Comprehensive analysis of lncRNA-mRNA regulatory network in Populus associated with xylem development

Na Sun; Yufen Bu; Xinyuan Wu; Xiaocen Ma; Haobo Yang; Liang Du; Xiaojuan Li; Jianwei Xiao; Jinxing Lin; Yanping Jing

doi:10.1016/j.jplph.2023.154055

Comprehensive analysis of lncRNA-mRNA regulatory network in Populus associated with xylem development

J Plant Physiol. 2023 Aug:287:154055. doi: 10.1016/j.jplph.2023.154055. Epub 2023 Jul 18.

Authors

Na Sun¹, Yufen Bu², Xinyuan Wu³, Xiaocen Ma⁴, Haobo Yang⁵, Liang Du⁶, Xiaojuan Li⁷, Jianwei Xiao⁸, Jinxing Lin⁹, Yanping Jing¹⁰

Affiliations

¹ State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China; The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: sunna@bjfu.edu.cn.
² State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China; The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: buyufen@bjfu.edu.cn.
³ State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China; The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: wuxinyuan@bjfu.edu.cn.
⁴ State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China; The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: fly_mxc@bjfu.edu.cn.
⁵ State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China; The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: yanghaobo942@bjfu.edu.cn.
⁶ State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China; The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: duliang@bjfu.edu.cn.
⁷ The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: lixj@bjfu.edu.cn.
⁸ The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: xiaojianwei@bjfu.edu.cn.
⁹ The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: linjx@ibcas.ac.cn.
¹⁰ State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China; The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, Beijing Forestry University, No. 35 Qinghua East Road, Beijing, 100083, China. Electronic address: ypjing@bjfu.edu.cn.

PMID: 37506405
DOI: 10.1016/j.jplph.2023.154055

Abstract

Long noncoding RNAs (lncRNAs) play essential roles in numerous biological processes in plants, such as regulating the gene expression. However, only a few studies have looked into their potential functions in xylem development. High-throughput sequencing of P. euramericana 'Zhonglin46' developing and mature xylem was performed in this study. Through sequencing analysis, 14,028 putative lncRNA transcripts were identified, including 4525 differentially expressed lncRNAs (DELs). Additional research revealed that in mature xylem, a total of 2320 DELs were upregulated and 2205 were downregulated compared to developing xylem. Meanwhile, there were a total of 8122 differentially expressed mRNAs (DEMs) that were upregulated and 16,424 that were downregulated in mature xylem compared with developing xylem. The cis- and trans-target genes of DELs were analyzed for Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment, which indicated that these DELs participate in controlling the phenylpropanoid and lignin biosynthesis pathway as well as the starch and sucrose metabolism pathway. Among the cis-regulated DELs, LNC_006291, LNC_006292, and LNC_006532 all participate in regulating multiple HCT gene family membranes. As targets, POPTR_001G045900v3 (CCR2) and POPTR_018G063500v3 (SUS) both have only one cis-regulatory lncRNA, referred to as LNC_000057 and LNC_006212, respectively. Moreover, LNC_004484 and two DELs named LNC_008014 and LNC_010781 were revealed to be important nodes in the co-expression network of trans-lncRNAs and mRNAs associated to the lignin biosynthesis pathway and cellulose and xylan biosynthetic pathways, respectively. Finally, quantitative real-time PCR (qRT-PCR) was used to confirme 34 pairs of lncRNA-mRNA. Taken together, these findings may help to clarify the regulatory role that lncRNAs play in xylem development and wood formation.

Keywords: Development; Populus euramericana 'Zhonglin46'; Xylem; lncRNA-mRNA.

MeSH terms

Gene Expression Profiling
Gene Regulatory Networks
Lignin
Populus* / genetics
RNA, Long Noncoding* / genetics
RNA, Long Noncoding* / metabolism
RNA, Messenger / genetics
Xylem / genetics
Xylem / metabolism

Substances

RNA, Messenger
RNA, Long Noncoding
Lignin