Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development
Abstract
Galactinol synthase is a pivotal enzyme involved in the synthesis of the raffinose family of oligosaccharides (RFOs) that function as transport carbohydrates in the phloem, as storage compounds in sink tissues and as soluble metabolites that combat both abiotic and biotic stress in several plant species. For hybrid poplar (Populus alba 9 grandidentata) overexpressing the Arabidopsis thaliana GolS3 (AtGolS3) gene showed clear effects on development; the extreme overexpressing lines were stunted and had cell wall traits characteristic of tension wood, whereas lines with only moderate up-regulation grew normally and had moderately altered secondary cell wall composition and ultrastructure. Stem cross-sections of the developing xylem revealed a significant increase in the number of vessels, as well as the clear presence of a G-layer in the fibres. Furthermore, AtGolS3-OE lines possessed higher cellulose and lower lignin contents, an increase in cellulose crystallinity, and significantly altered hemicellulose-derived carbohydrates, notably manifested by their mannose and xylose contents. Additionally, the transgenic plants displayed elevated xylem starch content. Transcriptome interrogation of the transgenic plants showed a significant up-regulation of genes involved in the synthesis of myo-inositol, along with genes involved in sucrose degradation. Our results suggest that the over expression of GolS and its product galactinolmore »
- Authors:
-
- Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Wood Science
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry; Wisconsin Energy Inst., Madison, WI (United States). Dept. of Energy Great Lakes Bioenergy Research Center
- Agricultural Research Council, Pretoria (South Africa). Biotechnology Platform
- Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Wood Science; Wisconsin Energy Inst., Madison, WI (United States). Dept. of Energy Great Lakes Bioenergy Research Center
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1374538
- Grant/Contract Number:
- FC02-07ER64494
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Plant Biotechnology Journal
- Additional Journal Information:
- Journal Volume: 15; Journal Issue: 7; Journal ID: ISSN 1467-7644
- Publisher:
- Society for Experimental Biology; Association of Applied Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; galactinol synthase; RFOs; tension wood; cellulose; lignin; sugar signalling
Citation Formats
Unda, Faride, Kim, Hoon, Hefer, Charles, Ralph, John, and Mansfield, Shawn D. Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development. United States: N. p., 2017.
Web. doi:10.1111/pbi.12682.
Unda, Faride, Kim, Hoon, Hefer, Charles, Ralph, John, & Mansfield, Shawn D. Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development. United States. https://doi.org/10.1111/pbi.12682
Unda, Faride, Kim, Hoon, Hefer, Charles, Ralph, John, and Mansfield, Shawn D. Sat .
"Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development". United States. https://doi.org/10.1111/pbi.12682. https://www.osti.gov/servlets/purl/1374538.
@article{osti_1374538,
title = {Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development},
author = {Unda, Faride and Kim, Hoon and Hefer, Charles and Ralph, John and Mansfield, Shawn D.},
abstractNote = {Galactinol synthase is a pivotal enzyme involved in the synthesis of the raffinose family of oligosaccharides (RFOs) that function as transport carbohydrates in the phloem, as storage compounds in sink tissues and as soluble metabolites that combat both abiotic and biotic stress in several plant species. For hybrid poplar (Populus alba 9 grandidentata) overexpressing the Arabidopsis thaliana GolS3 (AtGolS3) gene showed clear effects on development; the extreme overexpressing lines were stunted and had cell wall traits characteristic of tension wood, whereas lines with only moderate up-regulation grew normally and had moderately altered secondary cell wall composition and ultrastructure. Stem cross-sections of the developing xylem revealed a significant increase in the number of vessels, as well as the clear presence of a G-layer in the fibres. Furthermore, AtGolS3-OE lines possessed higher cellulose and lower lignin contents, an increase in cellulose crystallinity, and significantly altered hemicellulose-derived carbohydrates, notably manifested by their mannose and xylose contents. Additionally, the transgenic plants displayed elevated xylem starch content. Transcriptome interrogation of the transgenic plants showed a significant up-regulation of genes involved in the synthesis of myo-inositol, along with genes involved in sucrose degradation. Our results suggest that the over expression of GolS and its product galactinol may serve as a molecular signal that initiates metabolic changes, culminating in a change in cell wall development and potentially the formation of tension wood.},
doi = {10.1111/pbi.12682},
journal = {Plant Biotechnology Journal},
number = 7,
volume = 15,
place = {United States},
year = {Sat Mar 04 00:00:00 EST 2017},
month = {Sat Mar 04 00:00:00 EST 2017}
}
Web of Science
Works referenced in this record:
Isolation and characterization of galactinol synthases from hybrid poplar
journal, December 2011
- Unda, F.; Canam, T.; Preston, L.
- Journal of Experimental Botany, Vol. 63, Issue 5
The Carbohydrates in Birchwood.
journal, January 1952
- Gustafsson, Charley; Ollinmaa, Paavo J.; Saarnio, Jouko
- Acta Chemica Scandinavica, Vol. 6
Spatial and temporal expression profiling of cell-wall invertase genes during early development in hybrid poplar
journal, July 2008
- Canam, T.; Mak, S. W. Y.; Mansfield, S. D.
- Tree Physiology, Vol. 28, Issue 7
Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis
journal, February 2002
- Friml, Jiří; Wiśniewska, Justyna; Benková, Eva
- Nature, Vol. 415, Issue 6873
Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants
journal, April 2010
- Munnik, Teun; Vermeer, Joop E. M.
- Plant, Cell & Environment, Vol. 33, Issue 4
Carbohydrate regulation of leaf development: Prolongation of leaf senescence in Rubisco antisense mutants of tobacco
journal, January 2000
- Miller, Adam; Schlagnhaufer, Carl; Spalding, Martin
- Photosynthesis Research, Vol. 63, Issue 1, p. 1-8
Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase
journal, May 2009
- Barratt, D. H. P.; Derbyshire, P.; Findlay, K.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
Identification of Lignin and Polysaccharide Modifications in Populus Wood by Chemometric Analysis of 2D NMR Spectra from Dissolved Cell Walls
journal, September 2009
- Hedenström, Mattias; Wiklund-Lindström, Susanne; Öman, Tommy
- Molecular Plant, Vol. 2, Issue 5
Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure
journal, July 2009
- Coleman, H. D.; Yan, J.; Mansfield, S. D.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
Over-expression of an arabidopsis family A sucrose phosphate synthase (SPS) gene alters plant growth and fibre development
journal, April 2007
- Park, Ji-Young; Canam, Thomas; Kang, Kyu-Young
- Transgenic Research, Vol. 17, Issue 2
Perturbed Lignification Impacts Tree Growth in Hybrid Poplar—A Function of Sink Strength, Vascular Integrity, and Photosynthetic Assimilation
journal, September 2008
- Coleman, Heather D.; Samuels, A. Lacey; Guy, Robert D.
- Plant Physiology, Vol. 148, Issue 3
Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana
journal, February 2002
- Taji, Teruaki; Ohsumi, Chieko; Iuchi, Satoshi
- The Plant Journal, Vol. 29, Issue 4
Sucrose phosphate synthase and sucrose phosphate phosphatase interact in planta and promote plant growth and biomass accumulation
journal, April 2015
- Maloney, Victoria J.; Park, Ji-Young; Unda, Faride
- Journal of Experimental Botany, Vol. 66, Issue 14
Up-regulation of sucrose synthase and UDP-glucose pyrophosphorylase impacts plant growth and metabolism
journal, January 2006
- Coleman, Heather D.; Ellis, Dave D.; Gilbert, Margarita
- Plant Biotechnology Journal, Vol. 4, Issue 1
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
Sugar sensing and signalling networks in plants
journal, February 2005
- Rolland, F.; Sheen, J.
- Biochemical Society Transactions, Vol. 33, Issue 1
Studies on a Galactan from Tension Wood of Beech (Fagus silvatica L.).
journal, January 1962
- Meier, Hans; Dahlén, Monica; Frisell, Christer
- Acta Chemica Scandinavica, Vol. 16
From tropics to tundra: Global convergence in plant functioning
journal, December 1997
- Reich, P. B.; Walters, M. B.; Ellsworth, D. S.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 25
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Jasmonate-dependent expression of a galactinol synthase gene is involved in priming of systemic fungal resistance in Arabidopsis thaliana
journal, May 2010
- Cho, Song Mi; Kang, Eun Young; Kim, Mi Seong
- Botany, Vol. 88, Issue 5
Studies on the Leaf of Populus deltoides (Salicaceae): Ultrastructure, Plasmodesmatal Frequency, and Solute Concentrations
journal, August 1985
- Russin, William A.; Evert, Ray F.
- American Journal of Botany, Vol. 72, Issue 8
Analysis of retted and non retted flax fibres by chemical and enzymatic means
journal, August 2001
- Mooney, Caitriona; Stolle-Smits, Trinette; Schols, Henk
- Journal of Biotechnology, Vol. 89, Issue 2-3
Sucrose metabolism and cellulose biosynthesis in sunflower hypocotyls
journal, March 2002
- Kutschera, U.; Heiderich, A.
- Physiologia Plantarum, Vol. 114, Issue 3
Comparative interrogation of the developing xylem transcriptomes of two wood-forming species: Populus trichocarpa and Eucalyptus grandis
journal, February 2015
- Hefer, Charles A.; Mizrachi, Eshchar; Myburg, Alexander A.
- New Phytologist, Vol. 206, Issue 4
Secondary plasmodesmata formation in the minor-vein phloem of Cucumis melo L. and Cucurbita pepo L.
journal, July 1996
- Volk, GayleM.; Turgeon, Robert; Beebe, DwightU.
- Planta, Vol. 199, Issue 3
A Conserved Upstream Open Reading Frame Mediates Sucrose-Induced Repression of Translation
journal, June 2004
- Wiese, Anika; Elzinga, Nico; Wobbes, Barry
- The Plant Cell, Vol. 16, Issue 7
Investigating the molecular underpinnings underlying morphology and changes in carbon partitioning during tension wood formation in Eucalyptus
journal, November 2014
- Mizrachi, Eshchar; Maloney, Victoria J.; Silberbauer, Janine
- New Phytologist, Vol. 206, Issue 4
Galactinol Synthase from Kidney Bean Cotyledon and Zucchini Leaf (Purification and N-Terminal Sequences)
journal, October 1995
- Liu, J. J.; Odegard, W.; de Lumen, B. O.
- Plant Physiology, Vol. 109, Issue 2
Computerization of Ruland's X-ray method for determination of the crystallinity in polymers
journal, April 1973
- Vonk, C. G.
- Journal of Applied Crystallography, Vol. 6, Issue 2
A Role for Inositol 1,4,5-Trisphosphate in Gravitropic Signaling and the Retention of Cold-Perceived Gravistimulation of Oat Shoot Pulvini
journal, March 2001
- Perera, Imara Y.; Heilmann, Ingo; Chang, Soo Chul
- Plant Physiology, Vol. 125, Issue 3
Biosynthesis of cellulose-enriched tension wood in Populus : global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis
journal, January 2006
- Andersson-Gunnerås, Sara; Mellerowicz, Ewa J.; Love, Jonathan
- The Plant Journal, Vol. 45, Issue 2
Galactinol synthase1 . A Novel Heat Shock Factor Target Gene Responsible for Heat-Induced Synthesis of Raffinose Family Oligosaccharides in Arabidopsis
journal, October 2004
- Panikulangara, Tressa Jacob; Eggers-Schumacher, Gabriele; Wunderlich, Markus
- Plant Physiology, Vol. 136, Issue 2
A 13 C NMR Study of Milled Wood Lignins from Hybrid Salix Clones
journal, January 1992
- Landucci, Lawrence L.; Deka, Ganesh C.; Roy, D. N.
- Holzforschung, Vol. 46, Issue 6
Products of leaf primary carbon metabolism modulate the developmental programme determining plant morphology
journal, January 2006
- Raines, C.
- Journal of Experimental Botany, Vol. 57, Issue 9
Identification of quantitative trait loci for wood quality and growth across eight full-sib coastal Douglas-fir families
journal, June 2007
- Ukrainetz, Nicholas K.; Ritland, Kermit; Mansfield, Shawn D.
- Tree Genetics & Genomes, Vol. 4, Issue 2
p-Hydroxybenzoate groups in the lignin of aspen (populus tremula)
journal, January 1955
- Smith, D. C. C.
- Journal of the Chemical Society (Resumed), Vol. 0, Issue 0, p. 2347-2351
A unified hypothesis of mechanoperception in plants
journal, October 2006
- Telewski, F. W.
- American Journal of Botany, Vol. 93, Issue 10
Whole plant cell wall characterization using solution-state 2D NMR
journal, August 2012
- Mansfield, Shawn D.; Kim, Hoon; Lu, Fachuang
- Nature Protocols, Vol. 7, Issue 9
Generation of Monoclonal Antibodies against Plant Cell-Wall Polysaccharides (I. Characterization of a Monoclonal Antibody to a Terminal [alpha]-(1->2)-Linked Fucosyl-Containing Epitope
journal, February 1994
- Puhlmann, J.; Bucheli, E.; Swain, M. J.
- Plant Physiology, Vol. 104, Issue 2
Downregulation of Cinnamoyl-Coenzyme A Reductase in Poplar: Multiple-Level Phenotyping Reveals Effects on Cell Wall Polymer Metabolism and Structure
journal, November 2007
- Leplé, Jean-Charles; Dauwe, Rebecca; Morreel, Kris
- The Plant Cell, Vol. 19, Issue 11
Raffinose and Stachyose Accumulation, Galactinol Synthase Expression, and Winter Injury of Contrasting Alfalfa Germplasms
journal, January 2003
- Cunningham, S. M.; Nadeau, P.; Castonguay, Y.
- Crop Science, Vol. 43, Issue 2
Engineering Plants for Elevated CO 2 : A Relationship between Starch Degradation and Sugar Sensing
journal, May 2004
- Sharkey, T. D.; Laporte, M.; Lu, Y.
- Plant Biology, Vol. 6, Issue 3
Characterization and comparative analysis of Arabidopsis phosphatidylinositol phosphate 5-kinase 10 reveals differences in Arabidopsis and human phosphatidylinositol phosphate kinases
journal, May 2005
- Perera, Imara Y.; Davis, Amanda J.; Galanopoulou, Dia
- FEBS Letters, Vol. 579, Issue 16
Sugar perception and signaling—an update
journal, October 2009
- Hanson, Johannes; Smeekens, Sjef
- Current Opinion in Plant Biology, Vol. 12, Issue 5
SUGAR SENSING AND SIGNALING IN PLANTS: Conserved and Novel Mechanisms
journal, June 2006
- Rolland, Filip; Baena-Gonzalez, Elena; Sheen, Jen
- Annual Review of Plant Biology, Vol. 57, Issue 1
Myo-inositol and beyond – Emerging networks under stress
journal, October 2011
- Valluru, Ravi; Van den Ende, Wim
- Plant Science, Vol. 181, Issue 4
Transcriptome profiles of hybrid poplar (Populus trichocarpa × deltoides) reveal rapid changes in undamaged, systemic sink leaves after simulated feeding by forest tent caterpillar (Malacosoma disstria)
journal, July 2010
- Philippe, Ryan N.; Ralph, Steven G.; Mansfield, Shawn D.
- New Phytologist, Vol. 188, Issue 3
Structural and functional heterogeneity in phloem loading and transport
journal, January 2013
- Slewinski, Thomas L.; Zhang, Cankui; Turgeon, Robert
- Frontiers in Plant Science, Vol. 4
Specific type of secondary cell wall formed by plant fibers
journal, May 2010
- Gorshkova, T. A.; Gurjanov, O. P.; Mikshina, P. V.
- Russian Journal of Plant Physiology, Vol. 57, Issue 3
Heterologous expression and functional characterization of two hybrid poplar cell-wall invertases
journal, August 2008
- Canam, Thomas; Unda, Faride; Mansfield, Shawn D.
- Planta, Vol. 228, Issue 6
Xylogenesis in tissue culture: Taxol effects on microtubule reorientation and lateral association in differentiating cells
journal, June 1985
- Falconer, Marcia M.; Seagull, R. W.
- Protoplasma, Vol. 128, Issue 2-3
The Chemistry of Reaction Wood. Part II. The Polysaccharides of Eucalyptus goniocalyx and Pinus radiata
journal, January 1958
- Schwerin, Gerda
- Holzforschung, Vol. 12, Issue 2
Invertases. Primary Structures, Functions, and Roles in Plant Development and Sucrose Partitioning
journal, September 1999
- Sturm, Arnd
- Plant Physiology, Vol. 121, Issue 1
Hydroxycinnamates in lignification
journal, August 2009
- Ralph, John
- Phytochemistry Reviews, Vol. 9, Issue 1, p. 65-83
Expression of a GALACTINOL SYNTHASE Gene in Tomato Seeds Is Up-Regulated before Maturation Desiccation and Again after Imbibition whenever Radicle Protrusion Is Prevented
journal, January 2003
- Downie, Bruce; Gurusinghe, Sunitha; Dahal, Petambar
- Plant Physiology, Vol. 131, Issue 3
Immunocytochemical characterization of tension wood: Gelatinous fibers contain more than just cellulose
journal, June 2008
- Bowling, Andrew J.; Vaughn, Kevin C.
- American Journal of Botany, Vol. 95, Issue 6
Effect of initial moisture content and chip size on the bioconversion efficiency of softwood lignocellulosics
journal, January 2004
- Cullis, Ian F.; Saddler, John N.; Mansfield, Shawn D.
- Biotechnology and Bioengineering, Vol. 85, Issue 4
Varied growth, biomass and cellulose content in tobacco expressing yeast-derived invertases
journal, June 2006
- Canam, Thomas; Park, Ji-Young; Yu, Ka Yun
- Planta, Vol. 224, Issue 6
Modifications in Lignin and Accumulation of Phenolic Glucosides in Poplar Xylem upon Down-regulation of Caffeoyl-Coenzyme A O-Methyltransferase, an Enzyme Involved in Lignin Biosynthesis
journal, August 2000
- Meyermans, Hugo; Morreel, Kris; Lapierre, Catherine
- Journal of Biological Chemistry, Vol. 275, Issue 47, p. 36899-36909
Isolation of high-quality RNA from gymnosperm and angiosperm trees
journal, May 2004
- Kolosova, Natalia; Miller, Barbara; Ralph, Steven
- BioTechniques, Vol. 36, Issue 5
Effect of initial moisture content and chip size on the bioconversion efficiency of softwood lignocellulosics
journal, January 2004
- Cullis, Ian F.; Saddler, John N.; Mansfield, Shawn D.
- Biotechnology and Bioengineering, Vol. 85, Issue 4
Heterologous expression and functional characterization of two hybrid poplar cell-wall invertases
journal, August 2008
- Canam, Thomas; Unda, Faride; Mansfield, Shawn D.
- Planta, Vol. 228, Issue 6
Over-expression of an arabidopsis family A sucrose phosphate synthase (SPS) gene alters plant growth and fibre development
journal, April 2007
- Park, Ji-Young; Canam, Thomas; Kang, Kyu-Young
- Transgenic Research, Vol. 17, Issue 2
Characterization and comparative analysis of Arabidopsis phosphatidylinositol phosphate 5-kinase 10 reveals differences in Arabidopsis and human phosphatidylinositol phosphate kinases
journal, May 2005
- Perera, Imara Y.; Davis, Amanda J.; Galanopoulou, Dia
- FEBS Letters, Vol. 579, Issue 16
Myo-inositol and beyond – Emerging networks under stress
journal, October 2011
- Valluru, Ravi; Van den Ende, Wim
- Plant Science, Vol. 181, Issue 4
Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis
journal, February 2002
- Friml, Jiří; Wiśniewska, Justyna; Benková, Eva
- Nature, Vol. 415, Issue 6873
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana
journal, February 2002
- Taji, Teruaki; Ohsumi, Chieko; Iuchi, Satoshi
- The Plant Journal, Vol. 29, Issue 4
Engineering Plants for Elevated CO 2 : A Relationship between Starch Degradation and Sugar Sensing
journal, May 2004
- Sharkey, T. D.; Laporte, M.; Lu, Y.
- Plant Biology, Vol. 6, Issue 3
Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure
journal, July 2009
- Coleman, H. D.; Yan, J.; Mansfield, S. D.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase
journal, May 2009
- Barratt, D. H. P.; Derbyshire, P.; Findlay, K.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
On the utility of nitrogen in leaves
journal, December 1997
- Loomis, R. S.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 25
Isolation and characterization of galactinol synthases from hybrid poplar
journal, December 2011
- Unda, F.; Canam, T.; Preston, L.
- Journal of Experimental Botany, Vol. 63, Issue 5
Sucrose phosphate synthase and sucrose phosphate phosphatase interact in planta and promote plant growth and biomass accumulation
journal, April 2015
- Maloney, Victoria J.; Park, Ji-Young; Unda, Faride
- Journal of Experimental Botany, Vol. 66, Issue 14
Identification of Lignin and Polysaccharide Modifications in Populus Wood by Chemometric Analysis of 2D NMR Spectra from Dissolved Cell Walls
journal, September 2009
- Hedenström, Mattias; Wiklund-Lindström, Susanne; Öman, Tommy
- Molecular Plant, Vol. 2, Issue 5
Expression of a GALACTINOL SYNTHASE Gene in Tomato Seeds Is Up-Regulated before Maturation Desiccation and Again after Imbibition whenever Radicle Protrusion Is Prevented
journal, January 2003
- Downie, Bruce; Gurusinghe, Sunitha; Dahal, Petambar
- Plant Physiology, Vol. 131, Issue 3
Generation of Monoclonal Antibodies against Plant Cell-Wall Polysaccharides (I. Characterization of a Monoclonal Antibody to a Terminal [alpha]-(1->2)-Linked Fucosyl-Containing Epitope
journal, February 1994
- Puhlmann, J.; Bucheli, E.; Swain, M. J.
- Plant Physiology, Vol. 104, Issue 2
Galactinol Synthase from Kidney Bean Cotyledon and Zucchini Leaf (Purification and N-Terminal Sequences)
journal, October 1995
- Liu, J. J.; Odegard, W.; de Lumen, B. O.
- Plant Physiology, Vol. 109, Issue 2
Invertases. Primary Structures, Functions, and Roles in Plant Development and Sucrose Partitioning
journal, September 1999
- Sturm, Arnd
- Plant Physiology, Vol. 121, Issue 1
A Conserved Upstream Open Reading Frame Mediates Sucrose-Induced Repression of Translation
journal, June 2004
- Wiese, Anika; Elzinga, Nico; Wobbes, Barry
- The Plant Cell, Vol. 16, Issue 7
Downregulation of Cinnamoyl-Coenzyme A Reductase in Poplar: Multiple-Level Phenotyping Reveals Effects on Cell Wall Polymer Metabolism and Structure
journal, November 2007
- Leplé, Jean-Charles; Dauwe, Rebecca; Morreel, Kris
- The Plant Cell, Vol. 19, Issue 11
Transcriptional and Hormonal Regulation of Gravitropism of Woody Stems in Populus
journal, September 2015
- Gerttula, Suzanne; Zinkgraf, Matthew; Muday, Gloria K.
- The Plant Cell
Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants
journal, April 2010
- Munnik, Teun; Vermeer, Joop E. M.
- Plant, Cell & Environment, Vol. 33, Issue 4
Up-regulation of sucrose synthase and UDP-glucose pyrophosphorylase impacts plant growth and metabolism
journal, January 2006
- Coleman, Heather D.; Ellis, Dave D.; Gilbert, Margarita
- Plant Biotechnology Journal, Vol. 4, Issue 1
Structural and functional heterogeneity in phloem loading and transport
journal, January 2013
- Slewinski, Thomas L.; Zhang, Cankui; Turgeon, Robert
- Frontiers in Plant Science, Vol. 4
A unified hypothesis of mechanoperception in plants
journal, October 2006
- Telewski, F. W.
- American Journal of Botany, Vol. 93, Issue 10
Works referencing / citing this record:
The Formation of Structural Abnormalities in Karelian Birch Wood is Associated with Auxin Inactivation and Disrupted Basipetal Auxin Transport
journal, June 2019
- Novitskaya, Ludmila L.; Tarelkina, Tatiana V.; Galibina, Natalia A.
- Journal of Plant Growth Regulation, Vol. 39, Issue 1
Branching out: a new era of investigating physiological processes in forest trees using genomic tools
journal, February 2018
- Tsai, Chung-Jui; Harding, Scott A.; Cooke, Janice E. K.
- Tree Physiology, Vol. 38, Issue 3
Maize HSFA 2 and HSBP 2 antagonistically modulate raffinose biosynthesis and heat tolerance in Arabidopsis
journal, July 2019
- Gu, Lei; Jiang, Tao; Zhang, Chunxia
- The Plant Journal, Vol. 100, Issue 1