DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Translational Control of Arabidopsis Meristem Stability and Organogenesis by the Eukaryotic Translation Factor eIF3h

Abstract

Essentially all aboveground plant tissues develop from the stem cells in the primary shoot apical meristem. Proliferation of the stem cell population in the Arabidopsis shoot apical meristem is tightly controlled by a feedback loop formed primarily by the homeodomain transcription factor WUSCHEL (WUS) and the CLAVATA ligand-receptor system. In this study, it is shown that mutation of a translation initiation factor, eIF3h, causes a tendency to develop a strikingly enlarged shoot apical meristem with elevated and ectopic expression of WUS and CLAVATA3 (CLV3). Many of the mRNAs that function in apical meristem maintenance possess upstream open reading frames (uORFs), translational attenuators that render translation partially dependent on eIF3h. Specifically, the mRNA for the receptor kinase, CLV1, is undertranslated in the eif3h mutant as shown by transient and transgenic expression assays. Concordant phenotypic observations include defects in organ polarity and in translation of another uORF-containing mRNA, ASYMMETRIC LEAVES 1 (AS1), in eif3h. In summary, the expression of developmental regulatory mRNAs is attenuated by uORFs, and this attenuation is balanced in part by the translation initiation factor, eIF3h. Thus, translational control plays a key role in Arabidopsis stem cell regulation and organogenesis.

Authors:
 [1];  [1];  [1];  [1];  [1]
  1. University of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Univ. of Tennessee, Knoxville, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1904581
Grant/Contract Number:  
FG02-96ER20223; IS3901-06C
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 9; Journal Issue: 4; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; messenger RNA; protein translation; leaves; meristems; shoot apical meristem; Arabidopsis thaliana; seedings; inflorescences

Citation Formats

Zhou, Fujun, Roy, Bijoyita, Dunlap, John R., Enganti, Ramya, and von Arnim, Albrecht G. Translational Control of Arabidopsis Meristem Stability and Organogenesis by the Eukaryotic Translation Factor eIF3h. United States: N. p., 2014. Web. doi:10.1371/journal.pone.0095396.
Zhou, Fujun, Roy, Bijoyita, Dunlap, John R., Enganti, Ramya, & von Arnim, Albrecht G. Translational Control of Arabidopsis Meristem Stability and Organogenesis by the Eukaryotic Translation Factor eIF3h. United States. https://doi.org/10.1371/journal.pone.0095396
Zhou, Fujun, Roy, Bijoyita, Dunlap, John R., Enganti, Ramya, and von Arnim, Albrecht G. Tue . "Translational Control of Arabidopsis Meristem Stability and Organogenesis by the Eukaryotic Translation Factor eIF3h". United States. https://doi.org/10.1371/journal.pone.0095396. https://www.osti.gov/servlets/purl/1904581.
@article{osti_1904581,
title = {Translational Control of Arabidopsis Meristem Stability and Organogenesis by the Eukaryotic Translation Factor eIF3h},
author = {Zhou, Fujun and Roy, Bijoyita and Dunlap, John R. and Enganti, Ramya and von Arnim, Albrecht G.},
abstractNote = {Essentially all aboveground plant tissues develop from the stem cells in the primary shoot apical meristem. Proliferation of the stem cell population in the Arabidopsis shoot apical meristem is tightly controlled by a feedback loop formed primarily by the homeodomain transcription factor WUSCHEL (WUS) and the CLAVATA ligand-receptor system. In this study, it is shown that mutation of a translation initiation factor, eIF3h, causes a tendency to develop a strikingly enlarged shoot apical meristem with elevated and ectopic expression of WUS and CLAVATA3 (CLV3). Many of the mRNAs that function in apical meristem maintenance possess upstream open reading frames (uORFs), translational attenuators that render translation partially dependent on eIF3h. Specifically, the mRNA for the receptor kinase, CLV1, is undertranslated in the eif3h mutant as shown by transient and transgenic expression assays. Concordant phenotypic observations include defects in organ polarity and in translation of another uORF-containing mRNA, ASYMMETRIC LEAVES 1 (AS1), in eif3h. In summary, the expression of developmental regulatory mRNAs is attenuated by uORFs, and this attenuation is balanced in part by the translation initiation factor, eIF3h. Thus, translational control plays a key role in Arabidopsis stem cell regulation and organogenesis.},
doi = {10.1371/journal.pone.0095396},
journal = {PLoS ONE},
number = 4,
volume = 9,
place = {United States},
year = {Tue Apr 15 00:00:00 EDT 2014},
month = {Tue Apr 15 00:00:00 EDT 2014}
}

Works referenced in this record:

Regulation of Translation Initiation under Biotic and Abiotic Stresses
journal, February 2013

  • Echevarría-Zomeño, Sira; Yángüez, Emilio; Fernández-Bautista, Nuria
  • International Journal of Molecular Sciences, Vol. 14, Issue 3
  • DOI: 10.3390/ijms14034670

Involvement of ribosomal protein RPL27a in meristem activity and organ development
journal, May 2011


Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development: A comparative study of r-protein mutants
journal, January 2011


The Arabidopsis STV1 Protein, Responsible for Translation Reinitiation, Is Required for Auxin-Mediated Gynoecium Patterning
journal, October 2005

  • Nishimura, Taisuke; Wada, Takuji; Yamamoto, Kotaro T.
  • The Plant Cell, Vol. 17, Issue 11
  • DOI: 10.1105/tpc.105.036533

Arabidopsis CLV3 Peptide Directly Binds CLV1 Ectodomain
journal, January 2008


Known and novel post-transcriptional regulatory sequences are conserved across plant families
journal, January 2012


Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem
journal, August 2009

  • Gordon, S. P.; Chickarmane, V. S.; Ohno, C.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
  • DOI: 10.1073/pnas.0908122106

CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification
journal, September 2010


Regulation of phyllotaxis by polar auxin transport
journal, November 2003

  • Reinhardt, Didier; Pesce, Eva-Rachele; Stieger, Pia
  • Nature, Vol. 426, Issue 6964
  • DOI: 10.1038/nature02081

Ribosomes and translation in plant developmental control
journal, August 2012


Plant Stem Cell Niches
journal, June 2012


RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis
journal, November 2010

  • Kinoshita, Atsuko; Betsuyaku, Shigeyuki; Osakabe, Yuriko
  • Development, Vol. 137, Issue 22
  • DOI: 10.1242/dev.048199

Heterogeneity of Arabidopsis core promoters revealed by high-density TSS analysis
journal, October 2009


Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins
journal, February 2008

  • Pinon, V.; Etchells, J. P.; Rossignol, P.
  • Development, Vol. 135, Issue 7
  • DOI: 10.1242/dev.016469

Role of WUSCHEL in Regulating Stem Cell Fate in the Arabidopsis Shoot Meristem
journal, December 1998


Auxin Synthesized by the YUCCA Flavin Monooxygenases Is Essential for Embryogenesis and Leaf Formation in Arabidopsis
journal, August 2007


Ribosomal proteins promote leaf adaxial identity
journal, April 2008


Translational Regulation of Cytoplasmic mRNAs
journal, January 2013

  • Roy, Bijoyita; Arnim, Albrecht G. von
  • The Arabidopsis Book, Vol. 11
  • DOI: 10.1199/tab.0165

On the functions of the h subunit of eukaryotic initiation factor 3 in late stages of translation initiation
journal, January 2007


WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex
journal, October 2011

  • Yadav, Ram Kishor; Perales, Mariano; Gruel, Jérémy
  • Genes & Development, Vol. 25, Issue 19
  • DOI: 10.1101/gad.17258511

Regulation of CLV3 Expression by Two Homeobox Genes in Arabidopsis
journal, June 2002

  • Brand, Ulrike; Grünewald, Margit; Hobe, Martin
  • Plant Physiology, Vol. 129, Issue 2
  • DOI: 10.1104/pp.001867

Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis
journal, June 2007


Functional reconstitution of human eukaryotic translation initiation factor 3 (eIF3)
journal, December 2011

  • Sun, C.; Todorovic, A.; Querol-Audi, J.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
  • DOI: 10.1073/pnas.1116821108

MultipleMONOPTEROS-Dependent Pathways Are Involved in Leaf Initiation    
journal, August 2008

  • Schuetz, Mathias; Berleth, Thomas; Mattsson, Jim
  • Plant Physiology, Vol. 148, Issue 2
  • DOI: 10.1104/pp.108.119396

Control of cytoplasmic translation in plants: Control of cytoplasmic translation
journal, January 2012

  • Muench, Douglas G.; Zhang, Chi; Dahodwala, Murtaza
  • Wiley Interdisciplinary Reviews: RNA, Vol. 3, Issue 2
  • DOI: 10.1002/wrna.1104

A Role for Nonsense-Mediated mRNA Decay in Plants: Pathogen Responses Are Induced in Arabidopsis thaliana NMD Mutants
journal, February 2012


Influences of mRNA secondary structure on initiation by eukaryotic ribosomes.
journal, May 1986


Cellular Parameters of the Shoot Apical Meristem in Arabidopsis
journal, August 1998

  • Laufs, Patrick; Grandjean, Olivier; Jonak, Claudia
  • The Plant Cell, Vol. 10, Issue 8
  • DOI: 10.1105/tpc.10.8.1375

‘Ribozoomin’ – Translation Initiation from the Perspective of the Ribosome-bound Eukaryotic Initiation Factors (eIFs)
journal, July 2012


Reconstitution reveals the functional core of mammalian eIF3
journal, June 2007

  • Masutani, Mamiko; Sonenberg, Nahum; Yokoyama, Shigeyuki
  • The EMBO Journal, Vol. 26, Issue 14
  • DOI: 10.1038/sj.emboj.7601765

A Tobamovirus Genome That Contains an Internal Ribosome Entry Site Functionalin Vitro
journal, May 1997


The global translation profile in a ribosomal protein mutant resembles that of an eIF3 mutant
journal, December 2013


Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis
journal, December 2000

  • Byrne, Mary E.; Barley, Ross; Curtis, Mark
  • Nature, Vol. 408, Issue 6815
  • DOI: 10.1038/35050091

The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity
journal, February 2014

  • Mandel, Tali; Moreau, Fanny; Kutsher, Yaarit
  • Development, Vol. 141, Issue 4
  • DOI: 10.1242/dev.104687

WUSCHEL mediates stem cell homeostasis by regulating stem cell number and patterns of cell division and differentiation of stem cell progenitors
journal, November 2010

  • Yadav, Ram Kishor; Tavakkoli, Montreh; Reddy, G. Venugopala
  • Development, Vol. 137, Issue 21
  • DOI: 10.1242/dev.054973

TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h
journal, March 2013

  • Schepetilnikov, Mikhail; Dimitrova, Maria; Mancera-Martínez, Eder
  • The EMBO Journal, Vol. 32, Issue 8
  • DOI: 10.1038/emboj.2013.61

Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors
journal, November 2012

  • Rosado, A.; Li, R.; van de Ven, W.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 48
  • DOI: 10.1073/pnas.1214774109

WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis
journal, April 2005

  • Kwon, Chang Seob; Chen, Changbin; Wagner, Doris
  • Genes & Development, Vol. 19, Issue 8
  • DOI: 10.1101/gad.1276305

The Receptor Kinase CORYNE of Arabidopsis Transmits the Stem Cell–Limiting Signal CLAVATA3 Independently of CLAVATA1
journal, April 2008

  • Müller, Ralf; Bleckmann, Andrea; Simon, Rüdiger
  • The Plant Cell, Vol. 20, Issue 4
  • DOI: 10.1105/tpc.107.057547

Noise in eukaryotic gene expression
journal, April 2003

  • Blake, William J.; KÆrn, Mads; Cantor, Charles R.
  • Nature, Vol. 422, Issue 6932
  • DOI: 10.1038/nature01546

Plant Stem Cell Signaling Involves Ligand-Dependent Trafficking of the CLAVATA1 Receptor Kinase
journal, March 2011


CORONA, a Member of the Class III Homeodomain Leucine Zipper Gene Family in Arabidopsis, Regulates Stem Cell Specification and Organogenesis
journal, March 2005

  • Green, Kirsten A.; Prigge, Michael J.; Katzman, Rebecca B.
  • The Plant Cell, Vol. 17, Issue 3
  • DOI: 10.1105/tpc.104.026179

Transcriptional Control of a Plant Stem Cell Niche
journal, May 2010


Gene trapping of the Arabidopsis genome with a firefly luciferase reporter
journal, June 2003


Regulation of noise in the expression of a single gene
journal, April 2002

  • Ozbudak, Ertugrul M.; Thattai, Mukund; Kurtser, Iren
  • Nature Genetics, Vol. 31, Issue 1
  • DOI: 10.1038/ng869

A Tobamovirus Genome That Contains an Internal Ribosome Entry Site Functionalin Vitro
journal, May 1997


Introduction of mRNA to plant protoplasts using polyethylene glycol
journal, December 1993


Plant Stem Cell Signaling Involves Ligand-Dependent Trafficking of the CLAVATA1 Receptor Kinase
journal, March 2011


Transcriptome and Genome-Wide Analysis of the Arabidopsis Stem Cell Regulator WUS
journal, May 2010


The CLAVATA1Gene Encodes a Putative Receptor Kinase That Controls Shoot and Floral Meristem Size in Arabidopsis
journal, May 1997


The PHANTASTICA Gene Encodes a MYB Transcription Factor Involved in Growth and Dorsoventrality of Lateral Organs in Antirrhinum
journal, May 1998


Termination of Stem Cell Maintenance in Arabidopsis Floral Meristems by Interactions between WUSCHEL and AGAMOUS
journal, June 2001


Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis
journal, December 2000

  • Byrne, Mary E.; Barley, Ross; Curtis, Mark
  • Nature, Vol. 408, Issue 6815
  • DOI: 10.1038/35050091

TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h
journal, March 2013

  • Schepetilnikov, Mikhail; Dimitrova, Maria; Mancera-Martínez, Eder
  • The EMBO Journal, Vol. 32, Issue 8
  • DOI: 10.1038/emboj.2013.61

Noise in eukaryotic gene expression
journal, April 2003

  • Blake, William J.; KÆrn, Mads; Cantor, Charles R.
  • Nature, Vol. 422, Issue 6932
  • DOI: 10.1038/nature01546

Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis
journal, June 2007


Reconstitution reveals the functional core of mammalian eIF3
journal, June 2007

  • Masutani, Mamiko; Sonenberg, Nahum; Yokoyama, Shigeyuki
  • The EMBO Journal, Vol. 26, Issue 14
  • DOI: 10.1038/sj.emboj.7601765

Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem
journal, August 2009

  • Gordon, S. P.; Chickarmane, V. S.; Ohno, C.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
  • DOI: 10.1073/pnas.0908122106

Functional reconstitution of human eukaryotic translation initiation factor 3 (eIF3)
journal, December 2011

  • Sun, C.; Todorovic, A.; Querol-Audi, J.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
  • DOI: 10.1073/pnas.1116821108

Influences of mRNA secondary structure on initiation by eukaryotic ribosomes.
journal, May 1986


Plant Initiation Factor 3 Subunit Composition Resembles Mammalian Initiation Factor 3 and Has a Novel Subunit
journal, January 2001

  • Burks, Elizabeth A.; Bezerra, Paula P.; Le, Hahn
  • Journal of Biological Chemistry, Vol. 276, Issue 3
  • DOI: 10.1074/jbc.m007236200

WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex
journal, October 2011

  • Yadav, Ram Kishor; Perales, Mariano; Gruel, Jérémy
  • Genes & Development, Vol. 25, Issue 19
  • DOI: 10.1101/gad.17258511

MultipleMONOPTEROS-Dependent Pathways Are Involved in Leaf Initiation    
journal, August 2008

  • Schuetz, Mathias; Berleth, Thomas; Mattsson, Jim
  • Plant Physiology, Vol. 148, Issue 2
  • DOI: 10.1104/pp.108.119396

Cellular Parameters of the Shoot Apical Meristem in Arabidopsis
journal, August 1998

  • Laufs, Patrick; Grandjean, Olivier; Jonak, Claudia
  • The Plant Cell, Vol. 10, Issue 8
  • DOI: 10.1105/tpc.10.8.1375

CORONA, a Member of the Class III Homeodomain Leucine Zipper Gene Family in Arabidopsis, Regulates Stem Cell Specification and Organogenesis
journal, March 2005

  • Green, Kirsten A.; Prigge, Michael J.; Katzman, Rebecca B.
  • The Plant Cell, Vol. 17, Issue 3
  • DOI: 10.1105/tpc.104.026179

The Arabidopsis STV1 Protein, Responsible for Translation Reinitiation, Is Required for Auxin-Mediated Gynoecium Patterning
journal, October 2005

  • Nishimura, Taisuke; Wada, Takuji; Yamamoto, Kotaro T.
  • The Plant Cell, Vol. 17, Issue 11
  • DOI: 10.1105/tpc.105.036533

Auxin Synthesized by the YUCCA Flavin Monooxygenases Is Essential for Embryogenesis and Leaf Formation in Arabidopsis
journal, August 2007


The Receptor Kinase CORYNE of Arabidopsis Transmits the Stem Cell–Limiting Signal CLAVATA3 Independently of CLAVATA1
journal, April 2008

  • Müller, Ralf; Bleckmann, Andrea; Simon, Rüdiger
  • The Plant Cell, Vol. 20, Issue 4
  • DOI: 10.1105/tpc.107.057547

A suite of tools and application notes for in vivo protein interaction assays using bioluminescence resonance energy transfer (BRET)
journal, October 2006


Arabidopsis CLV3 Peptide Directly Binds CLV1 Ectodomain
journal, January 2008


Plant Stem Cell Niches
journal, June 2012


On the functions of the h subunit of eukaryotic initiation factor 3 in late stages of translation initiation
journal, January 2007


Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins
journal, February 2008

  • Pinon, V.; Etchells, J. P.; Rossignol, P.
  • Development, Vol. 135, Issue 7
  • DOI: 10.1242/dev.016469

RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis
journal, December 2010

  • Kinoshita, Atsuko; Betsuyaku, Shigeyuki; Osakabe, Yuriko
  • Development, Vol. 137, Issue 24
  • DOI: 10.1242/dev.061747

The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity
journal, February 2014

  • Mandel, Tali; Moreau, Fanny; Kutsher, Yaarit
  • Development, Vol. 141, Issue 4
  • DOI: 10.1242/dev.104687

A Role for Nonsense-Mediated mRNA Decay in Plants: Pathogen Responses Are Induced in Arabidopsis thaliana NMD Mutants
journal, February 2012


Regulation of Translation Initiation under Biotic and Abiotic Stresses
journal, February 2013

  • Echevarría-Zomeño, Sira; Yángüez, Emilio; Fernández-Bautista, Nuria
  • International Journal of Molecular Sciences, Vol. 14, Issue 3
  • DOI: 10.3390/ijms14034670

Works referencing / citing this record:

Please do not recycle! Translation reinitiation in microbes and higher eukaryotes
journal, December 2017

  • Gunišová, Stanislava; Hronová, Vladislava; Mohammad, Mahabub Pasha
  • FEMS Microbiology Reviews, Vol. 42, Issue 2
  • DOI: 10.1093/femsre/fux059