Single-cell transcriptomics unveils xylem cell development and evolution
Ontology highlight
ABSTRACT: The plant xylem tissue is responsible for water transportation, mechanical support and lateral growth, and can be utilized as wood. The seed plant xylem has a radial system composed of ray parenchyma cells and an axial system of fusiform cells, including tracheids in gymnosperms and vessel elements and libriform fibers in angiosperms. Little is known about the developmental programs and evolutionary relationships of these xylem cell types. Here we show that the radial and axial systems of stem-differentiating xylem are differentially conserved across four divergent woody angiosperms. Through transcriptomic profiling of single cells and cell-type regions isolated by laser capture microdissection, we identified cell types corresponding to single-cell clusters in Populus trichocarpa. Cross-species analyses of single-cell trajectories demonstrated highly conserved development in ray lineages across angiosperms. While the core eudicots P. trichocarpa and Eucalyptus grandis share nearly identical fusiform cell lineages, the tracheids in the basal eudicot Trochodendron aralioides, an evolutionarily reversed character, exhibited an expression pattern highly similar to that of vessel elements. It suggests that water transportation, instead of mechanical support, is the dominant feature of tracheary elements. Furthermore, we found that the more basal angiosperm Liriodendron chinense has a distinct fusiform lineage. This evo-developmental framework of xylem cell lineages provides a comprehensive understanding of the formation of the most abundant tissue on Earth.
ORGANISM(S): Liriodendron chinense Trochodendron aralioides Eucalyptus grandis Populus trichocarpa
Project description:PtrHSFB3-1 and PtrMYB092 are xylem specific genes in xylem of P. trichocarpa, and their expression levels are down regulated most significantly in tension wood. These two transcription factors were transiently overexpressed in stem differentiating xylem (SDX) of P. trichocarpa , and transcriptomic sequencing was performed to identify the regulatory effects of the two transcription factors on wood formation related genes.
Project description:Global gene expression pattern of phloem and xylem tissue were determined using a Nimblegen microarray based on JGI v1.1 gene models. Xylem tissue from both Populus trichocarpa Nisqually-1 and Populus tremula X Populus alba hybrid were used in the study.
Project description:Wood in conifers is mainly composed of tracheids. Some taxa, such as Pinus, present tracheids also in the rays, but are axial tracheids which constitute the vast majority of secondary xylem. Nevertheless, radial and axial parenchyma surrounding constitutive and traumatic resin ducts is known to serve as crucial reserve storage. These reserves are mobilized in response to traumatism, insect and pathogen attacks and defoliation, allowing the synthesis of resin, healing and, in few taxa, even resprouting. However, due to the low proportion of parenchymatic cells in secondary xylem relevant genes involved in their differentiation may have been missed in studies of transcriptomics of conifer wood formation. In this study we have used Pinus canariensis as a model species, given its comparatively high proportion of axial parenchyma. We have prepared two normalized libraries from its cambial zone, covering early- and late-wood differentiation. We have de novo assembled a transcriptome, and have analyzed the transcriptional profiles during the growing season, getting a more complete picture of wood formation in conifers. SUBMITTER_CITATION: Chano, V., López de Heredia, U., Collada, C., et al. (2017). Transcriptomic analysis of juvenile wood formation during the growing season in Pinus canariensis. Holzforschung, 0(0), pp. -. Retrieved 8 Aug. 2017, from doi:10.1515/hf-2017-0014
Project description:Global gene expression pattern of phloem and xylem tissue were determined using a Nimblegen microarray based on JGI v1.1 gene models. Xylem tissue from both Populus trichocarpa Nisqually-1 and Populus tremula X Populus alba hybrid were used in the study. Xylem tissue: Three biological replicates were hybridized to three arrays Phloem tissue: Two biological replicates were hybridized to two arrays
Project description:Tangential sections of 30 µm thickness were taken across the secondary phloem and developing secondary xylem, sections were then pooled to represent the tissues from specific developmental stages. Phloem (P) comprises 3 sections, the cambium (C) - 2 sections, the radial expansion zone (E) - 4 sections, the first to third xylem development zones (X1-X3) - 3 sections each, and the forth to sixth xylem development zones (X4-X6) - 6 sections each.
Project description:Seasonal nitrogen (N) storage and reuse is important to the N-use efficiency of temperate deciduous trees. In poplar, bark storage proteins (BSPs) accumulate in protein storage vacuoles of the bark parenchyma and xylem ray cells in the fall. During spring growth, N from stored BSPs is remobilized and utilized by growing shoots. The goal of this study is to investigate global gene expression changes in the bark during BSP remobilization and shoot regrowth under long-day conditions. Long-day (LD) grown poplar (Populus trichocarpa, Nisqually-1) plants were transferred to short-day (SD) for 8 weeks at 20°C followed by an addition 12 weeks of SD at 10°C (day) and 4°C (night). Following this treatment plants were then moved to LD and 20°C for 3 weeks for regrowth. Bark samples were collected from plants released from dormancy just prior to transfer to LD and at weekly intervals for 3 weeks after exposure to LD at 20°C.
Project description:(paper abstract) Wood is a renewable resource that serves as a sustainable raw material for energy, fuels and materials. A basic understanding of the cambial meristem and the origin of wood cells is critical for forest tree molecular breeding to increase the availability of woody raw materials. Gene expression per cell type in the cambium of poplar (Populus trichocarpa x P. deltoïdes cultivar Boelare) was investigated using poplar microarray. Cells were hand microdissected from lyophilized sections of vascular cambial zone sampled in growing poplar. Two cell types were isolated, fusiform cambial cells (FCCs) and ray cambial cells (RCCs). Results showed about one thousand genes differentially expressed per cell type. Microarray expression results were validated by a second cell sampling used for reverse northern dot blot and RT-PCR analysis. RCCs revealed specific photosynthetic competences involving at least 35 genes of the photosystems. RCCs revealed also a marked difference for intercellular transport involving notably aquaporin genes. Distinct classes of cell-wall related genes were detected in RCCs and FCCs. A candidate xyloglucan endotransglycosylase showed to be upregulated and highly expressed in FCCs and an extensin family gene was also very highly expressed in these cells. A candidate polygalacturonase was strikingly expressed specifically in RCCs. A marked expression of cytoskeleton genes was also reported for FCCs where profilin family genes were very highly expressed. Related to cell signaling and regulation, one of the most intriguing result was the observation of LAX1 gene specificity in FCCs whereas PIN genes were expressed in both cell types.
Project description:The synarcual is a specialized adaptation of the anterior axial skeleton comprising a putatively fused array of vertebral elements characteristic of jawed vertebrate (gnathostome) clades such as batoid and chimaeroid chondrichthyans, as well as a fossil group known as the placoderms. Placoderms represent the phylogenetically most basal jawed vertebrates and the presence of a synarcual in these and chondrichthyans may suggest a conserved vertebral type for jawed vertebrates, predating the divergence of stem and crown gnathostomes. Alternatively, synarcuals may have evolved independently in these lineages, exhibiting a remarkable case of morphological convergence. We investigated the early development of the cervicothoracic synarcual of an emerging model chondrichthyan, the Little skate Leucoraja erinacea, by combining x-ray computed tomography, classical histology, and a de novo transcriptome assembly for two developmental stages of the skate synarcual and post-synarcual axial skeletal elements.
Project description:P. maximowiczii × P. trichocarpa and P. nigra × P. maximowiczii plants were grown in the field, each pure and mixed with Robinia pseudoacacia, at two locations differing in soil nutrient levels. After 3 years of growing, samples of developing xylem were harvested and analyzed by RNA-seq.
Project description:<p>Wood, or secondary xylem, is the product of xylogenesis, a developmental process that begins with the proliferation of cambial derivatives and ends with mature xylem fibers and vessels with lignified secondary cell walls. Fully mature xylem has undergone a series of cellular processes, including cell division, cell expansion, secondary wall formation, lignification and programmed cell death. A complex network of interactions between transcriptional regulators and signal transduction pathways controls wood formation. However, the role of metabolites during this developmental process has not been comprehensively characterized. To evaluate the role of metabolites during wood formation, we performed a high spatial resolution metabolomics study of the wood-forming zone of Populus tremula, including laser dissected aspen ray and fiber cells. We show that metabolites show specific patterns within the wood-forming zone, following the differentiation process from cell division to cell death. The data from profiled laser dissected aspen ray and fiber cells suggests that these two cell types host distinctly different metabolic processes. Furthermore, by integrating previously published transcriptomic and proteomic profiles generated from the same trees, we provide an integrative picture of molecular processes, for example, deamination of phenylalanine during lignification is of critical importance for nitrogen metabolism during wood formation.</p><p><br></p><p><strong>UPLC-MS assay of Wood fibre and ray cell tissue</strong> is reported in the current study <strong>MTBLS1831</strong>.</p><p><strong>UPLC-MS assay of Wood ring and extraxylary tissue</strong> is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1797' rel='noopener noreferrer' target='_blank'><strong>MTBLS1797</strong></a>.</p><p><strong>GC-MS assay of Wood ring and extraxylary tissue</strong> is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1796' rel='noopener noreferrer' target='_blank'><strong>MTBLS1796</strong></a>.</p>