Single-cell and spatial omics reveal progressive loss of xylem developmental complexity across seed plants
Journal
The Plant Cell
Journal Volume
37
Journal Issue
11
Start Page
koaf253
ISSN
1040-4651
1532-298X
Date Issued
2025-10-19
Author(s)
Shuai, Peng
Hsieh, Jo-Wei Allison
Kao, Chung-Ting
Hu, Chen-Wei
Wang, Ray
Kuo, Shang-Che
Yen, Ming-Ren
Liou, Pin-Chien
Ho, Yi-Chi
Chu, Chia-Chen
Huang, Shuotian
Liu, Jiao
Zhang, Lixia
Luo, Yi-Jyun
Li, Quanzi
Hsu, Chuan-Chih
Huang, Chao-Li
Su, Jung-Chen
Tseng, Mei-Chun
Chen, Ying-Lan
Abstract
Secondary growth is a key characteristic evolved from seed plants and generates secondary xylem - the most abundant tissue on Earth. Recent studies have uncovered xylem developmental lineages in eudicots and magnoliids of angiosperms. However, xylem development in gymnosperms, the other representative clade of seed plants, remained elusive. We performed single-cell transcriptomics for xylem cells of conifers (Cunninghamia lanceolata), the major clade in gymnosperms. Using Seurat and scVI-based cross-species integration, we reconstructed the xylem differentiation trajectories and revealed that the radial system is conserved across seed plants, while the axial system in C. lanceolata exhibits a composite lineage architecture resembling both eudicots and magnoliids. To validate these trajectories, we established a multi-modal spatial framework incorporating spatial transcriptomics, spatial proteomics, and spatial metabolomics. These three spatial layers provided orthogonal evidence confirming cell-type identities and trajectory inference. Additionally, we identified a xylem cell population unique to gymnosperms, suggesting a lineage-specific specialization. Together, our findings uncover a more complex ancestral xylem architecture in gymnosperms and propose a progressive simplification of axial developmental programs from gymnosperms to angiosperms, highlighting a trajectory of reductive evolution in seed plant vascular development.
Publisher
Oxford University Press (OUP)
Type
journal article