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A transcriptional roadmap to wood formation.

ABSTRACT: The large vascular meristem of poplar trees with its highly organized secondary xylem enables the boundaries between different developmental zones to be easily distinguished. This property of wood-forming tissues allowed us to determine a unique tissue-specific transcript profile for a well defined developmental gradient. RNA was prepared from different developmental stages of xylogenesis for DNA microarray analysis by using a hybrid aspen unigene set consisting of 2,995 expressed sequence tags. The analysis revealed that the genes encoding lignin and cellulose biosynthetic enzymes, as well as a number of transcription factors and other potential regulators of xylogenesis, are under strict developmental stage-specific transcriptional regulation.

SUBMITTER: Hertzberg M

PROVIDER: S-EPMC64750 | biostudies-literature | 2001 Dec

REPOSITORIES: biostudies-literature

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A transcriptional roadmap to wood formation.

Hertzberg M M Aspeborg H H Schrader J J Andersson A A Erlandsson R R Blomqvist K K Bhalerao R R Uhlén M M Teeri T T TT Lundeberg J J Sundberg B B Nilsson P P Sandberg G G

Proceedings of the National Academy of Sciences of the United States of America 20011127 25

The large vascular meristem of poplar trees with its highly organized secondary xylem enables the boundaries between different developmental zones to be easily distinguished. This property of wood-forming tissues allowed us to determine a unique tissue-specific transcript profile for a well defined developmental gradient. RNA was prepared from different developmental stages of xylogenesis for DNA microarray analysis by using a hybrid aspen unigene set consisting of 2,995 expressed sequence tags. ...[more]

PMID: 11724959

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Project description:Enormous distinctions of the stem structure and cell types between gymnosperms and angiosperms tree species are expected to cause quite different wood physical and mechanical attributes, however, the molecular mechanisms underlying the differing wood morphology are still unclear. In this study, we compared the transcriptomes obtained by RNA-Seq between Populus alba × P. glandulosa clone 84K, and Larix kaempferi (Lamb.) Carr trees. Available genome resource served as reference for P. alba × P. glandulosa and the Iso-Seq results of a three-tissues mixture (xylem, phloem, and leaf) were used as the reference for L. kaempferi to compare the xylem-specifically expressed genes and their alternative splicing model. Through screening, we obtained 13,907 xylem-specifically expressed genes (5,954 up-regulated, 7,953 down-regulated) in the xylem of P. alba × P. glandulosa, and 2,596 xylem-specifically expressed genes (1,648 up-regulated, 948 down-regulated) in the xylem of L. kaempferi. From the GO and KEGG analyses, some genes associated with two wood formation-related pathways, namely those for phenylpropanoid biosynthesis, and starch and sucrose metabolism, were successfully screened. Then the distributions and gene expression models between P. alba × P. glandulosa and L. kaempferi in those pathways were compared, which suggested differential wood formation processes between the angiosperm and gymnosperm trees. Furthermore, a Weight Gene Co-expression Network Analysis (WGCNA) for total xylem-specifically expressed genes in two species was conducted, from which wood formation-related modules were selected to build a co-expression network for the two tree species. The genes within this co-expression network showed different co-expression relationships between the angiosperm and gymnosperm woody species. Comparing the alternative splicing events for wood formation-related genes suggests a different post-transcriptional regulation process exists between the angiosperm and gymnosperm trees. Our research thus provides the foundation for the in-depth investigation of different wood formation mechanisms of angiosperm and gymnosperm species.

Project description:Thickening of tree stems is the result of secondary growth, accomplished by the meristematic activity of the vascular cambium. Secondary growth of the stem entails developmental cascades resulting in the formation of secondary phloem outwards and secondary xylem (i.e., wood) inwards of the stem. Signaling and transcriptional reprogramming by the phytohormone ethylene modifies cambial growth and cell differentiation, but the molecular link between ethylene and secondary growth remains unknown. We addressed this shortcoming by analyzing expression profiles and co-expression networks of ethylene pathway genes using the AspWood transcriptome database which covers all stages of secondary growth in aspen (Populus tremula) stems. ACC synthase expression suggests that the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is synthesized during xylem expansion and xylem cell maturation. Ethylene-mediated transcriptional reprogramming occurs during all stages of secondary growth, as deduced from AspWood expression profiles of ethylene-responsive genes. A network centrality analysis of the AspWood dataset identified EIN3D and 11 ERFs as hubs. No overlap was found between the co-expressed genes of the EIN3 and ERF hubs, suggesting target diversification and hence independent roles for these transcription factor families during normal wood formation. The EIN3D hub was part of a large co-expression gene module, which contained 16 transcription factors, among them several new candidates that have not been earlier connected to wood formation and a VND-INTERACTING 2 (VNI2) homolog. We experimentally demonstrated Populus EIN3D function in ethylene signaling in Arabidopsis thaliana. The ERF hubs ERF118 and ERF119 were connected on the basis of their expression pattern and gene co-expression module composition to xylem cell expansion and secondary cell wall formation, respectively. We hereby establish data resources for ethylene-responsive genes and potential targets for EIN3D and ERF transcription factors in Populus stem tissues, which can help to understand the range of ethylene targeted biological processes during secondary growth.

Dataset Information

A transcriptional roadmap to wood formation.

Publications

A transcriptional roadmap to wood formation.

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