Single-cell transcriptomics unveils xylem cell development and evolution

Abstract

Background Xylem, the most abundant tissue on Earth, is responsible for lateral growth in plants. Typical xylem has a radial system composed of ray parenchyma cells and an axial system of fusiform cells. In most angiosperms, fusiform cells comprise vessel elements for water transportation and libriform fibers for mechanical support, while both functions are performed by tracheids in other vascular plants such as gymnosperms. Little is known about the developmental programs and evolutionary relationships of these xylem cell types. Results Through both single-cell and laser capture microdissection transcriptomic profiling, we determine the developmental lineages of ray and fusiform cells in stem-differentiating xylem across four divergent woody angiosperms. Based on cross-species analyses of single-cell clusters and overlapping trajectories, we reveal highly conserved ray, yet variable fusiform, lineages across angiosperms. Core eudicots Populus trichocarpa and Eucalyptus grandis share nearly identical fusiform lineages, whereas the more basal angiosperm Liriodendron chinense has a fusiform lineage distinct from that in core eudicots. The tracheids in the basal eudicot Trochodendron aralioides, an evolutionarily reversed trait, exhibit strong transcriptomic similarity to vessel elements rather than libriform fibers. Conclusions This evo-devo framework provides a comprehensive understanding of the formation of xylem cell lineages across multiple plant species spanning over a hundred million years of evolutionary history.

Merit of integrating in situ transcriptomics and anatomical information for cell annotation and lineage construction in single-cell analyses of Populus

“…However, many studies have reported the discrepancy on tissue development and orthologous gene expression patterns between Arabidopsis and other species [ 4 , 5 ]. Take xylem development for example, Arabidopsis lacks one xylem cell type (ray parenchyma) and the development of another xylem cell type (libriform fiber) is incomplete with respect to woody eudicots [ 6 ]. The expression patterns of many genes involved in xylem development are also different between Arabidopsis and other woody species, such as Populus [ 4 – 6 ].…”

“…Take xylem development for example, Arabidopsis lacks one xylem cell type (ray parenchyma) and the development of another xylem cell type (libriform fiber) is incomplete with respect to woody eudicots [ 6 ]. The expression patterns of many genes involved in xylem development are also different between Arabidopsis and other woody species, such as Populus [ 4 – 6 ]. This functional and developmental diversity underscores the risks of using Arabidopsis marker genes for cell type annotation in woody eudicots.…”

“…1 D). Four recent studies reported the developmental lineages of differentiating xylem in poplar through scRNA-seq analyses [ 6 , 8 – 10 ] using the differentiating xylem protoplasts isolated by the same pipeline [ 11 ]. The first step of such protoplasting pipeline is stem debarking.…”

“…The subsequent protoplast isolation then allows the collection of differentiating xylem protoplasts (Fig. 1 E) [ 6 , 8 – 11 ]. Such anatomical results after debarking are very consistent among different species grown in various regions, such as North America, East Asia, and Australia [ 6 , 9 , 11 , 12 ].…”

Wood of trees: Cellular structure, molecular formation, and genetic engineering

“…The most remarkable observation is the presence of two types of cambium‐like cell pools within secondary vascular tissues, which provides a new perspective on vascular cambium initiation during wood development (Du et al, 2023; Li et al, 2023). The developmental lineages of ray and fusiform cells in developing xylem were determined by single‐cell and laser capture microdissection transcriptome profiling on four divergent woody angiosperms representing core and base eudicots (Tung et al, 2023). Furthermore, small conditional RNA sequencing data can be used to forecast gene redundancy during the wood‐forming process (Chen et al, 2021).…”