Single-cell and spatial omics reveal progressive loss of xylem developmental complexity across seed plants
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.
Authors
- Quanzi Li (ORCID: https://orcid.org/0000-0002-7405-4402)
- Leyan Zhang
- Ming‐Ren Yen (ORCID: https://orcid.org/0000-0002-9012-3244)
- Ying‐Lan Chen (ORCID: https://orcid.org/0000-0003-3145-7882)
- Peng Shuai (ORCID: https://orcid.org/0000-0002-1156-2338)
- Chung‐Ting Kao (ORCID: https://orcid.org/0000-0002-8232-963X)
- Ray Wang
- Te‐Lun Mai (ORCID: https://orcid.org/0000-0002-9356-6198)
- Mei‐Chun Tseng (ORCID: https://orcid.org/0000-0002-7970-5278)
- Yi‐Jyun Luo (ORCID: https://orcid.org/0000-0002-3418-3146)
- Shuotian Huang (ORCID: https://orcid.org/0000-0003-0612-1850)
- Chao‐Li Huang (ORCID: https://orcid.org/0000-0002-1059-432X)
- Yi-Chi Ho
- Jo‐Wei Allison Hsieh (ORCID: https://orcid.org/0000-0001-7017-3853)
- Chuan‐Chih Hsu (ORCID: https://orcid.org/0000-0002-7100-1401)
- Jung‐Chen Su (ORCID: https://orcid.org/0000-0002-8005-0897)
- Ying‐Chung Jimmy Lin (ORCID: https://orcid.org/0000-0001-7120-4690)
- Shang‐Che Kuo (ORCID: https://orcid.org/0000-0002-6773-8179)
- Chen-Wei Hu
- Chia-Chen Wu (ORCID: https://orcid.org/0000-0002-5403-253X)
- Pin‐Chien Liou
- Jiao Liu
- Chia-Chen Chu (ORCID: https://orcid.org/0000-0003-3026-9206)
Institutions
- Zhejiang A & F University (CN)
- National Yang Ming Chiao Tung University (TW)
- National Taiwan University (TW)
- Agriculture and Forestry University (NP)
- Genomics Research Center, Academia Sinica (TW)
- Institute of Plant and Microbial Biology, Academia Sinica (TW)
- Institute of Sociology, Academia Sinica (TW)
- Taiwan Forestry Research Institute (TW)
- Jiyang College of Zhejiang A&F University (CN)
- Research Institute of Forestry (CN)
- State Forestry and Grassland Administration (CN)
- Biodiversity Research Center, Academia Sinica (TW)
- Institute of Chemistry, Academia Sinica (TW)
- Zhejiang Academy of Forestry (CN)
- Fujian Agriculture and Forestry University (CN)
- University of California, Davis (US)
- Academia Sinica (TW)
- National Cheng Kung University (TW)
Publication Details
- Journal
- The Plant Cell
- Published
- 2025-10-16
- DOI
- https://doi.org/10.1093/plcell/koaf253
- Citations
- 5
- Primary Topic
- Plant Molecular Biology Research
- Type
- article
- Field-Weighted Citation Impact
- 8.75