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.
Highlights
Wood provides abundant biomass and important biomaterials for renewable sources and industrial products around the world
Osmotin-like proteins (OLPs) comprise a group of 24–26-kD proteins belonging to the pathogenesisrelated protein 5 (PR-5) family that were originally discovered in tobacco cells (Nicotiana tabacum L. var Wisconsin 38) under osmotic stress conditions [6]
Previous studies have identified that osmotin or OLPs accumulate in response to biotic and abiotic stresses, such as drought, salt, or cold stress, and possible mechanisms underlying the defense function of OLPs against biotic and abiotic stresses were proposed [11,12]
Summary
Wood provides abundant biomass and important biomaterials for renewable sources and industrial products around the world. The functions of a large number of genes related to wood traits have not been discovered and the molecular mechanisms of secondary wall thickening and secondary xylem formation in forest trees remain largely unknown [3,4,5]. Elucidation of the mechanisms underlying gene regulation in xylem formation and secondary cell wall synthesis during wood development would be instrumental in providing the molecular basis and technical approaches for genetic improvement of the wood properties of forest trees. The rice osmotin protein gene OsOSM1 is mainly expressed in the leaf sheath at the booting stage and is associated with development [8]. Involved in stem vascular tissue development, hybrid poplar (Populus trichocarpa × P. deltoides) TLP1, which is homologous to OLPs, is mainly expressed in vascular tissues of stems, petioles, and midveins [10]. Osmotins exhibit antifungal activity by inhibiting spore germination and lysis, hyphal growth, and spore viability [15]
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