Abstract

Plants have evolved regulatory mechanisms at multiple levels to regulate gene expression in order to improve their cold adaptability. However, limited information is available regarding the stress response at the chromatin and translational levels. Here, we characterize the chromatin accessibility, transcriptional, and translational landscapes of tea plants in vivo under chilling stress for the first time. Chilling stress significantly affected both the transcription and translation levels as well as the translation efficiency of tea plants. A total of 3010 genes that underwent rapid and independent translation under chilling stress were observed, and they were significantly enriched in the photosynthesis-antenna protein and phenylpropanoid biosynthesis pathways. A set of genes that were significantly responsive to cold at the transcription and translation levels, including four (+)-neomenthol dehydrogenases (MNDs) and two (E)-nerolidol synthases (NESs) arranged in tandem on the chromosomes, were also found. We detected potential upstream open reading frames (uORFs) on 3082 genes and found that tea plants may inhibit the overall expression of genes by enhancing the translation of uORFs under chilling stress. In addition, we identified distal transposase hypersensitive sites (THSs) and proximal THSs and constructed a transcriptional regulatory network for tea plants under chilling stress. We also identified 13 high-confidence transcription factors (TFs) that may play a crucial role in cold regulation. These results provide valuable information regarding the potential transcriptional regulatory network in plants and help to clarify how plants exhibit flexible responses to chilling stress.

Highlights

  • Plants worldwide are often challenged by various environmental conditions that threaten their growth, distribution, and yield, and low temperature is one of their major limitations

  • Overview of ATAC-seq, RNA-seq, and Ribo-seq To investigate the regulation of chilling stress responses in tea plant leaves from chromatin accessibility, transcriptional, and translational aspects, we collected samples from the control (CK) and the plants treated at 4 °C for 24 h (low temperature (LT)) and performed wholegenome ATAC-seq, RNA-seq and Ribo-seq analysis in vivo (Fig. 1)

  • We further discovered that the translation levels of some photosynthesis-related genes were independently inhibited under chilling stress

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Summary

Introduction

Plants worldwide are often challenged by various environmental conditions that threaten their growth, distribution, and yield, and low temperature is one of their major limitations. With the intense temperature cycles between warm and cold seasons, plants from temperate regions have evolved multilevel regulatory mechanisms to regulate gene expression to improve their cold adaptation[1]. This method is powerful, it has recently been mostly replaced by the assay for transposase-accessible chromatin with sequencing (ATAC-seq)[17]. This method employs high-activity Tn5 transposase to simultaneously cut nuclear DNA and insert the sequencing adapter and has the advantages of low input material requirements, high sensitivity, and greatly simplified operation steps[18,19]. To date, chromatin accessibility profiling using ATAC-seq has been mainly performed on model plants, such as Arabidopsis[22,23,24] and rice[25,26,27], and has never been applied to woody plants

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