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The Osmotin-Like Protein Gene PdOLP1 Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar.

ABSTRACT: 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.

SUBMITTER: Li S

PROVIDER: S-EPMC7312728 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundNitrogen 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.ResultsTranscriptome 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.ConclusionThis 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.

Project description:The secondary cell wall (SCW) in the xylem is one of the largest sink organs of carbon in woody plants, and is considered a promising sustainable bioresource for biofuels and biomaterials. To enhance SCW formation in poplar (Populus sp.) xylem, we developed a self-reinforced system of SCW-related transcription factors from Arabidopsis thaliana, involving VASCULAR-RELATED NAC-DOMAIN7 (VND7), SECONDARY WALL-ASSOCIATED NAC-DOMAIN PROTEIN 1/NAC SECONDARY WALL THICKENING-PROMOTING FACTOR3 (SND1/NST3), and MYB46. In this system, these transcription factors were fused with the transactivation domain VP16 and expressed under the control of the Populus trichocarpa CesA18 (PtCesA18) gene promoter, creating the chimeric genes PtCesA18pro::AtVND7:VP16, PtCesA18pro::AtSND1:VP16, and PtCesA18pro::AtMYB46:VP16. The PtCesA18 promoter is active in tissues generating SCWs, and can be regulated by AtVND7, AtSND1, and AtMYB46; thus, the expression levels of PtCesA18pro::AtVND7:VP16, PtCesA18pro::AtSND1:VP16, and PtCesA18pro::AtMYB46:VP16 are expected to be boosted in SCW-generating tissues. In the transgenic hybrid aspens (Populus tremula × tremuloides T89) expressing PtCesA18pro::AtSND1:VP16 or PtCesA18pro::AtMYB46:VP16 grown in sterile half-strength Murashige and Skoog growth medium, SCW thickening was significantly enhanced in the secondary xylem cells, while the PtCesA18pro::AtVND7:VP16 plants showed stunted xylem formation, possibly because of the enhanced programmed cell death (PCD) in the xylem regions. After acclimation, the transgenic plants were transferred from the sterile growth medium to pots of soil in the greenhouse, where only the PtCesA18pro::AtMYB46:VP16 aspens survived. A nuclear magnetic resonance footprinting cell wall analysis and enzymatic saccharification analysis demonstrated that PtCesA18pro::AtMYB46:VP16 influences cell wall properties such as the ratio of syringyl (S) and guaiacyl (G) units of lignin, the abundance of the lignin β-aryl ether and resinol bonds, and hemicellulose acetylation levels. Together, these data indicate that we have created a self-reinforced system using SCW-related transcription factors to enhance SCW accumulation.

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The Osmotin-Like Protein Gene PdOLP1 Is Involved in Secondary Cell Wall Biosynthesis during Wood Formation in Poplar.

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