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Reading between the Lines: RNA-seq Data Mining Reveals the Alternative Message of the Rice Leaf Transcriptome in Response to Heat Stress.

ABSTRACT: Rice (Oryza sativa L.) is a major food crop but heat stress affects its yield and grain quality. To identify mechanistic solutions to improve rice yield under rising temperatures, molecular responses of thermotolerance must be understood. Transcriptional and post-transcriptional controls are involved in a wide range of plant environmental responses. Alternative splicing (AS), in particular, is a widespread mechanism impacting the stress defence in plants but it has been completely overlooked in rice genome-wide heat stress studies. In this context, we carried out a robust data mining of publicly available RNA-seq datasets to investigate the extension of heat-induced AS in rice leaves. For this, datasets of interest were subjected to filtering and quality control, followed by accurate transcript-specific quantifications. Powerful differential gene expression (DE) and differential AS (DAS) identified 17,143 and 2162 heat response genes, respectively, many of which are novel. Detailed analysis of DAS genes coding for key regulators of gene expression suggests that AS helps shape transcriptome and proteome diversity in response to heat. The knowledge resulting from this study confirmed a widespread transcriptional and post-transcriptional response to heat stress in plants, and it provided novel candidates for rapidly advancing rice breeding in response to climate change.

SUBMITTER: Vitoriano CB

PROVIDER: S-EPMC8400768 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe rice leaf folder Cnaphalocrocis medinalis Güenée is a serious insect pest of rice in Asia. This pest occurs in summer, and it is sensitive to high temperature. However, the larvae exhibit heat acclimation/adaptation. To understand the underlying mechanisms, we established a heat-acclimated strain via multigenerational selection at 39 °C. After heat shock at 41 °C for 1 h, the transcriptomes of the heat-acclimated (S-39) and unacclimated (S-27) larvae were sequenced, using the unacclimated larvae without exposure to 41 °C as the control.ResultsFive generations of selection at 39 °C led larvae to acclimate to this heat stress. Exposure to 41 °C induced 1160 differentially expressed genes (DEGs) between the heat-acclimated and unacclimated larvae. Both the heat-acclimated and unacclimated larvae responded to heat stress via upregulating genes related to sensory organ development and structural constituent of eye lens, whereas the unacclimated larvae also upregulated genes related to structural constituent of cuticle. Compared to unacclimated larvae, heat-acclimated larvae downregulated oxidoreductase activity-related genes when encountering heat shock. Both the acclimated and unacclimated larvae adjusted the longevity regulating, protein processing in endoplasmic reticulum, antigen processing and presentation, MAPK and estrogen signaling pathway to responsed to heat stress. Additionally, the unacclimated larvae also adjusted the spliceosome pathway, whereas the heat-acclimated larvae adjusted the biosynthesis of unsaturated fatty acids pathway when encountering heat stress. Although the heat-acclimated and unacclimated larvae upregulated expression of heat shock protein genes under heat stress including HSP70, HSP27 and CRYAB, their biosynthesis, metabolism and detoxification-related genes expressed differentially.ConclusionsThe rice leaf folder larvae could acclimate to a high temperature via multigenerational heat selection. The heat-acclimated larvae induced more DEGs to response to heat shock than the unacclimated larvae. The changes in transcript level of genes were related to heat acclimation of larvae, especially these genes in sensory organ development, structural constituent of eye lens, and oxidoreductase activity. The DEGs between heat-acclimated and unacclimated larvae after heat shock were enriched in the biosynthesis and metabolism pathways. These results are helpful to understand the molecular mechanism underlying heat acclimation of insects.

Project description:BackgroundHeterosis is a phenomenon in which hybrids exhibit superior performance relative to parental phenotypes. In addition to the heterosis of above-ground agronomic traits on which most existing studies have focused, root heterosis is also an indispensable component of heterosis in the entire plant and of major importance to plant breeding. Consequently, systematic investigations of root heterosis, particularly in reproductive-stage rice, are needed. The recent advent of RNA sequencing technology (RNA-Seq) provides an opportunity to conduct in-depth transcript profiling for heterosis studies.ResultsUsing the Illumina HiSeq 2000 platform, the root transcriptomes of the super-hybrid rice variety Xieyou 9308 and its parents were analyzed at tillering and heading stages. Approximately 391 million high-quality paired-end reads (100-bp in size) were generated and aligned against the Nipponbare reference genome. We found that 38,872 of 42,081 (92.4%) annotated transcripts were represented by at least one sequence read. A total of 829 and 4186 transcripts that were differentially expressed between the hybrid and its parents (DGHP) were identified at tillering and heading stages, respectively. Out of the DGHP, 66.59% were down-regulated at the tillering stage and 64.41% were up-regulated at the heading stage. At the heading stage, the DGHP were significantly enriched in pathways related to processes such as carbohydrate metabolism and plant hormone signal transduction, with most of the key genes that are involved in the two pathways being up-regulated in the hybrid. Several significant DGHP that could be mapped to quantitative trait loci (QTLs) for yield and root traits are also involved in carbohydrate metabolism and plant hormone signal transduction pathways.ConclusionsAn extensive transcriptome dataset was obtained by RNA-Seq, giving a comprehensive overview of the root transcriptomes at tillering and heading stages in a heterotic rice cross and providing a useful resource for the rice research community. Using comparative transcriptome analysis, we detected DGHP and identified a group of potential candidate transcripts. The changes in the expression of the candidate transcripts may lay a foundation for future studies on molecular mechanisms underlying root heterosis.

Project description:Regulatory small RNAs (sRNAs) are known to play important roles in the Gram-positive bacterial pathogen Staphylococcus aureus; however, their existence is often overlooked, primarily because sRNA genes are absent from genome annotation files. Consequently, transcriptome sequencing (RNA-Seq)-based experimental approaches, performed using standard genome annotation files as a reference, have likely overlooked data for sRNAs. Previously, we created an updated S. aureus genome annotation file, which included annotations for 303 known sRNAs in USA300. Here, we utilized this updated reference file to reexamine publicly available RNA-Seq data sets in an attempt to recover lost information on sRNA expression, stability, and potential to encode peptides. First, we used transcriptomic data from 22 studies to identify how the expression of 303 sRNAs changed under 64 different experimental conditions. Next, we used RNA-Seq data from an RNA stability assay to identify highly stable/unstable sRNAs. We went on to reanalyze a ribosome profiling (Ribo-seq) data set to identify sRNAs that have the potential to encode peptides and to experimentally confirm the presence of three of these peptides in the USA300 background. Interestingly, one of these sRNAs/peptides, encoded at the tsr37 locus, influences the ability of S. aureus cells to autoaggregate. Finally, we reexamined two recently published in vivo RNA-Seq data sets, from the cystic fibrosis (CF) lung and a murine vaginal colonization study, and identified 29 sRNAs that may play a role in vivo Collectively, these results can help inform future studies of these important regulatory elements in S. aureus and highlight the need for ongoing curating and updating of genome annotation files.IMPORTANCE Regulatory small RNAs (sRNAs) are a class of RNA molecules that are produced in bacterial cells but that typically do not encode proteins. Instead, they perform a variety of critical functions within the cell as RNA. Most bacterial genomes do not include annotations for sRNA genes, and any type of analysis that is performed using a bacterial genome as a reference will therefore overlook data for sRNAs. In this study, we reexamined hundreds of previously generated S. aureus RNA-Seq data sets and reanalyzed them to generate data for sRNAs. To do so, we utilized an updated S. aureus genome annotation file, previously generated by our group, which contains annotations for 303 sRNAs. The data generated (which were previously discarded) shed new light on sRNAs in S. aureus, most of which are unstudied, and highlight certain sRNAs that are likely to play important roles in the cell.

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Reading between the Lines: RNA-seq Data Mining Reveals the Alternative Message of the Rice Leaf Transcriptome in Response to Heat Stress.

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