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Tissue-specific transcriptomic profiling of Plantago major provides insights for the involvement of vasculature in phosphate deficiency responses

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Abstract

The vasculature of higher plants is important with transport of both nutrient and information molecules. To understand the correspondence of this tissue in molecular responses under phosphate (Pi) deficiency, Plantago major, a model plant for vasculature biology study, was chosen in our analysis. After RNA-Seq and de novo transcriptome assembly of 24 libraries prepared from the vasculature of P. major, 37,309 unigenes with a mean length of 1571 base pairs were obtained. Upon 24 h of Pi deficiency, 237 genes were shown to be differentially expressed in the vasculature of P. major. Among these genes, only 27 have been previously identified to be specifically expressed in the vasculature tissues in other plant species. Temporal expression of several marker genes associated with Pi deficiency showed that the time period of first 24 h is at the beginning stage of more dynamic expression patterns. In this study, we found several physiological processes, e.g., “phosphate metabolism and remobilization”, “sucrose metabolism, loading and synthesis”, “plant hormone metabolism and signal transduction”, “transcription factors”, and “metabolism of other minerals”, were mainly involved in early responses to Pi deficiency in the vasculature. A number of vasculature genes with promising roles in Pi deficiency adaptation have been identified and deserve further functional characterization. This study clearly demonstrated that plant vasculature is actively involved in Pi deficiency responses and understanding of this process may help to create plants proficient to offset Pi deficiency.

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Abbreviations

EST:

Expressed sequence tag

FPKM:

Fragments per kilobase per transcript per million mapped reads

NR:

NCBI non-redundant protein sequences

COG:

Clusters of Orthologous Groups of proteins

KEGG:

Kyoto Encyclopedia of Genes and Genomes

GO:

Gene ontology

Pfam:

Protein family

Swiss-Prot:

A manually annotated and reviewed protein sequence database

DEG:

Differentially expressed gene

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Acknowledgements

We appreciate the technical support from the Purdue Genomics Core Facility Center for RNA-sEq. We are grateful to Dr. Na Liu for critical comments on the manuscript.

Funding

This study was supported by the Purdue Center for Plant Biology Seed Grant (2018).

Author information

Authors and Affiliations

  1. Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA

    Jing Huang, Xiangjun Zhou, Chao Xia, Shujuan Wang, Congshan Xu, Manrong Zha & Cankui Zhang

  2. Biost Technology Co., Ltd, Beijing, 102206, China

    Zhiqiang Huang

  3. Department of Soil and Environmental Sciences, University College of Agriculture, University of Sargodha, Sargodha, 40100, Pakistan

    Muhammad Imran

  4. The Institute of Sericulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, Zhejiang, China

    Yan Liu

  5. Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, 47907, USA

    Cankui Zhang

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  1. Jing Huang
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  2. Zhiqiang Huang
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  9. Yan Liu
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Contributions

CZ and JH conceived and designed the experiments; JH, CX, MZ, SW, CX, IM and YL prepared Plantago major plants and constructed libraries; JH and XZ conducted GUS staining experiment in Arabidopsis; JH performed quantitative real-time PCR; ZH and JH performed bioinformatic analysis; JH and CZ wrote the manuscript; CZ, XZ and IM revised and finalized the manuscript.

Corresponding author

Correspondence to Cankui Zhang.

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Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Data availability

The transcriptomic datasets are available in NCBI with Accession Number SRR6488353 to SRR6488376. This Transcriptome Shotgun Assembly project has been deposited at DDBJ/EMBL/GenBank under the accession GGVT00000000. The version described in this paper is the first version, GGVT01000000.

Additional information

Communicated by L. Xiong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file 1: Table S1

Statistical analysis of RNA-Seq data. (DOCX 15 kb) (DOCX 14 KB)

Supplementary file 2: Table S2

Read count numbers and NR annotation of all unigenes. (XLSX 5280 kb) (XLSX 5279 KB)

Supplementary file 3: Fig. S1

Sequence length distribution of transcripts and unigenes assembled from the illumina-sequenced reads. The y-axis indicated the number of transcripts or unigenes in different ranges of sequence length. The x-axis indicated different ranges of sequence length. (DOCX 82 kb) (DOCX 81 KB)

Supplementary file 4: Table S3

Summary of the functional annotation of assembled unigenes. (DOCX 13 kb) (DOCX 12 KB)

Supplementary file 5: Fig. S2

Histogram of GO (gene ontology) classifications of assembled unigenes for P. major vasculature. The unigenes are classified into three main categories: biological process, cellular component and molecular function. For each category, the nine highest GO terms were listed and the rest of the other GO terms are combined as “others”. The y-axis indicated the number of unigenes in different categories. The x-axis indicated different sub-categories of unigenes in each main category. (DOCX 283 kb) (DOCX 282 KB)

Supplementary file 6: Fig. S3

KEGG pathway classifications of assembled unigenes associated with P. major vasculature. The top 20 most enriched pathways were listed to demonstrate the major physiological processes in P. major vasculature. The y-axis indicated different pathways. The x-axis indicated the number of unigenes involved in these pathways. (DOCX 23 kb) (DOCX 22 KB)

Supplementary file 7: Table S4

All differentially upregulated genes in P. major vasculature under phosphate deficiency. (XLSX 22 kb) (XLSX 21 KB)

Supplementary file 8: Table S5

All differentially downregulated genes in P. major vasculature under phosphate deficiency. (XLSX 23 kb) (XLSX 22 KB)

Supplementary file 9: Table S6

Differentially expressed genes that have been indicated to be specifically expressed in the vasculature in previous studies. (DOCX 15 kb) (DOCX 14 KB)

Supplementary file 10: Table S7

Primer sequences for quantitative real time PCR. (DOCX 13 kb) (DOCX 12 KB)

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Huang, J., Huang, Z., Zhou, X. et al. Tissue-specific transcriptomic profiling of Plantago major provides insights for the involvement of vasculature in phosphate deficiency responses. Mol Genet Genomics 294, 159–175 (2019). https://doi.org/10.1007/s00438-018-1496-4

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