Advertisement

Journal of Plant Research

, Volume 128, Issue 4, pp 643–652 | Cite as

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

  • Mineko Konishi
  • Shuichi YanagisawaEmail author
Regular Paper

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.

Keywords

Arabidopsis thaliana Auxin Dof transcription factor Dof5.8 MONOPTEROS Vascular patterning 

Notes

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.).

Supplementary material

10265_2015_712_MOESM1_ESM.pdf (244 kb)
Supplementary material 1 (PDF 244 kb)
10265_2015_712_MOESM2_ESM.xlsx (296 kb)
Supplementary material 2 (XLSX 295 kb)

References

  1. Ayre BG, Blair JE, Turgeon R (2003) Functional and phylogenetic analyses of a conserved regulatory program in the phloem of minor veins. Plant Physiol 133:1229–1239PubMedCentralPubMedCrossRefGoogle Scholar
  2. 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 197:737–750PubMedCrossRefGoogle Scholar
  3. 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 134:1653–1662PubMedCrossRefGoogle Scholar
  4. 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 127:1667–1675PubMedCentralPubMedCrossRefGoogle Scholar
  5. 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 181:96–104PubMedCrossRefGoogle Scholar
  6. 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 136:1643–1651PubMedCrossRefGoogle Scholar
  7. Donner TJ, Sherr I, Scarpella E (2009) Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves. Development 136:3235–3246PubMedCrossRefGoogle Scholar
  8. 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 22:349–363PubMedCentralPubMedCrossRefGoogle Scholar
  9. 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 157:2069–2080PubMedCentralPubMedCrossRefGoogle Scholar
  10. 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 17:75–86PubMedCrossRefGoogle Scholar
  11. Fridborg I, Kuusk S, Robertson M, Sundberg E (2001) The Arabidopsis protein SHI represses gibberellin responses in Arabidopsis and barley. Plant Physiol 127:937–948PubMedCentralPubMedCrossRefGoogle Scholar
  12. 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 345:933–937PubMedCrossRefGoogle Scholar
  13. 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 61:312–323PubMedCrossRefGoogle Scholar
  14. Gardiner J, Sherr I, Scarpella E (2010) Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves. Int J Dev Biol 54:1389–1396PubMedCrossRefGoogle Scholar
  15. 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 14:1253–1263PubMedCentralPubMedCrossRefGoogle Scholar
  16. 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 21:3518–3534PubMedCentralPubMedCrossRefGoogle Scholar
  17. 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 514:351–354PubMedCrossRefGoogle Scholar
  18. 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 309:293–297PubMedCrossRefGoogle Scholar
  19. Kassel O, Herrlich P (2007) Crosstalk between the glucocorticoid receptor and other transcription factors: molecular aspects. Mol Cell Endocrinol 275:13–29PubMedCrossRefGoogle Scholar
  20. 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 397:673–678PubMedCrossRefGoogle Scholar
  21. 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 64:524–535PubMedCrossRefGoogle Scholar
  22. Konishi M, Yanagisawa S (2007) Sequential activation of two Dof transcription factor gene promoters during vascular development in Arabidopsis thaliana. Plant Physiol Biochem 45:623–629PubMedCrossRefGoogle Scholar
  23. Konishi M, Yanagisawa S (2008) Ethylene signaling in Arabidopsis involves feedback regulation via the elaborate control of EBF2 expression by EIN3. Plant J 55:821–831PubMedCrossRefGoogle Scholar
  24. 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 63:269–282PubMedCrossRefGoogle Scholar
  25. 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 66:283–291PubMedCentralPubMedCrossRefGoogle Scholar
  26. 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 47:99–111PubMedCrossRefGoogle Scholar
  27. 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 4:164PubMedCentralPubMedGoogle Scholar
  28. 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 103:6055–6060PubMedCentralPubMedCrossRefGoogle Scholar
  29. Luehrsen KR, de Wet JR, Walbot V (1992) Transient expression analysis in plants using firefly luciferase reporter gene. Methods Enzymol 216:397–414PubMedGoogle Scholar
  30. Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339PubMedCentralPubMedCrossRefGoogle Scholar
  31. 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 130:111–119PubMedCentralPubMedCrossRefGoogle Scholar
  32. 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 63:1937–1949PubMedCentralPubMedCrossRefGoogle Scholar
  33. 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 131:3445–3455PubMedCrossRefGoogle Scholar
  34. Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027PubMedCentralPubMedCrossRefGoogle Scholar
  35. 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 464:913–916PubMedCrossRefGoogle Scholar
  36. 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 228:651–662PubMedCrossRefGoogle Scholar
  37. 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 47:10–24PubMedCrossRefGoogle Scholar
  38. 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 175:425–438PubMedCrossRefGoogle Scholar
  39. 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 56:779–792PubMedCrossRefGoogle Scholar
  40. 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 47:112–123PubMedCrossRefGoogle Scholar
  41. 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 180:798–808PubMedCrossRefGoogle Scholar
  42. 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 63:3185–3197PubMedCentralPubMedCrossRefGoogle Scholar
  43. 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 9:1963–1971PubMedCentralPubMedCrossRefGoogle Scholar
  44. 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 49:387–398PubMedCrossRefGoogle Scholar
  45. Yanagisawa S (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J 21:281–288PubMedCrossRefGoogle Scholar
  46. Yanagisawa S (2002) The Dof family of plant transcription factors. Trends Plant Sci 7:555–560PubMedCrossRefGoogle Scholar
  47. Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391PubMedCrossRefGoogle Scholar
  48. Yanagisawa S, Sheen J (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10:75–89PubMedCentralPubMedCrossRefGoogle Scholar
  49. Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525PubMedCrossRefGoogle Scholar
  50. 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 101:7833–7838PubMedCentralPubMedCrossRefGoogle Scholar
  51. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572PubMedCrossRefGoogle Scholar
  52. 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 53:368–380PubMedCrossRefGoogle Scholar
  53. 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 20:2763–2782PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  1. 1.Biotechnology Research CenterThe University of TokyoBunkyo-KuJapan

Personalised recommendations