Genome and transcriptome of Selaginella kraussiana reveal evolution of root apical meristems in vascular plants

Wu Liu; Gui Cai; Ning Zhai; Hua Wang; Tengfei Tang; Yuyun Zhang; Zhiyao Zhang; Lijun Sun; Yijing Zhang; Tom Beeckman; Lin Xu

doi:10.1016/j.cub.2023.08.061

Genome and transcriptome of Selaginella kraussiana reveal evolution of root apical meristems in vascular plants

Curr Biol. 2023 Oct 9;33(19):4085-4097.e5. doi: 10.1016/j.cub.2023.08.061. Epub 2023 Sep 15.

Authors

Wu Liu¹, Gui Cai², Ning Zhai¹, Hua Wang¹, Tengfei Tang², Yuyun Zhang², Zhiyao Zhang³, Lijun Sun³, Yijing Zhang⁴, Tom Beeckman⁵, Lin Xu⁶

Affiliations

¹ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai 200032, China.
² National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai 200032, China; University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing 100049, China.
³ School of Life Sciences, Nantong University, Nantong 226019, China.
⁴ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai 200032, China; State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Department of Biochemistry, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai 200438, China.
⁵ Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Ghent, Belgium; VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium.
⁶ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai 200032, China. Electronic address: xulin@cemps.ac.cn.

PMID: 37716350
DOI: 10.1016/j.cub.2023.08.061

Abstract

The evolution of roots allowed vascular plants to adapt to land environments. Fossil evidence indicates that roots evolved independently in euphyllophytes (ferns and seed plants) and lycophytes, the two lineages of extant vascular plants. Based on a high-quality genome assembly, mRNA sequencing (mRNA-seq) data, and single-cell RNA-seq data for the lycophyte Selaginella kraussiana, we show that the two root origin events in lycophytes and euphyllophytes adopted partially similar molecular modules in the regulation of root apical meristem (RAM) development. In S. kraussiana, the RAM initiates from the rhizophore primordium guided by auxin and duplicates itself by dichotomous branching. The auxin signaling pathway directly upregulates euAINTEGUMENTAb (SkeuANTb), and then SkeuANTb directly promotes the expression of SkeuANTa and the WUSCHEL-RELATED HOMEOBOX13b (SkWOX13b) for RAM maintenance, partially similar to the molecular pathway involving the euANT-branch PLETHORA (AtPLT) genes and AtWOX5 in root initiation in the seed plant Arabidopsis thaliana. Other molecular modules, e.g., SHORT-ROOT and SCARECROW, also have partially similar expression patterns in the RAMs of S. kraussiana and A. thaliana. Overall, our study not only provides genome and transcriptome tools of S. kraussiana but also indicates the employment of some common molecular modules in RAMs during root origins in lycophytes and euphyllophytes.

Keywords: PLT; RAM; Selaginella kraussiana; WOX; euANT; root evolution.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Gene Expression Regulation, Plant
Indoleacetic Acids / metabolism
Meristem / metabolism
Plant Roots
RNA, Messenger / metabolism
Selaginellaceae* / genetics
Tracheophyta*
Transcriptome

Substances

Indoleacetic Acids
RNA, Messenger