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

Title: Grasses suppress shoot-borne roots to conserve water during drought

Abstract

Many important crops are members of the Poaceae family, which develop root systems characterized by a high degree of root initiation from the belowground basal nodes of the shoot, termed the crown. Although this postembryonic shoot-borne root system represents the major conduit for water uptake, little is known about the effect of water availability on its development. Here in this study, we demonstrate that in the model C4 grass Setaria viridis, the crown locally senses water availability and suppresses postemergence crown root growth under a water deficit. This response was observed in field and growth room environments and in all grass species tested. Luminescence-based imaging of root systems grown in soil-like media revealed a shift in root growth from crown-derived to primary root-derived branches, suggesting that primary root-dominated architecture can be induced in S. viridis under certain stress conditions. Crown roots of Zea mays and Setaria italica, domesticated relatives of teosinte and S. viridis, respectively, show reduced sensitivity to water deficit, suggesting that this response might have been influenced by human selection. Lastly, enhanced water status of maize mutants lacking crown roots suggests that under a water deficit, stronger suppression of crown roots actually may benefit crop productivity.

Authors:
 [1];  [1];  [2];  [3];  [4];  [4];  [1];  [5];  [4]; ORCiD logo [6];  [4]; ORCiD logo [7]; ORCiD logo [4]; ORCiD logo [1]
  1. Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305,
  2. Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305,, Coordination for the Improvement of Higher Education Personnel (CAPES) Foundation, Ministry of Education of Brazil, Brasilia-DF 70.040-020, Brazil,
  3. Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305,, Unidad de Genómica Avanzada, Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 36821 Irapuato, Mexico,
  4. Donald Danforth Plant Science Center, St. Louis, MO 63162,
  5. Department of Biotechnology, College of Life Sciences and Biotechnology, Yonsei University, Seoul 03722, Korea,
  6. Donald Danforth Plant Science Center, St. Louis, MO 63162,, Plant Physiology and Genetics Research, Agricultural Research Unit, US Department of Agriculture, St. Louis, MO 63132,
  7. Crop Functional Genomics, Institute of Crop Science and Resource Conservation, University of Bonn, D-53113 Bonn, Germany
Publication Date:
Research Org.:
Carnegie Inst. of Science, Stanford, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1263687
Alternate Identifier(s):
OSTI ID: 1469568
Grant/Contract Number:  
SC0008769
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: 31; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; root development; drought; Poaceae; Setaria; Zea mays

Citation Formats

Sebastian, Jose, Yee, Muh-Ching, Goudinho Viana, Willian, Rellán-Álvarez, Rubén, Feldman, Max, Priest, Henry D., Trontin, Charlotte, Lee, Tak, Jiang, Hui, Baxter, Ivan, Mockler, Todd C., Hochholdinger, Frank, Brutnell, Thomas P., and Dinneny, José R. Grasses suppress shoot-borne roots to conserve water during drought. United States: N. p., 2016. Web. doi:10.1073/pnas.1604021113.
Sebastian, Jose, Yee, Muh-Ching, Goudinho Viana, Willian, Rellán-Álvarez, Rubén, Feldman, Max, Priest, Henry D., Trontin, Charlotte, Lee, Tak, Jiang, Hui, Baxter, Ivan, Mockler, Todd C., Hochholdinger, Frank, Brutnell, Thomas P., & Dinneny, José R. Grasses suppress shoot-borne roots to conserve water during drought. United States. https://doi.org/10.1073/pnas.1604021113
Sebastian, Jose, Yee, Muh-Ching, Goudinho Viana, Willian, Rellán-Álvarez, Rubén, Feldman, Max, Priest, Henry D., Trontin, Charlotte, Lee, Tak, Jiang, Hui, Baxter, Ivan, Mockler, Todd C., Hochholdinger, Frank, Brutnell, Thomas P., and Dinneny, José R. Fri . "Grasses suppress shoot-borne roots to conserve water during drought". United States. https://doi.org/10.1073/pnas.1604021113.
@article{osti_1263687,
title = {Grasses suppress shoot-borne roots to conserve water during drought},
author = {Sebastian, Jose and Yee, Muh-Ching and Goudinho Viana, Willian and Rellán-Álvarez, Rubén and Feldman, Max and Priest, Henry D. and Trontin, Charlotte and Lee, Tak and Jiang, Hui and Baxter, Ivan and Mockler, Todd C. and Hochholdinger, Frank and Brutnell, Thomas P. and Dinneny, José R.},
abstractNote = {Many important crops are members of the Poaceae family, which develop root systems characterized by a high degree of root initiation from the belowground basal nodes of the shoot, termed the crown. Although this postembryonic shoot-borne root system represents the major conduit for water uptake, little is known about the effect of water availability on its development. Here in this study, we demonstrate that in the model C4 grass Setaria viridis, the crown locally senses water availability and suppresses postemergence crown root growth under a water deficit. This response was observed in field and growth room environments and in all grass species tested. Luminescence-based imaging of root systems grown in soil-like media revealed a shift in root growth from crown-derived to primary root-derived branches, suggesting that primary root-dominated architecture can be induced in S. viridis under certain stress conditions. Crown roots of Zea mays and Setaria italica, domesticated relatives of teosinte and S. viridis, respectively, show reduced sensitivity to water deficit, suggesting that this response might have been influenced by human selection. Lastly, enhanced water status of maize mutants lacking crown roots suggests that under a water deficit, stronger suppression of crown roots actually may benefit crop productivity.},
doi = {10.1073/pnas.1604021113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 31,
volume = 113,
place = {United States},
year = {Fri Jul 15 00:00:00 EDT 2016},
month = {Fri Jul 15 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1604021113

Citation Metrics:
Cited by: 71 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Genetic Dissection of Root Formation in Maize (Zea mays) Reveals Root-type Specific Developmental Programmes
journal, February 2004


Transcriptional Regulation of ROS Controls Transition from Proliferation to Differentiation in the Root
journal, November 2010


Isolation and characterization of rtcs, a maize mutant deficient in the formation of nodal roots
journal, November 1996


GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems
journal, August 2015

  • Rellán-Álvarez, Rubén; Lobet, Guillaume; Lindner, Heike
  • eLife, Vol. 4
  • DOI: 10.7554/eLife.07597

Root Architecture and Plant Productivity
journal, September 1995


Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009


The influence of alternative pathways of respiration that utilize branched-chain amino acids following water shortage in Arabidopsis : Influence of the ETF/ETFQO pathway under water stress
journal, March 2016

  • Pires, Marcel V.; Pereira Júnior, Adilson A.; Medeiros, David B.
  • Plant, Cell & Environment, Vol. 39, Issue 6
  • DOI: 10.1111/pce.12682

A Re-Examination of the Relative Turgidity Technique for Estimating Water Deficits in Leaves
journal, January 1962

  • Barrs, Hd; Weatherley, Pe
  • Australian Journal of Biological Sciences, Vol. 15, Issue 3
  • DOI: 10.1071/BI9620413

Improved scoring of functional groups from gene expression data by decorrelating GO graph structure
journal, April 2006


The divining root: moisture-driven responses of roots at the micro- and macro-scale
journal, January 2015

  • Robbins, Neil E.; Dinneny, José R.
  • Journal of Experimental Botany, Vol. 66, Issue 8
  • DOI: 10.1093/jxb/eru496

Setaria viridis : A Model for C 4 Photosynthesis
journal, August 2010

  • Brutnell, Thomas P.; Wang, Lin; Swartwood, Kerry
  • The Plant Cell, Vol. 22, Issue 8
  • DOI: 10.1105/tpc.110.075309

Genome-wide characterization of microRNA in foxtail millet (Setaria italica)
journal, January 2013


The nodal roots of Zea : their development in relation to structural features of the stem
journal, November 1986

  • Hoppe, D. C.; McCully, M. E.; Wenzel, C. L.
  • Canadian Journal of Botany, Vol. 64, Issue 11
  • DOI: 10.1139/b86-335

Circadian rhythms of hydraulic conductance and growth are enhanced by drought and improve plant performance
journal, November 2014

  • Caldeira, Cecilio F.; Jeanguenin, Linda; Chaumont, François
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms6365

Specific and sensitive quantitative RT-PCR of miRNAs with DNA primers
journal, January 2011

  • Balcells, Ingrid; Cirera, Susanna; Busk, Peter K.
  • BMC Biotechnology, Vol. 11, Issue 1
  • DOI: 10.1186/1472-6750-11-70

Bioinformatic identification and experimental validation of miRNAs from foxtail millet (Setaria italica)
journal, August 2014


Low Crown Root Number Enhances Nitrogen Acquisition from Low-Nitrogen Soils in Maize
journal, April 2014


Roots of the Second Green Revolution
journal, January 2007

  • Lynch, Jonathan P.
  • Australian Journal of Botany, Vol. 55, Issue 5
  • DOI: 10.1071/BT06118

From weeds to crops: genetic analysis of root development in cereals
journal, January 2004


Gene Ontology: tool for the unification of biology
journal, May 2000

  • Ashburner, Michael; Ball, Catherine A.; Blake, Judith A.
  • Nature Genetics, Vol. 25, Issue 1
  • DOI: 10.1038/75556

Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012


R/qtl: QTL mapping in experimental crosses
journal, May 2003


NAC transcription factors in plant multiple abiotic stress responses: progress and prospects
journal, October 2015


Phytozome: a comparative platform for green plant genomics
journal, November 2011

  • Goodstein, David M.; Shu, Shengqiang; Howson, Russell
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr944

Bioconductor: open software development for computational biology and bioinformatics
journal, September 2004

  • Gentleman, Robert C.; Carey, Vincent J.; Bates, Douglas M.
  • Genome Biology, Vol. 5, Issue 10, p. R80
  • DOI: 10.1186/gb-2004-5-10-r80

Methods to Promote Germination of Dormant Setaria viridis Seeds
journal, April 2014


Rice Plant Development: from Zygote to Spikelet
journal, January 2005

  • Itoh, Jun-Ichi; Nonomura, Ken-Ichi; Ikeda, Kyoko
  • Plant and Cell Physiology, Vol. 46, Issue 1
  • DOI: 10.1093/pcp/pci501

Comprehensive Analysis of NAC Family Genes in Oryza sativa and Arabidopsis thaliana
journal, January 2003


Brachypodium distachyon and Setaria viridis : Model Genetic Systems for the Grasses
journal, April 2015


NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems
journal, January 2013


Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses
journal, March 2011

  • Li, P.; Brutnell, T. P.
  • Journal of Experimental Botany, Vol. 62, Issue 9
  • DOI: 10.1093/jxb/err096

Genetic Design and Statistical Power of Nested Association Mapping in Maize
journal, January 2008


Post-embryonic root organogenesis in cereals: branching out from model plants
journal, August 2013


Genetic control of root development in rice, the model cereal
journal, April 2010