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Transcriptional repression caused by Dof5.8 is involved in proper vein network formation in Arabidopsis thaliana leaves

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Abstract

Vascular plants have a network of vasculature in their leaves, which supplies water and nutrients and exports photoassimilates to other tissues. The vascular network is patterned during the development of leaf primordia through the induction of provascular differentiation by auxin. Arabidopsis thaliana Dof5.8, encoding a Dof-type transcription factor, is expressed early in provascular cells under the control of the MONOPTEROS transcription factor, also known as auxin response factor 5 (ARF5). Here, we report the effect of overexpressing Dof5.8 in provascular cells on the formation of the vascular network. Overexpression of Dof5.8 inhibited the formation of higher-order veins in cotyledons and leaves, probably through transcriptional repression by Dof5.8. The expression of auxin-associated transcription factor genes, DORNRöSCHEN and SHI-RELATED SEQUENCE 5, was downregulated in the Dof5.8 overexpressors, and overexpression of these genes partially rescued the impaired formation of higher-order veins in Dof5.8-overexpressing lines, suggesting that the overexpression of Dof5.8 modulates the auxin response and leads to impaired vein formation in A. thaliana.

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References

  • Ayre BG, Blair JE, Turgeon R (2003) Functional and phylogenetic analyses of a conserved regulatory program in the phloem of minor veins. Plant Physiol 133:1229–1239

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baylis T, Cierlik I, Sundberg E, Mattsson J (2013) SHORT INTERNODES/STYLISH genes, regulators of auxin biosynthesis, are involved in leaf vein development in Arabidopsis thaliana. New Phytol 197:737–750

    Article  CAS  PubMed  Google Scholar 

  • Chandler JW, Cole M, Flier A, Grewe B, Werr W (2007) The AP2 transcription factors DORNRöSCHEN and DORNRöSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development 134:1653–1662

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Parra MA, Anderberg RJ, Carrington JC (2001) Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of tobacco etch virus. Plant Physiol 127:1667–1675

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ckurshumova W, Scarpella E, Goldstein RS, Berleth T (2011) Double-filter identification of vascular-expressed genes using Arabidopsis plants with vascular hypertrophy and hypotrophy. Plant Sci 181:96–104

    Article  CAS  PubMed  Google Scholar 

  • Cole M, Chandler J, Weijers D, Jacobs B, Comelli P, Werr W (2009) DORNRöSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo. Development 136:1643–1651

    Article  CAS  PubMed  Google Scholar 

  • Donner TJ, Sherr I, Scarpella E (2009) Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves. Development 136:3235–3246

    Article  CAS  PubMed  Google Scholar 

  • Eklund DM, Staldal V, Valsecchi I, Cierlik I, Eriksson C, Hiratsu K, Ohme-Takagi M, Sundstrom JF, Thelander M, Ezcurra I, Sundberg E (2010) The Arabidopsis thaliana STYLISH1 protein acts as a transcriptional activator regulating auxin biosynthesis. Plant Cell 22:349–363

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eklund DM, Cierlik I, Staldal V, Claes AR, Vestman D, Chandler J, Sundberg E (2011) Expression of Arabidopsis SHORT INTERNODES/STYLISH family genes in auxin biosynthesis zones of aerial organs is dependent on a GCC box-like regulatory element. Plant Physiol 157:2069–2080

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fornara F, Panigrahi KC, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86

    Article  CAS  PubMed  Google Scholar 

  • Fridborg I, Kuusk S, Robertson M, Sundberg E (2001) The Arabidopsis protein SHI represses gibberellin responses in Arabidopsis and barley. Plant Physiol 127:937–948

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Furuta KM, Yadav SR, Lehesranta S, Belevich I, Miyashima S, Heo JO, Vatén A, Lindgren O, De Rybel B, Van Isterdael G, Somervuo P, Lichtenberger R, Rocha R, Thitamadee S, Tahtiharju S, Auvinen P, Beeckman T, Jokitalo E, Helariutta Y (2014) Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Science 345:933–937

    Article  CAS  PubMed  Google Scholar 

  • Gabriele S, Rizza A, Martone J, Circelli P, Costantino P, Vittorioso P (2010) The Dof protein DAG1 mediates PIL5 activity on seed germination by negatively regulating GA biosynthetic gene AtGA3ox1. Plant J 61:312–323

    Article  CAS  PubMed  Google Scholar 

  • Gardiner J, Sherr I, Scarpella E (2010) Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves. Int J Dev Biol 54:1389–1396

    Article  CAS  PubMed  Google Scholar 

  • Gualberti G, Papi M, Bellucci L, Ricci I, Bouchez D, Camilleri C, Costantino P, Vittorioso P (2002) Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. Plant Cell 14:1253–1263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo Y, Qin G, Gu H, Qu LJ (2009) Dof5.6/HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in Arabidopsis. Plant Cell 21:3518–3534

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hiratsu K, Ohta M, Matsui K, Ohme-Takagi M (2002) The SUPERMAN protein is an active repressor whose carboxy-terminal repression domain is required for the development of normal flowers. FEBS Lett 514:351–354

    Article  CAS  PubMed  Google Scholar 

  • Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309:293–297

    Article  CAS  PubMed  Google Scholar 

  • Kassel O, Herrlich P (2007) Crosstalk between the glucocorticoid receptor and other transcription factors: molecular aspects. Mol Cell Endocrinol 275:13–29

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Konishi M, Shigyo M, Yoneyama T, Yanagisawa S (2010) Characterization of plant eukaryotic translation initiation factor 6 (eIF6) genes: the essential role in embryogenesis and their differential expression in Arabidopsis and rice. Biochem Biophys Res Commun 397:673–678

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Kim SJ, Abbasi N, Bressan RA, Yun DJ, Yoo SD, Kwon SY, Choi SB (2010) The DOF transcription factor Dof5.1 influences leaf axial patterning by promoting Revoluta transcription in Arabidopsis. Plant J 64:524–535

    Article  CAS  PubMed  Google Scholar 

  • Konishi M, Yanagisawa S (2007) Sequential activation of two Dof transcription factor gene promoters during vascular development in Arabidopsis thaliana. Plant Physiol Biochem 45:623–629

    Article  CAS  PubMed  Google Scholar 

  • Konishi M, Yanagisawa S (2008) Ethylene signaling in Arabidopsis involves feedback regulation via the elaborate control of EBF2 expression by EIN3. Plant J 55:821–831

    Article  CAS  PubMed  Google Scholar 

  • Konishi M, Yanagisawa S (2010) Identification of a nitrate-responsive cis-element in the Arabidopsis NIR1 promoter defines the presence of multiple cis-regulatory elements for nitrogen response. Plant J 63:269–282

    Article  CAS  PubMed  Google Scholar 

  • Konishi M, Donner TJ, Scarpella E, Yanagisawa S (2015) MONOPTEROS directly activates the auxin-inducible promoter of the Dof5.8 transcription factor gene in Arabidopsis thaliana leaf provascular cells. J Exp Bot 66:283–291

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kuusk S, Sohlberg JJ, Magnus Eklund D, Sundberg E (2006) Functionally redundant SHI family genes regulate Arabidopsis gynoecium development in a dose-dependent manner. Plant J 47:99–111

    Article  CAS  PubMed  Google Scholar 

  • Le Hir R, Bellini C (2013) The plant-specific dof transcription factors family: new players involved in vascular system development and functioning in Arabidopsis. Front Plant Sci 4:164

    PubMed Central  PubMed  Google Scholar 

  • Lee JY, Colinas J, Wang JY, Mace D, Ohler U, Benfey PN (2006) Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc Natl Acad Sci USA 103:6055–6060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Luehrsen KR, de Wet JR, Walbot V (1992) Transient expression analysis in plants using firefly luciferase reporter gene. Methods Enzymol 216:397–414

    CAS  PubMed  Google Scholar 

  • Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mena M, Cejudo FJ, Isabel-Lamoneda I, Carbonero P (2002) A role for the DOF transcription factor BPBF in the regulation of gibberellin-responsive genes in barley aleurone. Plant Physiol 130:111–119

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rueda-Romero P, Barrero-Sicilia C, Gómez-Cadenas A, Carbonero P, Onate-Sánchez L (2012) Arabidopsis thaliana DOF6 negatively affects germination in non-after-ripened seeds and interacts with TCP14. J Exp Bot 63:1937–1949

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scarpella E, Francis P, Berleth T (2004) Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131:3445–3455

    Article  CAS  PubMed  Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916

    Article  CAS  PubMed  Google Scholar 

  • Schneidereit A, Imlau A, Sauer N (2008) Conserved cis-regulatory elements for DNA-binding-with-one-finger and homeo-domain-leucine-zipper transcription factors regulate companion cell-specific expression of the Arabidopsis thaliana SUCROSE TRANSPORTER 2 gene. Planta 228:651–662

    Article  CAS  PubMed  Google Scholar 

  • Skirycz A, Reichelt M, Burow M, Birkemeyer C, Rolcik J, Kopka J, Zanor MI, Gershenzon J, Strnad M, Szopa J, Mueller-Roeber B, Witt I (2006) DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J 47:10–24

    Article  CAS  PubMed  Google Scholar 

  • Skirycz A, Jozefczuk S, Stobiecki M, Muth D, Zanor MI, Witt I, Mueller-Roeber B (2007) Transcription factor AtDOF4;2 affects phenylpropanoid metabolism in Arabidopsis thaliana. New Phytol 175:425–438

    Article  CAS  PubMed  Google Scholar 

  • Skirycz A, Radziejwoski A, Busch W, Hannah MA, Czeszejko J, Kwasniewski M, Zanor MI, Lohmann JU, De Veylder L, Witt I, Mueller-Roeber B (2008) The DOF transcription factor OBP1 is involved in cell cycle regulation in Arabidopsis thaliana. Plant J 56:779–792

    Article  CAS  PubMed  Google Scholar 

  • Sohlberg JJ, Myrenas M, Kuusk S, Lagercrantz U, Kowalczyk M, Sandberg G, Sundberg E (2006) STY1 regulates auxin homeostasis and affects apical-basal patterning of the Arabidopsis gynoecium. Plant J 47:112–123

    Article  CAS  PubMed  Google Scholar 

  • Staldal V, Sohlberg JJ, Eklund DM, Ljung K, Sundberg E (2008) Auxin can act independently of CRC, LUG, SEU, SPT and STY1 in style development but not apical-basal patterning of the Arabidopsis gynoecium. New Phytol 180:798–808

    Article  PubMed  Google Scholar 

  • Sugiyama T, Ishida T, Tabei N, Shigyo M, Konishi M, Yoneyama T, Yanagisawa S (2012) Involvement of PpDof1 transcriptional repressor in the nutrient condition-dependent growth control of protonemal filaments in Physcomitrella patens. J Exp Bot 63:3185–3197

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wenzel CL, Schuetz M, Yu Q, Mattsson J (2007) Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49:387–398

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa S (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J 21:281–288

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa S (2002) The Dof family of plant transcription factors. Trends Plant Sci 7:555–560

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa S, Sheen J (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10:75–89

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA 101:7833–7838

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Ye ZH (2012) MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol 53:368–380

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Tom J. Guilfoyle (University of Missouri) for generously providing DR5-GUS seeds. This research was supported in part by the Japan Society for the Promotion of Science (no. 22380043 and 25252014 for S.Y., and no. 25840099 for M.K.).

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  1. Biotechnology Research Center, The University of Tokyo, Yayoi 1-1-1, Bunkyo-Ku, Tokyo, 113-8657, Japan

    Mineko Konishi & Shuichi Yanagisawa

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  1. Mineko Konishi
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  2. Shuichi Yanagisawa
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Correspondence to Shuichi Yanagisawa.

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Konishi, M., Yanagisawa, S. Transcriptional repression caused by Dof5.8 is involved in proper vein network formation in Arabidopsis thaliana leaves. J Plant Res 128, 643–652 (2015). https://doi.org/10.1007/s10265-015-0712-0

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