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Combination analysis of single-molecule long-read and Illumina sequencing provides insights into the anthocyanin accumulation mechanism in an ornamental grass, Pennisetum setaceum cv. Rubrum

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Abstract

Key message

Combination analysis of single-molecule long-read and Illumina sequencing provide full-length transcriptome information and shed new light on the anthocyanin accumulation mechanism of Pennisetum setaceum cv. ‘Rubrum’.

Abstract

Pennisetum setaceum cv. ‘Rubrum’ is an ornamental grass with purple leaves widely used in landscaping. However, the current next-generation sequencing (NGS) transcriptome information of this species is not satisfactory due to the difficulties in obtaining full-length transcripts. Furthermore, the molecular mechanisms of anthocyanin accumulation in P. setaceum have not been thoroughly studied. In this study, we used PacBio full-length transcriptome sequencing (SMRT) combined with NGS technology to build and improve the transcriptomic datasets and reveal the molecular mechanism of anthocyanin accumulation in P. setaceum cv. ‘Rubrum’. Therefore, 280,413 full-length non-chimeric reads sequences were obtained using the SMRT technology. We obtained 97,450 high-quality non-redundant transcripts and identified 5352 alternative splicing events. In addition, 93,066 open reading frames (ORFs), including 57,457 full ORFs and 2910 long non-coding RNA (lncRNAs) were screened out. Furthermore, 10,795 differentially expressed genes were identified using NGS. We also explored key genes, synthesis pathways, and detected lncRNA involved in anthocyanin accumulation, providing new insights into anthocyanin accumulation in P. setaceum cv. ‘Rubrum’. To our best knowledge, we provided the full-length transcriptome information of P. setaceum cv. ‘Rubrum’ for the first time. The results of this study will provide baseline information for gene function studies and pave the way for future P. setaceum cv. ‘Rubrum’ breeding projects.

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Data availability

The PacBio and Illumina sequencing data used in this study has been submitted to the BioProject database of National Center for Biotechnology Information (PRJNA741859, https://dataview.ncbi.nlm.nih.gov/object/PRJNA744323?reviewer=ivb94nq6f5qteehsn84kakpmo; PRJNA744323 https://dataview.ncbi.nlm.nih.gov/object/PRJNA741859?reviewer=14da3so0n8gbcig59abfjr5fh7).

Abbreviations

ANS:

Anthocyanidin synthase

AS:

Alternative splicing events

CCS:

Circular consensus

CDS:

Putative coding sequences

CHI:

Chalcone isomerase

CHS:

Chalcone synthase

COG:

Cluster of orthologous groups

DEGs:

Differentially expressed genes

DETs:

Differentially expressed transcripts

DFR:

Dihydroflavonol 4-reductase

F3H  :

Flavonoid 3-hydroxylase

 F3'H:

Flavonoid 3′-hydroxylase

 FLNC:

Full-length non-chimeric reads

FPKM:

Fragments per kilobase of transcript per million fragments

GO:

Gene ontology

HQ:

High quality isoforms

ICE:

Iterative isoform-clustering program

KEGG:

Kyoto encyclopedia of genes and genomes

LncRNA:

Long non-coding RNA

LQ:

Low quality isoforms

NFL:

Non-full-length

NGS:

Next generation sequencing

NR:

NCBI non-redundant protein databases

ORF:

Open reading frame

ROI:

Reads of insert

SMRT:

PacBio single-molecule long-read sequencing technology

TFs:

Transcription factors

UFGT:

Anthocyanidin 3-glycosyltransferase

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Acknowledgements

We acknowledge the Biomarker Corporation (Beijing, China) for the facilities and expertise of Illumina platform for libraries construction and sequencing.

Funding

This research was supported by the National Natural Science Foundation of China (31901397) and Scientific Funds of Beijing Academy of Agriculture and Forestry Sciences (KJCX20210431, CZZJ202210, KJCX20220103). Each of the funding bodies granted the funds based on a research proposal. They had no influence over the experimental design, data analysis or interpretation, or writing the manuscript.

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Authors and Affiliations

  1. Institute of Grassland, Flowers, and Ecology, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China

    Lingyun Liu, Ke Teng, Xifeng Fan, Chao Han, Hui Zhang & Juying Wu

  2. College of Grassland Science, Beijing Forestry University, Beijing, 100083, China

    Zhihui Chang

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  1. Lingyun Liu
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  2. Ke Teng
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  3. Xifeng Fan
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  4. Chao Han
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  5. Hui Zhang
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  7. Zhihui Chang
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Contributions

KT and XF conceived the study and designed the experiments. LL performed the experiment. LL analyzed the data with suggestions by JW, HZ, CH. LL wrote the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Ke Teng or Xifeng Fan.

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Supplementary Information

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11103_2022_1264_MOESM1_ESM.tif

Supplementary file1 (TIF 8697 KB)—Figure S1 NGS sequencing data evaluation and biological repetitions dependency examination. A Comparison diagram of FPKM density distribution of each sample. The abscissa represents the logarithm of the corresponding sample FPKM, and the ordinate of the point represents the probability density. B The logarithmic distribution of sample expression level FPKM. C The correlation of expression dependent heat map of the sample.

Supplementary file2 (PNG 159 KB)—Figure S2 Distribution of transcription factor types.

Supplementary file3 (TIF 1111 KB)—Figure S3 The length distribution of the predicted CDS-encoded protein.

11103_2022_1264_MOESM4_ESM.png

Supplementary file4 (PNG 67 KB)—Figure S4 Statistical graph of lncRNAs predicted by CPC analysis, CNCI analysis, Pfam protein domain analysis, and CPAT analysis.

Supplementary file5 (XLSX 401 KB)—Table S1 Summary of the candidate AS events.

Supplementary file6 (XLSX 57 KB)—Table S2 Prediction results of the target mRNAs for lncRNAs.

11103_2022_1264_MOESM7_ESM.xlsx

Supplementary file7 (XLSX 11 KB)—Table S3 Pigment contents of different flavonoids in green leaves, lilac leaves and purple leaves.

Supplementary file8 (XLSX 10 KB)—Table S4 Sequences of the primers used for qRT-PCR verification.

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Liu, L., Teng, K., Fan, X. et al. Combination analysis of single-molecule long-read and Illumina sequencing provides insights into the anthocyanin accumulation mechanism in an ornamental grass, Pennisetum setaceum cv. Rubrum. Plant Mol Biol 109, 159–175 (2022). https://doi.org/10.1007/s11103-022-01264-x

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