Single-cell transcriptomics unveils xylem cell development and evolution

Chia-Chun Tung¹, Shang-Che Kuo², Chia-Ling Yang³, Jhong-He Yu¹, Chia-En Huang¹, Pin-Chien Liou¹, Ying-Hsuan Sun⁴, Peng Shuai⁵, Jung-Chen Su⁶, Chuan Ku^2,3, Ying-Chung Jimmy Lin^1,2*

¹Department of Life Science and Institute of Plant Biology, National Taiwan University, Taipei, Taiwan
²Genome and Systems Biology Degree Program, National Taiwan University and Academia Sinica, Taipei, Taiwan
³Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan
⁴Department of Forestry, National Chung Hsing University, Taipei, Taiwan
⁵College of Forestry, Fujian Agriculture and Forestry University, Fuzhou, China
⁶Department of Pharmacy, National Yang Ming Chiao Tung University, Taipei, Taiwan

* Presenter:Ying-Chung Jimmy Lin, email:ycjimmylin@ntu.edu.tw

As the most abundant tissue on Earth, xylem 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 are a combination of vessel elements for water transportation and libriform fibers for mechanical support, while both functions are performed together by tracheids in other vascular plants. However, little is known about the developmental programs and evolutionary relationships of these xylem cell types. Through both single-cell and laser-capture microdissection transcriptomic profiling, here we demonstrate the developmental lineages of ray and fusiform cells in stem-differentiating xylem across four divergent woody angiosperms. Cross-species analyses of single-cell trajectories reveal highly conserved ray, yet variable fusiform, lineages across angiosperms. Core eudicots Populus trichocarpa and Eucalyptus grandis share nearly identical fusiform lineages. The tracheids in the basal eudicot Trochodendron aralioides, an evolutionarily reversed character, exhibit strong transcriptomic similarity to vessel elements but not libriform fibers, suggesting that water transportation, instead of mechanical support, is the major feature. We also found that the more basal angiosperm Liriodendron chinense has a fusiform lineage distinct from that in core eudicots. This evo-developmental 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. Within the past one and half years, four separate research groups have published their studies in the top 5% journals on elucidating stem-differentiating xylem development using single-cell RNA sequencing. Such striking intensity appears to reflect the criticality of this subject matter as well as the competitive and collaborative nature among the scientific community. Yet, these four articles led to four conflicting models on stem-differentiating xylem development. In an attempt to sort out this puzzle, we reached out to the other corresponding authors to determine the current most plausible model.

Keywords: Xylem development, Single-cell Sequencing, Woody angiosperms