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

Title: The Populus Superoxide Dismutase Gene Family and Its Responses to Drought Stress in Transgenic Poplar Overexpressing a Pine Cytosolic Glutamine Synthetase (GS1a)

Abstract

Glutamine synthetase (GS) plays a central role in plant nitrogen assimilation, a process intimately linked to soil water availability. We previously showed that hybrid poplar (Populus tremula X alba, INRA 717-1B4) expressing ectopically a pine cytosolic glutamine synthetase gene (GS1a) display enhanced tolerance to drought. Preliminary transcriptome profiling revealed that during drought, members of the superoxide dismutase (SOD) family were reciprocally regulated in GS poplar when compared with the wild-type control, in all tissues examined. SOD was the only gene family found to exhibit such patterns. In silico analysis of the Populus genome identified 12 SOD genes and two genes encoding copper chaperones for SOD (CCSs). The poplar SODs form three phylogenetic clusters in accordance with their distinct metal co-factor requirements and gene structure. Nearly all poplar SODs and CCSs are present in duplicate derived from whole genome duplication, in sharp contrast to their predominantly single-copy Arabidopsis orthologs. Drought stress triggered plant-wide down-regulation of the plastidic copper SODs (CSDs), with concomitant up-regulation of plastidic iron SODs (FSDs) in GS poplar relative to the wild type; this was confirmed at the activity level. We also found evidence for coordinated downregulation of other copper proteins, including plastidic CCSs and polyphenol oxidases, inmore » GS poplar under drought conditions. Both gene duplication and expression divergence have contributed to the expansion and transcriptional diversity of the Populus SOD/CCS families. Coordinated down-regulation of major copper proteins in drought-tolerant GS poplars supports the copper cofactor economy model where copper supply is preferentially allocated for plastocyanins to sustain photosynthesis during drought. Our results also extend previous findings on the compensatory regulation between chloroplastic CSDs and FSDs, and suggest that this copper-mediated mechanism represents a common response to oxidative stress and other genetic manipulations, as in GS poplars, that affect photosynthesis.« less

Authors:
 [1];  [2];  [1]
  1. Rutgers University, New Brunswick, NJ (United States)
  2. University of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
Rutgers University, Newark, NJ (United States)
Sponsoring Org.:
USDOE; ArborGen LLC
OSTI Identifier:
1903953
Grant/Contract Number:  
GO12026-314
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 8; 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; Arabidopsis thaliana; poplars; superoxide dismutase; leaves; genetically modified plants; drought adaption; protein sequencing; plant genomics

Citation Formats

Molina-Rueda, Juan Jesús, Tsai, Chung Jui, and Kirby, Edward G. The Populus Superoxide Dismutase Gene Family and Its Responses to Drought Stress in Transgenic Poplar Overexpressing a Pine Cytosolic Glutamine Synthetase (GS1a). United States: N. p., 2013. Web. doi:10.1371/journal.pone.0056421.
Molina-Rueda, Juan Jesús, Tsai, Chung Jui, & Kirby, Edward G. The Populus Superoxide Dismutase Gene Family and Its Responses to Drought Stress in Transgenic Poplar Overexpressing a Pine Cytosolic Glutamine Synthetase (GS1a). United States. https://doi.org/10.1371/journal.pone.0056421
Molina-Rueda, Juan Jesús, Tsai, Chung Jui, and Kirby, Edward G. Fri . "The Populus Superoxide Dismutase Gene Family and Its Responses to Drought Stress in Transgenic Poplar Overexpressing a Pine Cytosolic Glutamine Synthetase (GS1a)". United States. https://doi.org/10.1371/journal.pone.0056421. https://www.osti.gov/servlets/purl/1903953.
@article{osti_1903953,
title = {The Populus Superoxide Dismutase Gene Family and Its Responses to Drought Stress in Transgenic Poplar Overexpressing a Pine Cytosolic Glutamine Synthetase (GS1a)},
author = {Molina-Rueda, Juan Jesús and Tsai, Chung Jui and Kirby, Edward G.},
abstractNote = {Glutamine synthetase (GS) plays a central role in plant nitrogen assimilation, a process intimately linked to soil water availability. We previously showed that hybrid poplar (Populus tremula X alba, INRA 717-1B4) expressing ectopically a pine cytosolic glutamine synthetase gene (GS1a) display enhanced tolerance to drought. Preliminary transcriptome profiling revealed that during drought, members of the superoxide dismutase (SOD) family were reciprocally regulated in GS poplar when compared with the wild-type control, in all tissues examined. SOD was the only gene family found to exhibit such patterns. In silico analysis of the Populus genome identified 12 SOD genes and two genes encoding copper chaperones for SOD (CCSs). The poplar SODs form three phylogenetic clusters in accordance with their distinct metal co-factor requirements and gene structure. Nearly all poplar SODs and CCSs are present in duplicate derived from whole genome duplication, in sharp contrast to their predominantly single-copy Arabidopsis orthologs. Drought stress triggered plant-wide down-regulation of the plastidic copper SODs (CSDs), with concomitant up-regulation of plastidic iron SODs (FSDs) in GS poplar relative to the wild type; this was confirmed at the activity level. We also found evidence for coordinated downregulation of other copper proteins, including plastidic CCSs and polyphenol oxidases, in GS poplar under drought conditions. Both gene duplication and expression divergence have contributed to the expansion and transcriptional diversity of the Populus SOD/CCS families. Coordinated down-regulation of major copper proteins in drought-tolerant GS poplars supports the copper cofactor economy model where copper supply is preferentially allocated for plastocyanins to sustain photosynthesis during drought. Our results also extend previous findings on the compensatory regulation between chloroplastic CSDs and FSDs, and suggest that this copper-mediated mechanism represents a common response to oxidative stress and other genetic manipulations, as in GS poplars, that affect photosynthesis.},
doi = {10.1371/journal.pone.0056421},
journal = {PLoS ONE},
number = 2,
volume = 8,
place = {United States},
year = {Fri Feb 22 00:00:00 EST 2013},
month = {Fri Feb 22 00:00:00 EST 2013}
}

Works referenced in this record:

Copper Delivery by the Copper Chaperone for Chloroplast and Cytosolic Copper/Zinc-Superoxide Dismutases: Regulation and Unexpected Phenotypes in an Arabidopsis Mutant
journal, November 2009

  • Cohu, Christopher M.; Abdel-Ghany, Salah E.; Gogolin Reynolds, Kathryn A.
  • Molecular Plant, Vol. 2, Issue 6
  • DOI: 10.1093/mp/ssp084

Conserved Patterns in the Cu,Zn Superoxide Dismutase Family
journal, May 1994

  • Bordo, Domenico; Djinovic, Kristina; Bolognesi, Martino
  • Journal of Molecular Biology, Vol. 238, Issue 3
  • DOI: 10.1006/jmbi.1994.1298

[gamma]-Aminobutyric Acid Stimulates Ethylene Biosynthesis in Sunflower
journal, September 1997

  • Kathiresan, A.; Tung, P.; Chinnappa, C. C.
  • Plant Physiology, Vol. 115, Issue 1
  • DOI: 10.1104/pp.115.1.129

SLIM: a sliding linear model for estimating the proportion of true null hypotheses in datasets with dependence structures
journal, November 2010


Rapid Isolation of High‐Quality Total RNA from Taxus and Ginkgo
journal, January 2004

  • Liao, Zhihua; Chen, Min; Guo, Liang
  • Preparative Biochemistry and Biotechnology, Vol. 34, Issue 3
  • DOI: 10.1081/PB-200026790

ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites
journal, January 1999

  • Emanuelsson, Olof; Nielsen, Henrik; Heijne, Gunnar Von
  • Protein Science, Vol. 8, Issue 5
  • DOI: 10.1110/ps.8.5.978

Clustal W and Clustal X version 2.0
journal, September 2007


Plant copper chaperones
journal, August 2002

  • Wintz, H.; Vulpe, C.
  • Biochemical Society Transactions, Vol. 30, Issue 4
  • DOI: 10.1042/bst0300732

Prediction of Peroxisomal Targeting Signal 1 Containing Proteins from Amino Acid Sequence
journal, May 2003

  • Neuberger, Georg; Maurer-Stroh, Sebastian; Eisenhaber, Birgit
  • Journal of Molecular Biology, Vol. 328, Issue 3
  • DOI: 10.1016/S0022-2836(03)00319-X

Intraorganellar Distribution of Superoxide Dismutase in Plant Peroxisomes (Glyoxysomes and Leaf Peroxisomes)
journal, December 1988

  • Sandalio, Luisa M.; Del Río, Luis A.
  • Plant Physiology, Vol. 88, Issue 4
  • DOI: 10.1104/pp.88.4.1215

AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7
journal, March 2005


Regulation of Copper Homeostasis by Micro-RNA in Arabidopsis
journal, April 2007

  • Yamasaki, Hiroaki; Abdel-Ghany, Salah E.; Cohu, Christopher M.
  • Journal of Biological Chemistry, Vol. 282, Issue 22
  • DOI: 10.1074/jbc.M700138200

Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii
journal, October 2009


Transgenic poplar characterized by ectopic expression of a pine cytosolic glutamine synthetase gene exhibits enhanced tolerance to water stress
journal, July 2004


Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

Ancestral polyploidy in seed plants and angiosperms
journal, April 2011

  • Jiao, Yuannian; Wickett, Norman J.; Ayyampalayam, Saravanaraj
  • Nature, Vol. 473, Issue 7345
  • DOI: 10.1038/nature09916

Iron- and manganese-containing superoxide dismutases can be distinguished by analysis of their primary structures
journal, March 1988


Computational Method to Predict Mitochondrially Imported Proteins and their Targeting Sequences
journal, November 1996


Characterization and developmental expression of a glutamate decarboxylase from maritime pine
journal, September 2010

  • Molina-Rueda, Juan Jesús; Pascual, María Belén; Cánovas, Francisco M.
  • Planta, Vol. 232, Issue 6
  • DOI: 10.1007/s00425-010-1268-9

Destruction of tryptophan residues by hydrogen peroxide in iron-superoxide dismutase
journal, July 1984


Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana
journal, June 2009


Alternative Splicing Studies of the Reactive Oxygen Species Gene Network in Populus Reveal Two Isoforms of High-Isoelectric-Point Superoxide Dismutase    
journal, January 2009

  • Srivastava, Vaibhav; Srivastava, Manoj Kumar; Chibani, Kamel
  • Plant Physiology, Vol. 149, Issue 4
  • DOI: 10.1104/pp.108.133371

Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data
journal, February 2009

  • Ruijter, J. M.; Ramakers, C.; Hoogaars, W. M. H.
  • Nucleic Acids Research, Vol. 37, Issue 6
  • DOI: 10.1093/nar/gkp045

Superoxide Dismutase
journal, November 1969


Differential Expression of CuZn- and Fe-Superoxide Dismutase Genes of Tobacco during Development, Oxidative Stress, and Hormonal Treatments
journal, January 1997


The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia.
journal, January 1989


Drought stress and reactive oxygen species: production, scavenging and signaling
journal, March 2008

  • Cruz de Carvalho, Maria Helena
  • Plant Signaling & Behavior, Vol. 3, Issue 3
  • DOI: 10.4161/psb.3.3.5536

Soil nutrients and water availability interact to influence willow growth and chemistry but not leaf beetle performance
journal, April 2003


Superoxide Dismutases
journal, June 1975


Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants
journal, November 2005


Differential regulation of superoxide dismutases in plants exposed to environmental stress.
journal, August 1991

  • Tsang, E. W.; Bowler, C.; Hérouart, D.
  • The Plant Cell, Vol. 3, Issue 8
  • DOI: 10.1105/tpc.3.8.783

Primer3Plus, an enhanced web interface to Primer3
journal, May 2007

  • Untergasser, A.; Nijveen, H.; Rao, X.
  • Nucleic Acids Research, Vol. 35, Issue Web Server
  • DOI: 10.1093/nar/gkm306

Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase
journal, August 2004


Two P-Type ATPases Are Required for Copper Delivery in Arabidopsis thaliana Chloroplasts
journal, March 2005

  • Abdel-Ghany, Salah E.; Müller-Moulé, Patricia; Niyogi, Krishna K.
  • The Plant Cell, Vol. 17, Issue 4
  • DOI: 10.1105/tpc.104.030452

miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula
journal, December 2009


Metal Ion Chaperone Function of the Soluble Cu(I) Receptor Atx1
journal, October 1997


MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods
journal, May 2011

  • Tamura, K.; Peterson, D.; Peterson, N.
  • Molecular Biology and Evolution, Vol. 28, Issue 10
  • DOI: 10.1093/molbev/msr121

Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes
journal, June 2002


Java Treeview--extensible visualization of microarray data
journal, June 2004


Superoxide Dismutase in Arabidopsis: An Eclectic Enzyme Family with Disparate Regulation and Protein Localization
journal, October 1998

  • Kliebenstein, Daniel J.; Monde, Rita-Ann; Last, Robert L.
  • Plant Physiology, Vol. 118, Issue 2
  • DOI: 10.1104/pp.118.2.637

Expression of a conifer glutamine synthetase gene in transgenic poplar
journal, November 1999

  • Gallardo, Fernando; Fu, Jianming; Cantón, Francisco R.
  • Planta, Vol. 210, Issue 1, p. 19-26
  • DOI: 10.1007/s004250050649

miR398 regulation in rice of the responses to abiotic and biotic stresses depends on CSD1 and CSD2 expression
journal, January 2011

  • Lu, Yuzhu; Feng, Zhen; Bian, Liying
  • Functional Plant Biology, Vol. 38, Issue 1
  • DOI: 10.1071/FP10178

Role of superoxide dismutases (SODs) in controlling oxidative stress in plants
journal, May 2002

  • Alscher, Ruth Grene; Erturk, Neval; Heath, Lenwood S.
  • Journal of Experimental Botany, Vol. 53, Issue 372
  • DOI: 10.1093/jxb/53.372.1331

Spliceosomal intron size expansion in domesticated grapevine (Vitis vinifera)
journal, March 2011


Cloning and characterization of a novel splicing isoform of the iron-superoxide dismutase gene in rice (Oryza sativa L.)
journal, October 2005


Superoxide dismutase of plant cell vacuoles
journal, March 2009

  • Pradedova, E. V.; Isheeva, O. D.; Salyaev, R. K.
  • Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology, Vol. 3, Issue 1
  • DOI: 10.1134/S1990747809010048

Characterization of iron superoxide dismutase cDNAs from plants obtained by genetic complementation in Escherichia coli.
journal, December 1990

  • Van Camp, W.; Bowler, C.; Villarroel, R.
  • Proceedings of the National Academy of Sciences, Vol. 87, Issue 24
  • DOI: 10.1073/pnas.87.24.9903

Statistical analysis of a small set of time-ordered gene expression data using linear splines
journal, November 2002


Impact of drought and leaf development stage on enzymatic antioxidant system of twoPopulus deltoides×nigraclones
journal, April 2006

  • Marron, Nicolas; Maury, Stéphane; Rinaldi, Cécile
  • Annals of Forest Science, Vol. 63, Issue 3
  • DOI: 10.1051/forest:2006012

The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia.
journal, January 1989


Conserved Patterns in the Cu,Zn Superoxide Dismutase Family
journal, May 1994

  • Bordo, Domenico; Djinovic, Kristina; Bolognesi, Martino
  • Journal of Molecular Biology, Vol. 238, Issue 3
  • DOI: 10.1006/jmbi.1994.1298

Expression of a conifer glutamine synthetase gene in transgenic poplar
journal, November 1999

  • Gallardo, Fernando; Fu, Jianming; Cantón, Francisco R.
  • Planta, Vol. 210, Issue 1, p. 19-26
  • DOI: 10.1007/s004250050649

Iron- and manganese-containing superoxide dismutases can be distinguished by analysis of their primary structures
journal, March 1988


Superoxide dismutases
journal, May 1989


Plant copper chaperones
journal, August 2002

  • Wintz, H.; Vulpe, C.
  • Biochemical Society Transactions, Vol. 30, Issue 4
  • DOI: 10.1042/bst0300732

Soil nutrients and water availability interact to influence willow growth and chemistry but not leaf beetle performance
journal, April 2003


Statistical analysis of a small set of time-ordered gene expression data using linear splines
journal, November 2002


Transgenic poplar characterized by ectopic expression of a pine cytosolic glutamine synthetase gene exhibits enhanced tolerance to water stress
journal, July 2004


[gamma]-Aminobutyric Acid Stimulates Ethylene Biosynthesis in Sunflower
journal, September 1997

  • Kathiresan, A.; Tung, P.; Chinnappa, C. C.
  • Plant Physiology, Vol. 115, Issue 1
  • DOI: 10.1104/pp.115.1.129

Superoxide Dismutase in Arabidopsis: An Eclectic Enzyme Family with Disparate Regulation and Protein Localization
journal, October 1998

  • Kliebenstein, Daniel J.; Monde, Rita-Ann; Last, Robert L.
  • Plant Physiology, Vol. 118, Issue 2
  • DOI: 10.1104/pp.118.2.637

Intraorganellar Distribution of Superoxide Dismutase in Plant Peroxisomes (Glyoxysomes and Leaf Peroxisomes)
journal, December 1988

  • Sandalio, Luisa M.; Del Río, Luis A.
  • Plant Physiology, Vol. 88, Issue 4
  • DOI: 10.1104/pp.88.4.1215

Two P-Type ATPases Are Required for Copper Delivery in Arabidopsis thaliana Chloroplasts
journal, March 2005

  • Abdel-Ghany, Salah E.; Müller-Moulé, Patricia; Niyogi, Krishna K.
  • The Plant Cell, Vol. 17, Issue 4
  • DOI: 10.1105/tpc.104.030452

Differential regulation of superoxide dismutases in plants exposed to environmental stress.
journal, August 1991

  • Tsang, E. W.; Bowler, C.; Hérouart, D.
  • The Plant Cell, Vol. 3, Issue 8
  • DOI: 10.1105/tpc.3.8.783

ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites
journal, January 1999

  • Emanuelsson, Olof; Nielsen, Henrik; Heijne, Gunnar Von
  • Protein Science, Vol. 8, Issue 5
  • DOI: 10.1110/ps.8.5.978

Computational Method to Predict Mitochondrially Imported Proteins and their Targeting Sequences
journal, November 1996


Drought stress and reactive oxygen species: production, scavenging and signaling
journal, March 2008

  • Cruz de Carvalho, Maria Helena
  • Plant Signaling & Behavior, Vol. 3, Issue 3
  • DOI: 10.4161/psb.3.3.5536

Works referencing / citing this record:

Genome-Wide Characterization and Expression Profiles of the Superoxide Dismutase Gene Family inGossypium
journal, January 2016

  • Zhang, Jingbo; Li, Bo; Yang, Yang
  • International Journal of Genomics, Vol. 2016
  • DOI: 10.1155/2016/8740901

Genome-wide characterization and expression analyses of superoxide dismutase (SOD) genes in Gossypium hirsutum
journal, May 2017


Concurrent Overexpression of OsGS1;1 and OsGS2 Genes in Transgenic Rice (Oryza sativa L.): Impact on Tolerance to Abiotic Stresses
journal, June 2018

  • James, Donald; Borphukan, Bhabesh; Fartyal, Dhirendra
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.00786

Molecular Characterization of MaCCS, a Novel Copper Chaperone Gene Involved in Abiotic and Hormonal Stress Responses in Musa acuminata cv. Tianbaojiao
journal, March 2016

  • Feng, Xin; Chen, Fanglan; Liu, Weihua
  • International Journal of Molecular Sciences, Vol. 17, Issue 4
  • DOI: 10.3390/ijms17040441