osa-miR156e also had the bushy phenotype, which showed osa-miR156 may control apical dominance and tiller outgrowth via regulating the strigolactones signaling pathway. Furthermore, the extent of impaired morphology was correlated with the expression level of osa-miR156e. In an attempt to genetically improve rice architecture, ectopic expression of osa-miR156e under the GAL4-UAS system or OsTB1 promoter was conducted. According to agronomic trait analysis, pTB1:osa-miR156e transgenic plants significantly improved the grain yield per plant compared to plants overexpressing osa-miR156e, even though the yield was still inferior to the wild type, making it a very interesting albeit negative result. Our results suggested that osa-miR156 could serve as a potential tool for modifying rice plant architecture through genetic manipulation of the osa-miR156 expression level.

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
Fig. 6

Similar content being viewed by others

References

  • Aguilar-Martinez JA, Poza-Carrion C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19(2):458–472

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301(5633):653–657

    Article  PubMed  Google Scholar 

  • Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51(6):1019–1029

    Article  CAS  PubMed  Google Scholar 

  • Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50(8):1416–1424

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beveridge CA (2006) Axillary bud outgrowth: sending a message. Curr Opin Plant Biol 9(1):35–40

    Article  CAS  PubMed  Google Scholar 

  • Bhogale S, Mahajan AS, Natarajan B, Rajabhoj M, Thulasiram HV, Banerjee AK (2014) MicroRNA156: a potential graft-transmissible microRNA that modulates plant architecture and tuberization in Solanum tuberosum ssp. andigena. Plant Physiol 164(2):1011–1027

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen S, Jin W, Wang M, Zhang F, Zhou J, Jia Q, Wu Y, Liu F, Wu P (2003) Distribution and characterization of over 1000 T-DNA tags in rice genome. Plant J 36(1):105–113

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33(20):e179

    Article  PubMed Central  PubMed  Google Scholar 

  • Cho SH, Coruh C, Axtell MJ (2012) miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell 24(12):4837–4849

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Choi MS, Woo MO, Koh EB, Lee J, Ham TH, Seo HS, Koh HJ (2012) Teosinte Branched 1 modulates tillering in rice plants. Plant Cell Rep 31(1):57–65

    Article  CAS  PubMed  Google Scholar 

  • Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL, Zhang Q, Wang S (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20(10):1250–1255

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39(4):544–549

    Article  CAS  PubMed  Google Scholar 

  • Chuck G, Whipple C, Jackson D, Hake S (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137(8):1243–1250

    Article  CAS  PubMed  Google Scholar 

  • Ferreira e Silva GF, Silva EM, Azevedo Mda S, Guivin MA, Ramiro DA, Figueiredo CR, Carrer H, Peres LE, Nogueira FT (2014) microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development. Plant J 78(4):604–618

    Article  CAS  PubMed  Google Scholar 

  • Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49(4):683–693

    Article  CAS  PubMed  Google Scholar 

  • Gao Z, Qian Q, Liu X, Yan M, Feng Q, Dong G, Liu J, Han B (2009) Dwarf 88, a novel putative esterase gene affecting architecture of rice plant. Plant Mol Biol 71(3):265–276

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455(7210):189–194

    Article  CAS  PubMed  Google Scholar 

  • Guo S, Xu Y, Liu H, Mao Z, Zhang C, Ma Y, Zhang Q, Meng Z, Chong K (2013) The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat Commun 4:1566

    Article  PubMed Central  PubMed  Google Scholar 

  • Hsing YI, Chern CG, Fan MJ, Lu PC, Chen KT, Lo SF, Sun PK, Ho SL, Lee KW, Wang YC, Huang WL, Ko SS, Chen S, Chen JL, Chung CI, Lin YC, Hour AL, Wang YW, Chang YC, Tsai MW, Lin YS, Chen YC, Yen HM, Li CP, Wey CK, Tseng CS, Lai MH, Huang SC, Chen LJ, Yu SM (2007) A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant Mol Biol 63(3):351–364

    Article  CAS  PubMed  Google Scholar 

  • Hultquist JF, Dorweiler JE (2008) Feminized tassels of maize mop1 and ts1 mutants exhibit altered levels of miR156 and specific SBP-box genes. Planta 229(1):99–113

    Article  CAS  PubMed  Google Scholar 

  • Hwan Lee J, Joon Kim J, Ahn JH (2012) Role of SEPALLATA3 (SEP3) as a downstream gene of miR156-SPL3-FT circuitry in ambient temperature-responsive flowering. Plant Signal Behav 7(9):1151–1154

    Article  PubMed Central  PubMed  Google Scholar 

  • Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46(1):79–86

    Article  CAS  PubMed  Google Scholar 

  • Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Choi JH, Cho SY, Cha SS, Kim SI, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22(6):561–570

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42(6):541–544

    Article  CAS  PubMed  Google Scholar 

  • Jung JH, Ju Y, Seo PJ, Lee JH, Park CM (2012) The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. Plant J 69(4):577–588

    Article  CAS  PubMed  Google Scholar 

  • Khush GS (1995) Breaking the Yield Frontier of Rice. GeoJournal 35(3):329–332

    Article  Google Scholar 

  • Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH (2012) The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol 159(1):461–478

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lal S, Pacis LB, Smith HM (2011) Regulation of the SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE genes/microRNA156 module by the homeodomain proteins PENNYWISE and POUND-FOOLISH in Arabidopsis. Mol Plant 4(6):1123–1132

    Article  CAS  PubMed  Google Scholar 

  • Leyser O (2003) Regulation of shoot branching by auxin. Trends Plant Sci 8(11):541–545

    Article  CAS  PubMed  Google Scholar 

  • Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422(6932):618–621

    Article  CAS  PubMed  Google Scholar 

  • Li S, Yang X, Wu F, He Y (2012) HYL1 controls the miR156-mediated juvenile phase of vegetative growth. J Exp Bot 63(7):2787–2798

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liang D, Wu C, Li C, Xu C, Zhang J, Kilian A, Li X, Zhang Q, Xiong L (2006) Establishment of a patterned GAL4-VP16 transactivation system for discovering gene function in rice. Plant J 46(6):1059–1072

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21(5):1512–1525

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lin Q, Wang D, Dong H, Gu S, Cheng Z, Gong J, Qin R, Jiang L, Li G, Wang JL, Wu F, Guo X, Zhang X, Lei C, Wang H, Wan J (2012) Rice APC/C(TE) controls tillering by mediating the degradation of MONOCULM 1. Nat Commun 3:752

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu W, Wu C, Fu Y, Hu G, Si H, Zhu L, Luan W, He Z, Sun Z (2009) Identification and characterization of HTD2: a novel gene negatively regulating tiller bud outgrowth in rice. Planta 230(4):649–658

    Article  CAS  PubMed  Google Scholar 

  • Luo L, Li W, Miura K, Ashikari M, Kyozuka J (2012) Control of tiller growth of rice by OsSPL14 and Strigolactones, which work in two independent pathways. Plant Cell Physiol 53(10):1793–1801

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42(6):545–549

    Article  CAS  PubMed  Google Scholar 

  • Peng S, Laza RC, Visperas RM, Sanico AL, Cassman KL, Khush GS (2000) Grain yield of rice cultivars and lines developed in Philippines since 1996. Crop Sci 40:307–314

    Article  Google Scholar 

  • Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genet Dev 19(4):374–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sallaud C, Meynard D, van Boxtel J, Gay C, Bes M, Brizard JP, Larmande P, Ortega D, Raynal M, Portefaix M, Ouwerkerk PB, Rueb S, Delseny M, Guiderdoni E (2003) Highly efficient production and characterization of T-DNA plants for rice (Oryza sativa L.) functional genomics. Theor Appl Genet 106(8):1396–1408

    CAS  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(4):517–527

    Article  CAS  PubMed  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(1–2):183–195

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Baurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26(4):1792–1807

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tabuchi H, Zhang Y, Hattori S, Omae M, Shimizu-Sato S, Oikawa T, Qian Q, Nishimura M, Kitano H, Xie H, Fang X, Yoshida H, Kyozuka J, Chen F, Sato Y (2011) LAX PANICLE2 of rice encodes a novel nuclear protein and regulates the formation of axillary meristems. Plant Cell 23(9):3276–3287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33(3):513–520

    Article  CAS  PubMed  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455(7210):195–200

    Article  CAS  PubMed  Google Scholar 

  • Usami T, Horiguchi G, Yano S, Tsukaya H (2009) The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty. Development 136(6):955–964

    Article  CAS  PubMed  Google Scholar 

  • Wang JW (2014) Regulation of flowering time by the miR156-mediated age pathway. J Exp Bot 65:4731–4745

    Article  Google Scholar 

  • Wang Y, Li J (2011) Branching in rice. Curr Opin Plant Biol 14(1):94–99

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Schwab R, Czech B, Mica E, Weigel D (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20(5):1231–1243

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749

    Article  CAS  PubMed  Google Scholar 

  • Weigel D, Ahn JH, Blazquez MA, Borevitz JO, Christensen SK, Fankhauser C, Ferrandiz C, Kardailsky I, Malancharuvil EJ, Neff MM, Nguyen JT, Sato S, Wang ZY, Xia Y, Dixon RA, Harrison MJ, Lamb CJ, Yanofsky MF, Chory J (2000) Activation tagging in Arabidopsis. Plant Physiol 122(4):1003–1013

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539–3547

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu C, Li X, Yuan W, Chen G, Kilian A, Li J, Xu C, Zhou DX, Wang S, Zhang Q (2003) Development of enhancer trap lines for functional analysis of the rice genome. Plant J 35(3):418–427

    Article  CAS  PubMed  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(4):750–759

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J, Wang Y, Zhang M (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS ONE 7(1):e30039

    Article  PubMed Central  CAS  PubMed  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(1):280–293

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xie K, Shen J, Hou X, Yao J, Li X, Xiao J, Xiong L (2012) Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiol 158(3):1382–1394

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xing S, Salinas M, Garcia-Molina A, Hohmann S, Berndtgen R, Huijser P (2013) SPL8 and miR156-targeted SPL genes redundantly regulate Arabidopsis gynoecium differential patterning. Plant J 75(4):566–577

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Wang Y, Yu Y, Duan J, Liao Z, Xiong G, Meng X, Liu G, Qian Q, Li J (2012) Degradation of MONOCULM 1 by APC/C(TAD1) regulates rice tillering. Nat Commun 3:750

    Article  PubMed Central  PubMed  Google Scholar 

  • Yang L, Xu M, Koo Y, He J, Poethig RS (2013) Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. eLife 2:e00260

    PubMed Central  PubMed  Google Scholar 

  • Yu S, Galvao VC, Zhang YC, Horrer D, Zhang TQ, Hao YH, Feng YQ, Wang S, Schmid M, Wang JW (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 24(8):3320–3332

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yuan W, Li X, Chang Y, Wen R, Chen G, Zhang Q, Wu C (2009) Mutation of the rice gene PAIR3 results in lack of bivalent formation in meiosis. Plant J 59(2):303–315

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Li C, Wu C, Xiong L, Chen G, Zhang Q, Wang S (2006) RMD: a rice mutant database for functional analysis of the rice genome. Nucleic Acids Res 34(Database issue):D745–D748

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang J, Guo D, Chang Y, You C, Li X, Dai X, Weng Q, Chen G, Liu H, Han B, Zhang Q, Wu C (2007) Non-random distribution of T-DNA insertions at various levels of the genome hierarchy as revealed by analyzing 13 804 T-DNA flanking sequences from an enhancer-trap mutant library. Plant J 49(5):947–959

    Article  CAS  PubMed  Google Scholar 

  • Zheng X, Deng W, Luo K, Duan H, Chen Y, McAvoy R, Song S, Pei Y, Li Y (2007) The cauliflower mosaic virus (CaMV) 35S promoter sequence alters the level and patterns of activity of adjacent tissue- and organ-specific gene promoters. Plant Cell Rep 26:1195–1203

    Article  CAS  PubMed  Google Scholar 

  • Zou J, Zhang S, Zhang W, Li G, Chen Z, Zhai W, Zhao X, Pan X, Xie Q, Zhu L (2006) The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J 48(5):687–698

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by 863 Project Grant 2012AA10A303, National Natural Science Foundation of China Grant 30970172, and the Program for New Century Excellent Talents in University.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhihui Chen.

Additional information

Communicated by E. Guiderdoni.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 403 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, Z., Gao, X. & Zhang, J. Alteration of osa-miR156e expression affects rice plant architecture and strigolactones (SLs) pathway. Plant Cell Rep 34, 767–781 (2015). https://doi.org/10.1007/s00299-015-1740-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1740-x

Keywords

Navigation