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

Molina-Rueda, Juan Jesús; Tsai, Chung Jui; Kirby, Edward G.

doi:10.1371/journal.pone.0056421

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

Journal Article · Fri Feb 22 00:00:00 EST 2013 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0056421· OSTI ID:1903953

Molina-Rueda, Juan Jesús ^[1]; Tsai, Chung Jui ^[2]; Kirby, Edward G. ^[1]

Rutgers University, New Brunswick, NJ (United States)
University of Georgia, Athens, GA (United States)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Rutgers University, Newark, NJ (United States)

Sponsoring Organization:: USDOE; ArborGen LLC

Grant/Contract Number:: GO12026-314

OSTI ID:: 1903953

Journal Information:: PLoS ONE, Vol. 8, Issue 2; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

Copper Delivery by the Copper Chaperone for Chloroplast and Cytosolic Copper/Zinc-Superoxide Dismutases: Regulation and Unexpected Phenotypes in an Arabidopsis Mutant Cohu, Christopher M.; Abdel-Ghany, Salah E.; Gogolin Reynolds, Kathryn A. Molecular Plant, Vol. 2, Issue 6 https://doi.org/10.1093/mp/ssp084	journal	November 2009
Conserved Patterns in the Cu,Zn Superoxide Dismutase Family Bordo, Domenico; Djinovic, Kristina; Bolognesi, Martino Journal of Molecular Biology, Vol. 238, Issue 3 https://doi.org/10.1006/jmbi.1994.1298	journal	May 1994
Isolation, Chromosomal Localization, and Differential Expression of Mitochondrial Manganese Superoxide Dismutase and Chloroplastic Copper/Zinc Superoxide Dismutase Genes in Wheat1 Wu, Guohai; Wilen, Ronald W.; Robertson, Albert J. Plant Physiology, Vol. 120, Issue 2 https://doi.org/10.1104/pp.120.2.513	journal	June 1999
[gamma]-Aminobutyric Acid Stimulates Ethylene Biosynthesis in Sunflower Kathiresan, A.; Tung, P.; Chinnappa, C. C. Plant Physiology, Vol. 115, Issue 1 https://doi.org/10.1104/pp.115.1.129	journal	September 1997
SLIM: a sliding linear model for estimating the proportion of true null hypotheses in datasets with dependence structures Wang, Hong-Qiang; Tuominen, Lindsey K.; Tsai, Chung-Jui Bioinformatics, Vol. 27, Issue 2 https://doi.org/10.1093/bioinformatics/btq650	journal	November 2010
Rapid Isolation of High‐Quality Total RNA from Taxus and Ginkgo Liao, Zhihua; Chen, Min; Guo, Liang Preparative Biochemistry and Biotechnology, Vol. 34, Issue 3 https://doi.org/10.1081/PB-200026790	journal	January 2004
ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites Emanuelsson, Olof; Nielsen, Henrik; Heijne, Gunnar Von Protein Science, Vol. 8, Issue 5 https://doi.org/10.1110/ps.8.5.978	journal	January 1999
Clustal W and Clustal X version 2.0 Larkin, M. A.; Blackshields, G.; Brown, N. P. Bioinformatics, Vol. 23, Issue 21, p. 2947-2948 https://doi.org/10.1093/bioinformatics/btm404	journal	September 2007
Plant copper chaperones Wintz, H.; Vulpe, C. Biochemical Society Transactions, Vol. 30, Issue 4 https://doi.org/10.1042/bst0300732	journal	August 2002
Prediction of Peroxisomal Targeting Signal 1 Containing Proteins from Amino Acid Sequence Neuberger, Georg; Maurer-Stroh, Sebastian; Eisenhaber, Birgit Journal of Molecular Biology, Vol. 328, Issue 3 https://doi.org/10.1016/S0022-2836(03)00319-X	journal	May 2003
Intraorganellar Distribution of Superoxide Dismutase in Plant Peroxisomes (Glyoxysomes and Leaf Peroxisomes) Sandalio, Luisa M.; Del Río, Luis A. Plant Physiology, Vol. 88, Issue 4 https://doi.org/10.1104/pp.88.4.1215	journal	December 1988
AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7 Abdel-Ghany, Salah E.; Burkhead, Jason L.; Gogolin, Kathryn A. FEBS Letters, Vol. 579, Issue 11 https://doi.org/10.1016/j.febslet.2005.03.025	journal	March 2005
Regulation of Copper Homeostasis by Micro-RNA in Arabidopsis Yamasaki, Hiroaki; Abdel-Ghany, Salah E.; Cohu, Christopher M. Journal of Biological Chemistry, Vol. 282, Issue 22 https://doi.org/10.1074/jbc.M700138200	journal	April 2007
Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii Wang, Yu Cheng; Qu, Guan Zheng; Li, Hong Yan Molecular Biology Reports, Vol. 37, Issue 2 https://doi.org/10.1007/s11033-009-9884-9	journal	October 2009
Transgenic poplar characterized by ectopic expression of a pine cytosolic glutamine synthetase gene exhibits enhanced tolerance to water stress El-Khatib, R. T.; Hamerlynck, E. P.; Gallardo, F. Tree Physiology, Vol. 24, Issue 7 https://doi.org/10.1093/treephys/24.7.729	journal	July 2004
Spatiotemporal Analysis of Copper Homeostasis in Populus trichocarpa Reveals an Integrated Molecular Remodeling for a Preferential Allocation of Copper to Plastocyanin in the Chloroplasts of Developing Leaves Ravet, Karl; Danford, Forest L.; Dihle, Alysha Plant Physiology, Vol. 157, Issue 3 https://doi.org/10.1104/pp.111.183350	journal	September 2011
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
Enhanced tolerance to methyl viologen-induced oxidative stress and high temperature in transgenic potato plants overexpressing the CuZnSOD, APX and NDPK2 genes Kim, Myoung Duck; Kim, Yun-Hee; Kwon, Suk-Yoon Physiologia Plantarum, Vol. 140, Issue 2 https://doi.org/10.1111/j.1399-3054.2010.01392.x	journal	September 2010
Ancestral polyploidy in seed plants and angiosperms Jiao, Yuannian; Wickett, Norman J.; Ayyampalayam, Saravanaraj Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09916	journal	April 2011
Iron- and manganese-containing superoxide dismutases can be distinguished by analysis of their primary structures Parker, Michael W.; Blake, Colin C. F. FEBS Letters, Vol. 229, Issue 2 https://doi.org/10.1016/0014-5793(88)81160-8	journal	March 1988
Computational Method to Predict Mitochondrially Imported Proteins and their Targeting Sequences Claros, Manuel G.; Vincens, Pierre European Journal of Biochemistry, Vol. 241, Issue 3 https://doi.org/10.1111/j.1432-1033.1996.00779.x	journal	November 1996
Characterization and developmental expression of a glutamate decarboxylase from maritime pine Molina-Rueda, Juan Jesús; Pascual, María Belén; Cánovas, Francisco M. Planta, Vol. 232, Issue 6 https://doi.org/10.1007/s00425-010-1268-9	journal	September 2010
Destruction of tryptophan residues by hydrogen peroxide in iron-superoxide dismutase Yamakura, Fumiyuki Biochemical and Biophysical Research Communications, Vol. 122, Issue 2 https://doi.org/10.1016/S0006-291X(84)80080-7	journal	July 1984
Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana Jia, Xiaoyun; Wang, Wang-Xia; Ren, Ligang Plant Molecular Biology, Vol. 71, Issue 1-2 https://doi.org/10.1007/s11103-009-9508-8	journal	June 2009
Alternative Splicing Studies of the Reactive Oxygen Species Gene Network in Populus Reveal Two Isoforms of High-Isoelectric-Point Superoxide Dismutase Srivastava, Vaibhav; Srivastava, Manoj Kumar; Chibani, Kamel Plant Physiology, Vol. 149, Issue 4 https://doi.org/10.1104/pp.108.133371	journal	January 2009
Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data Ruijter, J. M.; Ramakers, C.; Hoogaars, W. M. H. Nucleic Acids Research, Vol. 37, Issue 6 https://doi.org/10.1093/nar/gkp045	journal	February 2009
Superoxide Dismutase McCord, Joe M.; Fridovich, Irwin Journal of Biological Chemistry, Vol. 244, Issue 22 https://doi.org/10.1016/S0021-9258(18)63504-5	journal	November 1969
Differential Expression of CuZn- and Fe-Superoxide Dismutase Genes of Tobacco during Development, Oxidative Stress, and Hormonal Treatments Kurepa, J.; Herouart, D.; van Montagu, M. Plant and Cell Physiology, Vol. 38, Issue 4 https://doi.org/10.1093/oxfordjournals.pcp.a029190	journal	January 1997
The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. Bowler, C.; Alliotte, T.; De Loose, M. The EMBO Journal, Vol. 8, Issue 1 https://doi.org/10.1002/j.1460-2075.1989.tb03345.x	journal	January 1989
Drought stress and reactive oxygen species: production, scavenging and signaling Cruz de Carvalho, Maria Helena Plant Signaling & Behavior, Vol. 3, Issue 3 https://doi.org/10.4161/psb.3.3.5536	journal	March 2008
Soil nutrients and water availability interact to influence willow growth and chemistry but not leaf beetle performance Lower, Steven S.; Orians, Colin M. Entomologia Experimentalis et Applicata, Vol. 107, Issue 1 https://doi.org/10.1046/j.1570-7458.2003.00037.x	journal	April 2003
Superoxide Dismutases Fridovich, I. Annual Review of Biochemistry, Vol. 44, Issue 1 https://doi.org/10.1146/annurev.bi.44.070175.001051	journal	June 1975
Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants Tewari, Rajesh Kumar; Kumar, Praveen; Sharma, Parma Nand Planta, Vol. 223, Issue 6 https://doi.org/10.1007/s00425-005-0160-5	journal	November 2005
Differential regulation of superoxide dismutases in plants exposed to environmental stress. Tsang, E. W.; Bowler, C.; Hérouart, D. The Plant Cell, Vol. 3, Issue 8 https://doi.org/10.1105/tpc.3.8.783	journal	August 1991
Primer3Plus, an enhanced web interface to Primer3 Untergasser, A.; Nijveen, H.; Rao, X. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm306	journal	May 2007
Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase Jing, Zhong Ping; Gallardo, Fernando; Pascual, María Belén New Phytologist, Vol. 164, Issue 1 https://doi.org/10.1111/j.1469-8137.2004.01173.x	journal	August 2004
Two P-Type ATPases Are Required for Copper Delivery in Arabidopsis thaliana Chloroplasts Abdel-Ghany, Salah E.; Müller-Moulé, Patricia; Niyogi, Krishna K. The Plant Cell, Vol. 17, Issue 4 https://doi.org/10.1105/tpc.104.030452	journal	March 2005
miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula Trindade, Inês; Capitão, Cláudio; Dalmay, Tamas Planta, Vol. 231, Issue 3 https://doi.org/10.1007/s00425-009-1078-0	journal	December 2009
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
Metal Ion Chaperone Function of the Soluble Cu(I) Receptor Atx1 Pufahl, R. A. Science, Vol. 278, Issue 5339 https://doi.org/10.1126/science.278.5339.853	journal	October 1997
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Vandesompele, Jo; De Preter, Katleen; Pattyn, Filip Genome Biology, Vol. 3, Issue 7 https://doi.org/10.1186/gb-2002-3-7-research0034	journal	June 2002
Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in Arabidopsis Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance Sunkar, Ramanjulu; Kapoor, Avnish; Zhu, Jian-Kang The Plant Cell, Vol. 18, Issue 8 https://doi.org/10.1105/tpc.106.041673	journal	July 2006
Java Treeview--extensible visualization of microarray data Saldanha, A. J. Bioinformatics, Vol. 20, Issue 17 https://doi.org/10.1093/bioinformatics/bth349	journal	June 2004
Superoxide Dismutase in Arabidopsis: An Eclectic Enzyme Family with Disparate Regulation and Protein Localization Kliebenstein, Daniel J.; Monde, Rita-Ann; Last, Robert L. Plant Physiology, Vol. 118, Issue 2 https://doi.org/10.1104/pp.118.2.637	journal	October 1998
Expression of a conifer glutamine synthetase gene in transgenic poplar Gallardo, Fernando; Fu, Jianming; Cantón, Francisco R. Planta, Vol. 210, Issue 1, p. 19-26 https://doi.org/10.1007/s004250050649	journal	November 1999
miR398 regulation in rice of the responses to abiotic and biotic stresses depends on CSD1 and CSD2 expression Lu, Yuzhu; Feng, Zhen; Bian, Liying Functional Plant Biology, Vol. 38, Issue 1 https://doi.org/10.1071/FP10178	journal	January 2011
Role of superoxide dismutases (SODs) in controlling oxidative stress in plants Alscher, Ruth Grene; Erturk, Neval; Heath, Lenwood S. Journal of Experimental Botany, Vol. 53, Issue 372 https://doi.org/10.1093/jxb/53.372.1331	journal	May 2002
Spliceosomal intron size expansion in domesticated grapevine (Vitis vinifera) Jiang, Ke; Goertzen, Leslie R. BMC Research Notes, Vol. 4, Issue 1 https://doi.org/10.1186/1756-0500-4-52	journal	March 2011
Cloning and characterization of a novel splicing isoform of the iron-superoxide dismutase gene in rice (Oryza sativa L.) Feng, Wang; Hongbin, Wang; Bing, Liu Plant Cell Reports, Vol. 24, Issue 12 https://doi.org/10.1007/s00299-005-0030-4	journal	October 2005
Superoxide dismutase of plant cell vacuoles Pradedova, E. V.; Isheeva, O. D.; Salyaev, R. K. Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology, Vol. 3, Issue 1 https://doi.org/10.1134/S1990747809010048	journal	March 2009
Characterization of iron superoxide dismutase cDNAs from plants obtained by genetic complementation in Escherichia coli. Van Camp, W.; Bowler, C.; Villarroel, R. Proceedings of the National Academy of Sciences, Vol. 87, Issue 24 https://doi.org/10.1073/pnas.87.24.9903	journal	December 1990
Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus przewalskii Lei, Yanbao; Yin, Chunying; Li, Chunyang Physiologia Plantarum, Vol. 127, Issue 2 https://doi.org/10.1111/j.1399-3054.2006.00638.x	journal	June 2006
Statistical analysis of a small set of time-ordered gene expression data using linear splines de Hoon, M. J. L.; Imoto, S.; Miyano, S. Bioinformatics, Vol. 18, Issue 11 https://doi.org/10.1093/bioinformatics/18.11.1477	journal	November 2002
Impact of drought and leaf development stage on enzymatic antioxidant system of twoPopulus deltoides×nigraclones Marron, Nicolas; Maury, Stéphane; Rinaldi, Cécile Annals of Forest Science, Vol. 63, Issue 3 https://doi.org/10.1051/forest:2006012	journal	April 2006
A Heterocomplex of Iron Superoxide Dismutases Defends Chloroplast Nucleoids against Oxidative Stress and Is Essential for Chloroplast Development in Arabidopsis Myouga, Fumiyoshi; Hosoda, Chieko; Umezawa, Taishi The Plant Cell, Vol. 20, Issue 11 https://doi.org/10.1105/tpc.108.061341	journal	November 2008
Superoxide dismutases Fridovich, I. Journal of Biological Chemistry, Vol. 264, Issue 14 https://doi.org/10.1016/s0021-9258(18)83102-7	journal	May 1989

Cited By (8)

Genome-Wide Characterization and Expression Profiles of the Superoxide Dismutase Gene Family inGossypium Zhang, Jingbo; Li, Bo; Yang, Yang International Journal of Genomics, Vol. 2016 https://doi.org/10.1155/2016/8740901	journal	January 2016
Genome-wide characterization and expression analyses of superoxide dismutase (SOD) genes in Gossypium hirsutum Wang, Wei; Zhang, Xiaopei; Deng, Fenni BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3768-5	journal	May 2017
Physiological and Molecular Responses to Variation of Light Intensity in Rubber Tree (Hevea brasiliensis Muell. Arg.) Wang, Li-feng PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0089514	journal	February 2014
Genome-wide investigation of superoxide dismutase (SOD) gene family and their regulatory miRNAs reveal the involvement in abiotic stress and hormone response in tea plant (Camellia sinensis) Zhou, Chengzhe; Zhu, Chen; Fu, Haifeng PLOS ONE, Vol. 14, Issue 10 https://doi.org/10.1371/journal.pone.0223609	journal	October 2019
Concurrent Overexpression of OsGS1;1 and OsGS2 Genes in Transgenic Rice (Oryza sativa L.): Impact on Tolerance to Abiotic Stresses James, Donald; Borphukan, Bhabesh; Fartyal, Dhirendra Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00786	journal	June 2018
Molecular Characterization of MaCCS, a Novel Copper Chaperone Gene Involved in Abiotic and Hormonal Stress Responses in Musa acuminata cv. Tianbaojiao Feng, Xin; Chen, Fanglan; Liu, Weihua International Journal of Molecular Sciences, Vol. 17, Issue 4 https://doi.org/10.3390/ijms17040441	journal	March 2016
Chitosan Application in Vineyards (Vitis vinifera L. cv. Tinto Cão) Induces Accumulation of Anthocyanins and Other Phenolics in Berries, Mediated by Modifications in the Transcription of Secondary Metabolism Genes Singh, Rupesh Kumar; Martins, Viviana; Soares, Bruno International Journal of Molecular Sciences, Vol. 21, Issue 1 https://doi.org/10.3390/ijms21010306	journal	January 2020
Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum) Jiang, Wenqiang J.; Yang, Lei Y.; He, Yiqin H. https://doi.org/10.7287/peerj.preprints.27402v1	journal	December 2018

Similar Records

GENETIC MODIFICATION OF GIBBERELLIC ACID SIGNALING TO PROMOTE CARBON SEQUESTRATION IN TREE ROOTS AND STEMS

Technical Report · Tue Mar 05 00:00:00 EST 2013 · OSTI ID:1903953

Busov, Victor

CRISPR/Cas9-based gene activation and base editing in Populus

Journal Article · Fri May 05 00:00:00 EDT 2023 · Horticulture Research (online) · OSTI ID:1903953

Yao, Tao; Yuan, Guoliang; Lu, Haiwei; +6 more

Multiplex knockout of trichome-regulating MYB duplicates in hybrid poplar using a single gRNA

Journal Article · Thu Mar 17 00:00:00 EDT 2022 · Plant Physiology (Bethesda) · OSTI ID:1903953

Bewg, William P.; Harding, Scott A.; Engle, Nancy L.; +14 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Arabidopsis thaliana
poplars
superoxide dismutase
leaves
genetically modified plants
drought adaption
protein sequencing
plant genomics

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

Citation Formats

References (57)

Cited By (8)

Similar Records

Related Subjects