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Genome-wide identification and association analysis for virus-responsive lncRNAs in rice (Oryza sativa L.)

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Abstract

Long non-coding RNAs (lncRNAs) produced by the plant genome are essential regulators of diverse biological processes. Despite increasing knowledge on the role of lncRNAs in plant development, their action in response to plant disease, especially in rice, is poorly understood. In this study, the comprehensive disease-responding lncRNA profile in rice response to rice black-streaked dwarf virus (RBSDV) and rice stripe virus (RSV) was investigated for the first time. Transcriptomic analysis of rice leaves infected with these two pathogens had identified 1925 lncRNAs, of which 724 were derived from alternative splicing (AS) events. Differentially expression analysis identified 344 and 176 differentially expression lncRNAs (DELs) in RBSDV vs CK and RSV vs CK, respectively. The targets of these DELs mainly associated with multiple immune-related pathways, such as “plant hormone signal transduction,” and “phenylpropanoid biosynthesis”, and ‘plant-pathogen interaction’. For further analyzing the regulatory relationship among transcription factors, lncRNAs, and mRNAs, the gene regulatory network was constructed by performing GENIE3. Finally, a total of 2484 TF-lncRNA-target pairs, including 60 TFs (as regulatory factors), 21 lncRNAs regulated by TFs and targeting mRNAs (as regulatory factors and targets), and 1064 mRNAs (as targets) were obtained, and all transcripts from TF-lncRNA-target pairs were up-regulated in both comparisons. In these transcripts, each lncRNA regulated by corresponding TF can regulate the TF-targeted mRNA, suggesting that TF may regulate the mRNA via the corresponding lncRNA. This study identified lncRNAs related to multiple viruses infection in rice, which provides another layer of candidates that regulate rice and virus interactions.

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Data availability

We deposited the raw data in Sequence Read Archive (SRA) at the National Center for Biotechnology Information (NCBI) and the accession number was PRJNA699905.

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Funding

This work was supported by grants from the China National Transgenic Plant Research and Commercialization Project (Grant No. 2016ZX08001-002) and Shandong Province Natural Science Foundation (ZR2019MC009).

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Contributions

CZ and LG designed the work. LG performed the data analysis. WC and JC wrote the manuscript and performed the experiments. QG, RW, YL and CL edited the manuscript and provided valuable suggestions during the experiment.

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Correspondence to Liming Gan or Changxiang Zhu.

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The authors declare no conflict of interest.

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Supplementary Information

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10725_2022_833_MOESM1_ESM.pdf

Supplementary file1 (PDF 1421 kb) RT-PCR was used to detect whether RBSDV and RSV were successfully colonized in corresponding samples. The length of detected coat proteins from RBSDV and RSV were 400bp and 300bp, respectively.

10725_2022_833_MOESM2_ESM.pdf

Supplementary file2 (PDF 742 kb) Validation of 10 co-upregulated expressed lncRNAs from cluster by qRT-PCR. The values were represented by means of the gene expression levels ± standard deviations (SD) (n = 3 biological replicates). *P < 0.05, ***P < 0.001 represented statistical significance.

Supplementary file3 (PDF 29 kb) Distribution of identified transcription factors (TFs) from all samples.

Supplementary file4 (XLSX 7763 kb)

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Cao, W., Cao, J., Gao, J. et al. Genome-wide identification and association analysis for virus-responsive lncRNAs in rice (Oryza sativa L.). Plant Growth Regul 98, 65–76 (2022). https://doi.org/10.1007/s10725-022-00833-w

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  • DOI: https://doi.org/10.1007/s10725-022-00833-w

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