Identification of miRNAs and their targets in the liverwort Marchantia polymorpha by integrating RNA-Seq and degradome analyses

Pin Chun Lin, Chia Wei Lu, Bing Nan Shen, Guan Z. Lee, John L. Bowman, Mario A. Arteaga-Vazquez, Li Yu Daisy Liu, Syuan Fei Hong, Chu-Fang Lo, Gong Min Su, Takayuki Kohchi, Kimitsune Ishizaki, Sabine Zachgo, Felix Althoff, Mizuki Takenaka, Katsuyuki T. Yamato, Shih Shun Lin

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Bryophytes (liverworts, hornworts and mosses) comprise the three earliest diverging lineages of land plants (embryophytes). Marchantia polymorpha, a complex thalloid Marchantiopsida liverwort that has been developed into a model genetic system, occupies a key phylogenetic position. Therefore, M. polymorpha is useful in studies aiming to elucidate the evolution of gene regulation mechanisms in plants. In this study, we used computational, transcriptomic, small RNA and degradome analyses to characterize microRNA (miRNA)-mediated pathways of gene regulation in M. polymorpha. The data have been integrated into the open access ContigViews-miRNA platform for further reference. In addition to core components of the miRNA pathway, 129 unique miRNA sequences, 11 of which could be classified into seven miRNA families that are conserved in embryophytes (miR166a, miR390, miR529c, miR171-3p, miR408a, miR160 and miR319a), were identified. A combination of computational and degradome analyses allowed us to identify and experimentally validate 249 targets. In some cases, the target genes are orthologous to those of other embryophytes, but in other cases, the conserved miRNAs target either paralogs or members of different gene families. In addition, the newly discovered Mpo-miR11707.1 and Mpo-miR11707.2 are generated from a common precursor and target MpARGONAUTE1 (LW1759). Two other newly discovered miRNAs, Mpo-miR11687.1 and MpomiR11681.1, target the MADS-box transcription factors MpMADS1 and MpMADS2, respectively. Interestingly, one of the pentatricopeptide repeat (PPR) gene family members, MpPPR-66 (LW9825), the protein products of which are generally involved in various steps of RNA metabolism, has a long stem-loop transcript that can generate MpomiR11692.1 to autoregulate MpPPR-66 (LW9825) mRNA. This study provides a foundation for further investigations of the RNA-mediated silencing mechanism in M. polymorpha as well as of the evolution of this gene silencing pathway in embryophytes.

Original languageEnglish
Pages (from-to)339-358
Number of pages20
JournalPlant and Cell Physiology
Volume57
Issue number2
DOIs
Publication statusPublished - 2016 Feb 1

Fingerprint

Marchantia
Hepatophyta
Marchantia polymorpha
embryophytes
Embryophyta
MicroRNAs
microRNA
mosses and liverworts
RNA
genes
Bryophyta
Genes
Anthocerotophyta
protein products
gene silencing
transcriptomics
Genetic Models
transcription factors
Gene Silencing
RNA Interference

All Science Journal Classification (ASJC) codes

  • Physiology
  • Plant Science
  • Cell Biology

Cite this

Lin, P. C., Lu, C. W., Shen, B. N., Lee, G. Z., Bowman, J. L., Arteaga-Vazquez, M. A., ... Lin, S. S. (2016). Identification of miRNAs and their targets in the liverwort Marchantia polymorpha by integrating RNA-Seq and degradome analyses. Plant and Cell Physiology, 57(2), 339-358. https://doi.org/10.1093/pcp/pcw020
Lin, Pin Chun ; Lu, Chia Wei ; Shen, Bing Nan ; Lee, Guan Z. ; Bowman, John L. ; Arteaga-Vazquez, Mario A. ; Daisy Liu, Li Yu ; Hong, Syuan Fei ; Lo, Chu-Fang ; Su, Gong Min ; Kohchi, Takayuki ; Ishizaki, Kimitsune ; Zachgo, Sabine ; Althoff, Felix ; Takenaka, Mizuki ; Yamato, Katsuyuki T. ; Lin, Shih Shun. / Identification of miRNAs and their targets in the liverwort Marchantia polymorpha by integrating RNA-Seq and degradome analyses. In: Plant and Cell Physiology. 2016 ; Vol. 57, No. 2. pp. 339-358.
@article{a6003aa97617405aa4e1d8ad9b6a482b,
title = "Identification of miRNAs and their targets in the liverwort Marchantia polymorpha by integrating RNA-Seq and degradome analyses",
abstract = "Bryophytes (liverworts, hornworts and mosses) comprise the three earliest diverging lineages of land plants (embryophytes). Marchantia polymorpha, a complex thalloid Marchantiopsida liverwort that has been developed into a model genetic system, occupies a key phylogenetic position. Therefore, M. polymorpha is useful in studies aiming to elucidate the evolution of gene regulation mechanisms in plants. In this study, we used computational, transcriptomic, small RNA and degradome analyses to characterize microRNA (miRNA)-mediated pathways of gene regulation in M. polymorpha. The data have been integrated into the open access ContigViews-miRNA platform for further reference. In addition to core components of the miRNA pathway, 129 unique miRNA sequences, 11 of which could be classified into seven miRNA families that are conserved in embryophytes (miR166a, miR390, miR529c, miR171-3p, miR408a, miR160 and miR319a), were identified. A combination of computational and degradome analyses allowed us to identify and experimentally validate 249 targets. In some cases, the target genes are orthologous to those of other embryophytes, but in other cases, the conserved miRNAs target either paralogs or members of different gene families. In addition, the newly discovered Mpo-miR11707.1 and Mpo-miR11707.2 are generated from a common precursor and target MpARGONAUTE1 (LW1759). Two other newly discovered miRNAs, Mpo-miR11687.1 and MpomiR11681.1, target the MADS-box transcription factors MpMADS1 and MpMADS2, respectively. Interestingly, one of the pentatricopeptide repeat (PPR) gene family members, MpPPR-66 (LW9825), the protein products of which are generally involved in various steps of RNA metabolism, has a long stem-loop transcript that can generate MpomiR11692.1 to autoregulate MpPPR-66 (LW9825) mRNA. This study provides a foundation for further investigations of the RNA-mediated silencing mechanism in M. polymorpha as well as of the evolution of this gene silencing pathway in embryophytes.",
author = "Lin, {Pin Chun} and Lu, {Chia Wei} and Shen, {Bing Nan} and Lee, {Guan Z.} and Bowman, {John L.} and Arteaga-Vazquez, {Mario A.} and {Daisy Liu}, {Li Yu} and Hong, {Syuan Fei} and Chu-Fang Lo and Su, {Gong Min} and Takayuki Kohchi and Kimitsune Ishizaki and Sabine Zachgo and Felix Althoff and Mizuki Takenaka and Yamato, {Katsuyuki T.} and Lin, {Shih Shun}",
year = "2016",
month = "2",
day = "1",
doi = "10.1093/pcp/pcw020",
language = "English",
volume = "57",
pages = "339--358",
journal = "Plant and Cell Physiology",
issn = "0032-0781",
publisher = "Oxford University Press",
number = "2",

}

Lin, PC, Lu, CW, Shen, BN, Lee, GZ, Bowman, JL, Arteaga-Vazquez, MA, Daisy Liu, LY, Hong, SF, Lo, C-F, Su, GM, Kohchi, T, Ishizaki, K, Zachgo, S, Althoff, F, Takenaka, M, Yamato, KT & Lin, SS 2016, 'Identification of miRNAs and their targets in the liverwort Marchantia polymorpha by integrating RNA-Seq and degradome analyses', Plant and Cell Physiology, vol. 57, no. 2, pp. 339-358. https://doi.org/10.1093/pcp/pcw020

Identification of miRNAs and their targets in the liverwort Marchantia polymorpha by integrating RNA-Seq and degradome analyses. / Lin, Pin Chun; Lu, Chia Wei; Shen, Bing Nan; Lee, Guan Z.; Bowman, John L.; Arteaga-Vazquez, Mario A.; Daisy Liu, Li Yu; Hong, Syuan Fei; Lo, Chu-Fang; Su, Gong Min; Kohchi, Takayuki; Ishizaki, Kimitsune; Zachgo, Sabine; Althoff, Felix; Takenaka, Mizuki; Yamato, Katsuyuki T.; Lin, Shih Shun.

In: Plant and Cell Physiology, Vol. 57, No. 2, 01.02.2016, p. 339-358.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Identification of miRNAs and their targets in the liverwort Marchantia polymorpha by integrating RNA-Seq and degradome analyses

AU - Lin, Pin Chun

AU - Lu, Chia Wei

AU - Shen, Bing Nan

AU - Lee, Guan Z.

AU - Bowman, John L.

AU - Arteaga-Vazquez, Mario A.

AU - Daisy Liu, Li Yu

AU - Hong, Syuan Fei

AU - Lo, Chu-Fang

AU - Su, Gong Min

AU - Kohchi, Takayuki

AU - Ishizaki, Kimitsune

AU - Zachgo, Sabine

AU - Althoff, Felix

AU - Takenaka, Mizuki

AU - Yamato, Katsuyuki T.

AU - Lin, Shih Shun

PY - 2016/2/1

Y1 - 2016/2/1

N2 - Bryophytes (liverworts, hornworts and mosses) comprise the three earliest diverging lineages of land plants (embryophytes). Marchantia polymorpha, a complex thalloid Marchantiopsida liverwort that has been developed into a model genetic system, occupies a key phylogenetic position. Therefore, M. polymorpha is useful in studies aiming to elucidate the evolution of gene regulation mechanisms in plants. In this study, we used computational, transcriptomic, small RNA and degradome analyses to characterize microRNA (miRNA)-mediated pathways of gene regulation in M. polymorpha. The data have been integrated into the open access ContigViews-miRNA platform for further reference. In addition to core components of the miRNA pathway, 129 unique miRNA sequences, 11 of which could be classified into seven miRNA families that are conserved in embryophytes (miR166a, miR390, miR529c, miR171-3p, miR408a, miR160 and miR319a), were identified. A combination of computational and degradome analyses allowed us to identify and experimentally validate 249 targets. In some cases, the target genes are orthologous to those of other embryophytes, but in other cases, the conserved miRNAs target either paralogs or members of different gene families. In addition, the newly discovered Mpo-miR11707.1 and Mpo-miR11707.2 are generated from a common precursor and target MpARGONAUTE1 (LW1759). Two other newly discovered miRNAs, Mpo-miR11687.1 and MpomiR11681.1, target the MADS-box transcription factors MpMADS1 and MpMADS2, respectively. Interestingly, one of the pentatricopeptide repeat (PPR) gene family members, MpPPR-66 (LW9825), the protein products of which are generally involved in various steps of RNA metabolism, has a long stem-loop transcript that can generate MpomiR11692.1 to autoregulate MpPPR-66 (LW9825) mRNA. This study provides a foundation for further investigations of the RNA-mediated silencing mechanism in M. polymorpha as well as of the evolution of this gene silencing pathway in embryophytes.

AB - Bryophytes (liverworts, hornworts and mosses) comprise the three earliest diverging lineages of land plants (embryophytes). Marchantia polymorpha, a complex thalloid Marchantiopsida liverwort that has been developed into a model genetic system, occupies a key phylogenetic position. Therefore, M. polymorpha is useful in studies aiming to elucidate the evolution of gene regulation mechanisms in plants. In this study, we used computational, transcriptomic, small RNA and degradome analyses to characterize microRNA (miRNA)-mediated pathways of gene regulation in M. polymorpha. The data have been integrated into the open access ContigViews-miRNA platform for further reference. In addition to core components of the miRNA pathway, 129 unique miRNA sequences, 11 of which could be classified into seven miRNA families that are conserved in embryophytes (miR166a, miR390, miR529c, miR171-3p, miR408a, miR160 and miR319a), were identified. A combination of computational and degradome analyses allowed us to identify and experimentally validate 249 targets. In some cases, the target genes are orthologous to those of other embryophytes, but in other cases, the conserved miRNAs target either paralogs or members of different gene families. In addition, the newly discovered Mpo-miR11707.1 and Mpo-miR11707.2 are generated from a common precursor and target MpARGONAUTE1 (LW1759). Two other newly discovered miRNAs, Mpo-miR11687.1 and MpomiR11681.1, target the MADS-box transcription factors MpMADS1 and MpMADS2, respectively. Interestingly, one of the pentatricopeptide repeat (PPR) gene family members, MpPPR-66 (LW9825), the protein products of which are generally involved in various steps of RNA metabolism, has a long stem-loop transcript that can generate MpomiR11692.1 to autoregulate MpPPR-66 (LW9825) mRNA. This study provides a foundation for further investigations of the RNA-mediated silencing mechanism in M. polymorpha as well as of the evolution of this gene silencing pathway in embryophytes.

UR - http://www.scopus.com/inward/record.url?scp=84964818704&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84964818704&partnerID=8YFLogxK

U2 - 10.1093/pcp/pcw020

DO - 10.1093/pcp/pcw020

M3 - Article

C2 - 26861787

AN - SCOPUS:84964818704

VL - 57

SP - 339

EP - 358

JO - Plant and Cell Physiology

JF - Plant and Cell Physiology

SN - 0032-0781

IS - 2

ER -