Xylem Cell Wall Formation In Pioneer Roots And Stems Of Populus Trichocarpa (Torr. & Gray)
Katarzyna Marzec-Schmidt, A. Ludwików, N. Wojciechowska, Anna Kasprowicz-Maluśki, J. Mucha, A. Bagniewska-Zadworna
Published 2019 · Biology, Medicine
Download PDFAnalyze on Scholarcy
Regulation of gene expression, as determined by the genetics of the tree species, is a major factor in determining wood quality. Therefore, the identification of genes that play a role in xylogenesis is extremely important for understanding the mechanisms shaping the plant phenotype. Efforts to develop new varieties characterized by higher yield and better wood quality will greatly benefit from recognizing and understanding the complex transcriptional network underlying wood development. The present study provides a detailed comparative description of the changes that occur in genes transcription and the biosynthesis of cell-wall-related compounds during xylogenesis in Populus trichocarpa pioneer roots and stems. Even though results of microarray analysis indicated that only approximately 10% of the differentially expressed genes were common to both organs, many fundamental mechanisms were similar; e.g. the pattern of expression of genes involved in the biosynthesis of cell wall proteins, polysaccharides, and lignins. Gas chromatography time-of-flight mass spectrometry (GC-TOF-MS) shows that the composition of monosaccharides was also very similar, with an increasing amount of xylose building secondary cell wall hemicellulose and pectins, especially in the stems. While hemicellulose degradation was typical for stems, possibly due to the intensive level of cell wall lignification. Notably, the main component of lignins in roots were guiacyl units, while syringyl units were dominant in stems, where fibers are especially needed for support. Our study is the first comprehensive analysis, at the structural and molecular level, of xylogenesis in under- and aboveground tree parts, and clearly reveals the great complexity of molecular mechanisms underlying cell wall formation and modification during xylogenesis in different plant organs.
This paper references
The Microtubule-Associated Protein AtMAP70-5 Regulates Secondary Wall Patterning in Arabidopsis Wood Cells
Edouard Pesquet (2010)
Lignin biosynthesis in Norway spruce : from a model system to the tree
S. Koutaniemi (2007)
Developmental complexity of arabinan polysaccharides and their processing in plant cell walls.
Yves Verhertbruggen (2009)
Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 Directly Regulates the Genes That Govern Programmed Cell Death and Secondary Wall Formation during Xylem Differentiation[C][W]
Kyoko Ohashi-Ito (2010)
Wood Cell-Wall Structure Requires Local 2D-Microtubule Disassembly by a Novel Plasma Membrane-Anchored Protein
Y. Oda (2010)
Physiological roles of plant glycoside hydrolases
Z. Minic (2007)
W. Boerjan (2003)
An epitope of rice threonine- and hydroxyproline-rich glycoprotein is common to cell wall and hydrophobic plasma-membrane glycoproteins
M. Smallwood (2004)
Occurrence of autophagy during pioneer root and stem development in Populus trichocarpa
Natalia Wojciechowska (2019)
Functional Characterization of the Poplar R2R3-MYB Transcription Factor PtoMYB216 Involved in the Regulation of Lignin Biosynthesis during Wood Formation
Qiaoyan Tian (2013)
Root and Root System Terminology
R. Sutton (1983)
Contrasting the morphology, anatomy and fungal colonization of new pioneer and fibrous roots.
M. Zadworny (2011)
Seasonal reorganization of the xylem
X. Li (2010)
PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements
H. Mi (2017)
Developmental programmed cell death in plants.
H. Kuriyama (2002)
Avoiding transport bottlenecks in an expanding root system: xylem vessel development in fibrous and pioneer roots under field conditions.
A. Bagniewska-Zadworna (2012)
Cell Wall Polysaccharide Synthesis
D. Mohnen (2009)
Arabidopsis AtCUL3a and AtCUL3b Form Complexes with Members of the BTB/POZ-MATH Protein Family1
H. Weber (2005)
The Woody-Preferential Gene EgMYB88 Regulates the Biosynthesis of Phenylpropanoid-Derived Compounds in Wood
Marçal Soler (2016)
Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists
D. Huang (2009)
Programmed cell death of tracheary elements as a paradigm in plants
H. Fukuda (2004)
Populus GT43 family members group into distinct sets required for primary and secondary wall xylan biosynthesis and include useful promoters for wood modification.
Christine Ratke (2015)
Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia.
K. Obara (2001)
A genomic approach to investigate developmental cell death in woody tissues of Populus trees
Charleen Moreau (2004)
Low Lignin Mutants and Reduction of Lignin Content in Grasses for Increased Utilisation of Lignocellulose
Cecilie S. L. Christensen (2019)
Cytoskeletal organization during xylem cell differentiation
Y. Oda (2006)
Cell wall loosening by expansins.
D. Cosgrove (1998)
Cold alkali can extract phenolic acids that are ether linked to cell wall components in dicotyledonous plants (buckwheat, soybean and flax)
V. Lozovaya (1999)
The Cellulose Synthase Gene Superfamily and Biochemical Functions of Xylem-Specific Cellulose Synthase-Like Genes in Populus trichocarpa1[W][OA]
S. Suzuki (2006)
Biosynthesis of plant cell walls
M. Handford (2006)
Post mortem function of AtMC9 in xylem vessel elements.
Benjamin Bollhöner (2013)
Cell wall hemicelluloses as mobile carbon stores in non‐reproductive plant tissues
G. Hoch (2007)
A proteoglycan mediates inductive interaction during plant vascular development
H. Motose (2004)
Seasonal reorganization of the xylem transcriptome at different tree ages reveals novel insights into wood formation in Pinus radiata.
X. Li (2010)
Biosynthesis of plant cell walls,” in Biomass Recalcitrance
D. Mohnen (2008)
Pectic homogalacturonan masks abundant
Complexity of the transcriptional network controlling secondary wall biosynthesis.
R. Zhong (2014)
Novel vascular cell-specific genes whose expression is regulated temporally and spatially during vascular system development.
T. Demura (1994)
New insights into pioneer root xylem
A. Stelmasik (2014)
Development of the root system of northern red oak (Quercus rubra L.). Harvard Forest
W H Lyford (1980)
New insights into pioneer root xylem development: evidence obtained from Populus trichocarpa plants grown under field conditions.
A. Bagniewska-Zadworna (2014)
Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies.
E. Yates (1996)
Role of the Extensin Superfamily in Primary Cell Wall Architecture1
D. T. Lamport (2011)
Cellulose and callose synthesis and organization in focus, what's new?
R. Schneider (2016)
R2R3-MYB gene pairs in Populus: evolution and contribution to secondary wall formation and flowering time.
Guohua Chai (2014)
Populus: arabidopsis for forestry. Do we need a model tree?
Gail Taylor (2002)
Genome-Wide Analysis of the Fasciclin-Like Arabinogalactan Protein Gene Family Reveals Differential Expression Patterns, Localization, and Salt Stress Response in Populus
Lina Zang (2015)
The cell biology of lignification in higher plants.
Jaime Barros (2015)
Tracheary element differentiation.
S. Turner (2007)
The Pectic Polysaccharides of Primary Cell Walls
M. A. O’Neill (1990)
Localization of Pectic Galactan in Tomato Cell Walls Using a Monoclonal Antibody Specific to (1[->]4)-[beta]-D-Galactan
L. Jones (1997)
APL regulates vascular tissue identity in Arabidopsis
M. Bonke (2003)
Transcriptome sequencing and profiling of expressed genes in cambial zone and differentiating xylem of Japanese cedar (Cryptomeria japonica)
Kentaro Mishima (2013)
Molecular Cloning and Characterization of cDNAs Associated with Tracheary Element Differentiation in Cultured Zinnia Cells
T. Demura (1993)
Genome-wide identification, classification
L. Jun (2012)
Regulation of secondary cell wall biosynthesis by poplar R2R3 MYB transcription factor PtrMYB152 in Arabidopsis
S. Wang (2014)
Neighboring Parenchyma Cells Contribute to Arabidopsis Xylem Lignification, while Lignification of Interfascicular Fibers Is Cell Autonomous[W]
R. Smith (2013)
An Arabidopsis Gene Regulatory Network for Secondary Cell Wall Synthesis
M. Taylor-Teeples (2015)
Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans[W][OA]
Edouard Pesquet (2013)
LACCASE Is Necessary and Nonredundant with PEROXIDASE for Lignin Polymerization during Vascular Development in Arabidopsis[C][W]
Q. Zhao (2013)
Genome-wide identification, classification and expression analysis of genes encoding putative fasciclin-like arabinogalactan proteins in Chinese cabbage (Brassica rapa L.)
L. Jun (2012)
Xyloglucan Endotransglycosylases Have a Function during the Formation of Secondary Cell Walls of Vascular Tissues Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007773.
V. Bourquin (2002)
Autolysis during in vitro tracheary element differentiation: formation and location of the perforation.
J. Nakashima (2000)
Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties.
E. Mellerowicz (2008)
Genome-wide comparison of two poplar genotypes with different growth rates
S. Hao (2011)
G. Chai (2014)
On Vessel Member Differentiation in the Bean (Phaseolus vulgaris L.)
K. Esau (1978)
Eucalyptus hairy roots, a fast, efficient and versatile tool to explore function and expression of genes involved in wood formation.
Anna Plasencia (2016)
Carbohydrate-Active Enzymes Involved in the Secondary Cell Wall Biogenesis in Hybrid Aspen1
H. Aspeborg (2005)
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
D. Huang (2008)
Cold alkali can extract phenolic acids that are ether linked to cell wall components in Dicotyledonous plants ( buckwheat , flax and soybean )
V. V. Lozovaya (1999)
Wood formation in trees.
C. Plomion (2001)
AspWood: High-Spatial-Resolution Transcriptome Profiles Reveal Uncharacterized Modularity of Wood Formation in Populus tremula[OPEN]
David Sundell (2017)
ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death
L. Muñiz (2008)
Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls
S. E. Marcus (2008)
Genome-wide comparison of two
T. Zhao (2011)
Wood Chemistry and Biotechnology (Pulp and Paper Chemistry and Technology)
M Ek (2009)
Molecular cloning and characterization
T. Demura (1993)
ZEN1 Is a Key Enzyme in the Degradation of Nuclear DNA during Programmed Cell Death of Tracheary Elements Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006411.
J. Ito (2002)
A unique program for cell death in xylem fibers of Populus stem.
C. Courtois-Moreau (2009)
An extended set of monoclonal antibodies to pectic homogalacturonan.
Yves Verhertbruggen (2009)
Comprehensive Compositional Analysis of Plant Cell Walls (Lignocellulosic biomass) Part II: Carbohydrates
Cliff E. Foster (2010)
J. S. Christensen (1970)
Programmed cell death of tracheary elements as a paradigm
H. Fukuda (2000)
The structure, function, and biosynthesis
D. Mohnen (2009)
Revolutionary Times in Our Understanding of Cell Wall Biosynthesis and Remodeling in the Grasses1
G. Fincher (2009)
Emerging strategies of lignin engineering and degradation for cellulosic biofuel production.
J. Weng (2008)
Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus.
C. MacMillan (2010)
Genome-wide analysis of the lignin toolbox of Eucalyptus grandis.
V. Carocha (2015)
Tensional stress generation
T. A. Gorshkova (2012)
Localization of pectic galactan
L. Jones (1997)
TRICHOME BIREFRINGENCE and Its Homolog AT5G01360 Encode Plant-Specific DUF231 Proteins Required for Cellulose Biosynthesis in Arabidopsis1[W][OA]
Volker Bischoff (2010)
Laccase from Sycamore Maple (Acer pseudoplatanus) Polymerizes Monolignols.
R. Sterjiades (1992)
Cooperative lignification of xylem tracheary elements
Henrik Serk (2015)
XYLOGENESIS: INITIATION, PROGRESSION, AND CELL DEATH.
H. Fukuda (1996)
Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot
M. Smallwood (2004)
Extracellular laccases and peroxidases from sycamore maple (Acer pseudoplatanus) cell-suspension cultures
R. Sterjiades (2004)
Programmed cell death during vascular system formation
H. Fukuda (1997)
The structure, function, and biosynthesis of plant cell wall pectic polysaccharides.
K. Caffall (2009)
Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition.
E. Mellerowicz (2012)
Novel vascular cell-specific genes
T. Demura (1994)
Populus: Arabidopsis for forestry
G. Taylor (2002)
This paper is referenced by
From the Soft to the Hard: Changes in Microchemistry During Cell Wall Maturation of Walnut Shells
Nannan Xiao (2020)
Comparative Transcriptomic Analysis of the Development of Sepal Morphology in Tomato (Solanum Lycopersicum L.)
J. Liu (2020)
Allies or Enemies: The Role of Reactive Oxygen Species in Developmental Processes of Black Cottonwood (Populus trichocarpa)
Katarzyna Marzec-Schmidt (2020)