Abstract
Key message
The genomic location and stage-specific expression pattern of many long non-coding RNAs reveal their critical role in regulating protein-coding genes crucial in pollen developmental progression and male germ line specification.
Abstract
Long non-coding RNAs (lncRNAs) are transcripts longer than 200 bp with no apparent protein-coding potential. Multiple investigations have revealed high expression of lncRNAs in plant reproductive organs in a cell and tissue-specific manner. However, their potential role as essential regulators of molecular processes involved in sexual reproduction remains largely unexplored. We have used developing field mustard (Brassica rapa) pollen as a model system for investigating the potential role of lncRNAs in reproductive development. Reference-based transcriptome assembly performed to update the existing genome annotation identified novel expressed protein-coding genes and long non-coding RNAs (lncRNAs), including 4347 long intergenic non-coding RNAs (lincRNAs, 1058 expressed) and 2,045 lncRNAs overlapping protein-coding genes on the opposite strand (lncNATs, 780 expressed). The analysis of expression profiles reveals that lncRNAs are significant and stage-specific contributors to the gene expression profile of developing pollen. Gene co-expression networks accompanied by genome location analysis identified 38 cis-acting lincRNA, 31 cis-acting lncNAT, 7 trans-acting lincRNA and 14 trans-acting lncNAT to be substantially co-expressed with target protein-coding genes involved in biological processes regulating pollen development and male lineage specification. These findings provide a foundation for future research aiming at developing strategies to employ lncRNAs as regulatory tools for gene expression control during reproductive development.
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Data availability
All data generated in this study are available in the article and its Supplementary Materials. The Poly-A strand-specific RNA-Sequencing data were deposited in NCBI SRA under PRJNA529957 and rRNA depletion RNA-Seq data were deposited in NCBI SRA under PRJNA763698.
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This research was supported by Spartan HPC (Lev Lafayette GS, Linh Vu, Bernard Meade October 27, 2016 (Meade et al. 2017)) at the University of Melbourne, Australia.
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The research was supported by ARC Discovery grant DP0988972 and McKenzie Fellowship.
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Samples collection and RNA isolation, ADA; data curation and analysis, N.L. and AAG; initial draft preparation, N.L. and AAG; review and editing, MBS and PLB; supervision, MBS and PLB. All authors have read and agreed to the published version of the manuscript.
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Lohani, N., Golicz, A.A., Allu, A.D. et al. Genome-wide analysis reveals the crucial role of lncRNAs in regulating the expression of genes controlling pollen development. Plant Cell Rep 42, 337–354 (2023). https://doi.org/10.1007/s00299-022-02960-0
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DOI: https://doi.org/10.1007/s00299-022-02960-0