Multi-organ single-cell transcriptomic atlas identifies QrIAA14 as a candidate negative regulator of adventitious root development in Quercus robur
- 1Forest Ecology and Conservation in the Upper Reaches of the Yangtze River Key Laboratory of Sichuan Province, College of Forestry, Sichuan Agricultural University, Chengdu, China
- 2Ecological Conservation, Restoration and Resource Utilization in Forest and Wetland Key Laboratory of Sichuan Province, Sichuan Academy of Forestry, Chengdu, China
Abstract
Plant organ development involves coordinated cell fate transitions across multiple tissues, yet the cellular programs underlying organ-specific differentiation in woody plants remain poorly understood, particularly the mechanisms limiting efficient root development during vegetative propagation of oak species. Here, we generated a comprehensive single-cell transcriptomic landscape of leaf, stem, and root tissues of Quercus robur to resolve developmental trajectories at cellular resolution. A total of 41,471 high-quality cells were classified into 30 distinct clusters, enabling the identification of major cell types and organ-specific transcriptional features across three vegetative organs. Pseudotime analyses exhibited the developmental programs related to guard cell differentiation in leaves, vascular formation in stems, and root tissue development. Additionally, combining scRNA-seq, bulk transcriptome profiling, and phytohormone investigations, we identified auxin signaling as an important regulator during adventitious root development process. Notably, QrIAA14-1, an IAA14 homolog, was preferential enrichment in root hair, near-root hair cells and root cap along root developmental trajectories, which was further supported by RT-qPCR and in situ hybridization assays. Furthermore, the overexpression of QrIAA14-1 significantly inhibited oak root elongation, resulting in around 64.46% reduction in adventitious root length compared with control plants, providing mechanistic insight into the limitations of root development in oak. Together, this study provides the first high-resolution single-cell atlas of cellular organization and developmental dynamics across oak vegetative organs and identifies the candidate regulator genes associated with root development, offering new insights into the regulatory mechanisms of woody plant root regeneration and clonal propagation. Author summary: Oaks are important forest trees with high ecological and economic value, but many oak species show poor efficiency in vegetative propagation because newly regenerated shoots often form roots inefficiently. This poor rooting ability limits the preservation and large-scale use of elite oak genotypes. In this study, we generated a single-cell transcriptomic atlas of leaf, stem, and root tissues in Quercus robur, revealing the cellular composition and developmental programs of major vegetative organs in oak. We further combined this single-cell resource with bulk RNA sequencing, phytohormone measurements, gene expression analyses, RNA in situ hybridization, and transgenic assays to investigate adventitious root development. Our results showed that auxin signaling is significantly associated with oak root regeneration. We identified QrIAA14-1, an auxin-related gene, as a candidate negative regulator of adventitious root development. Overexpression of QrIAA14-1 reduced adventitious root elongation, suggesting that this gene may contribute to the limited rooting capacity of oak. These findings provide a useful resource for studying woody plant development and may help improve clonal propagation strategies in oaks.
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BibTeX
@article{hui2026multiorgan,
title = {{Multi-organ single-cell transcriptomic atlas identifies QrIAA14 as a candidate negative regulator of adventitious root development in Quercus robur}},
author = {Wenkai Hui and Jiayue Li and Hao Li and Hongyi Wu and Yi He and Shuangying Yang and Xiong Huang and Hanbo Yang and Gang Chen and Peng Zhu and Xiaohong Chen and Xingcui Xiao and Yu Zhong and Zhenfeng Xu and Fang He},
journal = {PLOS Genetics},
year = {2026},
month = sep,
doi = {10.1371/journal.pgen.1012300},
url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1012300},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Multi-organ single-cell transcriptomic atlas identifies QrIAA14 as a candidate negative regulator of adventitious root development in Quercus robur
AU - Wenkai Hui
AU - Jiayue Li
AU - Hao Li
AU - Hongyi Wu
AU - Yi He
AU - Shuangying Yang
AU - Xiong Huang
AU - Hanbo Yang
AU - Gang Chen
AU - Peng Zhu
AU - Xiaohong Chen
AU - Xingcui Xiao
AU - Yu Zhong
AU - Zhenfeng Xu
AU - Fang He
PY - 2026
DA - 2026/09/01
JO - PLOS Genetics
DO - 10.1371/journal.pgen.1012300
UR - https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1012300
AB - Plant organ development involves coordinated cell fate transitions across multiple tissues, yet the cellular programs underlying organ-specific differentiation in woody plants remain poorly understood, particularly the mechanisms limiting efficient root development during vegetative propagation of oak species. Here, we generated a comprehensive single-cell transcriptomic landscape of leaf, stem, and root tissues of Quercus robur to resolve developmental trajectories at cellular resolution. A total of 41,471 high-quality cells were classified into 30 distinct clusters, enabling the identification of major cell types and organ-specific transcriptional features across three vegetative organs. Pseudotime analyses exhibited the developmental programs related to guard cell differentiation in leaves, vascular formation in stems, and root tissue development. Additionally, combining scRNA-seq, bulk transcriptome profiling, and phytohormone investigations, we identified auxin signaling as an important regulator during adventitious root development process. Notably, QrIAA14-1, an IAA14 homolog, was preferential enrichment in root hair, near-root hair cells and root cap along root developmental trajectories, which was further supported by RT-qPCR and in situ hybridization assays. Furthermore, the overexpression of QrIAA14-1 significantly inhibited oak root elongation, resulting in around 64.46% reduction in adventitious root length compared with control plants, providing mechanistic insight into the limitations of root development in oak. Together, this study provides the first high-resolution single-cell atlas of cellular organization and developmental dynamics across oak vegetative organs and identifies the candidate regulator genes associated with root development, offering new insights into the regulatory mechanisms of woody plant root regeneration and clonal propagation. Author summary: Oaks are important forest trees with high ecological and economic value, but many oak species show poor efficiency in vegetative propagation because newly regenerated shoots often form roots inefficiently. This poor rooting ability limits the preservation and large-scale use of elite oak genotypes. In this study, we generated a single-cell transcriptomic atlas of leaf, stem, and root tissues in Quercus robur, revealing the cellular composition and developmental programs of major vegetative organs in oak. We further combined this single-cell resource with bulk RNA sequencing, phytohormone measurements, gene expression analyses, RNA in situ hybridization, and transgenic assays to investigate adventitious root development. Our results showed that auxin signaling is significantly associated with oak root regeneration. We identified QrIAA14-1, an auxin-related gene, as a candidate negative regulator of adventitious root development. Overexpression of QrIAA14-1 reduced adventitious root elongation, suggesting that this gene may contribute to the limited rooting capacity of oak. These findings provide a useful resource for studying woody plant development and may help improve clonal propagation strategies in oaks.
SN - 1553-7404
ER -