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Growth increase of Arabidopsis by forced expression of rice 45S rRNA gene

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Forced expression of rice 45S rRNA gene conferred ca. 2-fold increase of above-ground growth in transgenic Arabidopsis . This growth increase was probably brought by cell proliferation, not by cell enlargement.

Abstract

Recent increase in carbon dioxide emissions is causing global climate change. The use of plant biomass as alternative energy source is one way to reduce these emissions. Therefore, reinforcement of plant biomass production is an urgent key issue to overcome both depletion of fossil energies and emission of carbon dioxide. Here, we created transgenic Arabidopsis with a 2-fold increase in above-ground growth by forced expression of the rice 45S rRNA gene using the maize ubiquitin promoter. Although the size of guard cells and ploidy of leaf-cells were similar between transgenic and control plants, numbers of stomata and pavement cells were much increased in the transgenic leaf. This data suggested that cell number, not cell expansion, was responsible for the growth increase, which might be brought by the forced expression of exogenous and full-length 45S rRNA gene. The expression level of rice 45S rRNA transcripts was very low, possibly triggering unknown machinery to enhance cell proliferation. Although microarray analysis showed enhanced expression of ethylene-responsive transcription factors, these factors might respond to ethylene induced by abiotic/biotic stresses or genomic incompatibility, which might be involved in the expression of species-specific internal transcribed spacer (ITS) sequences within rice 45S rRNA transcripts. Further analysis of the mechanism underlying the growth increase will contribute to understanding the regulation of the cell proliferation and the mechanism of hybrid vigor.

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References

  • Appels R, Dvořák J (1982) Relative rates of divergence of spacer and gene sequences within the rDNA region of species in the Triticeae: implications for the maintenance of homogeneity of a repeated gene family. Theor Appl Genet 63:361–365

    Article  CAS  PubMed  Google Scholar 

  • Bourdon V, Harvey A, Lonsdale DM (2001) Introns and their positions affect the translational activity of mRNA in plant cells. EMBO Rep 2:394–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan AC, Hiscock SJ, Abbott RJ (2014) Interspecific crossing and genetic mapping reveal intrinsic genomic incompatibility between two Senecio species that form a hybrid zone on Mount Etna, Sicily. Heredity 113: 195–204

  • Breuer C, Kawamura A, Ichikawa T, Tominaga-Wada R, Wada T, Kondou Y, Muto S, Matsui M, Sugimoto K (2009) The trihelix transcription factor GTL1 regulates ploidy-dependent cell growth in the Arabidopsis trichome. Plant Cell 21:2307–2322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breuer C, Morohashi K, Kawamura A, Takahashi N, Ishida T, Umeda M, Grotewold E, Sugimoto K (2012) Transcriptional repression of the APC/C activator CCS52A1 promotes active termination of cell growth. EMBO J 31:4488–4501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZJ (2010) Molecular mechanism of polyploidy and hybrid vigor. Trends Plant Sci 15:57–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgen Res 5:213–218

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Darwin CR (1876) The effects of cross- and self-fertilization in the vegetable kingdom, John Murry

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788

    Article  CAS  PubMed  Google Scholar 

  • Fujikura U, Horiguchi G, Ponce MR, Micol JL, Tsukaya H (2009) Coordination of cell proliferation and cell expansion mediated by ribosome related processes in the leaves of Arabidopsis thaliana. Plant J 59:499–508

    Article  CAS  PubMed  Google Scholar 

  • Fujimoto R, Taylor JM, Shirasawa S, Peacock WJ, Dennis ES (2012) Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc Natl Acad Sci USA 109:7109–7114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukui K, Ohmido N, Kushu GS (1994) Variability in rDNA loci in the genus Oryza detected through fluorescence in situ hybridization. Theor Appl Genet 87:893–899

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez N, De Bodt S, Sulpice R, Jikumaru Y, Chae E, Dhondt S, Van Daele T, De Milde L, Weigel D, Kamiya Y, Stitt M, Beemster GT, Inzé D (2010) Increased leaf size: different means to an end. Plant Physiol 153:1261–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hershey JWB, Merrick WC (2000) The pathway and mechanism of initiation of protein synthesis. In: Soneberg N et al (eds) Translational control of gene expression. Cold Spring Harbor Press, NY, pp 33–88

    Google Scholar 

  • Herzog H (1982) Relation of source and sink during the grain-filling period in wheat and some aspects of its regulation. Physiol Plant 56:155–160

    Article  CAS  Google Scholar 

  • Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432

    Article  CAS  PubMed  Google Scholar 

  • Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:122–133

    Article  Google Scholar 

  • Horiguchi G, Van Lijsebettens M, Candela H, Micol JL, Tsukaya H (2012) Ribosomes and translation in plant developmental control. Plant Sci 191–192:24–34

    Article  PubMed  Google Scholar 

  • Huang S, Raman AS, Ream JE, Fujiwara H, Cerny RE, Brown SM (1998) Overexpression of 20-oxidase confers a gibberellin-overproduction phenotype in Arabidopsis. Plant Physiol 118:773–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishimaru K, Hirotsu N, Madoka Y, Murakami N, Hara N, Onodera H, Kashiwagi T, Ujiie K, Shimizu B, Onishi A, Miyagawa H, Katoh A (2013) Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat Genet 45:707–711

    Article  CAS  PubMed  Google Scholar 

  • Ito T, Kim GT, Shinozaki K (2000) Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J 22:257–264

    Article  CAS  PubMed  Google Scholar 

  • Jones JW (1926) Hybrid vigor in rice. J Am Soc Agron 18:423–428

    Article  Google Scholar 

  • Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J, Rosenkranz R, Stabler N, Schonfeld B, Kreuzaler, Peterhansel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol 25:593–599

    Article  CAS  PubMed  Google Scholar 

  • Lavania UC, Srivastava S, Lavania S, Basu S, Misra NK, Mukai Y (2012) Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation. Plant J 71:539–549

    Article  CAS  PubMed  Google Scholar 

  • Li J, Yang H, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek B, Murphy AS, Gilroy S, Gaxiola R (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310:121–125

    Article  CAS  PubMed  Google Scholar 

  • Licausi F, Ohme-Takagi M, Parata P (2013) APETALA2/Ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649

    Article  CAS  PubMed  Google Scholar 

  • Lippman ZB, Zamir D (2007) Heterosis: revisiting the magic. Trends Genet 23:60–66

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo O, Piqueras R, Sanches-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424

    Article  CAS  PubMed  Google Scholar 

  • Masuda HP, Cabral LM, De Veylder L, Tanurdzic M, de Almeida Engler J, Geelen D, Inzé D, Martienssen RA, Ferreira PC, Hemerly AS (2008) ABAP1 is a novel plant Armadillo BTB protein involved in DNA replication and transcription. EMBO J 27:2746–2756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer RC, Törjék O, Becher M, Altmann T (2004) Heterosis of biomass production in Arabidopsis. Establishment during early development. Plant Physiol 134:1813–1823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyagawa Y, Tamoi M, Shigeoka S (2001) Overexpression of a cyanobacterial fructose-1,6-sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat Biotechnol 19:965–969

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nelissen H, Rymen B, Jikumaru Y, Demuynck K, Van Lijsebettens M, Kamiya Y, Inzé D, Beemster GT (2012) A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division. Curr Biol 22:1183–1189

    Article  CAS  PubMed  Google Scholar 

  • Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331

    Article  CAS  PubMed  Google Scholar 

  • Niimi H, Watanabe M, Serizawa H, Koba T, Nakamura I, Mii M (2015) Amiprophosmethyl-induced efficient in vitro production of polyploids in raphanobrassica with the aid of aminoethoxyvinylglycine (AVG) in the culture medium. Breed Sci 65:396–402

    Article  PubMed  PubMed Central  Google Scholar 

  • Odum EP (1969) The strategy of ecosystem development. Science 164:262–270

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  CAS  PubMed  Google Scholar 

  • Rahmstorf S, Cazenave A, Church JA, Hansen JE, Keeling RF, Parker DE, Somerville RCJ (2007) Recent Climate Observations Compared to Projections. Science 316:709

    Article  CAS  PubMed  Google Scholar 

  • Rojas CA, Hemerly AS, Ferreira PC (2010) Genetically modified crops for biomass increase. Genes and strategies. GM Crops 1:137–142

    Article  PubMed  Google Scholar 

  • Rosado A, Li R, van de Ven W, Hsu E, Raikhel NV (2012) Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors. Proc Natl Acad Sci USA 109:19537–19544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, Tanaka H, Kitano H, Matsuoka M (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24:105–109

    Article  CAS  PubMed  Google Scholar 

  • Satou M, Enoki H, Oikawa A, Ohta D, Saito K, Hachiya T, Sakakibara H, Kusano M, Fukushima A, Saito K, Kobayashi M, Nagata N, Myouga F, Shinozaki K, Motohashi R (2014) Integrated analysis of transcriptome and metabolome of Arabidopsis albino or pale green mutants with disrupted nuclear-encoded chloroplast proteins. Plant Mol Biol 85:411–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahata Y, Watanabe M, Watanabe Y (2006) Concentration and distribution pattern of glucosinolates in cruciferous vegetables. HortReserach 60:63–66

    CAS  Google Scholar 

  • Takesawa T, Ito M, Kanzaki H, Kameya N, Nakamura I (2002) Over-expression of ζ glutathione S-transferase in transgenic rice enhances germination and growth at low temperature. Mol Breed 9:93–101

    Article  CAS  Google Scholar 

  • Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13:3378–3388

    PubMed  PubMed Central  Google Scholar 

  • Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–383

    Article  CAS  PubMed  Google Scholar 

  • Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106:13875–13879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada T, Maruhashi W, Nakamura T, Niwa M (2001) Possible Involvement of auxin-induced ethylene in an apoptotic cell death during temperature-sensitive lethality expressed by hybrid between Nicotiana glutinosa and N. repanda. Plant Cell Physiol 42:923–930

    Article  CAS  PubMed  Google Scholar 

  • Yoshida A, Sasao M, Yasuno N, Takagi K, Daimon Y, Chen R, Yamazaki R, Tokunaga H, Kitaguchi Y, Sato Y, Nagamura Y, Ushijima T, Kumamaru T, Iida S, Maekawa M, Kyozuka J (2013) TAWAWA1, a regulator of rice inflorescence architecture, functions through the suppression of meristem phase transition. Proc Natl Acad Sci USA 110:767–772

    Article  CAS  PubMed  Google Scholar 

  • Zsogon A, Szakony D, Shi X, Byrne ME (2014) Ribosomal protein RPL27a promotes female gametophyte development in a dose-dependent manner. Plant Physiol 165:1133–1143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Dr. Valentine Otang Ntui for revising this manuscript.

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Correspondence to Ikuo Nakamura.

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Communicated by H. Ebinuma.

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Makabe, S., Motohashi, R. & Nakamura, I. Growth increase of Arabidopsis by forced expression of rice 45S rRNA gene. Plant Cell Rep 36, 243–254 (2017). https://doi.org/10.1007/s00299-016-2075-y

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