Abstract
Xylogenesis involves successive developmental processes - cambial division, cell expansion
and differentiation, cell death - each occurring along a gradient from the cambium
to the pith of the stem. Taking advantage of the high level of organisation of wood
tissues, we isolated cambial zone (CZ), differentiating xylem (DX) and mature xylem
(MX) from both tension wood (TW) and opposite wood (OW) of bent poplars. Four different
cDNA libraries were then constructed and used to generate 10 062 EST, reflecting the
genes expressed in the different wood tissues. For the most abundant clusters, the
EST distributions were compared between libraries in order to identify genes specific
or over-represented at some specific developmental stages. They clearly showed a developmental
shift between CZ and DX, whereas there is a continuity of development between DX and
MX. CZ was mainly characterized by clusters of genes involved in cell cycle, protein
synthesis and fate. Interestingly, two clusters with no assigned function were found
specific to the cambial zone. In DX and MX, clusters were mostly involved in methylation
of lignin precursors and microtubule cytoskeleton. In addition, in DX, EST from TW
and OW were compared: five clusters of arabinogalactan proteins, one for sucrose synthase
and one for fructokinase were specific or over-represented in TW. Moreover, a putative
transcription factor and a cluster of unknown function were also identified in DX-TW.
The informative comparison of multiple libraries prepared from wood tissues led to
the identification of genes - some with still unknown functions - putatively involved
in xylogenesis and tension wood formation.
Key words
EST - tension wood - cambium - xylem - poplar - gene expression
References
- 1
Allona I., Quinn M., Shoop E., Swope K., St-Cyr S., Carlis J., Riedl J., Retzel E.,
Campbell M. M., Sederoff R., Whetten R. W..
Analysis of xylem formation in pine by cDNA sequencing.
Proceedings of the National Academy of Science USA.
(1998);
95
9693-9698
- 2
Audic S., Claverie J. M..
The significance of digital gene expression profiles.
Genome Research.
(1997);
7
986-995
- 3
Baltz R., Domon C., Pillay D. T., Steinmetz A..
Characterization of a pollen-specific cDNA from sunflower encoding zinc finger protein.
Plant Journal.
(1992);
2
713-721
- 4
Bhalerao R., Keskitalo J., Sterky F., Erlandsson R., Björkbacka H., Birve S. J., Karlsson J.,
Gardeström P., Gustafsson P., Lundeberg J., Jansson S..
Gene expression in autumn leaves.
Plant Physiology.
(2003);
131
430-442
- 5
Boerjan W., Ralph J., Baucher M..
Lignin biosynthesis.
Annual Review of Plant Biology.
(2003);
54
519-546
- 6
Chaffey N., Barlow P., Sundberg B..
Understanding the role of the cytoskeleton in wood formation in angiosperm trees:
hybrid aspen (Populus tremula × P. tremuloides) as the model species.
Tree Physiology.
(2002);
22
239-249
- 7
Cyr R. J..
Microtubules in plant morphogenesis: role of the cortical array.
Annual Review of Cell Biology.
(1994);
10
153-180
- 8
Gaspar Y., Johnson K. L., McKenna J. A., Bacic A., Schultz C. J..
The complex structures of arabinogalactan-proteins and the journey towards understanding
function.
Plant Molecular Biology.
(2001);
47
161-176
- 9
Haigler C. H., Ivanova-Datcheva M., Hogan P. S., Salnikov V. V., Hwang S., Martin K.,
Delmer D. P..
Carbon partitioning to cellulose synthesis.
Plant Molecular Biology.
(2001);
47
29-51
- 10
Hertzberg M., Aspeborg H., Schrader J., Andersson A., Erlandsson R., Blomqvist K.,
Bhalerao R., Uhlén M., Teeri T. T., Lundeberg J., Sundberg B., Nilsson P., Sandberg G..
A transcriptional roadmap to wood formation.
Proceedings of the National Academy of Science USA.
(2001);
98
14732-14737
- 11
John M. E., Crow L. J..
Gene expression in cotton (Gossypium hirsutum L.) fiber: cloning of the mRNAs.
Proceedings of the National Academy of Science USA.
(1992);
89
5769-5773
- 12
John M. E..
Structural characterization of genes corresponding to cotton fiber mRNA E6: reduced
E6 protein in transgenic plants by antisense gene.
Plant Molecular Biology.
(1996);
30
297-306
- 13
Jourez B..
Le bois de tension 1. Définition et distribution dans l'arbre.
Biotechnol. Agron. Soc. Environ..
(1997);
1
100-112
- 14
Karlin S., Altschul S. F..
Methods for assessing the statistical significance of molecular sequence features
by using general scoring schemes.
Proceedings of the National Academy of Science USA.
(1990);
87
2264-2268
- 15
Kirst M., Johnson A. F., Baucom C., Ulrich E., Hubbard K., Staggs R., Paule C., Retzel E.,
Whetten R., Sederoff R..
Apparent homology of expressed genes from wood-forming tissues of loblolly pine (Pinus taeda L.) with Arabidopsis thaliana.
.
Proceedings of the National Academy of Science USA.
(2003);
100
7383-7388
- 16
Kohler A., Delaruelle C., Martin D., Encelot N., Martin F..
The poplar root transcriptome: analysis of 7000 expressed sequence tags.
FEBS Letters.
(2003);
542
37-41
- 17 Larson P. R.. The Vascular Cambium. Berlin; Springer-Verlag (1994): 99-154
- 18
Ludevid D., Höfte H., Himelblau E., Chrispeels M. J..
The expression pattern of the tonoplast intrinsic protein γ-TIP in Arabidopsis thaliana is correlated with cell enlargement.
Plant Physiology.
(1992);
100
1633-1639
- 19
Majewska-Sawka A., Nothnagel E. A..
The multiple roles of arabinogalactan proteins in plant development.
Plant Physiology.
(2000);
122
3-9
- 20
Maurel C., Chrispeels M. J..
Aquaporins. A molecular entry into plant water relations.
Plant Physiology.
(2001);
125
135-138
- 21
Mellerowicz E. J., Baucher M., Sundberg B., Boerjan W..
Unravelling cell wall formation in the woody dicot stem.
Plant Molecular Biology.
(2001);
47
239-274
- 22
Miller R. T., Christoffels A. G., Gopalakrishnan C., Burke J., Ptitsyn A. A., Broveak T. R.,
Hide W. A..
A comprehensive approach to clustering of expressed human sequence: the sequence tag
alignment and consensus knowledge base.
Genome Research.
(1999);
9
1143-1155
- 23
Prodhan A. K. M. A., Funada R., Ohtani J., Abe H., Fukazawa K..
Orientation of microfibrils and microtubules in developing tension-wood fibres of
Japanese ash (Fraxinus mandshurica var. japonica).
.
Planta.
(1995);
196
577-585
- 24
Ronning C. M., Stegalkina S. S., Ascenzi R. A., Bougri O., Hart A. L., Utterbach T. R.,
Vanaken S. E., Riedmuller S. B., White J. A., Cho J., Pertea G. M., Lee Y., Karamycheva S.,
Sultana R., Tsai J., Quackenbush J., Griffiths H. M., Restrepo S., Smart C. D., Fry W. E.,
Van Der Hoeven R., Tanksley S., Zhang P., Jin H., Yamamoto M. L., Baker B. J., Buell C. R..
Comparative analyses of potato expressed sequence tag libraries.
Plant Physiology.
(2003);
131
419-429
- 25
Schultz C. J., Johnson K. L., Currie G., Bacic A..
The classical arabinogalactan protein gene family of Arabidopsis.
.
Plant Cell.
(2000);
12
1751-1767
- 26
Scurfield G..
Reaction wood: its structure and function.
Science.
(1973);
179
647-655
- 27
Sterky F., Regan S., Karlsson J., Hertzberg M., Rohde A., Holmberg A., Amini B., Bhalerao R.,
Larsson M., Villaroel R., Van Montagu M., Sandberg G., Olsson O., Teeri T. T., Boerjan W.,
Gustafsson P., Uhlén M., Sundberg B., Lundeberg J..
Gene discovery in the wood-forming tissues of poplar: Analysis of 5692 expressed sequence
tags.
Proceedings of the National Academy of Science USA.
(1998);
95
13330-13335
- 28
Thomma B. P. H. J., Cammue B. P. A., Thevissen K..
Plant defensins.
Planta.
(2002);
216
193-202
- 29
Vander Mijnsbrugge K., Meyermans H., Van Montagu M., Bauw G., Boerjan W..
Wood formation in poplar: identification, characterization, and seasonal variation
of xylem proteins.
Planta.
(2000);
210
589-598
- 30
Whetten R., Sun Y. H., Zhang Y., Sederoff R. R..
Functional genomics and cell wall biosynthesis in loblolly pine.
Plant Molecular Biology.
(2001);
47
275-291
- 31
Wu L., Joshi C. P., Chiang V. L..
A xylem-specific cellulose synthase gene from aspen (Populus tremuloides) is responsive to mechanical stress.
Plant Journal.
(2000);
6
495-502
- 32
Wullschleger S. D., Jansson S., Taylor G..
Genomics and forest biology: Populus emerges as the perennial favorite.
Plant Cell.
(2002);
14
2651-2655
- 33
Zhang Y., Brown G., Whetten R., Loopstra C. A., Neale D., Kieliszewski M. J., Sederoff R. R..
An arabinogalactan protein associated with secondary cell wall formation in differentiating
xylem of loblolly pine.
Plant Molecular Biology.
(2003);
52
91-102
A. Déjardin
Unité Amélioration, Génétique et Physiologie Forestières
INRA Orléans
Avenue de la Pomme de Pin
BP 20619 Ardon
45166 Olivet Cédex
France
eMail: dejardin@orleans.inra.fr
Section Editor: H. Rennenberg