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 a...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-01-01
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| Series: | Genome Biology |
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| Online Access: | https://doi.org/10.1186/s13059-022-02845-1 |
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| author | Chia-Chun Tung Shang-Che Kuo Chia-Ling Yang Jhong-He Yu Chia-En Huang Pin-Chien Liou Ying-Hsuan Sun Peng Shuai Jung-Chen Su Chuan Ku Ying-Chung Jimmy Lin |
| author_facet | Chia-Chun Tung Shang-Che Kuo Chia-Ling Yang Jhong-He Yu Chia-En Huang Pin-Chien Liou Ying-Hsuan Sun Peng Shuai Jung-Chen Su Chuan Ku Ying-Chung Jimmy Lin |
| author_sort | Chia-Chun Tung |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-24T12:39:18Z |
| format | Article |
| id | doaj.art-54b1e7b82bd5433ea4b32cd369d93e0e |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-04-24T12:39:18Z |
| publishDate | 2023-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-54b1e7b82bd5433ea4b32cd369d93e0e2024-04-07T11:20:24ZengBMCGenome Biology1474-760X2023-01-0124113710.1186/s13059-022-02845-1Single-cell transcriptomics unveils xylem cell development and evolutionChia-Chun Tung0Shang-Che Kuo1Chia-Ling Yang2Jhong-He Yu3Chia-En Huang4Pin-Chien Liou5Ying-Hsuan Sun6Peng Shuai7Jung-Chen Su8Chuan Ku9Ying-Chung Jimmy Lin10Department of Life Science, National Taiwan UniversityGenome and Systems Biology Degree Program, National Taiwan University and Academia SinicaInstitute of Plant and Microbial Biology, Academia SinicaInstitute of Plant Biology, National Taiwan UniversityInstitute of Plant Biology, National Taiwan UniversityInstitute of Plant Biology, National Taiwan UniversityDepartment of Forestry, National Chung Hsing UniversityCollege of Forestry, Fujian Agriculture and Forestry UniversityDepartment of Pharmacy, National Yang Ming Chiao Tung UniversityGenome and Systems Biology Degree Program, National Taiwan University and Academia SinicaDepartment of Life Science, National Taiwan UniversityAbstract 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.https://doi.org/10.1186/s13059-022-02845-1Single-cell RNA sequencingXylemLibriform fiberVessel elementTracheidRay parenchyma cell |
| spellingShingle | Chia-Chun Tung Shang-Che Kuo Chia-Ling Yang Jhong-He Yu Chia-En Huang Pin-Chien Liou Ying-Hsuan Sun Peng Shuai Jung-Chen Su Chuan Ku Ying-Chung Jimmy Lin Single-cell transcriptomics unveils xylem cell development and evolution Genome Biology Single-cell RNA sequencing Xylem Libriform fiber Vessel element Tracheid Ray parenchyma cell |
| title | Single-cell transcriptomics unveils xylem cell development and evolution |
| title_full | Single-cell transcriptomics unveils xylem cell development and evolution |
| title_fullStr | Single-cell transcriptomics unveils xylem cell development and evolution |
| title_full_unstemmed | Single-cell transcriptomics unveils xylem cell development and evolution |
| title_short | Single-cell transcriptomics unveils xylem cell development and evolution |
| title_sort | single cell transcriptomics unveils xylem cell development and evolution |
| topic | Single-cell RNA sequencing Xylem Libriform fiber Vessel element Tracheid Ray parenchyma cell |
| url | https://doi.org/10.1186/s13059-022-02845-1 |
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