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Genome-wide analysis of spatiotemporal gene expression patterns during floral organ development in Brassica rapa

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Abstract

Flowering is a key agronomic trait that directly influences crop yield and quality and serves as a model system for elucidating the molecular basis that controls successful reproduction, adaptation, and diversification of flowering plants. Adequate knowledge of continuous series of expression data from the floral transition to maturation is lacking in Brassica rapa. To unravel the genome expression associated with the development of early small floral buds (< 2 mm; FB2), early large floral buds (2-4 mm; FB4), stamens (STs) and carpels (CPs), transcriptome profiling was carried out with a Br300K oligo microarray. The results showed that at least 6848 known nonredundant genes (30% of the genes of the Br300K) were differentially expressed during the floral transition from vegetative tissues to maturation. Functional annotation of the differentially expressed genes (DEGs) (fold change ≥ 5) by comparison with a close relative, Arabidopsis thaliana, revealed 6552 unigenes (4579 upregulated; 1973 downregulated), including 131 Brassica-specific and 116 functionally known floral Arabidopsis homologs. Additionally, 1723, 236 and 232 DEGs were preferentially expressed in the tissues of STs, FB2, and CPs. These DEGs also included 43 transcription factors, mainly AP2/ERF–ERF, NAC, MADS-MIKC, C2H2, bHLH, and WRKY members. The differential gene expression during flower development induced dramatic changes in activities related to metabolic processes (23.7%), cellular (22.7%) processes, responses to the stimuli (7.5%) and reproduction (1%). A relatively large number of DEGs were observed in STs and were overrepresented by photosynthesis-related activities. Subsequent analysis via semiquantitative RT-PCR, histological analysis performed with in situ hybridization of BrLTP1 and transgenic reporter lines (BrLTP promoter::GUS) of B. rapa ssp. pekinensis supported the spatiotemporal expression patterns. Together, these results suggest that a temporally and spatially regulated process of the selective expression of distinct fractions of the same genome leads to the development of floral organs. Interestingly, most of the differentially expressed floral transcripts were located on chromosomes 3 and 9. This study generated a genome expression atlas of the early floral transition to maturation that represented the flowering regulatory elements of Brassica rapa.

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Acknowledgements

This study was supported by the Postdoctoral Fellowship Program of the National Institute of Agricultural Science; the Rural Program for Agricultural Science and Technology Development (Project No. PJ01247202); and the Next-Generation Biogreen 21 Program (Project No. PJ01334002), Rural Development Administration, Korea.

Funding

This study was funded by the National Institute of Agricultural Science (Project No. PJ01247202) and Rural Development Administration, Korea (PJ01334002).

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  1. Muhammad Amjad Nawaz

    Present address: Education Scientific Center of Nanotechnology, Far Eastern Federal University, Vladivostok, Russian Federation

  2. Soo In Lee and Muthusamy Muthusamy contributed equally to this study.

Authors and Affiliations

  1. Department of Agricultural Biotechnology, National Institute of Agricultural Sciences (NAS), RDA, Jeonju, 54874, Korea

    Soo In Lee, Muthusamy Muthusamy, Muhammad Amjad Nawaz, Joon Ki Hong, Myung-Ho Lim, Jin A. Kim & Mi-Jeong Jeong

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Contributions

SL, JK and MJ conceived and designed the study. MM and MN conducted the bioinformatics analysis, analyzed the data and drafted the manuscript. MM, and SL submitted the array data to the NCBI Gene Expression Omnibus database. SL, JK, JH, ML and MJ revised the manuscript. All the authors agreed on the contents of the paper.

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Correspondence to Soo In Lee.

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Conflict of interest

Soo In Lee declares that he has no conflict of interest. Muthusamy Muthusamy declares that he has no conflict of interest. Muhammad Amjad Nawaz declares that he has no conflict of interest. Joon Ki Hong declares that he has no conflict of interest. Myung-Ho Lim declares that he has no conflict of interest. Jin A Kim declares that she has no conflict of interest. Mi-Jeong Jeong declares that she has no conflict of interest.

Data availability statement

The complete set of genome-wide expression data from this study was submitted to the Gene Expression Omnibus database (https://www.ncbi.nlm.nih.gov/geo/) under accession number GSE128989, and the necessary information was also submitted as supplementary data in this article.

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Lee, S.I., Muthusamy, M., Nawaz, M.A. et al. Genome-wide analysis of spatiotemporal gene expression patterns during floral organ development in Brassica rapa. Mol Genet Genomics 294, 1403–1420 (2019). https://doi.org/10.1007/s00438-019-01585-5

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