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Plant Molecular Biology

, Volume 56, Issue 2, pp 255–270 | Cite as

MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen

  • Barbara Karpinska
  • Marlene Karlsson
  • Manoj Srivastava
  • Anneli Stenberg
  • Jarmo Schrader
  • Fredrik Sterky
  • Rishikesh Bhalerao
  • Gunnar Wingsle
Article

Abstract

More than 120,000 poplar ESTs have been sequenced from 20 different cDNA libraries by the Swedish Centre for Tree Functional Genomics. We screened this EST collection for MYB transcription factors involved in secondary vascular tissue formation, and genes assigned as PttMYB3Ra, PttMYB4a and PttMYB21a were selected for further characterisation. Three MYB genes showed different expression patterns in various organs, tissues and stem sub-sections representing different developmental stages of vascular tissue formation. Furthermore, the analysis showed that PttMYB21a expression was much higher in secondary cell wall formation zone of xylem and phloem fibers than in other developmental zones. Transgenic hybrid aspen plants, expressing the 3′-part of the PttMYB21a gene in antisense orientation were generated to assess the function of PttMYB21a gene in vascular tissue formation and lignification. All transgenic lines showed reduced growth and had fewer internodes compared to the wild-type. The analysis of selected lines showed that acid soluble lignin present in the bark was higher in transgenic lines as compared to wild-type plants. Moreover a higher transcript level of caffeoyl-CoA 3-O-methyltransferase [CCoAOMT]; EC 2.1.1.104) was found in the phloem of the transgenic plants, suggesting that PttMYB21a might function as a transcriptional repressor.

gene regulation gravity hormones hybrid aspen MYB transcription factors sucrose wood 

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References

  1. Aloni, R.1980.Role of auxin and sucrose in the differentiation of sieve and tracheary elements in plant tissue cultures. Planta 150:255–263.Google Scholar
  2. Aloni, R.1995.The induction of vascular tissues by auxin and cytokinin.In:P.J. Davies (Ed.),Plant Hormones Physiology, Biochemistry and Molecular Biology.Kluwer Academic Publishers, Dordrecht,The Netherlands,pp.531–546.Google Scholar
  3. Aloni, R.2000.Foliar and axial aspects of vascular differentiation:hypothesis and evidence.J.Plant Growth Regul.20:22–34.Google Scholar
  4. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W.and Lipman, D.J.1997.Gapped BLAST and PSI-BLAST:a new generation of protein database search programs.Nucl.Acids Res.25:3389–3402.PubMedGoogle Scholar
  5. Araki, N., Fujita, M., Saiki, H.and Harada, H.1982. Transition of the fibre wall structure from normal wood to tension wood in Robinia pseudoacacia L.and Populus euramericana Guinier.Mokuzai Gakkaishi.28:267–273.Google Scholar
  6. Awano, T., Takabe, K.and Fujita, M.2002.Xylan deposition on secondary wall of Fagus crenata bers.Protoplasma 219:106–115.PubMedGoogle Scholar
  7. Bevan, M.W.1984.Binary Agrobacterium vectors for plant transformation.Nucl.Acids Res.12:8711–8721.Google Scholar
  8. Chang, S., Puryear, J.and Cairney, J.1993.A simple and effcient method for isolating RNA from pine trees.Plant Mol.Biol.Rep.11:113–116.Google Scholar
  9. Chen, C., Meyermans, H., Burggraeve, B., De Rycke, R.M., Inoue, K., DeVleesschauwer, V., Steenackers, M.,Van Montagu, M.C., Emgler, G.J.and Boerjan, W.A.2000. Cell-specific and conditional expression of caffeoyl-coen-zyme A-3-O-methyltransferase in poplar.Plant Physiol.123:853–867.PubMedGoogle Scholar
  10. Church, G.M.and Gilbert, W.1984.Genomic sequencing.Proc.Natl.Acad.Sci.USA 81:1991–1995.PubMedGoogle Scholar
  11. Coenen, C.and Lomax, T.L.1997.Auxin-cytokinin interactions in higher plants:old problems and new tools.Trends Plant Sci.2:321–356.Google Scholar
  12. Demura, T.and Fukuda, H.1993.Molecular cloning and characterization of cDNAs associated with tracheary element differentiation in cultured zinnia cells.Plant Physiol.103:815–821.PubMedGoogle Scholar
  13. Denekamp, M.and Smeekens, S.C.2003.Integration of wounding and osmotic stress signals determines the expression of the AtMYB102 transcription factor gene.Plant Physiol.132:1415–1423.PubMedGoogle Scholar
  14. Dubois, M., Giles, K.A., Hamilton, J.K., Rebers, P.A.and Smith, F.1956.Colorimetric method for the determination of sugars and related substances.Anal.Chem.28:350–356.Google Scholar
  15. Gocal, G.F.W., Sheldon, C.C., Gubler F., Moritz, T., Bagnall, D.J., MacMillan, C.P., Song, F.L., Parish, R.W., Dennis, E.S., Weigel, D.and King, R.W.2001.GAMYB-like genes, flowering,and gibberellin signaling in Arabidopsis.Plant Physiol.127:1682–1693.PubMedGoogle Scholar
  16. Gubler, F., Kalla, R.,Roberts, J.K.and Jacobsen, J.V.1995.Gibberellin-regulated expression of a myb gene in barleyaleurone cells:evidence for Myb transactivation of a high-pI α-amylase gene promoter.Plant Cell 7:1879–1891.PubMedGoogle Scholar
  17. Gubler, F., Raventos, D., Keys, M., Watts, R., Mundy, J.and Jacobsen J.V.1999.Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone.Plant J.17:1–9.PubMedGoogle Scholar
  18. Guerineau, F.and Mullineaux, P.1993.Plant transformation and expression vectors.In:R.R.D. Croy (Ed.),Plant Molecular Biology Labfax,BIOS Scientific Publishers, Oxford,UK,pp.121–147.Google Scholar
  19. Hertzberg, M.and Olsson, O.1998.Molecular characterization of a novel plant homeobox gene expressed in the maturing xylem zone of Populus tremula x tremuloides. Plant J.16:285–295.PubMedGoogle Scholar
  20. Hertzberg, M., Sievertzon, M., Aspeborg, H., Nilsson, P., Sandberg, G.and Lundeberg, J.2001.cDNA microarray analysis of small plant tissue samples using a cDNA tag target ampli cation protocol.Plant J.25:585–591.PubMedGoogle Scholar
  21. Hertzberg, M., Aspeborg, H., Schrader, J., Andersson, A., Erlandsson, R., Blomqvist, K., Bhalerao, R., Uhlen, M., Teeri, T.T., Lundeberg, J., Sundberg, B., Nilsson, P.and Sandberg, G.2001a.A transcriptional roadmap to wood formation.Proc.Natl.Acad.Sci.USA 98:14732–14737.PubMedGoogle Scholar
  22. Hoeren, F.U., Dolferus, R., Wu, Y.R., Peacock, W.J.and Dennis, E.S.1998.Evidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase gene(ADH1)by low oxygen.Genetics 149:479–490.Google Scholar
  23. Israelsson, M., Eriksson, M.E., Hertzberg, M., Aspeborg, H., Nilsson, P.and Moritz, T.2003. Changes in gene expression in the wood-forming tissue of transgenic hybrid aspen with increased secondary growth. Plant Mol.Biol.52:893–903.PubMedGoogle Scholar
  24. Ito, M., Araki, S., Matsunaga, S., Itoh, T., Nishihama, R., Machida, Y., Doonan, J.H.and Watanabe, A.2001.G2 /M-phase-speci c transcription during the plant cell cycle is mediated by c-Myb-like transcription factors.Plant Cell13:1891–1905.PubMedGoogle Scholar
  25. Iturriaga, G., Leyns, L., Villegas, A., Gharaibeh, R., Salamini, F. and Bartels, D.1996.A family of novel myb-related genes from the resurrection plant Craterostigma plantagineum are specifically expressed in callus and roots in response to ABA or desiccation.Plant Mol.Biol.32:707–716.PubMedGoogle Scholar
  26. Jin, H.and Martin, C.1999.Multifunctionality and diversity within the plant MYB-gene family.Plant Mol.Biol.41:577–585.PubMedGoogle Scholar
  27. Jin, H., Cominelli, E., Bailey, P., Parr, A., Mehrtens, F., Jones, J., Tonelli, C., Weisshaar, B.and Martin, C.2000.Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis.EMBO J.19:6150–6161.PubMedGoogle Scholar
  28. Kirk, T.K.and Obst, J.R.1988.Lignin determination.Method Enzymol.161:87–101.Google Scholar
  29. Kranz, H.D., Denekamp, M., Greco, R., Jin, H., Leyva, A., Meissner, R.C., Petroni, K., Urzainqui, A., Bevan, M., Martin, C., Smeekens, S., Tonelli, C., Paz-Ares, J.and Weisshaar, B.1998.Towards functional characterisation of the members of the R2R3-MYB gene family from Arabid-opsis thaliana.Plant J.16:263–276.PubMedGoogle Scholar
  30. Lauvergeat, V., Rech, P., Jauneau, A., Guez, C., Coutos-Thevenot, P.and Grima-Pettenati, J.2002.The vascular expression pattern directed by the Eucalyptus gunnii cinnamyl alcohol dehydrogenase EgCAD2 promoter is conserved among woody and herbaceous plant species.Plant Mol.Biol.50:497–509.PubMedGoogle Scholar
  31. Lee, M.M.and Schiefelbein, J.1999.WEREWOLF,a MYB-related protein in Arabidopsis,is a position dependent regulator of epidermal cell patterning.Cell 99:473–483.PubMedGoogle Scholar
  32. Little, C.H.A.and Savidge, R.A.1981 The role of plant growth regulators in forest tree cambial growth.Plant Growth Regul.6:137–169.Google Scholar
  33. Little, C.H.A.and Pharis, R.P.1995.Hormonal control of radial and longitudinal growth in the tree stem.In:B.L. Garther (Ed.)Plant stems.Physiology and functional morphology.Academic Press, San Diego,pp.281–319.Google Scholar
  34. Magaraggia, F., Solinas, G., Valle, G., Giovinazzo, G. and Coraggio, I.1997.Maturation and translation mechanisms involved in the expression of a myb gene of rice.Plant Mol.Biol.35:1003–1008.PubMedGoogle Scholar
  35. Mellerowicz, E., Baucher, M., Sundberg, B.and Boerjan, W. 2001.Unravelling cell wall formation in the woody dicot stem.Plant Mol.Biol.47:239–274.PubMedGoogle Scholar
  36. Moritz, T.and Sunberg, B.1996.Endogenous cytokinin in the vascular cambial region of Pinus sylvestris during activity and dormancy.Physiol.Plant.98:693–698.Google Scholar
  37. Newman, L.J.and Campbell, M.M.2000.MYB proteins and xylem differentiation.In:R. Savidge, J. Barnett and R. Napier (Eds.),Cell and Molecular Biology of Wood Formation.BIOS Scientific Publishers Ltd, Oxford, pp.437–444.Google Scholar
  38. Newman, L.J., Perazza, D.E., Juda, L.and Campbell, M.M.2004.Involvement of the R2R3-MYB,At MYB61,in the ectopic ligni cation and dark-photomorphogenic components of the det3 mutant phenotphype.Plant J.37:239–250.PubMedGoogle Scholar
  39. Nilsson, O., Alde´n, T., Sitbon, F., Little, C.H.A., Chalupa, V., Sandberg, G.and Olsson, O.1992.Spatial pattern of cauliflower mosaic virus 35S promoter-luciferase expression in transgenic hybrid aspen trees.Transgenic Research 1:209–220.Google Scholar
  40. Ogata, K., Hojo, H., Aimoto, S., Nakai, T., Nakamura, H., Sarai, A., Ishii, S.and Nishimura, Y.1992.Solution structure of a DNA-binding unit of MYB –a helix turn helixelated motif with conserved tryptophans forming a hydrophobic core.Proc.Natl.Acad.Sci.USA 89:6428–6432.PubMedGoogle Scholar
  41. Oh, S., Park, S.and Han, K.-H.2003.Transcriptional regulation of secondary growth in Arabidopsis thaliana. J.Exp.Bot.54:2709–2722.PubMedGoogle Scholar
  42. Oppenheimer, D.G., Herman, P.L., Sivakumaran, S.,Esch, J. and Marks, M.D.1991.A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules.Cell 67:483–493.PubMedGoogle Scholar
  43. Patzlaff, A., McInnis, S., Courtenary, A., Surman, C., New-man, L.J., Smith, C., Bevan, M.W., Mansfield, S., Whetten, R.W., Sederoff, R.R.and Campbell, M.M.2003.Characterisation of a pine MYB that regulates lignification.Plant J.36:743–754.PubMedGoogle Scholar
  44. Romero, I., Fuertes, A., Benito, M.J., Malpica, J.M., Leyva, A.and Paz-Ares, J.1998.More than 80 R2R3-MYB regulatory genes in the genome of Arabidpsis thaliana. Plant J.14:273–284.PubMedGoogle Scholar
  45. Schrader, J., Moyle, R., Bhalerao, R.R., Hertzberg, M., Lundeberg, J., Nilsson, P.and Bhalerao, R.P.2004.Cambialmeristem dormancy in trees involves extensive remodeling of the transcriptome.Plant J.40:173–187.PubMedGoogle Scholar
  46. Sitbon, F., Hennion, S., Little, C.H.A.and Sundberg, B.1999. Enhanced ethylene production and peroxidase activity in IAA-overproducing transgenic tobacco plants is associated with increased lignin content and altered lignin composition. Plant Sci.141:165–173.Google Scholar
  47. Stracke, R., Werber, M.and Weisshaar, B.2001.The R2R3-MYB gene family in Arabidopsis thaliana.Curr.Opin.Plant Biol.4:447–456.PubMedGoogle Scholar
  48. Sundberg, B., Uggla, C.and Tuominen, H.2000.Cambial growth and auxin gradients.In:R. Savidge, J. Barnett and R. Napier (Eds.),Cell and Molecular Biology of Wood Formation.BIOS Scientific Publishers Ltd, Oxford,pp. 169–188.Google Scholar
  49. Tamagnone, L., Merida, A., Parr, A., Mackay, S.,Culianez-Macia, F.A., Roberts, K.and Martin, C.1998.The AmMYB308 and AmMYB330 transcription factors from Antirrhinum regulate phenylpropanoid and lignin biosynthe-sis in transgenic tobacco.Plant Cell 10:135–154.PubMedGoogle Scholar
  50. Timell, T.E.1969.The chemical composition of tension wood. Svensk Papperstidning 72:173–181.Google Scholar
  51. Tuominen, H., Puech, L., Fink, S.and Sundberg, G.1997.A radial gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen.Plant Physiol.115:577–585.PubMedGoogle Scholar
  52. Uggla, C., Moritz, T., Sandberg, G.and Sundberg, B.1996. Auxin as a positional signal in pattern formation in plants. Proc.Natl.Acad.Sci.USA 93:9282–9286.PubMedGoogle Scholar
  53. Uggla, C., Magel, E., Moritz, T.and Sundberg, B.2001. Function and dynamics of auxin and carbohydrates during earlywood/latewood transition in Scots pine.Plant Physiol.125:2029–2039.PubMedGoogle Scholar
  54. Urao, T., Yamaguchi-Shinozaki, K., Urao, S.and Shinozaki, K.1993.An Arabidopsis myb homologue is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence.Plant Cell 5:1529–1539.PubMedGoogle Scholar
  55. Yamaguchi, M., Fabian, T., Sauter, M., Bhalerao, R.P., Schrader, J., Sandberg, G., Umeda, M.and Uchimiya, H. 2000.Activation of CDK-activating kinase is dependent on interaction with H-type cyclins in plants.Plant J.24:11–20.PubMedGoogle Scholar
  56. Yang, Y.and Klessig, D.F.1996.Isolation and characterization of a tobacco mosaic virus-inducible myb homologue from tobacco.Proc.Natl.Acad.Sci.USA93:14972–14977.PubMedGoogle Scholar
  57. Zhong, R., Morrison, W.H., Himmelsbach, D.S. Poole, F.L. and Ye, Z-H.2000.Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody oplar plants.Plant Physiol.124:563–578.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Barbara Karpinska
    • 1
  • Marlene Karlsson
    • 2
  • Manoj Srivastava
    • 2
  • Anneli Stenberg
    • 2
  • Jarmo Schrader
    • 2
  • Fredrik Sterky
    • 3
  • Rishikesh Bhalerao
    • 2
  • Gunnar Wingsle
    • 2
  1. 1.Department of BotanyStockholm UniversityStockholmSweden
  2. 2.Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural ScienceUmea Plant Science CentreUmeaSweden
  3. 3.Department of BiotechnologyKTH Royal Institute of TechnologyStockholmSweden

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