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Title: Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity

Abstract

Significance Plants both control and are controlled by the global climate. Grasses in natural and agricultural systems participate in the exchange of atmospheric CO 2 for biosphere-derived oxygen and water vapor via microscopic epidermal valves (stomata), but how these stomata are made in grasses is unknown. Using genetic screens and targeted genome editing, we identify and characterize master transcriptional regulators of stomatal initiation in the wheat relative Brachypodium . Surprisingly, the unique stomatal form and pattern of grasses is regulated by orthologs of Arabidopsis stomatal basic helix–loop–helix (bHLH) transcription factors, although the function of individual genes and regulation of their protein products have diverged. This finding suggests that the stomatal core bHLH transcription factors are excellent breeding targets to enhance performance in grasses.

Authors:
 [1];  [1];  [2]; ORCiD logo [3];  [4]
  1. Department of Biology, Stanford University, Stanford, CA 94305,
  2. Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305,
  3. Department of Energy Joint Genome Institute, Walnut Creek, CA 94598
  4. Department of Biology, Stanford University, Stanford, CA 94305,, Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305,
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1260426
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 113 Journal Issue: 29; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Raissig, Michael T., Abrash, Emily, Bettadapur, Akhila, Vogel, John P., and Bergmann, Dominique C. Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity. United States: N. p., 2016. Web. doi:10.1073/pnas.1606728113.
Raissig, Michael T., Abrash, Emily, Bettadapur, Akhila, Vogel, John P., & Bergmann, Dominique C. Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity. United States. https://doi.org/10.1073/pnas.1606728113
Raissig, Michael T., Abrash, Emily, Bettadapur, Akhila, Vogel, John P., and Bergmann, Dominique C. Tue . "Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity". United States. https://doi.org/10.1073/pnas.1606728113.
@article{osti_1260426,
title = {Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity},
author = {Raissig, Michael T. and Abrash, Emily and Bettadapur, Akhila and Vogel, John P. and Bergmann, Dominique C.},
abstractNote = {Significance Plants both control and are controlled by the global climate. Grasses in natural and agricultural systems participate in the exchange of atmospheric CO 2 for biosphere-derived oxygen and water vapor via microscopic epidermal valves (stomata), but how these stomata are made in grasses is unknown. Using genetic screens and targeted genome editing, we identify and characterize master transcriptional regulators of stomatal initiation in the wheat relative Brachypodium . Surprisingly, the unique stomatal form and pattern of grasses is regulated by orthologs of Arabidopsis stomatal basic helix–loop–helix (bHLH) transcription factors, although the function of individual genes and regulation of their protein products have diverged. This finding suggests that the stomatal core bHLH transcription factors are excellent breeding targets to enhance performance in grasses.},
doi = {10.1073/pnas.1606728113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 29,
volume = 113,
place = {United States},
year = {Tue Jul 05 00:00:00 EDT 2016},
month = {Tue Jul 05 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1606728113

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Works referenced in this record:

Termination of asymmetric cell division and differentiation of stomata
journal, December 2006

  • Pillitteri, Lynn Jo; Sloan, Daniel B.; Bogenschutz, Naomi L.
  • Nature, Vol. 445, Issue 7127
  • DOI: 10.1038/nature05467

Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses
journal, June 2009

  • Liu, T.; Ohashi-Ito, K.; Bergmann, D. C.
  • Development, Vol. 136, Issue 13
  • DOI: 10.1242/dev.032938

Gene Regulatory Networks and the Evolution of Animal Body Plans
journal, February 2006


Targeted mutagenesis in rice using CRISPR-Cas system
journal, September 2013

  • Miao, Jin; Guo, Dongshu; Zhang, Jinzhe
  • Cell Research, Vol. 23, Issue 10
  • DOI: 10.1038/cr.2013.123

Generation and Characterization of the Western Regional Research Center Brachypodium T-DNA Insertional Mutant Collection
journal, September 2012


Arabidopsis Stomatal Initiation Is Controlled by MAPK-Mediated Regulation of the bHLH SPEECHLESS
journal, November 2008


A Set of Modular Binary Vectors for Transformation of Cereals
journal, November 2007

  • Himmelbach, Axel; Zierold, Uwe; Hensel, Götz
  • Plant Physiology, Vol. 145, Issue 4
  • DOI: 10.1104/pp.107.111575

Patterns on the insect wing
journal, August 2007

  • Parchem, Ronald J.; Perry, Michael W.; Patel, Nipam H.
  • Current Opinion in Genetics & Development, Vol. 17, Issue 4
  • DOI: 10.1016/j.gde.2007.05.006

SCREAM/ICE1 and SCREAM2 Specify Three Cell-State Transitional Steps Leading to Arabidopsis Stomatal Differentiation
journal, July 2008

  • Kanaoka, Masahiro M.; Pillitteri, Lynn Jo; Fujii, Hiroaki
  • The Plant Cell, Vol. 20, Issue 7
  • DOI: 10.1105/tpc.108.060848

Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells
journal, September 2014


Interaction of Photoperiod and Vernalization Determines Flowering Time of Brachypodium distachyon
journal, December 2013

  • Ream, Thomas S.; Woods, Daniel P.; Schwartz, Christopher J.
  • Plant Physiology, Vol. 164, Issue 2
  • DOI: 10.1104/pp.113.232678

Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR
journal, January 2008


The Mechanical Diversity of Stomata and Its Significance in Gas-Exchange Control
journal, November 2006


Transcription factor control of asymmetric cell divisions that establish the stomatal lineage
journal, December 2006

  • MacAlister, Cora A.; Ohashi-Ito, Kyoko; Bergmann, Dominique C.
  • Nature, Vol. 445, Issue 7127
  • DOI: 10.1038/nature05491

Functional specialization of stomatal bHLHs through modification of DNA-binding and phosphoregulation potential
journal, October 2014

  • Davies, K. A.; Bergmann, D. C.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 43
  • DOI: 10.1073/pnas.1411766111

Arabidopsis FAMA Controls the Final Proliferation/Differentiation Switch during Stomatal Development
journal, October 2006


Molecular Framework of a Regulatory Circuit Initiating Two-Dimensional Spatial Patterning of Stomatal Lineage
journal, July 2015


Photorespiration and the Evolution of C 4 Photosynthesis
journal, June 2012


Identification of PAN2 by Quantitative Proteomics as a Leucine-Rich Repeat–Receptor-Like Kinase Acting Upstream of PAN1 to Polarize Cell Division in Maize
journal, November 2012

  • Zhang, Xiaoguo; Facette, Michelle; Humphries, John A.
  • The Plant Cell, Vol. 24, Issue 11
  • DOI: 10.1105/tpc.112.104125

PAN1: A Receptor-Like Protein That Promotes Polarization of an Asymmetric Cell Division in Maize
journal, January 2009


The SCAR/WAVE complex polarizes PAN receptors and promotes division asymmetry in maize
journal, January 2015

  • Facette, Michelle R.; Park, Yeri; Sutimantanapi, Dena
  • Nature Plants, Vol. 1, Issue 2
  • DOI: 10.1038/nplants.2014.24

Stomatal differentiation: the beginning and the end
journal, December 2015


Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis
journal, October 1986


The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea
journal, January 2016

  • Olsen, Jeanine L.; Rouzé, Pierre; Verhelst, Bram
  • Nature, Vol. 530, Issue 7590
  • DOI: 10.1038/nature16548

A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta
journal, September 2003

  • Curtis, Mark D.; Grossniklaus, Ueli
  • Plant Physiology, Vol. 133, Issue 2, p. 462-469
  • DOI: 10.1104/pp.103.027979

High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3
journal, November 2007


ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis
journal, April 2003


Evolutionary History of the Grasses
journal, March 2001


Molecular Profiling of Stomatal Meristemoids Reveals New Component of Asymmetric Cell Division and Commonalities among Stem Cell Populations in Arabidopsis
journal, September 2011

  • Pillitteri, Lynn Jo; Peterson, Kylee M.; Horst, Robin J.
  • The Plant Cell, Vol. 23, Issue 9
  • DOI: 10.1105/tpc.111.088583