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Title: Quantitative proteome profile of water deficit stress responses in eastern cottonwood ( Populus deltoides) leaves

Abstract

Drought stress is a recurring feature of world climate and the single most important factor influencing agricultural yield worldwide. Plants display highly variable, species-specific responses to drought and these responses are multifaceted, requiring physiological and morphological changes influenced by genetic and molecular mechanisms. Moreover, the reproducibility of water deficit studies is very cumbersome, which significantly impedes research on drought tolerance, because how a plant responds is highly influenced by the timing, duration, and intensity of the water deficit. Despite progress in the identification of drought-related mechanisms in many plants, the molecular basis of drought resistance remains to be fully understood in trees, particularly in poplar species because their wide geographic distribution results in varying tolerances to drought. Herein, we aimed to better understand this complex phenomenon in eastern cottonwood ( Populus deltoides) by performing a detailed contrast of the proteome changes between two different water deficit experiments to identify functional intersections and divergences in proteome responses. We investigated plants subjected to cyclic water deficit and compared these responses to plants subjected to prolonged acute water deficit. In total, we identified 108,012 peptide sequences across both experiments that provided insight into the quantitative state of 22,737 Populus gene models and 8,199more » functional protein groups in response to drought. Together, these datasets provide the most comprehensive insight into proteome drought responses in poplar to date and a direct proteome comparison between short period dehydration shock and cyclic, post-drought re-watering. Altogether, this investigation provides novel insights into drought avoidance mechanisms that are distinct from progressive drought stress. Additionally, we identified proteins that have been associated as drought-relevant in previous studies. Importantly, we highlight the RD26 transcription factor as a gene regulated at both the transcript and protein level, regardless of species and drought condition, and, thus, represents a key, universal drought marker for Populus species.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1];  [1];  [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1];  [2]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Chinese Academy of Sciences (CAS), Beijing (China)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1435308
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 13; Journal Issue: 2; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; water resources; gene ontologies; leaves; proteomes; plant resistance to abiotic stress; transcription factors; poplars; drought adaptation

Citation Formats

Abraham, Paul E., Garcia, Benjamin J., Gunter, Lee E., Jawdy, Sara S., Engle, Nancy L., Yang, Xiaohan, Jacobson, Daniel A., Hettich, Robert L., Tuskan, Gerald A., Tschaplinski, Timothy J., and Zhang, Jin -Song. Quantitative proteome profile of water deficit stress responses in eastern cottonwood (Populus deltoides) leaves. United States: N. p., 2018. Web. doi:10.1371/journal.pone.0190019.
Abraham, Paul E., Garcia, Benjamin J., Gunter, Lee E., Jawdy, Sara S., Engle, Nancy L., Yang, Xiaohan, Jacobson, Daniel A., Hettich, Robert L., Tuskan, Gerald A., Tschaplinski, Timothy J., & Zhang, Jin -Song. Quantitative proteome profile of water deficit stress responses in eastern cottonwood (Populus deltoides) leaves. United States. doi:10.1371/journal.pone.0190019.
Abraham, Paul E., Garcia, Benjamin J., Gunter, Lee E., Jawdy, Sara S., Engle, Nancy L., Yang, Xiaohan, Jacobson, Daniel A., Hettich, Robert L., Tuskan, Gerald A., Tschaplinski, Timothy J., and Zhang, Jin -Song. Thu . "Quantitative proteome profile of water deficit stress responses in eastern cottonwood (Populus deltoides) leaves". United States. doi:10.1371/journal.pone.0190019. https://www.osti.gov/servlets/purl/1435308.
@article{osti_1435308,
title = {Quantitative proteome profile of water deficit stress responses in eastern cottonwood (Populus deltoides) leaves},
author = {Abraham, Paul E. and Garcia, Benjamin J. and Gunter, Lee E. and Jawdy, Sara S. and Engle, Nancy L. and Yang, Xiaohan and Jacobson, Daniel A. and Hettich, Robert L. and Tuskan, Gerald A. and Tschaplinski, Timothy J. and Zhang, Jin -Song},
abstractNote = {Drought stress is a recurring feature of world climate and the single most important factor influencing agricultural yield worldwide. Plants display highly variable, species-specific responses to drought and these responses are multifaceted, requiring physiological and morphological changes influenced by genetic and molecular mechanisms. Moreover, the reproducibility of water deficit studies is very cumbersome, which significantly impedes research on drought tolerance, because how a plant responds is highly influenced by the timing, duration, and intensity of the water deficit. Despite progress in the identification of drought-related mechanisms in many plants, the molecular basis of drought resistance remains to be fully understood in trees, particularly in poplar species because their wide geographic distribution results in varying tolerances to drought. Herein, we aimed to better understand this complex phenomenon in eastern cottonwood (Populus deltoides) by performing a detailed contrast of the proteome changes between two different water deficit experiments to identify functional intersections and divergences in proteome responses. We investigated plants subjected to cyclic water deficit and compared these responses to plants subjected to prolonged acute water deficit. In total, we identified 108,012 peptide sequences across both experiments that provided insight into the quantitative state of 22,737 Populus gene models and 8,199 functional protein groups in response to drought. Together, these datasets provide the most comprehensive insight into proteome drought responses in poplar to date and a direct proteome comparison between short period dehydration shock and cyclic, post-drought re-watering. Altogether, this investigation provides novel insights into drought avoidance mechanisms that are distinct from progressive drought stress. Additionally, we identified proteins that have been associated as drought-relevant in previous studies. Importantly, we highlight the RD26 transcription factor as a gene regulated at both the transcript and protein level, regardless of species and drought condition, and, thus, represents a key, universal drought marker for Populus species.},
doi = {10.1371/journal.pone.0190019},
journal = {PLoS ONE},
issn = {1932-6203},
number = 2,
volume = 13,
place = {United States},
year = {2018},
month = {2}
}

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Works referenced in this record:

Genes commonly regulated by water-deficit stress in Arabidopsis thaliana
journal, September 2004


Methylglyoxal: An Emerging Signaling Molecule in Plant Abiotic Stress Responses and Tolerance
journal, September 2016

  • Hoque, Tahsina S.; Hossain, Mohammad A.; Mostofa, Mohammad G.
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.01341

Plant drought stress: effects, mechanisms and management
journal, March 2009

  • Farooq, M.; Wahid, A.; Kobayashi, N.
  • Agronomy for Sustainable Development, Vol. 29, Issue 1
  • DOI: 10.1051/agro:2008021

DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008


Stress-Related Gene Expression Reflects Morphophysiological Responses to Water Deficit
journal, May 2017

  • Rymaszewski, Wojciech; Vile, Denis; Bediee, Alexis
  • Plant Physiology, Vol. 174, Issue 3
  • DOI: 10.1104/pp.17.00318

Defining the Boundaries and Characterizing the Landscape of Functional Genome Expression in Vascular Tissues of Populus using Shotgun Proteomics
journal, November 2011

  • Abraham, Paul; Adams, Rachel; Giannone, Richard J.
  • Journal of Proteome Research, Vol. 11, Issue 1
  • DOI: 10.1021/pr200851y

Gene regulation network behind drought escape, avoidance and tolerance strategies in black poplar ( Populus nigra L.)
journal, June 2017


Proteins responding to drought and high-temperature stress in Populus × euramericana cv. ‘74/76’
journal, June 2008


ProteomeXchange provides globally coordinated proteomics data submission and dissemination
journal, March 2014

  • Vizcaíno, Juan A.; Deutsch, Eric W.; Wang, Rui
  • Nature Biotechnology, Vol. 32, Issue 3
  • DOI: 10.1038/nbt.2839

Clonal and seasonal differences in leaf osmotic potential and organic solutes of five hybrid poplar clones grown under field conditions
journal, October 1998


XAP5 CIRCADIAN TIMEKEEPER Regulates Ethylene Responses in Aerial Tissues of Arabidopsis
journal, December 2010

  • Ellison, Cory T.; Vandenbussche, Filip; Van Der Straeten, Dominique
  • Plant Physiology, Vol. 155, Issue 2
  • DOI: 10.1104/pp.110.164277

Two Mechanosensitive Channel Homologs Influence Division Ring Placement in Arabidopsis Chloroplasts
journal, August 2011

  • Wilson, Margaret E.; Jensen, Gregory S.; Haswell, Elizabeth S.
  • The Plant Cell, Vol. 23, Issue 8
  • DOI: 10.1105/tpc.111.088112

REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms
journal, July 2011


The CRAPome: a contaminant repository for affinity purification–mass spectrometry data
journal, July 2013

  • Mellacheruvu, Dattatreya; Wright, Zachary; Couzens, Amber L.
  • Nature Methods, Vol. 10, Issue 8
  • DOI: 10.1038/nmeth.2557

Plant Productivity and Environment
journal, October 1982


Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
journal, August 2005


pTAC10, a Key Subunit of Plastid-Encoded RNA Polymerase, Promotes Chloroplast Development
journal, March 2017

  • Chang, Sun Hyun; Lee, Sangyool; Um, Tae Young
  • Plant Physiology, Vol. 174, Issue 1
  • DOI: 10.1104/pp.17.00248

Time-Series Transcriptomics Reveals That AGAMOUS-LIKE22 Affects Primary Metabolism and Developmental Processes in Drought-Stressed Arabidopsis
journal, February 2016

  • Bechtold, Ulrike; Penfold, Christopher A.; Jenkins, Dafyd J.
  • The Plant Cell, Vol. 28, Issue 2
  • DOI: 10.1105/tpc.15.00910

Plant responses to drought and rewatering
journal, June 2010

  • Xu, Zhenzhu; Zhou, Guangsheng; Shimizu, Hideyuki
  • Plant Signaling & Behavior, Vol. 5, Issue 6
  • DOI: 10.4161/psb.5.6.11398

Dynamic profiling of the protein life cycle in response to pathogens
journal, February 2015


Four distinct types of dehydration stress memory genes in Arabidopsis thaliana
journal, January 2013


Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase
journal, January 2003

  • Halford, N. G.; Hey, S.; Jhurreea, D.
  • Journal of Experimental Botany, Vol. 54, Issue 382
  • DOI: 10.1093/jxb/erg038

Poplar as a feedstock for biofuels: A review of compositional characteristics
journal, March 2010

  • Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A.
  • Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2
  • DOI: 10.1002/bbb.206

Drought resistance of two hybrid Populus clones grown in a large-scale plantation
journal, October 1998


FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis
journal, July 2016

  • Li, Dongming; Fu, Xing; Guo, Lin
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 33
  • DOI: 10.1073/pnas.1602960113

The stomatal response of red alder and black cottonwood to changing water status
journal, December 1982

  • Pezeshki, S. R.; Hinckley, T. M.
  • Canadian Journal of Forest Research, Vol. 12, Issue 4
  • DOI: 10.1139/x82-115

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Functional Proteomics of Arabidopsis thaliana Guard Cells Uncovers New Stomatal Signaling Pathways
journal, December 2008


Water-deficit stress-induced anatomical changes in higher plants
journal, March 2008


Loss of hydraulic conductivity due to water stress in intact juveniles of Quercus rubra and Populus deltoides
journal, June 1992


Poplar under drought: Comparison of leaf and cambial proteomic responses
journal, August 2011


The role of ANAC072 in the regulation of chlorophyll degradation during age- and dark-induced leaf senescence
journal, May 2016


On the Dependency of Cellular Protein Levels on mRNA Abundance
journal, April 2016


ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks
journal, February 2009


Putting the Pieces Together: High-performance LC-MS/MS Provides Network-, Pathway-, and Protein-level Perspectives in Populus
journal, October 2012

  • Abraham, Paul; Giannone, Richard J.; Adams, Rachel M.
  • Molecular & Cellular Proteomics, Vol. 12, Issue 1
  • DOI: 10.1074/mcp.M112.022996

IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering
journal, August 2009

  • Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 8, Issue 8
  • DOI: 10.1021/pr900360j

The Perseus computational platform for comprehensive analysis of (prote)omics data
journal, June 2016

  • Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel
  • Nature Methods, Vol. 13, Issue 9
  • DOI: 10.1038/nmeth.3901

The Arabidopsis E3 SUMO Ligase SIZ1 Regulates Plant Growth and Drought Responses
journal, September 2007


Downregulation of N-terminal acetylation triggers ABA-mediated drought responses in Arabidopsis
journal, July 2015

  • Linster, Eric; Stephan, Iwona; Bienvenut, Willy V.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms8640

Cell Wall Metabolism in Response to Abiotic Stress
journal, February 2015

  • Le Gall, Hyacinthe; Philippe, Florian; Domon, Jean-Marc
  • Plants, Vol. 4, Issue 1
  • DOI: 10.3390/plants4010112

Proteomic analysis of de-etiolated rice seedlings upon exposure to light
journal, July 2007


A physiological and proteomic study of poplar leaves during ozone exposure combined with mild drought
journal, May 2013


MyriMatch:  Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007

  • Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C.
  • Journal of Proteome Research, Vol. 6, Issue 2
  • DOI: 10.1021/pr0604054

Significance of galactinol and raffinose family oligosaccharide synthesis in plants
journal, August 2015

  • Sengupta, Sonali; Mukherjee, Sritama; Basak, Papri
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00656

Analysis of Functions of VIP1 and Its Close Homologs in Osmosensory Responses of Arabidopsis thaliana
journal, August 2014


IDPQuantify: Combining Precursor Intensity with Spectral Counts for Protein and Peptide Quantification
journal, August 2013

  • Chen, Yao-Yi; Chambers, Matthew C.; Li, Ming
  • Journal of Proteome Research, Vol. 12, Issue 9
  • DOI: 10.1021/pr400438q

Interactions between drought and elevated CO 2 on osmotic adjustment and solute concentrations of tree seedlings
journal, October 1995


NADPH-dependent Reductases Involved in the Detoxification of Reactive Carbonyls in Plants
journal, December 2010

  • Yamauchi, Yasuo; Hasegawa, Ayaka; Taninaka, Ai
  • Journal of Biological Chemistry, Vol. 286, Issue 9
  • DOI: 10.1074/jbc.M110.202226

    Works referencing / citing this record:

    Plant Host-Associated Mechanisms for Microbial Selection
    journal, July 2019


    Plant Host-Associated Mechanisms for Microbial Selection
    journal, July 2019