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Gunnar Wingsle - Regulatory Proteins in the Lignification Process in Wood Print E-mail

show_ghroup_bw Wood is a major source of renewable raw materials that are widely used in the pulp, paper, and timber industries. Poplar has emerged as the model tree for woody species, and molecular tools have been developed that allow breakthrough science in this forest tree. In my research, a major focus has been on proteins that have been shown to play a role in wood development and more specifically in lignin biosynthesis. A major objective has been to develop and use advanced proteomic approaches to study their roles and related biological questions.
Gunnar_Wingsele_portrait

Reactive oxygen species (ROS)
ROS have recently been suggested to act as signalling molecules in the control of specialized processes, such as plant growth and defence, hormonal signalling, and development. Within the project, my group has explored the possibility to alter wood quality by the regulation of ROS at the plasmalemma/cell wall interface using transgenic methodology. A special type of superoxide dismutase with a high isoelectric point (hipI-SOD) has been mainly considered for this genetic manipulation due to its possible role as a regulator of hydrogen peroxide in the polymerization of lignin. Tthorough characterization of this protein in Poplar
has shown that it exists in two isoforms and in an additional spliced form. We are currently using these plants to study the underlying mechanisms of ROS-mediated regulation of cell wall development.
Specific transcription-MYB
Another group of proteins that has been identified as central to the regulation of phenylpropanoid metabolism is the MYB transcription factor family. Each MYB transcription factor contains a conserved DNA-binding domain, located in the N-terminal part of the protein. Some R2R3 MYB proteins bind AC elements in the promoters of several genes of the phenylpropanoid pathway, and thus have been assigned functions in the regulation of phenylpropanoid biosynthesis. For instance, one of these genes, PttMYB21, was found to be much more highly expressed in the secondary cell wall formation zone of xylem and phloem fibres than in other developmental zones. PttMYB21a antisense transgenic plants showed a phenotype with altered growth and elevated levels of total lignin in their vascular tissues. One of the intriguing features of the transgenic plants was the presence of lignin compounds with increased degrees of methoxylation. Moreover, elevated levels of caffeoyl-CoA 3-O-methyltransferase transcripts were found in the transgenic plants, suggesting that PttMYB21a could act as a transcriptional repressor.
wingsle_1
The Mediator and close functional relations between the Mediator modules and other transcriptional regulators (from Oudgenoeg et al. unpulished data)


General transcription The Mediator
In all eukaryotes, protein-encoding genes are transcribed by pol II. To perform its most basal functions, pol II requires five general transcription factors (GTFs). It is also now known that a Mediator, a 25 subunit protein complex, functions as a connector between the promoter-bound transcriptional regulators and pol II. The Mediator was first identified in Saccharomyces as an activity required for transcriptional activation in vitro. Later, it was identified as a multiprotein complex that provides an interface for activator and repressor proteins to transmit information from regulatory DNA elements to core promoters. A number of studies have determined that the Mediator is composed of three modules designated as “tail”, “head”, and “middle”. It is important for transcription control, modulating the frequency of initiation in responses to both positive and negative regulatory factors. Surprisingly, prior to our publication (Bäckstrom et al. 2007), there were had been no reports of the Mediator in plants. We are now studying Mediators that seems to play a role in lignin biosynthesis and wood development in Arabidopsis and Poplar.
sweden_greySvensk sammanfattning

Key publications

Karpinska B, Karlsson M, Srivastava M, Stenberg A, Schrader J, Sterky F, Bhalerao R, Wingsle G (2004) MYB transcrip- tion factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen. Plant Molecular Biology 56; 255-270.

Bäckström S, Elfving N, Nilsson R, Wingsle G, Björklund S (2007) Purification of mediator from Arabidopsis thaliana identifies PFT1 as the Med25 subunit. Mol Cell 26: 717-729

Bylesjö M, Nilsson R, Srivastava V, Grönlund A, Johansson AI, Jansson S, Karlsson J, Moritz T, Wingsle G, Trygg J. (2009) Integrated Analysis of Transcript, Protein and Metabolite Data to Study Lignin Biosynthesis in Hybrid Aspen. J. Prot. Res. 8:199-210.

Srivastava V, Srivastav MK, Chibani K, Nilsson R, Melzer M, Wingsle G (2009) Alternative Splicing Studies of the ROS Gene Network in Populus Reveals Two Isoforms of High Iso-electric point Superoxide Dismutase. Plant Physiol. 149: 1848-1859.

Srivastava V, Schinkel H, Witzell J, Hertzberg M, Torp M, Srivastava MK, Karpinska B, Melzer M, Wingsle G (2007) Downregulation of high-isoelectric-point extracellular superoxide dismutase mediates alterations in the metabolism of reactive oxygen species and developmental disturbances in hybrid aspen. Plant J 49: 135-148

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  1. Palm ME, Weise CF, Lundin C, Wingsle G, Nygren Y, Björn E, Naredi P, Wolf-Watz M, Wittung-Stafshede P
    Cisplatin binds human copper chaperone Atox1 and promotes unfolding in vitro
    Proceedings of the National Academy of Sciences of the United States of America: 2011 108:6951-6956
  2. Elfving N, Davoine C, Benlloch R, Blomberg J, Brännström K, Müller D, Nilsson A, Ulfstedt M, Ronne H, Wingsle G, Nilsson O, Björklund S
    The Arabidopsis thaliana Med25 mediator subunit integrates environmental cues to control plant development
    Proceedings of the National Academy of Sciences of the United States of America: 2011 108:8245-8250
  3. Bergemalm D, Forsberg K, Srivastava V, Graffmo KS, Andersen PM, Brännström T, Wingsle G, Marklund SL
    Superoxide dismutase-1 and other proteins in inclusions from transgenic amyotrophic lateral sclerosis model mice
    Journal of Neurochemistry; 2010 114:408-418
  4. Nilsson R, Bernfur K, Gustavsson N, Bygdell J, Wingsle G, Larsson C
    Proteomics of plasma membranes from poplar trees reveals tissue distribution of transporters, receptors, and proteins in cell wall formation
    Molecular & Cellular Proteomics: 2010 9:368-387
  5. Yanamandra K, Alexeyev O, Zamotin V, Srivastava V, Shchukarev A, Brorsson A-C, Tartaglia GG, Vogl T, Kayed R, Wingsle G, Olsson J, Dobson CM, Berg A, Elgh F, Morozova-Roche, LA
    Amyloid formation by the pro-inflammatory S100A8/A9 proteins in the ageing prostate
    PloS One: 2009 4:e5562
  6. Chibani K, Wingsle G, Jacquot J-P, Gelhaye E, Rouhier N
    Comparative Genomic Study of the Thioredoxin Family in Photosynthetic Organisms with Emphasis on Populus trichocarpa

    Molecular Plant: 2009 2(2):308-322
  7. Srivastava V, Srivastava MK, Chibani K, Nilsson R, Rouhier N, Melzer M, Wingsle G
    Alternative splicing studies of the reactive oxygen species gene network in Populus reveal two isoforms of high-isoelectric-point superoxide dismutase
    Plant Physiology: 2009 149:1848-1859
  8. Bylesjö M, Nilsson R, Srivastava V, Grönlund A, Johansson AI, Jansson S, Karlsson J, Moritz T, Wingsle G, Trygg J
    Integrated Analysis of Transcript, Protein and Metabolite Data To Study Lignin Biosynthesis in Hybrid Aspen
    Journal of Proteome Research: 2009 8:199-210
  9. Koh CS, Navrot N, Didierjean C, Rouhier N, Hirasawa M, Knaff DB, Wingsle G, Samian R, Jacquot J-P, Corbier C, Gelhaye E
    An atypical catalytic mechanism involving three cysteines of thioredoxin
    Journal of Biological Chemistry: 2008 283:23062-23072
  10. Overmeyer K, Kollist H, Tuominen H, Betz, C, Langebartels C, Wingsle G, Kangasjärvi S, Brader G, Mullineaux P, Kangasjärvi J
    Complex phenotypic profiles leading to ozone sensitivity in Arabidopsis thaliana mutants
    Plant, Cell and Environment: 2008 31: 1237-1249
  11. Bäckström S, Elfving N, Nilsson R, Wingsle G, Björklund S
    Purification of a Plant Mediator from Arabidopsis thaliana Identifies PFT1 as the Med25 Subunit
    Molecular Cell: 2007 26:717-729
  12. Martz F, Sutinen M-L, Derome K, Wingsle G, Julkunen-Tiitto R, Turunen M
    Effects of ultraviolet (UV) exclusion on the seasonal concentration of photosynthetic and UV-screening pigments in Scots pine needles
    Global Change Biology: 2007 13:252-265
  13. Srivastava V, Schinkel H, Witzell J, Hertzberg M, Torp M, Srivastava MK, Karpinska B, Melzer M, Wingsle G
    Downregulation of high-isoelectric-point extracellular superoxide dismutase mediates alterations in the metabolism of reactive oxygen species and developmental disturbances in hybrid aspen
    The Plant Journal: 2007 49:135-148
  14. Rouhier N, Gama F, Wingsle G, Gelhaye E, Gans P, Jacquot JP
    Engineering functional artificial hybrid proteins between poplar peroxiredoxin II and glutaredoxin or thioredoxin
    Biochemical and Biophysical Research Communications: 2006 341:1300-1308
  15. Ferreira S, Hjerno K, Larsen M, Wingsle G, Larsen P, Fey S, Roepstorff P, Pais MS
    Proteome profiling of Populus euphratica Oliv. Upon heat stress
    Annals of Botany: 2006 98:361-377
  16. Wiklund S, Karlsson M, Antti H, Johnels D, Sjostrom M, Wingsle G, Edlund U
    A new metabonomic strategy for analysing the growth process of the poplar tree
    Plant Biotechnology Journal: 2005 3:353-362
  17. Gelhaye E, Rouhier N, Gerard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson PI, Wingsle G, Hirasawa M, Knaff DB, Wang HM, Dizengremel P, Meyer Y, Jacquot JP
    A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase (vol 101, pg 14545, 2004)
    Proceedings of the National Academy of Sciences of the United States of America: 2005 102:3886-3886
  18. Hoglund S, Larsson S, Wingsle G
    Both hypersensitive and non-hypersensitive responses are associated with resistance in Salix viminalis against the gall midge Dasineura marginemtorquens
    J Exp Bot: 2005 56:3215-3222
  19. Karlsson M, Melzer M, Prokhorenko I, Johansson T, Wingsle G
    Hydrogen peroxide and expression of hipI-superoxide dismutase are associated with the development of secondary cell walls in Zinnia elegans
    J Exp Bot: 2005 56:2085-2093
  20. Rouhier N, Villarejo A, Srivastava M, Gelhaye E, Keech O, Droux M, Finkemeier I, Samuelsson G, Dietz KJ, Jacquot J-P, Wingsle G
    Identification of plant glutaredoxin targets
    Antioxid Redox Signal: 2005 7:919-929
  21. Louis J, Ounis A, Ducruet JM, Evain S, Laurila T, Thum T, Aurela M, Wingsle G, Alonso L, Pedros R, Moya I
    Remote sensing of sunlight-induced chlorophyll fluorescence and reflectance of Scots pine in the boreal forest during spring recovery
    Remote Sensing of Environment: 2005 96:37-48
  22. Gelhaye E, Rouhier N, Gerard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson P-I, Wingsle G, Hirasawa M, Knaff DB, Wang H, Dizengremel P, Meyer Y, Jacquot J-P
    A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase
    Proc Natl Acad Sci U S A: 2004 101:14545-14550
  23. Karpinska B, Karlsson M, Srivastava M, Stenberg A, Schrader J, Sterky F, Bhalerao R, Wingsle G
    MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen
    Plant Mol Biol: 2004 56:255-270
  24. Lovgren JM, Bylund GO, Srivastava MK, Lundberg LAC, Persson OP, Wingsle G, Wikstrom PM
    The PRC-barrel domain of the ribosome maturation protein RimM mediates binding to ribosomal protein S19 in the 30S ribosomal subunits
    Rna-a Publication of the Rna Society: 2004 10:1798-1812
  25. Karpinska B, Karlsson M, Schinkel H, Streller S, Suss KH, Melzer M, Wingsle G
    A novel superoxide dismutase with a high isoelectric point in higher plants. Expression, regulation, and protein localization
    Plant Physiology: 2001 126:1668-1677
  26. Schinkel H, Hertzberg M, Wingsle G
    A small family of novel CuZn-superoxide dismutases with high isoelectric points in hybrid aspen
    Planta: 2001 213:272-279
  27. Karpinska B, Wingsle G, Karpinski S
    Antagonistic effects of hydrogen peroxide and glutathione on acclimation to excess excitation energy in Arabidopsis
    IUBMB Life: 2000 50:21-26
  28. Wingsle G, Karpinski S, Hallgren JE
    Low temperature, high light stress and antioxidant defence mechanisms in higher plants
    Phyton-Annales Rei Botanicae: 1999 39:253-268
  29. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P
    Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis
    Science: 1999 284:654-657
  30. Tao DL, Oquist G, Wingsle G
    Active oxygen scavengers during cold acclimation of Scots pine seedlings in relation to freezing tolerance
    Cryobiology: 1998 37:38-45
  31. Schinkel H, Streller S, Wingsle G
    Multiple forms of extracellular superoxide dismutase in needles, stem tissues and seedlings of Scots pine
    Journal of Experimental Botany: 1998 49:931-936
  32. Wingsle G, Moritz T
    Analysis of ascorbate and dehydroascorbate in plant extracts by high-resolution selected ion monitoring gas chromatography mass spectrometry
    Journal of Chromatography A: 1997 782:95-103
  33. Streller S, Schinkel H, Wingsle G
    Apoplasmic CuZn-superoxide dismutase in Pinus sylvestris
    Phyton-Annales Rei Botanicae: 1997 37:271-276
  34. Krivosheeva A, Tao DL, Ottander C, Wingsle G, Dube SL, Oquist G
    Cold acclimation and photoinhibition of photosynthesis in Scots pine
    Planta: 1996 200:296-305
  35. Wingsle G, Karpinski S
    Differential redox regulation by glutathione of glutathione reductase and CuZn-superoxide dismutase gene expression in Pinus sylvestris L needles
    Planta: 1996 198:151-157
  36. Streller S, Karpinski S, Hallgren JE, Wingsle G
    4 Cytosolic-Type Cuzn-Superoxide Dismutases in Germinating-Seeds of Pinus-Sylvestris
    Physiologia Plantarum: 1994 92:443-450
  37. Streller S, Kromer S, Wingsle G
    Isolation and Purification of Mitochondrial Mn-Superoxide Dismutase from the Gymnosperm Pinus-Sylvestris L
    Plant and Cell Physiology: 1994 35:859-867
  38. Karpinski S, Karpinska B, Wingsle G, Hallgren JE
    Molecular Responses to Photooxidative Stress in Pinus-Sylvestris .1. Differential Expression of Nuclear and Plastid Genes in Relation to Recovery from Winter Stress
    Physiologia Plantarum: 1994 90:358-366
  39. Streller S, Wingsle G
    Pinus-Sylvestris L Needles Contain Extracellular Cuzn Superoxide-Dismutase
    Planta: 1994 192:195-201
  40. Mazzafera P, Wingsle G, Olsson O, Sandberg G
    S -Adenosyl -L -Methionine -Theobromine 1 -N -Methyltransferase, an Enzyme Catalyzing the Synthesis of Caffeine in Coffee
    Phytochemistry: 1994 37:1577-1584
  41. Wingsle G, Hallgren JE
    Influence of So2 and No2 Exposure on Glutathione, Superoxide-Dismutase and Glutathione-Reductase Activities in Scots Pine Needles
    Journal of Experimental Botany: 1993 44:463-470
  42. Karpinski S, Wingsle G, Karpinska B, Hallgren JE
    Molecular Responses to Photooxidative Stress in Pinus-Sylvestris (L) .2. Differential Expression of Cuzn-Superoxide Dismutases and Glutathione-Reductase
    Plant Physiology: 1993 103:1385-1391
  43. Wingsle G, Mattson A, Ekblad A, Hallgren JE, Selstam E
    Activities of Glutathione-Reductase and Superoxide-Dismutase in Relation to Changes of Lipids and Pigments Due to Ozone in Seedlings of Pinus-Sylvestris (L)
    Plant Science: 1992 82:167-178
  44. Karpinski S, Wingsle G, Olsson O, Hallgren JE
    Characterization of Cdnas Encoding Cuzn-Superoxide Dismutases in Scots Pine
    Plant Molecular Biology: 1992 18:545-555
  45. Karpinski S, Wingsle G, Karpinska B, Hallgren JE
    Differential Expression of Cuzn-Superoxide Dismutases in Pinus-Sylvestris Needles Exposed to So2 and No2
    Physiologia Plantarum: 1992 85:689-696
  46. Wingsle G, Strand M, Karpinski S, Hallgren JE
    Influence of So2 and No2 Exposure on Antioxidants and Photosynthesis in Needles of Pinus-Sylvestris
    Phyton-Annales Rei Botanicae: 1992 32:147-153
  47. Leverenz JW, Oquist G, Wingsle G
    Photosynthesis and Photoinhibition in Leaves of Chlorophyll-B-Less Barley in Relation to Absorbed Light
    Physiologia Plantarum: 1992 85:495-502
  48. Wingsle G, Gardestrom P, Hallgren JE, Karpinski S
    Isolation, Purification, and Subcellular-Localization of Isozymes of Superoxide-Dismutase from Scots Pine (Pinus-Sylvestris L) Needles
    Plant Physiology: 1991 95:21-28
  49. Rosenqvist E, Wingsle G, Ogren E
    Photoinhibition of Photosynthesis in Intact Willow Leaves in Response to Moderate Changes in Light and Temperature
    Physiologia Plantarum: 1991 83:390-396
  50. Palmqvist K, Sundblad LG, Wingsle G, Samuelsson G
    Acclimation of Photosynthetic Light Reactions During Induction of Inorganic Carbon Accumulation in the Green-Alga Chlamydomonas-Reinhardtii
    Plant Physiology: 1990 94:357-366
  51. Wingsle G, Sandberg G, Hallgren JE
    Determination of Glutathione in Scots Pine Needles by High-Performance Liquid-Chromatography as Its Monobromobimane Derivative
    Journal of Chromatography: 1989 479:335-344
  52. Wingsle G
    Purification and Characterization of Glutathione-Reductase from Scots Pine Needles
    Physiologia Plantarum: 1989 76:24-30
  53. Wingsle G, Nasholm T, Lundmark T, Ericsson A
    Induction of Nitrate Reductase in Needles of Scots Pine-Seedlings by Nox and No3
    Physiologia Plantarum: 1987 70:399-403

 
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