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Nitrogen-driven stem elongation in poplar is linked with wood modification and gene clusters for stress, photosynthesis and cell wall formation.

ABSTRACT: BACKGROUND:Nitrogen is an important nutrient, often limiting plant productivity and yield. In poplars, woody crops used as feedstock for renewable resources and bioenergy, nitrogen fertilization accelerates growth of the young, expanding stem internodes. The underlying molecular mechanisms of nitrogen use for extension growth in poplars are not well understood. The aim of this study was to dissect the nitrogen-responsive transcriptional network in the elongation zone of Populus trichocarpa in relation to extension growth and cell wall properties. RESULTS:Transcriptome analyses in the first two internodes of P. trichocarpa stems grown without or with nitrogen fertilization (5 mM NH4NO3) revealed 1037 more than 2-fold differentially expressed genes (DEGs). Co-expression analysis extracted a network containing about one-third of the DEGs with three main complexes of strongly clustered genes. These complexes represented three main processes that were responsive to N-driven growth: Complex 1 integrated growth processes and stress suggesting that genes with established functions in abiotic and biotic stress are also recruited to coordinate growth. Complex 2 was enriched in genes with decreased transcript abundance and functionally annotated as photosynthetic hub. Complex 3 was a hub for secondary cell wall formation connecting well-known transcription factors that control secondary cell walls with genes for the formation of cellulose, hemicelluloses, and lignin. Anatomical and biochemical analysis supported that N-driven growth resulted in early secondary cell wall formation in the elongation zone with thicker cell walls and increased lignin. These alterations contrasted the N influence on the secondary xylem, where thinner cell walls with lower lignin contents than in unfertilized trees were formed. CONCLUSION:This study uncovered that nitrogen-responsive elongation growth of poplar internodes is linked with abiotic stress, suppression of photosynthetic genes and stimulation of genes for cell wall formation. Anatomical and biochemical analysis supported increased accumulation of cell walls and secondary metabolites in the elongation zone. The finding of a nitrogen-responsive cell wall hub may have wider implications for the improvement of tree nitrogen use efficiency and opens new perspectives on the enhancement of wood composition as a feedstock for biofuels.

SUBMITTER: Euring D

PROVIDER: S-EPMC4302602 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Nitrogen-driven stem elongation in poplar is linked with wood modification and gene clusters for stress, photosynthesis and cell wall formation.

Euring Dejuan D Bai Hua H Janz Dennis D Polle Andrea A

BMC plant biology 20141230

<h4>Background</h4>Nitrogen is an important nutrient, often limiting plant productivity and yield. In poplars, woody crops used as feedstock for renewable resources and bioenergy, nitrogen fertilization accelerates growth of the young, expanding stem internodes. The underlying molecular mechanisms of nitrogen use for extension growth in poplars are not well understood. The aim of this study was to dissect the nitrogen-responsive transcriptional network in the elongation zone of Populus trichocar ...[more]

PMID: 25547614

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Project description:BackgroundCotton fiber is a single cell that arises from the epidermis of ovule. It is not only a main economic product of cotton, but an ideal material for studying on the growth and development of plant cell. Our previous study indicated that phytosterol content and the ratio of campesterol to sitosterol fluctuated regularly in cotton fiber development. However, what effects of modified phytosterol content and composition on the growth and development of cotton fiber cell is unknown. In this study, we overexpressed the GhSMT2-1, a cotton homologue of sterol C-24 methyltransferase 2 gene in transgenic upland cotton plants to modify phytosterol content and composition in fiber cells and investigated the changes on fiber elongation and secondary cell wall deposition.ResultsGhSMT2-1 overexpression led to changes of phytosterol content and the ratio of campesterol to sitosterol in fiber cell. At the rapid elongation stage of fiber cell, total phytosterol and sitosterol contents were increased while campesterol content was decreased in transgenic fibers when compared to control fibers. Accordingly, the ratio of campesterol to sitosterol declined strikingly. Simultaneously, the transgenic fibers were shorter and thicker than control fibers. Exogenous application of sitosterol or campesterol separately inhibited control fiber cell elongation in cotton ovule culture system in vitro. In addition, campesterol treatment partially rescued transgenic fiber elongation.ConclusionThese results elucidated that modification of phytosterol content and composition influenced fiber cell elongation and secondary cell wall formation. High sitosterol or low ratio of campesterol to sitosterol suppresses fiber elongation and/or promote secondary cell wall deposition. The roles of sitosterol and campesterol were discussed in fiber cell development. There might be a specific ratio of campesterol to sitosterol in different developmental stage of cotton fibers, in which GhSMT2-1 play an important role. Our study, at a certain degree, provides novel insights into the regulatory mechanisms of fiber cell development.

Project description:Osmotin-like proteins (OLPs) mediate defenses against abiotic and biotic stresses and fungal pathogens in plants. However, no OLPs have been functionally elucidated in poplar. Here, we report an osmotin-like protein designated PdOLP1 from Populus deltoides (Marsh.). Expression analysis showed that PdOLP1 transcripts were mainly present in immature xylem and immature phloem during vascular tissue development in P. deltoides. We conducted phenotypic, anatomical, and molecular analyses of PdOLP1-overexpressing lines and the PdOLP1-downregulated hybrid poplar 84K (Populus alba × Populus glandulosa) (Hybrid poplar 84K PagOLP1, PagOLP2, PagOLP3 and PagOLP4 are highly homologous to PdOLP1, and are downregulated in PdOLP1-downregulated hybrid poplar 84K). The overexpression of PdOLP1 led to a reduction in the radial width and cell layer number in the xylem and phloem zones, in expression of genes involved in lignin biosynthesis, and in the fibers and vessels of xylem cell walls in the overexpressing lines. Additionally, the xylem vessels and fibers of PdOLP1-downregulated poplar exhibited increased secondary cell wall thickness. Elevated expression of secondary wall biosynthetic genes was accompanied by increases in lignin content, dry weight biomass, and carbon storage in PdOLP1-downregulated lines. A PdOLP1 coexpression network was constructed and showed that PdOLP1 was coexpressed with a large number of genes involved in secondary cell wall biosynthesis and wood development in poplar. Moreover, based on transcriptional activation assays, PtobZIP5 and PtobHLH7 activated the PdOLP1 promoter, whereas PtoBLH8 and PtoWRKY40 repressed it. A yeast one-hybrid (Y1H) assay confirmed interaction of PtoBLH8, PtoMYB3, and PtoWRKY40 with the PdOLP1 promoter in vivo. Together, our results suggest that PdOLP1 is a negative regulator of secondary wall biosynthesis and may be valuable for manipulating secondary cell wall deposition to improve carbon fixation efficiency in tree species.

Dataset Information

Nitrogen-driven stem elongation in poplar is linked with wood modification and gene clusters for stress, photosynthesis and cell wall formation.

Publications

Nitrogen-driven stem elongation in poplar is linked with wood modification and gene clusters for stress, photosynthesis and cell wall formation.

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